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smithsonian contributions to botany • number 95

Ecology of the 

Podocarpaceae in 

Tropical Forests

Edited by

Benjamin L. Turner and

Lucas A. Cernusak
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smithsonian contributions to botany • number 95

Ecology of the 

Podocarpaceae in 

Tropical Forests

Edited by

Benjamin L. Turner and 

Lucas A. Cernusak

washington d.c.

2011
ABSTRACT

Turner, Benjamin L., and Lucas A. Cernusak, editors. Ecology of the Podocarpaceae in Tropical Forests. 

Smithsonian Contributions to Botany, number 95, viii + 207 pages, 70 figures, 18 tables, 2011.—The 

emergence of angiosperms in tropical forests at the expense of the gymnosperms, their ancestral relatives, 

was one of the most important events in the evolutionary history of terrestrial plants. Gymnosperms were 

nearly eliminated from the tropics after the evolution of angiosperms in the early Cretaceous, yet conifers 

of the Podocarpaceae are among the few gymnosperm families that persist in tropical forests worldwide. 

Podocarps are often considered to be restricted to montane sites in the tropics, a feature of their biogeography 

that is used by paleoecologists to reconstruct past forest communities. However, podocarps also occur in the 

lowland tropics, where they can be the dominant component of forest canopies. Podocarps have proved to 

be remarkably adaptable in many cases: members of the family have a semi-aquatic lifestyle, exhibit drought 

tolerance and resprouting, and include the only known parasitic gymnosperm. Other intriguing aspects 

of podocarp physiology include the mechanism of water transport in the leaves and the conspicuous root 

nodules, which are not involved in nitrogen fixation but instead house arbuscular mycorrhizal fungi. Perhaps 

most surprising, paleobotanical evidence indicates that far from being ‘relict’ members of tropical forest 

communities, podocarps have been dispersing into the tropics since the late Eocene epoch more than 30 

million years ago. These and other aspects of the Podocarpaceae explored in this volume have far-reaching 

implications for understanding the ecology and evolution of tropical rain forests.

Cover images: Left, nodules and root hairs on Prumnopitys ferruginea (see chapter 11); center, seedlings of Podocarpus guatemalensis growing in a shadehouse in Panama (see chapter 3); right, the semiaquatic podocarp Retrophyllum minus growing in a stream in New Caledonia (see chapter 4). Photo 

credits, left to right: I. A. Dickie, A. W. Cheesman, and J. W. Dalling.

Published by SMITHSONIAN INSTITUTION SCHOLARLY PRESS

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Library of Congress Cataloging-in-Publication Data

Ecology of the podocarpaceae in tropical forests / Benjamin L. Turner and Lucas Cernusak, editors.

 p. cm.—(Smithsonian contributions to botany ; no. 95)

Includes bibliographical references and index.

1. Podocarpaceae. 2. Tropical plants. I. Turner, Benjamin L. II. Cernusak, Lucas. III. Series: Smithsonian 

contributions to botany ; no. 95. 

QK494.5.P73P63 2011

585’.31734—dc22

2010042376

ISSN: 0081-024X (print); 1938-2812 (online)

The paper used in this publication meets the minimum requirements of the American National Standard for Permanence of Paper for Printed Library Materials Z39.48–1992.
Contents

PREFACE v

ACKNOWLEDGMENTS vii

SECTION I – EVOLUTIONARY HISTORY

1 Podocarp Evolution: A Molecular Phylogenetic Perspective 1

Edward Biffin, John G. Conran, and Andrew J. Lowe

2 Dispersal and Paleoecology of Tropical Podocarps 21

Robert J. Morley 

SECTION II – DISTRIBUTION AND ECOLOGY OF 

TROPICAL PODOCARPS

3 Ecology and Distribution of Neotropical Podocarpaceae 43

James W. Dalling, Phoebe Barkan, Peter J. Bellingham, 

John R. Healey, and Edmund V. J. Tanner

4 Ecology and Distribution of the Malesian Podocarps 57

Neal J. Enright and Tanguy Jaffré 

5 Podocarps in Africa: Temperate Zone Relicts or 

Rainforest Survivors? 79

Hylton Adie and Michael J. Lawes 

6 The Ecology of Podocarps in Tropical Montane Forests 

of Borneo: Distribution, Population Dynamics, and Soil 

Nutrient Acquisition 101

Kanehiro Kitayama, Shin-ichiro Aiba, Masayuki Ushio, 

Tatsuyuki Seino, and Yasuto Fujiki 
i v • smithsonian contributions to botany

SECTION III – A TEMPERATE PERSPECTIVE

7 Temperate and Tropical Podocarps: How Ecologically 

Alike Are They? 119

David A. Coomes and Peter J. Bellingham 

8 Ecology of Fire-Tolerant Podocarps in Temperate 

Australian Forests 141

Philip G. Ladd and Neal J. Enright 

SECTION IV – ECOPHYSIOLOGY AND ENVIRONMENT

9 Conifer–Angiosperm Interactions: Physiological Ecology 

and Life History 157

Christopher H. Lusk

10 A Functional Analysis of Podocarp Ecology 165

Timothy J. Brodribb

11 Podocarp Roots, Mycorrhizas, and Nodules 175

Ian A. Dickie and Robert J. Holdaway

SECTION V – SYNTHESIS

12 Podocarpaceae in Tropical Forests: A Synthesis 189

Lucas A. Cernusak, Hylton Adie, Peter J. Bellingham, 

Edward Biffin, Timothy J. Brodribb, David A. Coomes, 

James W. Dalling, Ian A. Dickie, Neal J. Enright, 

Kanehiro Kitayama, Philip G. Ladd, Hans Lambers, 

Michael J. Lawes, Christopher H. Lusk, Robert J. Morley, 

and Benjamin L. Turner 

SUBJECT INDEX 197

INDEX OF SCIENTIFIC NAMES 203
Preface

The emergence of angiosperms in tropical forests at the expense of the 

gymnosperms, their ancestral relatives, was one of the most important 

events in the evolutionary history of terrestrial plants. Although gymnosperms were an important component of the flora on the supercontinent of Gondwana, they were virtually eliminated from the tropics following 

the evolution of angiosperms in the Early Cretaceous. Modern tropical forests 

are overwhelmingly dominated by angiosperms, yet a few gymnosperms persist. 

What can they tell us about the ecology of tropical forests? 

Conifers of the Podocarpaceae are one of the few gymnosperms that inhabit 

tropical forests worldwide, although they remain the least well known of the 

three large conifer families. Podocarps occur throughout the Malesian, African, 

and neotropics and are common in temperate regions of Africa, Australasia, 

and South America. Tropical podocarps are often considered to be restricted to 

montane sites, a feature of their biogeography that is used by paleoecologists to 

reconstruct past forest communities. Yet they also occur in the lowland tropics, 

usually as rare individuals, but sometimes forming the dominant component of 

forest canopies.

In many cases podocarps have proved to be remarkably adaptable: members of the family have a semiaquatic lifestyle (Retrophyllum minus), exhibit 

drought tolerance and resprouting (Podocarpus drouynianus), and include the 

only known parasitic gymnosperm (Parasitaxus usta). Other intriguing aspects 

of their physiology include the mechanism of water transport in the leaves and 

the conspicuous root nodules, which are not involved in nitrogen fixation, but 

instead house arbuscular mycorrhizal fungi. Perhaps most surprising, paleobotanical evidence indicates that far from being “relict” members of tropical forest 

communities, podocarps have been dispersing actively into the tropics since the 

late Eocene epoch more than 30 million years ago. Clearly, there is much to be 

learned from tropical podocarps.

Arising from a workshop held at Macquarie University, Sydney, in February 

2009, this volume explores in detail the ecology of the Podocarpaceae in tropical 

forests. Three main themes are covered: 
v i • smithsonian contributions to botany

1. phylogeny and paleohistory of the Podocarpaceae in 

the tropics (chapters 1 and 2);

2. current distribution of podocarps in the African, American, and Asian tropics (chapters 3–6); and

3. ecology and ecophysiology of the Podocarpaceae in 

both temperate and tropical ecosystems (chapters 

7–11).

The volume concludes with a short synthesis that concisely summarizes the key conclusions of the workshop. 

The outcome is a truly interdisciplinary review of tropical 

podocarps, which we hope will inspire further research on 

these fascinating trees.

A NOTE ON NOMENCLATURE

The taxonomy of the podocarps is complex and the 

least understood of the three major conifer families, with 

many synonyms, recent revisions, and additions that are 

likely to continue in the near future. Here we have followed 

the nomenclature of Farjon (2001) with the exception of 

Parasitaxus usta in place of Parasitaxus ustus (T. Jaffré, 

UMR AMAP Institut de Recherche pour le Développement (IRD), Laboratoire de Botanique et d’Ecologie Végétale, Nouméa, New Caledonia, personal communication, 

November 2009). We also include Phyllocladus here as a 

podocarp; the status of this genus has been controversial, 

but its elevation to family level as Phyllocladaceae is not 

supported by phylogenetic analyses, as outlined in chapter 

1 of this volume. Finally, we use the term “tropical” here 

in a strict geographical sense, defined as the area between 

the Tropics of Cancer and Capricorn. The term should not 

be taken as synonymous with tropical climate, the extent 

of which has varied markedly in relatively recent geological history. 

Benjamin L. Turner

Smithsonian Tropical Research Institute, 

Apartado 0843-03092, Balboa, 

Ancón, Republic of Panama

Lucas A. Cernusak

Research School of Biology, 

The Australian National University, 

Canberra, ACT 0200, 

Australia
Acknowledgments

This volume is the product of a workshop held at Macquarie University, Sydney, Australia, 2–6 February 2009. The workshop was made 

possible by the ARC–New Zealand Research Network for Vegetation 

Function, funded by the Australian Research Council. These workshops were designed to promote novel thinking and personal interactions by 

bringing together small groups of scientists from diverse disciplines for a focused 

examination of a topic of considerable importance to plant science. We hope 

this workshop fulfilled these ideals. We thank Mark Westoby, Ian Wright, and 

Samantha Newton (all at Macquarie University) and Adrienne Nicotra (Australian National University) for their enthusiastic help in organizing the meeting. Lucas A. Cernusak was supported by a Postdoctoral Fellowship from the 

Australian Research Council (project number DP0771427). Finally, we thank a 

number of anonymous reviewers who provided detailed critical comments on 

the chapters. Their efforts have ensured the scientific excellence of this volume. 

1 Podocarp Evolution: 

A Molecular Phylogenetic 

Perspective

Edward Biffin, John G. Conran, 

and Andrew J. Lowe

ABSTRACT. Phylogenetic reconstructions of the relationships among extant taxa can 

be used to infer the nature of the processes that have generated contemporary patterns 

of biotic diversity. In this study, we present a molecular phylogenetic hypothesis for the 

conifer family Podocarpaceae based upon three DNA fragments that have been sampled 

for approximately 90 taxa. We use Bayesian relaxed-clock methods and four fossil constraints to estimate divergence times among the lineages of Podocarpaceae. Our dating 

analyses suggest that although the family is old (Triassic–Jurassic), the extant species 

groups are of recent evolutionary origin (mid- to late Cenozoic), a pattern that could 

reflect a temporal increase in the rate lineage accumulation or, alternatively, a high and 

constant rate of extinction. Our data do not support the hypothesis that Podocarpaceae 

have diversified at a homogeneous rate, instead providing strong evidence for a three- to 

eightfold increase in diversification associated with the Podocarpoid–Dacrydioid clade, 

which radiated in the mid- to late Cretaceous to the earliest Cenozoic, around 60–94 

mya. This group includes a predominance of taxa that develop broad leaves and/or leaflike shoots and are distributed predominantly throughout the tropics. Tropical podocarps 

with broad leaves may have experienced reduced extinction and/or increased speciation 

coincident with the radiation of the angiosperms, the expansion of megathermal forests, 

and relatively stable tropical climates that were widespread through the Tertiary.

INTRODUCTION

Patterns of species diversity reflect the balance of speciation and extinction 

over the evolutionary history of life. These, in turn, are parameters influenced 

by extrinsic factors, such as environmental condition and long-term processes 

of geological and climatic change, and intrinsic attributes of organisms, such 

as morphological innovations that increase the propensity for speciation or 

reduce the risk of extinction. The key aims of evolutionary biologists are to 

Edward Biffin, John G. Conran, and Andrew J. 

Lowe, Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Science, The University of Adelaide, 

Adelaide, South Australia 5005, Australia. Correspondence: E. Biffin, edward.biffin@adelaide

.edu.au.

Manuscript received 13 April 2010; accepted 

9 July 2010.
2 • smithsonian contributions to botany

explain patterns of diversity and, foremost, to determine 

whether there is evidence for significant heterogeneity in 

the “per lineage” patterns of diversity that require explanation (Sanderson and Wojciechowski, 1996; Magallón 

and Sanderson, 2001; Davies et al., 2004; Moore and 

Donoghue, 2007; Rabosky et al., 2007). Phylogenetic 

reconstructions of evolutionary relationships provide an 

indirect record of the speciation events that have led to extant species. Because evolutionary rates can be estimated 

from phylogenetic data, such reconstructions can help to 

elucidate the significance and drivers of biotic diversity 

patterns (Moore and Donoghue, 2007; Ricklefs, 2007).

Molecular phylogenetics has revolutionized the field 

of evolutionary biology. For instance, the molecular clock 

hypothesis predicts that the level of genetic divergence between any two lineages will be proportional to the time 

since divergence from a most recent common ancestor. 

Therefore, using external calibrations (e.g., timing of vicariance events, fossils of known age, and phylogenetic 

affinity) or known mutation rates, it is possible to estimate the age of all of the splits in a molecular phylogenetic tree (which often comprise a majority of splits with 

no associated fossil data to directly estimate the age). 

There has been justified criticism of the molecular clock 

hypothesis. In particular, there is strong evidence that in 

most lineages, the constancy of mutation rates in proteins 

or DNA sequences cannot be assumed (e.g., Ayala, 1997; 

Bromham and Penny, 2003). Recently developed methods, which attempt to incorporate heterogeneity into phylogenetic analysis by specifying a model of rate variation 

among lineages (referred to as relaxed-clock methods), 

are believed to provide more realistic estimates of divergence times in the absence of rate constancy (for recent 

reviews see Bromham and Penny, 2003; Rutschmann, 

2006). Furthermore, there have been promising developments in methods to account for uncertainty inherent 

in the fossil record; Bayesian methods, in particular, can 

incorporate fossil calibrations because parametric prior 

probability distributions make fewer assumptions (relative to “fixed”-point calibrations) concerning the nodal 

placement of a given fossil datum on a phylogenetic tree 

(Yang and Rannala, 2006; Sanders and Lee, 2007). With 

improved confidence in hypotheses, there has been a diversification of questions and associated methodologies 

developed around molecular clock phylogenies. These 

include the examination of vicariance versus dispersal explanations for diversity patterns (e.g., Crisp and Cook, 

2007), the timing of evolutionary radiations and/or extinctions and coincidence with environmental change 

(e.g., Davis et al., 2005), and estimation of the tempo of 

diversification using a statistical framework to contrast 

phylogenetic data with null expectations (e.g., Rabosky 

et al., 2007; Rabosky and Lovette, 2008).

The conifer family Podocarpaceae comprises approximately 173 species and 18 genera (Farjon, 1998) distributed 

primarily in the Southern Hemisphere, although extending 

northward as far as subtropical China and Japan and to 

Mexico and the Caribbean (see Enright and Jaffré, this volume; Dalling et al., this volume). The podocarps have a rich 

fossil record that suggests an origin in the Triassic and a distribution in both the Northern and Southern hemispheres 

through the Mesozoic, although by the Cenozoic the fossil 

record of the family is overwhelmingly southern (Hill and 

Brodribb, 1999). Currently, the Podocarpaceae comprise 

a majority of species-poor (Figure 1.1), range-restricted 

genera (e.g., Acmopyle, Lagarostrobos, Microcachrys,

Microstrobos, Saxegothaea) that are presumably relictual, 

as evidenced by the fossil record, which indicates broader 

distributions and greater species diversities in the past (Hill 

and Brodribb, 1999). Relatively few genera are species rich 

and widely distributed, although Podocarpus comprises approximately 105 species (Figure 1.1) and occurs on all continents except Antarctica and Europe. 

“Nearest living relative” comparisons of Podocarpaceae suggest the conservation of morphology, community associations, and ecological response over evolutionary 

time (Brodribb and Hill, 2004). From this perspective, the 

Podocarpaceae provide an outstanding opportunity to explore the influences of organism–environment interactions 

in the context of large-scale geological and climatic change 

in shaping patterns of extant distribution and diversity. For 

example, the majority of podocarp species presently occur 

within angiosperm-dominated humid forests. This pattern 

is of considerable interest to paleobotanists, ecologists, and 

biogeographers (e.g., Brodribb and Hill, 2004; Brodribb 

and Feild, 2008), given that conifers in general have been 

considered less competitive than angiosperms in productive environments (Bond, 1989). Using the ecophysiological tolerances of extant species as representative of closely 

allied extinct fossil taxa, it has been argued that characteristics such as leaf flattening and associated physiologies 

have promoted the persistence of Podocarpaceae in the face 

of angiosperm competition (Brodribb and Hill, 1997; Brodribb and Feild, 2008). However, within Australia, these 

characteristics may also be associated with range contraction and at least local extinction of several lineages as a 

consequence of increasing aridity in the Miocene–Pliocene 

(Hill and Brodribb, 1999; Brodribb and Hill, 2004). 

Here we use molecular (DNA sequence) data, first, to 

assess phylogenetic relationships among Podocarpaceae 

and, second, using a relaxed molecular clock approach, to 

estimate the timing of diversification events for the major 
number 95 • 3

lineages. From this perspective we explore macroevolutionary patterns within the family and specifically use the 

dated molecular phylogeny to test whether it is necessary 

to invoke among-lineage variation in diversification rates 

to explain the disparities in extant diversity among major 

groups of Podocarpaceae. Our results indicate a highly 

significant shift in diversification rates corresponding to 

approximately the Cretaceous–Tertiary boundary. The 

significance of this diversification rate shift is briefly explored in the context of the angiosperm radiation, biogeography, and ecophysiology.

Phylogenetic relationships 

in the Podocarpaceae

Previous Studies

There have been several previous phylogenetic studies of the Podocarpaceae, including those based upon 

morphology (Hart, 1987; Kelch, 1997, 1998) and molecular (DNA sequence) data (Kelch, 1998, 2002; Conran 

et al., 2000; Sinclair et al., 2002). A key focus of these 

studies has been the assessment of relationships for classification; for instance, the status of Phyllocladus has been 

controversial, although the elevation of this taxon to family level as Phyllocladaceae (e.g., Page, 1990a; Bobrov et 

al., 1999) is not supported by phylogenetic analyses to 

date (Conran et al., 2000; Quinn et al., 2002; Sinclair et 

al., 2002; Wagstaff, 2004; Rai et al., 2008). More generally, there have been conflicting results from morphological versus molecular data; for example, the morphological 

analyses reported in Kelch (1997) suggest that gross leaf 

morphology is a reasonable predictor of evolutionary 

relationships in the Podocarpaceae, whereas analyses of 

DNA sequences found that scalelike leaves were polyphyletic on the estimated topologies (Kelch, 1998; Conran et 

al., 2000; Sinclair et al., 2002). In this instance, there are, 

perhaps, reasonable grounds to favor the molecular over 

the morphological data, given the generally poor support 

FIGURE 1.1. Frequency distribution of species/genus for the Podocarpaceae (estimates according 

to Farjon, 1998).
4 • smithsonian contributions to botany

for relationships from morphology, and in contrast to the 

molecules, the morphological data are not entirely independent of the conclusions (i.e., leaf morphologies were 

included as characters). From a wide range of studies, issues with morphology include fewer variable characters 

compared to DNA sequences and homoplasy, which may 

be a consequence of the choice of characters and character 

construction (i.e., homology assessment) as much as convergent or parallel evolution (Givnish and Sytsma, 1997; 

Scotland et al., 2003). Nevertheless, morphological data 

will continue to be important in reconstructing phylogeny; 

for instance, they provide the only readily sourced information on extinct fossil taxa (Wiens, 2004). 

Phylogenetic studies to date have focused predominantly on generic relationships among members of the 

Podocarpaceae, but Hart (1987) and Kelch (1997) included, at best, a single taxon per genus, with a view to 

resolving deeper branches of the podocarp phylogeny. 

The studies of Conran et al. (2000), Kelch (2002), and 

Sinclair et al. (2002) included denser taxon sampling, so 

that generic monophyly could be assessed. Encouragingly, 

the evidence from both chloroplast and nuclear DNA is 

consistent with contemporary generic schemes (e.g., Page, 

1988, 1990b; Farjon, 1998), although there are a few minor exceptions. For example, Sundacarpus is nested within 

Prumnopitys with strong statistical support, according to 

Sinclair et al. (2002). 

Data and Phylogenetic Methods

There is a range of evolutionary questions that are 

best addressed using complete, or near complete, sampling 

of species, which is the eventual aim of the authors. In 

the present context, we present a preliminary phylogenetic 

analysis of the Podocarpaceae using a data set comprising 89 taxa (including two Araucariaceae as an out-group) 

that have been sequenced for two chloroplast genes (matK 

gene and the trnL–trnF intron and spacer region) and 

internal transcribed spacer 2 of nuclear ribosomal DNA 

(ITS2). Data not sourced from GenBank were sequenced 

de novo (Table 1.1). For sequencing methods, the reader 

is referred to Quinn et al. (2002; matK) and Sinclair et al. 

(2002; trnL–trnF and ITS2) and to Table 1.2, which details 

the primer combinations used for each fragment. Sequence 

alignment was performed using ClustalW (Thompson et 

al., 1994) and manual (“by eye”) adjustment. The aligned 

data matrix is available from the authors upon request. The 

molecular data were analyzed using Bayesian phylogenetic 

methods (as implemented in MrBayes version 3.1.2; Ronquist and Huelsenbeck, 2003). In the first instance, each of 

the matK, trnL–trnF intron and spacer, and ITS2 sequence 

alignments was analyzed separately, assuming a general 

time reversible (GTR) model of sequence evolution with 

Γ distributed rate variation among sites, and a proportion 

of sites were considered invariant (I) (run conditions as 

below). The topologies from each of the separate analyses 

were visually inspected to identify well-supported (posterior probability (PP) ≥ 0.95; i.e., the grouping is found in 

≥95% of the topologies sampled from the PP distribution) 

but conflicting resolutions among individual data sets 

(none found), and the data were concatenated and analyzed in combination using partitioned Bayesian analyses 

(i.e., topologies were derived by allowing each of the separate data partitions to evolve its best-fit set of GTR model 

parameters). Topologies were estimated from four independent runs of 1 × 106

 generations, sampling topology, 

and parameter values every hundredth generation, each 

with four starting chains (one cold, three heated). Convergence was assessed relative to the variance in parameter 

estimates between independent runs and by inspection of 

the convergence diagnostics that are summarized using the 

“sump” command in MrBayes. Majority rule consensus 

trees were generated using the “sumt” command, discarding trees generated during the burn-in, with the burn-in 

proportion determined by inspection of the convergence 

diagnostics. 

Some studies have reported high Bayesian posterior 

probability values corresponding to relatively weaker 

clade support from nonparametric bootstrapping (BS) 

for the same data set (see Alfaro et al., 2003, and references therein). In addition to Bayesian analyses, we used 

the maximum likelihood (ML) implementation GARLI 

(Zwickl, 2006) to estimate support for podocarp relationships. For these analyses, we used the concatenated alignment, a GTR + I + Γ model of sequence evolution with 

parameter values estimated from the data, and we performed 100 BS pseudoreplicates to estimate clade support.

Phylogenetic Relationships of the Podocarpaceae

The Bayesian majority rule consensus topology from 

the concatenated data analyses is presented in Figure 1.2. 

We recovered generally consistent topologies from Bayesian 

and ML analyses in terms of both resolution and statistical 

support: clades receiving a PP > 0.95 also had ML BS values 

of >80%, and there were no strongly supported conflicting resolutions among criteria. As with previous molecular phylogenies of the Podocarpaceae, the conventionally 

recognized genera are strongly supported as monophyletic, with the exception of Prumnopitys, which includes 
number 95 • 5

TABLE 1.1. Taxon sampling for DNA sequences. GenBank accession numbers are listed. An asterisk (*) indicates de novo sequencing; 

a dash (-) indicates missing data; and ITS2 = internal transcribed spacer 2.

Taxon matK trnL–trnF ITS2

Podocarpaceae

Acmopyle pancheri (Brong. & Gris) Pilger * AY083141/AY083097 AY083057

A. sahniana Buchholz & N. E. Gray * * *

Afrocarpus falcatus (Thunb.) C. N. Page AF457111 * *

A. gaussenii (Woltz) C. N. Page - AY083145/AY083101 AY083061

A. gracilior (Pilg.) C. N. Page - * *

A. mannii (Hooker f.) C. N. Page * * *

Dacrycarpus cinctus (Pilger) de Laub. * * *

D. compactus (Wasscher) de Laub. * * AY083055

D. dacrydioides (A. Rich) de Laub. * * *

D. imbricatus (Blume) de Laub. * * *

D. veillardii (Parl.) de Laub. * * *

Dacrydium araucarioides Brogn. & Gris - AY083138/AY083094 AY083054

D. balanse Brogn & Gris * * *

D. cupressinum Soland. ex Lamb. AF457112 AY03136/AY083092 AY083052

D. guillauminii Buchholz * * *

D. lycopodioides Brongniart et Grisebach * * *

D. nausoriense de Laub. * * *

D. nidulum de Laub. * * *

Falcatifolium falciforme (Parl.) de Laub. * * *

F. gruezoi de Laub. - AY083144/AY083100 AY083060

F. taxoides (Brongn. & Gris) de Laub. - AY083143/AY083099 AY083059

Halocarpus bidwillii (Hook. f. ex Kirk) Quinn * AY083128/AY083084 AY083044

H. biformis (Hook.) Quinn * AY083129/AY083085 AY083045

H. kirkii (F. Muell ex Parl.) Quinn AF457117 AY083130/AY083086 AY083046

Lagarostrobos franklinii (Hook. f.) Quinn * AY083132/AY083088 AY083048

Lepidothamnus fonkii Phil. S. Wagstaff - AY083119/AY083075 AY083035

L. laxifolius (Hook. f.) Quinn AF457114 AY083120/AY083076 AY083036

Manoao colensoi (Hook.) Molloy * * *

Microcachrys tetragona (Hook.) Hook. f. * AY083134/AY083090 AY083050

Microstrobos fitzgeraldii (F. Muell.) J. Garden & L. A. S. Johnson * AY083135/AY083091 AY0835051

M. niphophilus J. Garden & L. A. S. Johnson * * *

Nageia fleuryi (Hickel) de Laub. * * *

N. formosensis (Dummer) C. N. Page * * * 

N. nagi (Thunb.) O. Kuntze H. Katsurada AF228112 AY083147/AY083103 AY083063

N. wallichiana (Presl.) O. Kuntze * * *

Parasitaxus ustus (Veillard) de Laub. * AY083131/AY083087 AY083047

Phyllocladus alpinus Hook. f. Wardle AY442146 - AY442160

P. aspleniifolius (Labill.) Hook. f. AY442147 AY083117/AY083073 AY442167

P. hypophyllus Hook. f. J. Read AY442148 AY083116/AY083072 AY442156

P. toatoa Molloy AY442149 - AY442163

P. trichomanoides D. Don ex Cunn. AY442150 AY083118/AY083074 AY442165

Podocarpus affinis Seem. * * *

P. alpinus R. Br. ex Hook. f. * * *

P. annamiensis N. E. Gray - * *

P. aristulatus Parl. * * *

continued
6 • smithsonian contributions to botany

TABLE 1.1. (Continued)

Taxon matK trnL–trnF ITS2

Podocarpaceae

P. brassii Pilger in Engler * * -

P. chinensis (Roxb.) Wall. ex Forbes * * *

P. costalis C. Presl. * * *

P. cunninghamii Colenso - * *

P. dispermus White * * *

P. drouynianus F. Muell. * * *

P. elatus R. Br. ex Endl. AF457113 * *

P. elongatus (Aiton) L’Herit. ex Persoon * * -

P. gnidioides Carrière * * *

P. guatemalensis Standl. - AY083151/AY083107 AY083067

P. henkelii Stapf * * AY845209

P. lambertii Klotzsch ex Endl. * * *

P. latifolius (Thunb.) R. Br. ex Mirb. - * AY845215

P. lawrencei Hook. f. * * *

P. lawrencei * * *

P. lawrencei * * *

P. lawrencei * * *

P. longifoliolatus Pilger in Engler * AY083149/AY083105 AY083065

P. macrophyllus (Thunb.) Sweet AF228111 * *

P. matudae Lundell * * *

P. neriifolius D. Don in Lamb. * * *

P. nivalis Hook. f. * * *

P. nubigenus Lindley * * *

P. polystachyus R. Br. ex Endl. * * *

P. rumphii Blume * * *

P. salignus D. Don * AY083148/AY083104 AY083064

P. smithii de Laub. - * *

P. spinulosus (Smith) R. Br. * * *

P. sylvestris J. Buchholz * AY083152/AY083108 AY083068

P. totara D. Don * * *

Prumnopitys andina (Poepp. ex Endl.) de Laub. * AY083124/AY083080 AY083040

P. ferruginea (D. Don) de Laub. AF457115 AY083127/AY083083 AY083043

P. ferruginoides (Compton) de Laub. * AY083126/AY083082 AY083042

P. ladei (Bailey) de Laub. * AY083125/AY083081 AY083041

P. taxifolia (Soland. ex D. Don) de Laub. * AY083123/AY083079 AY083039

Retrophyllum comptonii (Buchh.) C. N. Page - * *

R. vitiense (Seeman) C. N. Page * * *

Saxegothaea conspicua Lindl. AF457116 AY083121/AY083077 AY083037

Sundacarpus amarus (Blume) C. N. Page * AY083122/AY083078 AY083038

Araucariaceae

Agathis australis (D. Don) Loudon EU025980 AY083115/AY083071 AY083031

Araucaria heterophylla (Salisb.) Franco AF456374 - *

Araucaria biramulata Buchholz - AY083114/AY083070 -
number 95 • 7

Sundacarpus (Prumnopitys sensu lato). The relationships 

among genera are also largely well supported. Strongly 

supported groupings include a “Podocarpoid” clade (Afrocarpus, Nageia, Podocarpus, Retrophyllum), a “Dacrydioid” clade (Dacrydium, Dacrycarpus, Falcatifolium), 

and a “Prumnopityoid” clade (Halocarpus, Lagarostrobos,

Manoao, Parasitaxus, Prumnopitys sensu lato) (Figure 1.2). 

These groupings were previously recovered by Conran et al. 

(2000), although with relatively weak support. At a lower 

taxonomic level, resolutions include the pairing of Manoao 

and Lagarostrobos, with Parasitaxus sister to these, a relationship that was suggested, but not statistically supported, 

in the analyses of Sinclair et al. (2002). Given the level of 

divergence, the segregation of Manoao from Lagarostrobos 

is reasonable on the basis of the present data, as is that of 

Falcatifolium from Dacrydium sensu stricto (cf. Conran et 

al., 2000). The deepest branches in the phylogeny are not 

strongly supported, although a group including Lepidothamnus, Phyllocladus, and the Prumnopityoid clade has 

a PP of 0.91 and a BS and ML bootstrap support of 60%, 

and the pairing of Lepidothamnus and Phyllocladus is also 

weakly supported (PP = 0.79, BS = 68%).

Although genera, and most intergeneric relationships, 

receive strong support from these data, relationships 

among species are relatively ambiguous. For instance, all 

resolutions within Afrocarpus, Dacrycarpus, Nageia, and 

Phyllocladus are, at best, weakly supported (PP ≤ 0.9), 

whereas within Dacrydium and Podocarpus the majority of nodes receive low levels of statistical support. On 

one hand, poor resolution may be a consequence of data 

conflict (i.e., individual data sets support conflicting resolutions), leading to topological ambiguity. Alternatively, 

there may be insufficient evidence to adequately resolve 

relationships, analogous to sampling error in small data 

sets (Graham et al., 1998). As noted above, there were 

no strongly supported conflicting resolutions noted in the 

visual inspection of topologies derived from individual 

data partitions, suggesting that the latter is a reasonable 

hypothesis. Furthermore, as the data are not uninformative per se, it could be argued that poor resolution among 

species is a consequence of relatively recent radiations, 

such that lineages have had insufficient time to accrue 

informative mutations. Typically, this scenario is associated with a broomlike topology (as discussed by Crisp et 

al., 2004), which is evident in the present data. Low-level 

studies of Afrocarpus (Barker et al., 2004), Phyllocladus

(Wagstaff, 2004), and Retrophyllum (Herbert et al., 2002) 

report similarly poor resolution among species, consistent 

with relatively recent origins (see Wagstaff, 2004, who explicitly considers divergence time estimates). The timing of 

radiations within the Podocarpaceae is addressed further 

in the next section.

Molecular dating analyses

In the present study, we use the Bayesian relaxed-clock 

implementation in BEAST (Drummond and Rambaut, 

2007) to estimate divergence times among lineages of the 

Podocarpaceae. BEAST uses a probabilistic model to describe the pattern of change in molecular rates through 

time and Markov chain Monte Carlo (MCMC) simulation 

sampling substitution rates, branch lengths, the individual 

parameters of the substitution model, and tree priors to derive the posterior probability of divergence time estimates 

(Drummond et al., 2006; Rutschmann, 2006). In contrast 

to other currently available molecular dating implementations, BEAST samples both tree topology and branch 

lengths, allowing the user to coestimate phylogeny and 

substitution rates. Departures from the molecular clock 

TABLE 1.2. PCR and sequencing primers.

Region Name Sequence 5'-3' Reference

matK matkF1 AAYAARCATAGATCTTGGCARCAAT This study

matK matkF2 TGYGAATCCATTHTAGTTCCYCTT This study

matK matKR1 AGSRATCTTTCBCSRTATCTCACATA This study

matK matKR2 TTAGCRCATGAAAGTAGAAGTA This study

trnL–trnF TabC CGAAATCGGTAGACGCTACG Taberlet et al. (1991)

trnL–trnF TabF TI’TGAACTGGTGACACGAG Taberlet et al. (1991)

ITS2 ITS3P GCCACGATGAAGAACGTAGCGA Modified from White et al. (1990)

ITS2 ITS4P CCGCTTATTGATATGCTTAAGCTCA Modified from White et al. (1990)
8 • smithsonian contributions to botany

FIGURE 1.2. Phylogenetic relationships (Bayesian analysis, 50% majority rule) in the Podocarpaceae inferred from a matK, trnL–trnF chloroplast intron and spacer, and ITS2 data set. Branch lengths are proportional to the inferred number of changes; dashed branches have a posterior probability (PP) < 0.95, and unless otherwise indicated, solid branches have a PP of 1.0. Genera are according to Farjon (1998), and higher-order groupings are according to Conran et al. (2000).
number 95 • 9

assumption are estimated from the data, with completely 

clocklike (i.e., a single rate across the tree) to highly heterogeneous (i.e., numerous rate changes among branches) 

models representing the opposite extremes of a spectrum 

of rate variation (Drummond et al., 2006). 

In BEAST, fossil calibrations are incorporated as prior 

probability distributions, including parametric distributions such as normal, lognormal, or exponential prior 

probabilities on the distribution of node ages. Given that 

many (if not most) fossil placements have a degree of uncertainty, this approach has advantages over the incorporation of fossil data as “fixed”-point calibrations on a 

particular node (see, e.g., Yang and Rannala, 2006; Benton and Donoghue, 2007; Sanders and Lee, 2007). For 

instance, a prior probability distribution can be designed 

with a peak probability corresponding to the age of a fossil and with decreasing, but nonzero, probabilities that 

the calibration node is either older or younger than the 

fossil age distributed according to a normal distribution 

(Sanders and Lee, 2007).

Divergence time estimates were derived from a chloroplast data set comprising the matK coding region and 

trnL–trnF spacer and intron for 92 taxa (90 representatives of the Podocarpaceae and 2 representatives of the Araucariaceae). Four fossil-derived constraints were used to 

calibrate molecular rates (Table 1.3). These were selected 

from the literature (e.g., Hill and Brodribb, 1999) on the 

basis of the oldest reasonably placed macrofossil age for 

the associated lineage. The incompleteness of the fossil record usually requires that a fossil assigned to a particular 

node provides the minimum age for that node (i.e., older 

fossils may yet be found), although fossil age constraints 

are often applied to the node that subtends the crown 

group, which may be significantly younger than the actual 

age of the fossil lineage (Magallón and Sanderson, 2001; 

Magallón, 2004; Renner, 2005). Where the accuracy of 

fossil placement is uncertain the most objective calibration 

method may be to fix the stem group (age) as the minimum 

age for the diversification of the descendant crown group 

(given that the fossil in question is correctly assigned to 

a lineage; Renner, 2005). In other words, the stem group 

node must be at least as old or older than a fossil belonging to that lineage. Maximum (upper) constraints are 

more difficult to establish (Benton and Donoghue, 2007), 

although a “soft” upper bound (i.e., with nonzero probabilities associated with all reasonable values) can be defined using an appropriate parametric distribution (Yang 

and Rannala, 2006; Sanders and Lee, 2007).

In the present study, the fossil-derived dates were used 

to provide the minimum age for the most recent common 

ancestor of the corresponding stem group. Uncertainty in 

the association between the calibration node and the fossil 

TABLE 1.3. Fossil calibration points used for divergence time estimation. Calibration node numbers correspond to Figure 1.3. Abbreviations: CI, confidence interval; HPD, highest posterior density.

Translated Posterior

Fossil lognormal prior (median, 95% 

Calibration node Reference age (median, 95% CI) HPD of node age)

1. Dacrydioid clade Dacrycarpus linifolius Wells and Hill Early 60 62

(Dacrycarpus, Dacrydium, emend. Hill and Carpenter (Hill and Eocene (50–102) (51–76)

Falcatifolium) Carpenter, 1991)

D. mucronatus Wells and Hill emend. 

Hill and Carpenter (Wells and Hill, 

1989; Hill and Carpenter, 1991)

2. Podocarpoid clade (Afrocarpus, Podocarpus strzeleckianus Townrow Early 60 57

Nageia, Podocarpus, Retrophyllum) (Townrow, 1965) Eocene (50–102) (49–67)

3. Prumnopityoid clade (Halocarpus, Prumnopitys limaniae Pole Paleocene 67 101

Lagarostrobos, Manoao, Parasitaxus, Prumnopitys sp. Mt Somers (Pole, 1998) (55–98) (73–135)

Prumnopitys) Prumnopitys opihiensis Pole (Pole, 1997)

4. Podocarpaceae (Podocarpaceae, Mataia podocarpoides (Ettingshausen) Upper 197 193

Araucariaceae) Townrow Triassic– (178–257) (177–223)

Nothodacrium warrenii Townrow Jurassic

Rissikia Townrow
1 0 • smithsonian contributions to botany

record was accommodated by providing a parametric (lognormal) prior probability distribution for the age of the 

node. The details of the fossil calibration priors are presented in Table 1.3 and are illustrated in Figure 1.3. In each 

instance, the estimated fossil age was used to define the 

zero offset of the lognormal calibration prior, thereby imposing a minimum age constraint approximating the fossil 

age on the relevant stem node. In addition to the above 

constraints, an upper age constraint of 300 mya was placed 

upon the age of the root. Although several extant lineages 

have been associated with microfossils extending back 

before the earliest known macrofossils (see Morley, this 

volume), we preferred the macrofossil evidence because 

of its greater complexity of characters. This allows greater 

confidence in the assignment of fossil material to extant 

lineages as the problems of homoplasy in the fossil record 

tend to increase with clade age (Wagner, 2000), which can 

readily mislead inferences when there are few characters 

for comparison (e.g., Willyard et al., 2007). Note that our 

calibration approach does not rule out much older ages 

(i.e., consistent with the microfossil dates) a priori as the 

calibration prior includes dates approximately twice as 

old as the macrofossil age in the 95% confidence interval 

(Table 1.3). We expect, however, that a detailed assessment 

of the fossil record of the Podocarpaceae is needed to identify synapomorphies uniting fossil and extant taxa (e.g., 

Saquet et al., 2009), rather than postulated relationships 

based upon gross morphological similarity. 

For the analyses in BEAST, a GTR + I + Γ model of 

sequence evolution was assumed with the substitution 

model parameters unlinked across data partitions. An 

uncorrelated lognormal model of rate variation among 

branches in the tree and a Yule prior on branch rates was 

also assumed a priori. Four independent MCMC runs, 

each of 5 × 106 steps, were performed and subsequently 

pooled (after excluding an appropriate burn-in fraction, as 

determined using Tracer version 1.4; Rambaut and Drummond, 2007) to derive the 95% highest posterior density 

of topology and parameter estimates. The topology presented in Figure 1.3 is the maximum clade credibility tree 

derived from the sample of 20,000 trees, with clade posterior probability and 95% highest posterior density (i.e., 

95% of topologies sampled from the posterior have values 

within this range) of divergence times indicated. As with 

the nonclock analyses, the genera and most of the deeper 

internal branches are strongly statistically supported. Furthermore, the relationships inferred among lineages are 

generally consistent among the clock and nonclock phylogenetic analyses (compare Figures 1.2 and 1.3).

Analyses of diversity

Temporal Patterns of Diversity

Although the family appears to be of ancient origin 

(mid-Mesozoic, 95% highest posterior density 177–223 

mya), the molecular dating analyses suggest that the 

majority of extant genera have arisen relatively recently 

(Upper Cretaceous to Cenozoic; Figure 1.3), whereas the 

extant crown groups of these genera are estimated to have 

diversified from predominantly the mid- to late Cenozoic. 

In Figure 1.4, the number of species in the phylogeny from 

the origination of the clade to the present (log scale) is 

plotted against the relative timing of inferred speciations 

(proportion of time since origination of the clade). This 

lineages-through-time plot shows a gradual increase in the 

rate of lineage accumulation and then an upturn at approximately 40 mya, reflecting the estimated recent timing 

of the origination of most extant lineages. 

Lineages-through-time plots have been widely used 

to infer macroevolutionary patterns; for instance, comparison of the data to a Yule (or pure birth) speciation 

model can be used to make inferences regarding the tempo 

of evolution (e.g., Harmon et al., 2003; Ricklefs, 2007; 

Rabosky and Lovette, 2008). Under a Yule model, there 

is an instantaneous rate of per lineage speciation and no 

extinction, giving an exponential increase in the number 

of lineages through time. Significant departures from this 

null model are indicative of temporal variation in the diversification rate (i.e., the per lineage rate of speciation 

and/or extinction; Harmon et al., 2003).

In Figure 1.5, the expectation under a Yule model 

was generated by connecting the point representing the 

first node in the phylogeny with the point representing the 

number of extant podocarp taxa (173) on the log-linear 

lineages-through-time plot. This resulting straight line 

provides the null hypothesis of exponential growth of lineages. To provide a confidence interval on the expectation 

of exponential growth, 100 phylogenies were simulated 

under a Yule model, each giving rise to 173 extant lineages. Clearly, the podocarp data show significant departure from the null model of exponential diversification, 

the comparison being consistent with the hypothesis that 

diversification rates in the Podocarpaceae have increased 

toward the present. However, there are other plausible hypotheses that can be assessed using more complex models 

of diversification.

In Figure 1.6, the lineages-through-time plot is compared with a constant birth-death model, which includes 
number 95 • 1 1

FIGURE 1.3. Maximum clade credibility tree derived from analyses of chloroplast (matK and trnL–trnF intron and spacer) DNA sequences using the Bayesian relaxed-clock implementation BEAST. Median node heights are indicated, and shaded horizontal bars represent the 95% highest posterior density of divergence times for that node. Dashed branches have a PP ≤ 0.95. Numbered nodes correspond to fossil calibrations as detailed in Table 1.3. Scale is in millions of years before present.
1 2 • smithsonian contributions to botany

an instantaneous rate of speciation and extinction. For 

the birth–death model, the extinction fraction was set to 

0.95 (i.e., lineages have a 5% chance of survival to the 

present), and a 95% confidence interval was generated 

from 100 simulated birth-death topologies, as described 

above. As with the actual data, the simulated topologies 

show a sharp upturn toward the present and provide a 

close approximation to the data across the full depth of 

the Podocarpaceae phylogeny. In this instance, the sharp 

upturn in the rate of lineage accumulation may be ascribed 

to the “pull of the present” (Nee et al., 1994). That is, at 

a high relative extinction rate, the probability of a lineage 

persisting into the present decreases with the age of the 

lineage, and therefore, recently evolved lineages are more 

likely to be observed in studies using only extant taxa. Recent simulation studies demonstrate that a similar upturn 

in lineages-through-time plots can also be generated under 

models with large declines in diversification rate, when 

the decline is mediated by a temporally increasing extinction rate (Rabosky and Lovette, 2008). Failure to consider 

extinction can lead to potentially spurious inferences of 

evolutionary tempo. 

Rabosky (2008) provides a method by which a relative extinction rate can be approximated from phylogenetic data, which is implemented in the LASER package 

(Rabosky, 2006) for the R programming language. This 

FIGURE 1.4. Lineages-through-time plot (log scale) for the Podocarpaceae based upon the relaxedclock analyses of chloroplast data. Sampling is reasonably complete for approximately 80% of the 

time since origination (dashed vertical line).
number 95 • 1 3

method uses (ultrametric) branch length estimates and 

standing diversity estimates of terminal taxa to derive a 

maximum likelihood estimate of diversification rate, which 

varies with the relative extinction fraction (e). The likelihood surface can be visualized across the range of values 

of e to determine the value that returns the maximum likelihood estimate of diversification rate. For the podocarp 

data, this analysis was performed on an ultrametric topology (median node heights estimated from the relaxed-clock 

analyses, above) sampled to generic level by pruning all but 

one representative per genus, with generic species richness 

estimates assigned to the terminals according to Farjon 

(1998) (see Figure 1.8). Figure 1.7 plots the likelihood surface for relative extinction fractions ranging from zero (no 

extinction) to 0.99 (99% of lineages go extinct) and suggests that (given the model) a relative extinction rate somewhat in excess of 0.9 (i.e., lineages have a <10% chance of 

surviving to the present) provides a reasonable approximation for these data. Although there are no direct estimates 

of an extinction rate for the Podocarpaceae derived from 

fossils, the inference of a high relative extinction rate seems 

reasonable in light of the levels of Cenozoic diversity of the 

Podocarpaceae in the Southern Hemisphere fossil record 

(Hill and Brodribb, 1999).

FIGURE 1.5. Lineages-through-time plot (log scale) for the Podocarpaceae compared to the expectation of exponential growth of lineages (Yule model; solid line). A 95% confidence interval on this 

expectation (dashed lines) was generated from 100 phylogenies simulated under a Yule model, each 

giving rise to 173 extant species.
1 4 • smithsonian contributions to botany

Shifts in Diversification Rate

The above estimate assumes that the podocarp phylogeny was generated under a constant rate of lineage 

diversification, an assumption that can be tested by contrasting the likelihood of a model that fits a homogeneous 

diversification rate to the data with one in which an ancestral diversification rate shifts at some point to a new 

diversification rate (Sanderson and Wojciechowski, 1996.; 

Rabosky et al., 2007). These analyses were performed in 

LASER, using the branch length and per genus diversities 

as above, and were repeated for 100 topologies sampled 

from the 95% highest posterior density of the BEAST runs 

to assess the robustness of the conclusion to variations in 

topology and branch length estimates. In the first instance, 

the relative extinction rate was set to 0.95, but subsequent 

analyses were performed using e = 0 to test that the conclusions were robust to the model assumptions. For both 

relative extinction rates and all sampled topologies, comparison of standing diversities with those expected under 

a uniform diversification rate rejects the null hypothesis of 

a homogeneous diversification rate for the Podocarpaceae 

(p < 1 × 10-5

, e = 0.95). That is, the observed levels of 

diversity among the podocarpaceous lineages are better 

FIGURE 1.6. Lineages-through-time plot (log scale) for the Podocarpaceae compared to the 

expectation under a constant birth–death speciation model. The dashed lines represent a 95% 

confidence interval generated from 100 phylogenies simulated under a time-homogenous extinction rate of 0.95.
number 95 • 1 5

accounted for by a model in which diversification rates 

have increased or decreased significantly at some point in 

the evolution of family. 

For the variable diversification rate model, the phylogenetic tree is sequentially split at each node, and a diversification rate is optimized onto each descendant lineage. 

The maximum likelihood diversification shift point is the 

node with the highest combined likelihood obtained by 

summing the lineage-specific likelihood estimates from 

each bipartite tree (Rabosky et al., 2007). For the podocarp data, the maximum likelihood shift point is located 

on the most recent common ancestor (MRCA) of the 

Dacrydioid and Podocarpoid clades (Figure 1.8). The extent of this shift ranges from an approximately threefold 

(e = 0) to an eightfold increase in diversification rate at 

e = 0.95. At e = 0.95, other nodes with a likelihood (L) approaching the inferred maximum likelihood shift include 

the immediate ancestor of the Podocarpoid–Dacrydioid 

clade and the successively deeper node (ΔL = 3.5 and 1.9, 

respectively, compared to the maximum likelihood shift 

point), the Podocarpus crown node (ΔL = 3.53), and the 

MRCA of Lepidothamnus, Phyllocladus, and the Prumnopityoid clade (ΔL = 4.9) (Figure 1.8). The latter is the 

largest diversification rate decrease inferred from these 

data. Among these, the two successive nodes immediately below the maximum likelihood shift point are perhaps a consequence of “trickle down,” that is, potentially 

spurious inference of rate shifts stemming from the nested 

nature of phylogenetic data and the high diversity of immediately more nested nodes (Moore et al., 2004). Similarly, the Podocarpoid–Dacrydioid clade not only includes 

Podocarpus but also unites other, relatively species rich, 

clades (e.g., the Dacrydioid clade with 35 species) and has 

a likelihood score exceeding the immediately more nested 

nodes. The identified maximum likelihood shift point was 

robust to variations in the modeled extinction fraction.

Timing and Correlates of Shifts

in Diversification Rate

A major event in the evolution of land plants was 

ecological radiation and taxonomic diversification of 

flowering plants, which is concomitantly associated with 

declining diversities among other plant groups, including 

conifers (e.g., Crane, 1987; Crane and Lidgard, 1989; 

McElwain et al., 2005). The major diversification of angiosperms is believed to have occurred in the mid- to Late 

Cretaceous (middle Albian to early Cenomanian, approximately 100–94 mya); for instance, there is a dramatic 

increase in the representation of angiosperms in regional 

palynofloras (from approximately <5% to >40%) over 

a 40 million year period from the mid-Cretaceous, consistent with rapid radiation (Crane, 1987). Although the 

timing is debated, angiosperm-dominated megathermal 

FIGURE 1.7. The likelihood of diversification rate estimates 

plotted against the relative extinction fraction under a model 

that assumes a homogenous diversification rate that varies 

with the extinction fraction. Analyses performed in LASER 

(Rabosky, 2006) using branch length and species richness 

data as in Figure 1.8.
1 6 • smithsonian contributions to botany FIGURE 1.8. Chronogram of the Podo- carpaceae derived from the Bayesian relaxed-clock analyses and pruned to include a single representative of each 

genus (Podocarpus sampled to subgenus). The estimated species richness of terminals is indicated. The Podocarpoid–Dacrydioid clade (indicated) represents the estimated maximum likelihood diversification rate shift point. Bold taxon names indicate genera with broad leaves or shoots.
number 95 • 1 7

forests appear to have expanded principally from the Albian (e.g., Davis et al., 2005) to the Cretaceous–Tertiary 

boundary (e.g., Morley, 2000). Interestingly, these dates 

accord with the inferred timing of the radiation of the 

Podocarpoid–Dacrydioid clade (Figure 1.3), which on the 

strength of the evidence presented here, has experienced 

higher speciation and/or lower extinction rates relative to 

other podocarp lineages (Figure 1.8).

Among conifers, the podocarps are unusual in that 

an overwhelming majority of taxa are restricted to humid 

environments, including angiosperm-dominated forests 

extending into the tropics. Explanations for this pattern 

have been sought from comparative ecophysiology and 

from the paleobotanical and paleoclimatic data (reviewed 

by Hill and Brodribb, 1999; Brodribb and Hill, 2004; 

Brodribb, this volume). Briefly, the relative success of the 

Podocarpaceae in wet forests has been ascribed to morphological/physiological traits, such as leaf flattening, and 

life history characteristics, including the longevity of individuals, which are believed to facilitate regeneration of the 

podocarps among the dense shade of broad-leaved angiosperms (Brodribb and Hill, 1997, 2004; see also Brodribb 

and Feild, 2008). However, the physiological mechanism 

related to persistence of podocarps in wet forest environments appears to be associated negatively with drought 

tolerance (Brodribb and Hill, 1998, 2004; Hill and Brodribb, 1999), and the demise of several Podocarpaceae 

genera in Australia has been linked to decreasing rainfall, 

increasingly seasonal rainfall regimes, and increased fire 

frequency and intensity through the Cenozoic (Hill and 

Brodribb, 1999; Brodribb and Hill, 2004).

The Podocarpoid–Dacrydioid clade comprises a predominance of taxa with broad leaves and shoots (Afrocarpus, most Dacrycarpus spp., Falcatifolium, Nageia,

Podocarpus, Retrophyllum; Figure 1.8). As suggested elsewhere (e.g., Brodribb and Hill, 2004), leaf/shoot flattening 

among podocarps probably arose prior to the major expansion of flowering plants but subsequently contributed 

to the persistence of those lineages in low-light conditions 

beneath angiosperm-dominated canopies. Furthermore, 

the species included in the Podocarpoid–Dacrydioid clade 

are, for the main part, concentrated in the tropics (cf. 

Kelch’s “tropical clade”; Kelch, 1997) and particularly the 

paleotropics. An exaptation to rainforests may have buffered those taxa from the extremes of historical climatic 

change relative to those experienced at higher latitudes 

(e.g., Dynesius and Jansson, 2000; Jansson and Davies, 

2008) and facilitated northward expansion of “Gondwanan” lineages with the close proximity of the Australian 

and Sunda plates from the mid- to late Tertiary (Morley, 

2003). Thus, a combination of ecophysiological adaptation/exaptation and the past and present distribution of 

suitable climates may have reduced the probability of 

extinction relative to imbricate-leaved lineages and facilitated range expansion and speciation. 

Contingency, Convergence, and Key Traits

In light of the above results, the fact that some of the 

genera with broad shoots (Acmopyle, Prumnopitys sensu 

lato, and Saxegothaea; Figure 1.8) or phylloclades (Phyllocladus) have failed to radiate at a rate comparable to 

the Podocarpoid–Dacrydioid clade requires explanation. 

Of these, Acmopyle, Phyllocladus, and Prumnopitys sensu 

lato have at least some representation within tropical regions. One possible interpretation is provided by historical 

contingency; that is, when the influence of a particular sort 

of character (for instance, on rates of speciation or extinction) is dependent on the proximity of other factors (de 

Queiroz, 2002). Fleshy fruits, for example, are associated 

with high rates of diversification among tropical rainforest understory angiosperms (Smith, 2001) but imperfectly 

in other contexts (Herrera, 1989). Certain putative “key 

traits” of angiosperms (vessels, reticulate venation, closed 

carpels) may have only achieved significance upon transition from the understory into high-light environments 

(Feild et al., 2004). Therefore, an imperfect correlation 

between a trait (or traits) and a particular mechanistic hypothesis to explain elevated diversification rates suggests 

the need to carefully consider other potentially significant 

associations (Donoghue, 2005). The long-term evolution 

of geographic range of the Podocarpaceae in the context 

of historical climatic/geological scenarios (e.g., Yesson and 

Culham, 2006; Moore and Donoghue, 2007) would be 

a fruitful avenue for further investigation given that it is 

“easier to move than evolve” (Donoghue, 2008:11551) 

and species–area effects can strongly influence past and 

present diversities (Jaramillo et al., 2006).

Furthermore, there can be different ways to construct 

an outwardly similar organ, and the various pathways can 

have different outcomes in terms of rates of lineage accumulation (Donoghue, 2005). In this context, the difference 

between parallel and convergent evolution may be significant. Given that leaf flattening is associated with several 

evolutionarily distant lineages in the Podocarpaceae (Figure 

1.8), it is probable that similarities are convergent (i.e., constructed from different starting points). This appears to be 

the case for Phyllocladus, which develops broad phyllodes 

rather than true leaves, the latter being the otherwise general condition within the family. Similarly, the development 
1 8 • smithsonian contributions to botany

of leaflike shoots of small distichous, flattened leaves in 

several divergent lineages may represent an adaptation to 

catch light on the rainforest floor, but these shoots are lost 

when trees reach the canopy. Detailed studies of morphological variation, ideally including fossil taxa, would help 

distinguish parallel from convergent evolution in candidate 

traits and refine mechanistic hypotheses.

Summary

We have presented a preliminary hypothesis of evolutionary relationships among the Podocarpaceae using 

molecular phylogenetic data. On this basis, we have incorporated fossil constraints to estimate molecular evolutionary rates and divergence times for lineages of the 

Podocarpaceae. In general, the molecular phylogeny is 

largely in agreement with conventionally (morphology) 

based classifications for the family, although relative to previous hypotheses there is a high level of confidence in most 

intergeneric relationships. However, there is weak support 

for the majority of relationships within genera, and we 

present evidence that the majority of species are of recent 

evolutionary origin. Although this could be taken to indicate an upturn in diversification rates toward the present, a 

similar pattern could be inferred, for example, under a homogenous rate of speciation and a high but constant rate of 

extinction. Although extinction rates appear to have been 

high among members of the Podocarpaceae, a major shift 

in diversification rate is estimated to be of mid- to Late 

Cretaceous age, which could reflect a response, in terms 

of reduced extinction and/or increased speciation rates, to 

the radiation and expansion of angiosperm-dominated forests. Although further work is needed, the results of this 

study highlight the potential of molecular phylogenetic approaches to develop and test a range of hypotheses in the 

context of evolutionary biology and ecology.

Acknowledgments

We thank Robert Morley (Palynova, UK), Steve Wagstaff (LandCare Research, NZ), Tim Brodribb (The University of Tasmania, Aust.) Robert Hill (The University 

of Adelaide, Aust.), and an anonymous reviewer for constructive comments on the manuscript and members of 

Working Group 51 (Tropical Podocarps) of the ARC–NZ 

Research Network for Vegetation Function for discussion 

and feedback. We acknowledge the support of the Australian Research Council (Discovery Project DP0665859 

awarded to AJL).

REFERENCES

Alfaro, M. E., S. Zoller, and F. Lutzoni. 2003. Bayes or Bootstrap? A 

Simulation Study Comparing the Performance of Bayesian Markov 

Chain Monte Carlo Sampling and Bootstrapping in Assessing Phylogenetic Confidence. Molec. Biol. Evol. 20: 255–266.

Ayala, F. J. 1997. Vagaries of the molecular clock. Proc. Natl. Acad. Sci. 

U.S.A. 94: 7776–7783.

Barker, N. P., E. M. Muller, and R. R. Mill. 2004. A Yellowwood by Any 

Other Name: Molecular Systematics and the Taxonomy of Podocarpus and the Podocarpaceae in Southern Africa. S. African J. Sci. 

100: 630–632.

Benton, M. J., and P. C. J. Donoghue. 2007. Paleontological Evidence to 

Date the Tree of Life. Molec. Biol. Evol. 24: 26–53.

Bobrov, A. V., A. P. Melikian, and E. Y. Yembaturova. 1999. Seed Morphology, Anatomy and Ultrastructure of Phyllocladus L. C. & 

A. Rich. ex Mirb. (Phyllocladaceae (Pilg.) Bessey) in Connection with 

the Generic System and Phylogeny. Ann. Bot. (London) 83: 601–618.

Bond, W. J. 1989. The Tortoise and the Hare: Ecology of Angiosperm 

Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 

227–249.

Brodribb, T. J. 2011 (this volume). A Functional Analysis of Podocarp 

Ecology. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 165–175. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Brodribb, T. J., and T. S. Feild. 2008. Evolutionary Significance of a FlatLeaved Pinus in Vietnamese Rainforest. New Phytol. 178: 201–209.

Brodribb, T. J., and R. S. Hill. 1997. The Light Response Characteristics 

of a Morphologically Diverse Group of Southern Hemisphere Conifers. Oecologia 110: 10–17.

Brodribb, T. J., and R. S. Hill. 1998. The Photosynthetic Drought Physiology of a Diverse Group of Southern Hemisphere Conifer Species 

Is Correlated with Minimum Seasonal Rainfall. Funct. Ecol. 12: 

465–471.

Brodribb, T. J., and R. S. Hill. 2004. The Rise and Fall of the Podocarpaceae in Australia—A Physiological Explanation. In The Evolution of Plant Physiology, A. R Hemsley and I. Poole, eds., pp. 

379–381. Academic Press, London, UK.

Bromham, L., and D. Penny. 2003. The Modern Molecular Clock. Nat. 

Rev. Genet. 4: 216–224.

Conran, J. G., G. G. Wood, P. G. Martin, J. M. Dowd, C. J. Quinn, P. A. 

Gadek, and R. A. Price. 2000. Generic Relationships within and 

between the Gymnosperm Families Podocarpaceae and Phyllocladaceae Based on an Analysis of the Chloroplast Gene rbcL. Austral. 

J. Bot. 48: 715–724.

Crane, P. R. 1987. Vegetational Consequences of the Angiosperm Diversification. In The Origins of Angiosperms and Their Biological 

Consequences, E. M. Friis, W. G. Chaloner, and P. R. Crane, eds., 

pp. 107–144. Cambridge University Press, Cambridge, UK.

Crane, P. R., and S. Lidgard. 1989. Angiosperm Diversification and 

Paleolatitudinal Gradients in Cretaceous Floristic Diversity. Science

246: 675–678.

Crisp, M. D., and L. G. Cook. 2007. A Congruent Molecular Signature of Vicariance across Multiple Plant Lineages. Molec. Phylogen. 

Evol. 43: 1106–1117.

Crisp, M. D., L. G. Cook, and D. A. Steane. 2004. Radiation of the Australian Flora: What Can Comparisons of Molecular Phylogenies 

across Multiple Taxa Tell Us about the Evolution of Diversity in 

Present-Day Communities? Philos. Trans. Roy. Soc. London, Ser. 

B 359: 1551–1571.

Dalling, J. W., P. Barkan, P. J. Bellingham, J. R. Healey, and E. V. J. Tanner. 2011 (this volume). Ecology and Distribution of Neotropical Podocarpaceae. In Ecology of the Podocarpaceae in Tropical 
number 95 • 1 9

Forests, B. L. Turner and L. A. Cernusak, eds., pp. 43–56. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution 

Scholarly Press, Washington, D.C.

Davies, T. J., T. G. Barraclough, M. W. Chase, P. S. Soltis, D. E. Soltis, 

and V. Savolainen. 2004. Darwin’s Abominable Mystery: Insights 

from a Supertree of the Angiosperms. Proc. Natl. Acad. Sci. U.S.A. 

101: 1904–1909.

Davis, C. C., C. O. Webb, K. J. Wurdack, C. A. Jaramillo, and M. J. 

Donoghue. 2005. Explosive Radiation of Malpighiales Supports 

a Mid-Cretaceous Origin of Modern Tropical Rain Forests. Amer. 

Naturalist 165: E36–E65.

de Queiroz, A. 2002. Contingent Predictability in Evolution: Key Traits 

and Diversification. Syst. Biol. 51: 917–929.

Donoghue, M. J. 2005. Key Innovations, Convergence, and Success: Macroevolutionary Lessons from Plant Phylogeny. Paleobiology 31: 77–93.

Donoghue, M. J. 2008. A Phylogenetic Perspective on the Distribution 

of Plant Diversity. Proc. Natl. Acad. Sci. U.S.A. 105: 11549–11555.

Drummond, A. J., S. W. Y. Ho, M. J. Phillips, and A. Rambaut. 2006. 

Relaxed Phylogenetics and Dating Confidence. PLoS Biol. 4: e88, 

doi:10.1371/journal.pbio.0040088.

Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian Evolutionary Analysis by Sampling Trees. BMC Evol. Biol. 7: 214, 

doi:10.1186/1471-2148-7-214.

Dynesius, M., and R. Jansson. 2000. Evolutionary Consequences of 

Changes in Species’ Geographical Distributions Driven by Milankovitch Climate Oscillations. Proc. Natl. Acad. Sci. U.S.A. 97: 

9115–9120.

Enright, N. J., and T. Jaffré. 2011 (this volume). Ecology and Distribution of the Malesian Podocarps. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 57–77. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Farjon, A. 1998. World Checklist and Bibliography of Conifers. Royal 

Botanical Gardens, Kew, Richmond, Surrey, UK.

Feild, T. S., N. C. Arens, J. A. Doyle, T. E. Dawson, and M. J. Donoghue. 

2004. Dark and Disturbed: A New Image of Early Angiosperm 

Ecology. Paleobiology 30: 82–107.

Givnish, T. J., and K. J. Sytsma. 1997. Homoplasy in Molecular vs. Morphological Data: The Likelihood of Correct Phylogenetic Inference.

In Molecular Evolution and Adaptive Radiation, T. J. Givnish and 

K. J. Sytsma, eds., pp. 55–102. Cambridge University Press, Cambridge, UK.

Graham, S. W., J. R. Kohn, B. R. Morton, J. E. Eckenwalder, and S. C. H. 

Barrett. 1998. Phylogenetic Congruence and Discordance among 

One Morphological and Three Molecular Data Sets from Pontederiaceae. Syst. Biol. 47: 545–567.

Harmon, L. J., J. A. Schulte, A. Larson, and J. B. Losos. 2003. Tempo 

and Mode of Evolutionary Radiation in Iguanian Lizards. Science

301: 961–964.

Hart, J. A. 1987. A Cladistic Analysis of Conifers: Preliminary Results. 

J. Arnold Arbor. 68: 269–307.

Herbert, J., P. M. Hollingsworth, M. F. Gardner, R. R. Mill, and P. I. 

Thomas. 2002. Conservation Genetics and Phylogenetics of New 

Caledonian Retrophyllum (Podocarpaceae) Species. New Zealand 

J. Bot. 40: 175–188.

Herrera, C. M. 1989. Seed Dispersal by Animals: A Role in Angiosperm 

Diversification? Amer. Naturalist 133: 309–322.

Hill, R. S., and T. J. Brodribb. 1999. Southern Conifers in Time and 

Space. Aust. J. Bot. 47: 639–696.

Hill, R. S., and R. J. Carpenter. 1991. Evolution of Acmopyle and Dacrycarpus (Podocarpaceae) Foliage as Inferred from Macrofossils in 

South-eastern Australia. Austral. Syst. Bot. 4: 449–479.

Jansson, R., and T. J. Davies. 2008. Global Variation in Diversification 

Rates of Flowering Plants: Energy vs. Climate Change. Ecol. Letters

11: 173–183.

Jaramillo, C., M. J. Rueda, and G. Mora. 2006. Cenozoic Plant Diversity 

in the Neotropics. Science 311: 1893–1896.

Kelch, D. G. 1997. Phylogeny of the Podocarpaceae Based on Morphological Evidence. Syst. Bot. 22: 113–131.

Kelch, D. G. 1998. Phylogeny of Podocarpaceae—Comparison of Evidence from Morphology and 18s rDNA. Amer. J. Bot. 85: 986–996.

Kelch, D. G. 2002. Phylogenetic Assessment of the Monotypic Genera 

Sundacarpus and Manoao (Coniferales: Podocarpaceae) Utilising 

Evidence from 18S rDNA Sequences. Austral. Syst. Bot. 15: 29–35.

Magallón, S. 2004. Dating Lineages: Molecular and Paleontological Approaches to the Temporal Framework of Clades. Int. J. Pl. Sci. 165: 

S7–S21.

Magallón, S., and M. J. Sanderson, 2001. Absolute Diversification Rates 

in Angiosperm Clades. Evolution 55: 1762–1780.

McElwain, J. C., K. J. Willis, and R. Lupia. 2005. Cretaceous CO2 Decline and the Radiation and Diversification of Angiosperms. In A 

History of Atmospheric CO2 and Its Effects on Plants, Animals and 

Ecosystems, J. R Ehrlinger, T. E. Cerling, and M. D. Dearing, eds., 

pp. 133–165. Ecological Studies, No. 177, Springer-Verlag, Berlin. 

Moore, B. R., M. A. K. Chan, and M. J. Donoghue. 2004. Detecting 

Diversification Rate Variation in Supertrees. In Phylogenetic Supertrees: Combining Information to Reveal the Tree of Life, O. R. P. 

Bininda-Emonds, ed., pp. 487–533. Kluwer Academic Press, Dordrecht, Netherlands.

Moore, B. R., and M. J. Donoghue. 2007. Correlates of Diversification in 

the Plant Clade Dipsacales: Geographic Movement and Evolutionary Innovation. Amer. Naturalist 170: S28–S55.

Morley, R. J. 2000. The Origin and Evolution of Tropical Rain Forests. 

John Wiley and Sons, Chichester, UK.

Morley, R. J. 2003. Interplate Dispersal Routes for Megathermal Angiosperms. Perspect. Pl. Ecol. Evol. Syst. 6: 5–20.

Morley, R. J. 2011 (this volume). Dispersal and Paleoecology of Tropical 

Podocarps. In Ecology of the Podocarpaceae in Tropical Forests, B. 

L. Turner and L. A. Cernusak, eds., pp. 21–41. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Nee, S., R. M. May, and P. H. Harvey. 1994. The Reconstructed Evolutionary Process. Philos. Trans. Roy. Soc. London, Ser. B 344: 305–311.

Page, C. N. 1988. New and Maintained Genera in the Conifer Families 

Podocarpaceae and Pinaceae. Notes Roy. Bot. Gard. Edinburgh 45: 

377–396.

Page, C. N. 1990a. Phyllocladaceae. In Volume 1: Pteridophytes and 

Gymnosperms, K. Kubitzki, ed., pp. 317–319, The Families and 

Genera of Vascular Plants. Springer-Verlag, Berlin.

Page, C. N. 1990b. Podocarpaceae. In Volume 1: Pteridophytes and 

Gymnosperms, K. Kubitzki, ed., pp. 332–336, The Families and 

Genera of Vascular Plants. Springer-Verlag, Berlin.

Pole, M. S. 1997. Paleocene Plant Macrofossils from Kakahu, South 

Canterbury, New Zealand. J. Roy. Soc. New Zealand 27: 371–400.

Pole, M. S. 1998. Paleocene Gymnosperms from Mt Somers, New Zealand. J. Roy. Soc. New Zealand 28: 375–403.

Quinn, C. J., R. A. Price, and P. A. Gadek. 2002. Familial Concepts and 

Relationships in the Conifers Based on rbcL and matK Sequence 

Comparisons. Kew Bull. 57: 513–531.

Rabosky, D. L. 2006. LASER: A Maximum Likelihood Toolkit for Detecting Temporal Shifts in Diversification Rates. Evol. Bioinform.

2: 257–260.

Rabosky, D. L. 2008. Testing for Diversification Rate Shifts on Phylogenetic Trees Using Combined Phylogenetic and Taxonomic Data. 

http://www.eeb.cornell.edu/Rabosky/dan/software_files/Rhelp_

Rabosky2007.pdf (accessed June 2008).

Rabosky, D. L., S. C. Donnellan, A. L. Tallaba, and I. J. Lovette. 2007. 

Exceptional Among-Lineage Variation in Diversification Rates during the Radiation of Australia’s Most Diverse Vertebrate Clade. 

Proc. Roy. Soc. London, Ser. B, Biol. Sci. 274: 2915–2923.
2 0 • smithsonian contributions to botany

Rabosky, D. L., and I. J. Lovette. 2008. Explosive Evolutionary Radiations: Decreasing Speciation or Increasing Extinction through 

Time? Evolution 62: 1866–1875.

Rai, H. S., P. A. Reeves, R. Peakall, R. G. Olmstead, and S. W. Graham. 

2008. Inference of Higher-Order Conifer Relationships from a 

Multi-locus Plastid Data Set. Botany 86: 658–669.

Rambaut, A., and A. J. Drummond. 2007. Tracer. Version 1.4. http://

beast.bio.ed.ac.uk/Tracer (accessed 9 Oct 2009). 

Renner, S. S. 2005. Relaxed Molecular Clocks for Dating Historical 

Plant Dispersal Events. Trends Pl. Sci. 10: 550–558.

Ricklefs, R. E. 2007. History and Diversity: Explorations at the Intersection of Ecology and Evolution. Amer. Naturalist 170: S56–S70.

Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian Phylogenetic Inference under Mixed Models. Bioinformatics 19: 1572–1574.

Rutschmann, F. 2006. Molecular Dating of Phylogenetic Trees: A Brief 

Review of Current Methods That Estimate Divergence Times. Diversity Distrib. 12: 35–48.

Sanders, K. L., and M. S. Y. Lee. 2007. Evaluating Molecular Clock Calibrations Using Bayesian Analyses with Soft and Hard Bounds. Biol. 

Lett. 3: 275–279.

Sanderson, M. J., and M. F. Wojciechowski. 1996. Diversification Rates 

in a Temperate Legume Clade: Are There “So Many Species” of 

Astragalus (Fabaceae)? Amer. J. Bot. 83: 1488–1502.

Saquet, H., P. H. Weston, C. L. Anderson, N. P Barker, D. J. Cantrill, 

A. R. Mast, and V. Savolainen. 2009. Contrasted Patterns of 

Hyperdiversification in Mediterranean Hotspots. Proc. Natl. Acad. 

Sci. U.S.A. 106: 221–225.

Scotland, R. W., R. G. Olmstead, and J. R. Bennett. 2003. Phylogeny 

Reconstruction: The Role of Morphology. Syst. Biol. 52: 539–548.

Sinclair, W. T., R. R. Mill, M. F. Gardner, P. Woltz, T. Jaffré, J. Preston, 

M. L. Hollingsworth, A. Ponge, and M. Moller. 2002. Evolutionary Relationships of the New Caledonian Heterotrophic Conifer, 

Parasitaxus usta (Podocarpaceae), Inferred from Chloroplast trnL–

F Intron/Spacer and Nuclear rDNA ITS2 Sequences. Pl. Syst. Evol. 

233: 79–104.

Smith, J. F. 2001. High Species Diversity in Fleshy-Fruited Tropical Understory Plants. Amer. Naturalist 147: 646–653.

Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet. 1991. Universal Primers for Amplification of Three Non-coding Regions of Chloroplast 

DNA. Pl. Molec. Biol. 17: 1105–1109.

Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: 

Improving the Sensitivity of Progressive Multiple Sequence Alignments through Sequence Weighting, Position Specific Gap Penalties 

and Weight Matrix Choice. Nucl. Acids Res. 22: 4673–4680.

Townrow, J. A. 1965. Notes on Tasmanian Pines. I. Some Lower Tertiary 

Podocarps. Pap. Proc. Roy. Soc. Tasmania 99: 87–107.

Wagner, P. J. 2000. Exhaustion of Morphological Character States 

among Fossil Taxa. Evolution 54: 365–386.

Wagstaff, S. J. 2004. Evolution and Biogeography of the Austral Genus 

Phyllocladus (Podocarpaceae). J. Biogeogr. 31: 1569–1577.

Wells, P. M., and R. S. Hill. 1989. Fossil imbricate-leaved Podocarpaceae 

from Tertiary sediments in Tasmania. Austral. Syst. Bot. 2: 387–

423.

White, T. J., T. Burns, S. Lee, and J. Taylor. 1990. Amplification and 

Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In 

PCR Protocols. A Guide to Methods and Applications, M. A. Innis, 

D. H. Gelfand, J. J. Sninsky, and T. J. White, eds., pp. 315–322. 

Academic Press, San Diego. 

Wiens, J. J. 2004. The Role of Morphological Data in Phylogeny Reconstruction. Syst. Biol. 53: 653–661.

Willyard, A., J. Syring, D. S. Gernandt, A. Liston, and R. Cronn. 2007. 

Fossil Calibration of Molecular Divergence Infers a Moderate Mutation Rate and Recent Radiations for Pinus. Molec. Biol. Evol.

24: 90–101.

Yang, Z., and B. Rannala. 2006. Bayesian Estimation of Species Divergence Times under a Molecular Clock Using Multiple Fossil Calibrations with Soft Bounds. Molec. Biol. Evol. 23: 212–226.

Yesson, C., and A. Culham. 2006. Phyloclimatic Modeling: Combining 

Phylogenetics and Bioclimatic Modeling. Syst. Biol. 55: 785–802. 

Zwickl, D. J. 2006. Genetic Algorithm Approaches for the Phylogenetic 

Analysis of Large Biological Sequences Datasets under Maximum 

Likelihood Criterion. Ph.D. diss., The University of Texas at Austin, 

Austin.
2 Dispersal and Paleoecology 

of Tropical Podocarps

Robert J. Morley

ABSTRACT. The paleoecology of tropical Podocarpaceae is reviewed for Africa and 

Southeast Asia. The family first appeared in the Triassic of Gondwana, after which it 

diversified through the Cretaceous and earliest Tertiary, and although some Northern Hemisphere Jurassic records are known, it has essentially remained a southern or 

southern-derived family until the present day. It seems to show a preference for areas of 

wet climate throughout its history. Podocarpus sensu lato dispersed into Southeast Asia 

during the late Eocene, and its present distribution is best explained by dispersal from 

India and possibly multiple long-distance dispersal events from Australia. Dacrydium

reached Southeast Asia during the early Oligocene, presumably by island hopping, via 

the Ninety East Ridge and India and subsequently expanded its range to Japan during 

the middle Miocene climatic optimum. It is likely that the dispersal pathway was via 

low-altitude heath forests. Dacrycarpus and Phyllocladus dispersed into New Guinea as 

the island became established during the late Miocene and then island hopped to Borneo 

during the mid-Pliocene. Dacrycarpus subsequently reached Sumatra and the Malay Peninsula during the Pleistocene. In Africa, Podocarpus sensu lato was probably present in 

upland areas during the mid-Tertiary but dispersed by island hopping between montane 

areas to West Africa in the late Pliocene. In both Africa and Southeast Asia, the Podocarpaceae have clearly increased their range within the low latitudes following mid-Pliocene 

global climate deterioration and the Northern Hemisphere ice expansion.

Introduction

The Podocarpaceae is an essentially Southern Hemisphere family of conifers, 

centered initially in Gondwana, subsequently in Australasia and southernmost 

South America, and currently in Malesia. The earliest firmly accepted podocarp macrofossils are from the Triassic of Gondwana, including Madagascar 

(Townrow, 1967; Axsmith et al., 1998; Anderson et al., 2007), with numerous 

subsequent records from the Jurassic of Patagonia (Gnaedinger, 2007), Africa 

(Townrow, 1967), India (Rao, 1943, 1947, 1949; Vishnu-Mittre, 1959; Suthar 

and Sharma, 1987; Srivastava and Gularia, 2006), Australasia (Townrow, 1967; 

Robert J. Morley, Palynova Limited, 1 Mow Fen 

Road, Littleport, Cambridgeshire, CB6 1PY, 

UK; and Department of Earth Sciences, Royal 

Holloway, University of London, Egham, Surrey 

TW20 0EX, UK. Correspondence: palynova@

btinternet.com.

Manuscript received 13 April 2010; accepted 

9 July 2010.
2 2 • smithsonian contributions to botany

Hill, 1994), and Antarctica (Oecipa, 1998). Podocarps 

were prominent across the Gondwanan region, including Patagonia (Archangelsky and Del Fueyo, 1989) and 

Antarctica (e.g., Poole and Cantrill, 2006), throughout the 

Cretaceous period (e.g., Dettmann, 1994; Douglas, 1994; 

Hill, 1994), with most modern genera appearing during 

the Cretaceous (Dettmann, 1994), possibly related to the 

onset of wetter and warmer climatic conditions associated 

with the opening of the Southern Ocean. Despite their 

mainly Gondwanan distribution, there are also scattered 

podocarp records from Laurasia, which include Scarburgia

from the Yorkshire Jurassic, described by Harris (1979) 

and with bi- and trisaccate pollen (Van Konijnenberg-van 

Cittert, 1971), and Harrisiocarpus from Poland (Reymanowna, 1987). There are also several Mesozoic records 

of Nageia-like leaves from East Asia (Krassilov, 1974; 

Kimura et al., 1988; Zhou, 1983), but since the Late Triassic, Nageia-like Stalagma samara Zhou from China has 

monocolpate pollen, which is unknown in Podocarpaceae. 

These may be from a different group of conifers that has 

independently evolved wide multiveined leaves, or they 

may reflect an extinct clade of early podocarps. Tertiary 

macrofossils attributed to Podocarpus from the middle 

Eocene of Europe (including England) are now, however, 

considered to belong to Pinaceae and the genus Cathaysia 

(Van Konijnenberg-van Cittert, personal communication). 

All Tertiary macrofossils from mid- and high-latitude localities are thus in the Southern Hemisphere. Most “Podocarpidites” pollen from the Laurasian Tertiary is unlikely 

to be related to the Podocarpaceae; these types are more 

likely to be from extinct Pinaceae, with pollen in which the 

typically finely reticulate sacci (typically more coarsely reticulate in podocarps) are larger than the body. However, 

some pollen referred to Podocarpus from the Miocene of 

Alaska is very convincing (Reinink-Smith and Leopold, 

1995) and may truly reflect the former extent of the genus. 

This paper reviews the history and paleoecology of the 

Podocarpaceae in the old-world tropics, through the Cretaceous, Tertiary, and Quaternary periods, based mainly 

on the pollen record. There are numerous misconceptions 

regarding the occurrence of conifers in the low latitudes, 

including that they are on the decline (de Laubenfels, 

1988), that they are remnants of a former mixed gymnosperm/angiosperm Cretaceous vegetation (Richards, 

1996:18), and that lowland podocarps have “descended” 

from montane taxa (de Laubenfels, 1988). The fossil record allows judgments to be made on each of these issues.

There are currently 105 species of Podocarpaceae in 

10 genera in Malesia (Enright and Jaffré, this volume) and 

possibly 17 in Africa in 2 genera (Adie and Lawes, this 

volume). In Africa, all species of Podocarpus and Afrocarpus are montane, whereas in Malesia, podocarps have 

common representatives in both montane and lowland 

habitats. Montane-restricted Malesian genera are Phyllocladus (with a single species), Falcatifolium (five species), 

Dacrycarpus (eight species), and Prumnopitys (two species). Genera with both montane and lowland representatives are Dacrydium (20 species, of which about 4 are 

common in lowland habitats) and Podocarpus (56 species, 

of which about 10 are lowland taxa). All species of Nageia

occur in the lowlands, although one ranges into the montane zone (based on de Laubenfels, 1988). Although lowland species may occur in low numbers in species-diverse 

mixed dipterocarp forests, they are primarily elements 

of localities with poor soil or drainage issues, such as in 

kerangas (heath forest), peat swamps, limestone, coastal 

forest on sand, and coastal bluffs (for further discussion, 

see Enright and Jaffré, this volume). 

Pollen types in

the Podocarpaceae

The pollen of Podocarpaceae are invariably mono-, 

bi-, or trisaccate, with a single exception: the monospecific genus Saxegothaea possesses inaperturate pollen, 

which prompted Erdtman (1965) to suggest that this genus should be transferred to the Araucariaceae and others 

to place it in its own family, Saxegothaeaceae (Gaussen, 

1973; Woltz, 1985). However, current opinion is in favor 

of the genus being retained in the Podocarpaceae (e.g., Mill 

and Stark-Schilling, 2009), and molecular evidence (Biffin et al., this volume) suggests that the genus is, indeed, 

within the Podocarpaceae, but in an isolated, near-basal 

position. Some Mesozoic macrofossil cones with in situ 

pollen variously attributed to the Podocarpaceae include 

Rissikia from the Jurassic of Australia, with bisaccate and 

striate-bisaccate pollen, as well as Nothodacrium from the 

Jurassic of Antarctica (Townrow, 1967) and Apterocladus

from the Early Cretaceous of Patagonia (Archangelsky, 

1966), both with “Callialasporites”-type pollen. Balme 

(1995) considered the latter two taxa to be araucarian and 

the former taxon (at least the male cone Masculostrobus 

warrenii ascribed to Nothodacrium warrenii) as a doubtful podocarp, based on its araucarian pollen. As noted 

above, Stalagma samara from the Late Triassic of China, 

attributed to Podocarpaceae by Zhou (1983), has monocolpate pollen and is therefore unlikely to be a podocarp. 

It is noteworthy that the trisaccate condition is restricted to the Podocarpaceae (except for aberrant grains) 
number 95 • 2 3

and also seems to be near basal to the group, with a fossil 

record extending to the Middle (e.g., Van Konijnenbergvan Cittert, 1971; Suthar and Sharma, 1987) and Early 

Jurassic (de Jersey, 1971). The immediate ancestor to the 

Podocarpaceae should therefore yield a pollen type from 

which the simple trisaccate condition seen in Trisaccites

(e.g., Baldoni and Taylor, 1982) could be readily derived.

The record of the Podocarpaceae from the low latitudes comes essentially from pollen (Figure 2.1). The dispersed pollen of the Podocarpaceae, both modern and 

fossil, were first described by Cookson (1947, 1953; Cookson and Pike, 1953a, 1953b, 1954), and modern pollen 

were subsequently described by Pocknall (1981). There is 

a fair correspondence between pollen types and the major 

genera, as summarized in Table 2.1. For genera that occur 

in the low-latitude Tertiary, Dacrycarpus has trisaccate 

pollen (Figure 2.1A), whereas Phyllocladus has bisaccate 

pollen with diminutive sacci (Figure 2.1C). The genus 

FIGURE 2.1. Pollen of the Podocarpaceae, showing (A) Dacrycarpidites antarcticus = Dacrycarpus pollen; (B) 

Podocarpidites sp., in Podocarpus, Nageia, Prumnopitys; (C) Phyllocladites palaeogenicus, in Phyllocladus hypophyllus; and (D) Lygistepollenites florinii, in most Dacrydium spp. Images A–C show modern pollen from The 

Australian Pollen and Spore Atlas (http://apsa.anu.edu.au); D is fossil pollen from Oligocene of Java (photo by Eko 

Budi Lelono).

TABLE 2.1. Podocarp pollen types from the Southeast Asian Tertiary. Microcachrydites antarcticus is only known from probable 

reworked specimens from New Guinea.

Taxon Dispersed pollen type Reference

Podocarpus Podocarpidites spp. Cookson (1947)

sensu lato

Dacrydium Lygistepollenites florinii Stover and Partridge 

(1973)

Dacrydium Dacrydium guillauminii type Erdtman (1965)

guillauminii

Dacrycarpus Dacrycarpidites antarcticus Cookson and Pike 

(1953a)

Phyllocladus Phyllocladites palaeogenicus Cookson and Pike 

(1954)

Microcachrys Microcachrydites antarcticus Cookson (1947)
2 4 • smithsonian contributions to botany

Podocarpus is typically characterized by bisaccate pollen, 

in which the sacci are often larger than the body (Figure 

2.1B). However, similar bisaccate pollen occurs in Lepidothamnus laxifolius (formerly placed in Dacrydium), and 

there are also some Pinus species with somewhat similar 

pollen, so records of bisaccate Podocarpus-type pollen or 

Podocarpidites species need not be conclusive evidence for 

the genus Podocarpus. Fossil pollen is typically referred 

to morphotaxa, as indicated in Figure 2.1 and Table 2.1. 

Dacrydium, as considered by Farjon (1998), contains 

just two pollen types: the “typical” form has a strongly 

rugulate body (Figure 2.1D) and is placed in the fossil taxon Lygistepollenites florinii, whereas monosaccate 

pollen occurs in Dacrydium guillauminii from New Caledonia and is reminiscent of Tsuga pollen in the Pinaceae. 

With the placement by Farjon (1998) of the New Zealand 

Dacrydium laxifolium (with Podocarpus-like pollen) into 

Lepidothamnus and the Tasmanian Dacrydium franklinii 

(with Phyllocladus-like pollen) into Lagarostrobos, the 

taxonomic significance of Dacrydium-type pollen has now 

been elevated, and the ambiguity previously discussed by 

Pocknall (1981) has disappeared with taxonomic revision.

Early Cretaceous Podocarps

Fossil woods occur widely in the Early Cretaceous 

of Africa and Indochina. The African woods have been 

reviewed by Dupéron-Laudoueneix (1991) and DupéronLaudoueneix and Dupéron (1995), and several examples 

suggest possible affinity (never definite) with the Podocarpaceae, such as Metapodocarpoxylon, which is one of the 

commonest elements (e.g., Philippe et al., 2003). They occur together with woods attributed to the Araucariaceae 

and the extinct gymnosperm family Cheirolepidiaceae. A 

second genus generally attributed to the Podocarpaceae 

is Protophyllocladoxylon, also present in the Early Cretaceous of Indochina. However, bisaccate pollen, which 

is ubiquitous in extant Podocarpaceae (with the exception of Saxegothaea, as noted above), is virtually absent 

from Early Cretaceous sediments of both regions (e.g., for 

the Ivory Coast and Senegal, see Jardine and Magloire, 

1965; for Indochina, see Racey et al., 1994, and Racey 

and Goodall, 2009), which are characterized by abundant 

Araucariacites and Classopollis pollen (the latter derived 

from the extinct gymnosperm family Cheirolepidiaceae). 

Since the attribution of these woods to the Podocarpaceae 

is mostly questioned (e.g., Philippe et al., 2003), it seems 

unlikely that these genera are from the Podocarpaceae, because podocarpoid bisaccate pollen would be expected to 

occur in the same- or equivalent-age sediments. However, 

the possibility needs to be considered that the woods are 

allied to Saxegothaea, which as noted above, has inaperturate, Araucaria-like pollen. Here, paleoclimate evidence 

helps to clarify the relationships. Lithological and palynological evidence indicates that the paleoclimate was warm 

and dry, and the absence of tree rings suggests aseasonality. Today, virtually all podocarps, including Saxegothaea, 

are essentially restricted to wet climates; this throws further doubt on the possible podocarpaceous affinity of the 

wood fossils. The ambiguity in attribution of many Mesozoic wood morphogenera to extant families has recently 

been emphasized by Philippe and Bamford (2008).

The only records of bisaccate pollen from the Early 

Cretaceous of equatorial Africa that may have affinity with 

the Podocarpaceae are specimens referred to the morphogenus Alisporites (a morphotaxon name previously used 

to mean bisaccate pollen compressed in polar view) from 

the Barremian and Aptian of Gabon (Doyle et al., 1977). 

These are small in size, fitting with the current size range 

of many Podocarpus species, and occur in assemblages 

overwhelmingly dominated by Classopollis and Exesipollenites tumulus (Cheirolepidiaceae). Similar forms occur 

in the stratigraphically equivalent succession in Brazil (Regali et al., 1975). The occurrences of Alisporites species 

characterize the “synrift” period of development of the 

early Atlantic Rift, when upwarping would have resulted 

in elevated regions marginal to the rift, as is the case today 

for the East African Rift. They become less common in the 

Aptian during the early postrift phase and are absent from 

the Albian onward (Figure 2.2). It is therefore possible that 

these bisaccates were derived from Podocarpaceae growing in upland settings along the proto-Atlantic upwarp, 

in the same manner as some Podocarpaceae today along 

the East African Rift Valley. They then disappeared from 

the region as the Atlantic Rift went through the postrift 

phase, during which period the uplands bordering the 

Mid-Atlantic Rift would have disappeared by a combination of erosion and subsidence.

The analysis by Muller (1968) from the Pedawan Formation is still the only significant study of Early Cretaceous palynofloras from Sundaland (southeastern Asia). 

The lower part of the formation is thought to be of early 

Albian to Aptian age and, as with similarly aged localities 

from Africa, yielded abundant Exesipollenites tumulus,

Classopollis spp., and Araucariacites spp. and very rare bisaccates of probable affinity with Laurasian conifers (Morley, 2000). Similarly, the Early Cretaceous Khorat Group, 

widespread across Indochina, is dominated by Classopollis pollen with few bisaccates (Racey et al., 1994). It is 
number 95 • 2 5

unlikely that the Podocarpaceae contributed significantly 

to the Early Cretaceous vegetation in this broad region. 

The Early Cretaceous of India is characterized by common Podocarpidites species, and these bisaccates are often 

accompanied by the trisaccate Microcachrydites antarcticus (S. Noon and P. Brenac, CoreLab Indonesia, personal 

communication), which also is common in the Early Cretaceous of New Guinea (R. J. Morley, unpublished data).

Late Cretaceous

Africa

The Late Cretaceous of West Africa is devoid of bisaccate pollen (Jardine and Magloire, 1965). The Late 

Cretaceous is characterized by the demise of equatorial 

gymnosperms, with Classopollis suddenly disappearing 

FIGURE 2.2. Distribution of possible Podocarpus pollen (as Alisporites spp.) in 

the Early Cretaceous “pre-salt” Cocobeach succession of Gabon (from Doyle et al., 

1977).
2 6 • smithsonian contributions to botany

from the region at the end of the Cenomanian, concomitant with the mid-Cretaceous rise of angiosperms (Figure 

2.3). Gymnosperms did retain a presence, with the diversification of the Gnetales, characterized by Ephedripites

species and elater-bearing pollen, but with wetter climates 

from the Campanian onward, the elater-bearing group 

became extinct and ephedroids became much reduced. 

Through the later Late Cretaceous, Araucariacean pollen 

remained present in significant quantities, only to disappear entirely from the record at the Cretaceous–Tertiary 

boundary, after which time there are no records of conifer 

pollen in West African assemblages until the cooling phase 

of the late Neogene. 

Southeast Asia

The upper part of the Pedawan Formation in Sarawak, dated as Turonian by Muller (1968) but more likely 

of Santonian age (Morley, 1998), is dominated by Araucariacites species and lacks any bisaccate pollen. It thus has 

similarities to the African equatorial palynoflora. 

India and New Guinea

Podocarp pollen (both bisaccate and the trisaccate 

Microcachrydites antarcticus) virtually disappears from 

the Indian record during the transition from the Early to 

Late Cretaceous, previously emphasized by Morley (2000) 

and confirmed from recent petroleum industry records of 

Noon and Brenac (personal communication). Similarly, in 

New Guinea records of M. antarcticus are absent from 

the Late Cretaceous. However, Podocarpidites records 

continue to occur infrequently in the Late Cretaceous of 

India (e.g., Baksi and Deb, 1981), and fossil wood referable to Podocarpoxylon has been recorded from the intertrappean beds (Trivedi and Srivastava, 1989; Srivastava 

and Gularia, 2006). In general, podocarps appear to have 

played little part in the Late Cretaceous vegetation either 

of equatorial Africa, India, or Southeast Asia, although 

with the limited coverage of the palynological record for 

this time period in some regions they could possibly have 

been present in any upland areas.

Tertiary and Quaternary

India

Scattered Podocarpidites records continue into the Paleocene of India (e.g., Saxena, 1991; Prasad et al., 2009) 

and can be locally common (V. Prasad, Birbal Sahni Institute, Lucknow, India, personal communication), although 

Kar (1985) considers that pollen from Podocarpidites

species from the Paleocene Matanomadh Formation of 

Kutch (northwest India) are reworked from the Early Cretaceous. The identity of Indian Paleogene Podocarpidites

with Podocarpus needs careful review; although some 

published illustrations (e.g., Prasad et al., 2009: fig. 5.12) 

could, indeed, be from Podocarpus, others (Prasad, personal communication) referred to the form genus Podocarpidites are larger than any known Podocarpaceae, and 

their affinity with Podocarpus sensu lato (s.l.) is thus questionable. It therefore seems that Podocarpus s.l. was a sporadic element of Indian early Tertiary vegetation. It was an 

element of vegetation on islands of the Ninety East Ridge 

in the Indian Ocean during the Paleocene and Oligocene 

(Kemp and Harris, 1975). 

Southeast Asia

The Paleocene palynological record for Southeast Asia 

is very poor. The Kayan Formation in Sarawak (see Figure 

2.4), interpreted to be mainly Late Cretaceous by Muller 

(1968), is most likely of Paleocene age. This succession 

is characterized by a low-diversity assemblage with the 

bisaccates Alisporites similis and Rugubivesiculites reductus, which are probably derived from Laurasian conifers 

rather than podocarps (Morley, 2000). Further, Paleocene 

assemblages from the Pre-Ngimbang Formation from the 

East Java Sea region (R. J. Morley, unpublished data) lack 

any bisaccates, as do assemblages from the early Eocene 

Waripi Formation of New Guinea.

The palynofloras noted above are all relatively low diversity assemblages, and none can be envisaged to really 

“sample” the flora of each period sufficiently to confidently 

judge that bisaccate-pollen-producing plants were definitely absent from the regional vegetation. This is not the 

case for the middle Eocene Nanggulan Formation of Central Java, where a study by Lelono (2000) exhaustively recorded the palynoflora, describing over 300 morphotypes 

without any records of bisaccate pollen during this period 

of high global temperatures (Zachos et al., 2001). The 

pattern thus parallels that in West Africa, where intensive 

studies for the period following the Cretaceous–Tertiary 

boundary event consistently demonstrate the absence of 

conifer pollen. It thus appears that the Cretaceous–Tertiary 

boundary bolide impact exterminated conifers from the 

lowland paleotropics, with the possible exception of the 

Indian subcontinent. Subsequent occurrences of tropical 

conifers in Southeast Asia and Africa are therefore likely 
number 95 • 2 7

FIGURE 2.3. Occurrence of gymnosperm and angiosperm pollen in the Cretaceous of West Africa 

(Senegal and Ivory Coast) from Morley (2000), extracted from Jardine and Magloire (1965).
2 8 • smithsonian contributions to botany

to be due to immigration with dispersal via land bridges, 

filter routes, or via long-distance dispersal events.

Podocarpus Sensu Lato

Podocarpus-type pollen has a very long history in 

Australasia (Dettmann, 1994), extending throughout the 

Cretaceous. Podocarpus macrofossils have also been reported from the Paleocene of Patagonia (South America), 

with multiple species, together with Retrophyllum (Wilf et 

al., 2003; Iglesias et al., 2007).

In contrast, the first record of Podocarpus-type pollen from the Southeast Asian region is from the late Eocene section of the Nanggulan Formation in Central Java 

(Lelono, 2000). Podocarp pollen gradually appeared during the middle to late Eocene transition (Figure 2.5). The 

specimens are all small bisaccates typical of Podocarpus 

s.l., with a comparatively small body and coarsely infrareticulate sacci. The specimens are roughly divided into three 

morphotypes depending on overall shape, which may indicate more than one species. They are assumed to reflect 

Podocarpus growing in montane settings since (1) more 

than one species may be involved and (2) the specimens are 

more prominent in more open marine settings, where the 

supraregional pollen component will be more prominent. 

Immigration from India following late Eocene cooling is 

suspected, as previously suggested by Morley (2000). 

From the early Oligocene onward, Podocarpus-type 

pollen occurs regularly in most stratigraphic intervals 

and in most areas, with regular records also from Vietnam, Taiwan, and China. There are also possible rare records from the Miocene of Siberia (Tomskaya, 1981) and 

Alaska (Reinink-Smith and Leopold, 2005), suggesting 

that Podocarpus may have ranged further north around 

the Pacific rim during the Miocene climatic optimum.

It is difficult to draw specific conclusions from the occurrence of Podocarpus pollen in Southeast Asian younger 

Tertiary sediments. Pollen occurs regularly in most sections, but in low numbers, and generally shows little 

change in abundance with depth in stratigraphic sections. 

Consequently, few judgments can be made with respect 

to its ecological significance. The commonest Podocarpus

pollen type is of small size and has a small body, reminiscent of the common coastal tree P. polystachyus. Where 

this type occurs regularly and without other Podocarpus

morphotypes, the pollen is assumed to come from a similar species growing in a coastal habitat. However, Podocarpus pollen often shows increased diversity, with the 

P. polystachyus pollen type being accompanied by larger 

types, which may possess a larger body, as in P. neriifolius. 

In such instances, the pollen is suspected to have been derived from montane settings. There is little evidence from 

pollen studies of peats, coals, or other organic-rich sediments to throw light on the former occurrences of Podocarpus that are currently associated with peat-forming 

settings, despite several Podocarpus species occurring today on peat swamps.

A good example suggesting derivation of Podocarpus

pollen from montane forests is from the Perning hominin 

site near Mojokerto in East Java (R. J. Morley, unpublished data), which is of latest Pliocene or earliest Pleistocene age (Huffman, 2001; Huffman and Zaim, 2003). 

At least three Podocarpus pollen types accompany regular 

Dacrycarpus imbricatus pollen in a setting without lowland forests because of a strongly seasonal lowland climate (but moist montane climate), and this occurrence is 

taken to reflect a well-developed montane forest growing 

on nearby volcanoes, in a setting analogous to the drier 

islands of Nusa Tenggara (Indonesia) today.

Following their initial dispersal into Southeast Asia, 

presumably as montane taxa, have Podocarpus s.l. species subsequently “descended into the lowlands” (sensu 

de Laubenfels, 1988), or have different Podocarpus

groups independently dispersed into the region from 

other areas? Since the current genera Podocarpus sensu 

stricto, Nageia, and Prumnopitys all have distributions 

that extend not only from Australasia to Malesia but also 

FIGURE 2.4. Paleocene and Eocene localities mentioned in the text.
number 95 • 2 9

FIGURE 2.5. Appearance of Podocarpus pollen in Southeast Asia in relation to the trend of global climate 

change as indicated by oxygen isotope data of Zachos et al. (2001).
3 0 • smithsonian contributions to botany

to South America (Prumnopitys, Nageia, Podocarpus), 

India (Nageia), and Africa (Podocarpus), it is likely that 

at least three or more dispersal events occurred to account 

for the Malesian populations of the Podocarpaceae producing the “Podocarpidites” pollen type. These events 

could have taken place at any time from the late Eocene 

onward, and thus the idea of “descent” is unlikely to apply since with lowland and upland taxa being from different genera, they are more likely attributable to different 

dispersal events. 

Podocarpus during the Late Quaternary

Many Podocarpus species are prominent in montane 

forests, and there is a good record for Podocarpus from 

numerous late Quaternary lake and peat deposits occurring across the region. The general pattern shows that for 

montane sites, lower montane forests expanded in area 

during the Last Glacial Maximum as equatorial temperatures became reduced (Cannon et al., 2009). At the same 

time upper montane forest was less well represented than 

today but expanded to its current distribution during the 

postglacial period (Flenley, 1995). Southern conifers are 

common elements in both lower and upper montane forests, and Podocarpus species are elements of both of these 

habitats. The behavior of podocarps with changing temperatures will be discussed further below in the sections on 

Dacrycarpus and Phyllocladus. 

Dacrydium

Dacrydium pollen is widespread throughout the Australian Tertiary, first appearing in the record in the Santonian stage of the Late Cretaceous (Dettmann, 1994). It is 

also reported from the late Oligocene/early Miocene of Patagonia (South America) by Barreda and Palazzesi (2007). 

Dacrydium pollen is distinctly absent from middle Eocene 

and older sediments of Southeast Asia. It was suggested 

by Morley (1998, 2000) that Dacrydium first appeared in 

the Sunda region in the Miocene following the onset of 

collision of the Australian and Asian plates, based on the 

sudden appearance of Dacrydium pollen in the latest part 

of the Talang Akar Formation (now dated as latest Oligocene) from the West Java Sea (Figure 2.6). This event also 

coincides approximately with a change from a seasonal 

to an ever-wet climate in that area. Recent studies in East 

Java by Lelono (2007) and Lelono and Morley (In press), 

however, suggest that Dacrydium may have a much earlier 

record, with common occurrences of Dacrydium pollen 

from the mid-Oligocene onward and regular occurrences 

also through the early Oligocene. These data suggest that 

Dacrydium had established itself in the Sunda region by 

the beginning of the Oligocene. The very common occurrence of Dacrydium pollen suggests that it was growing in 

lowland habitats. 

The earlier immigration of Dacrydium into the Sunda 

region raises questions as to its mode of dispersal and its 

ecology. During the early Oligocene there still would have 

been a wide ocean of perhaps 1,000 km between Sunda 

and Australia (Hall, 1998), so dispersal via a direct filter route from Australia is unlikely. For dispersal to have 

taken place via a land corridor, it is more likely to have 

arrived via India. Unpublished records from the Indian 

subcontinent by Noon and Brenac (personal communication) indicate that Dacrydium was already present there in 

the early Eocene (although now extinct). Since there are 

records of Dacrydium from the Paleocene and Oligocene 

of the Ninety East Ridge (Kemp and Harris, 1975), it is 

thought that Dacrydium, which is dispersed by birds, first 

dispersed into the Indian subcontinent, probably via island hopping, from Australasia via the Ninety East Ridge, 

prior to immigration into Southeast Asia during, or just 

prior to, the early Oligocene. 

FIGURE 2.6. Appearance of Australian elements in the Tertiary of 

West Java (from Morley, 2000).
number 95 • 3 1

The absence of Dacrydium from the earlier Oligocene 

in the West Java region is probably attributable to climatic 

factors. West Java experienced a seasonally dry climate during the early Oligocene (Morley, 2000), which would not 

have been suitable for Dacrydium, whereas ever-wet climates were more persistent in the East Java region throughout the middle Eocene to Oligocene (Lelono and Morley, 

In press). The dispersal of Dacrydium into the Southeast 

Asian region approximately during the early Oligocene 

also explains the occurrence of scattered Dacrydium pollen in the late Oligocene of Natuna Sea sediments and its 

common occurrence through the late Oligocene of the Cuu 

Long Basin off the shore of Vietnam (R. J. Morley, unpublished data), as well as in the Oligocene of China (Sun et al., 

1981). Following the Oligocene appearance of Dacrydium 

in the Sunda region, it spread quickly to China and reached 

as far north as Japan for a brief period during the midMiocene climatic maximum (Figure 2.7) about 16 mya, 

where it was a member of the Daijima flora (Tanai, 1972) 

and also to Korea (Yamanoi, 1992).

Dacrydium, Casuarinaceae, and Peat Swamps

Occurrences of common Dacrydium pollen from the 

Southeast Asian Cenozoic are almost invariably associated 

with common occurrences of Casuarina-type pollen (Casuarinaceae; Casuarina and Gymnostoma share the same 

pollen type). The two are also frequently associated with 

coals and lithologies rich in organic carbon, with examples 

occurring throughout the Miocene and Pliocene. Today, 

Gymnostoma and Dacrydium often occur in association 

in inland “kerapah”-type peat swamps and in kerangas 

vegetation (Brunig, 1974, 1990). One of the most wellknown peat swamps with vegetation consisting mostly 

of Gymnostoma nobilis and Dacrydium beccarii var subelatum occurs at Lawas, Brunei (see photo in Whitmore, 

1975:171). Termed an “anomalous” peat by Anderson 

(1964), the palynological succession of this peat was studied by in the early 1960s, although he only published a very 

rudimentary discussion of the succession (Muller, 1965). 

He passed the original results to the author in 1981, and 

FIGURE 2.7. Dispersal of gymnosperms into Southeast Asia (from Morley, 2000), showing 1, collision of 

the Australian and Asian plates; 2, immigration of Dacrycarpus into New Guinea (approximate); 3, uplift in 

eastern Indonesia associated with the Sorong Fault.
3 2 • smithsonian contributions to botany

the data are presented here for the first time (Figure 2.8). 

The peat succession formed over a brackish Rhizophora

(Rhizophoraceae) swamp with mangrove muds, which, in 

turn, overlay an interval with common Oncosperma (Arecaceae) pollen. Both Dacrydium- and Casuarina-type pollen are the most common elements of the palynoflora at 

the onset of peat formation, although Dacrydium seems to 

be more common in the middle part of the succession and 

Casuarina type more common in the upper part. 

Dacrydium has been found to be a common element of 

watershed peats in South Kalimantan (Morley, 1981) and 

occurs commonly in kerapah peats in Sarawak (Brunig, 

1974). However, it seems to be missing from basinal peats 

(the domed peats that occur behind mangrove swamps on 

coastal plains). The Lawas peat seems to be the only one 

where Dacrydium/Gymnostoma peat forms over a substrate of mangrove mud.

Many coals from the Southeast Asian Cenozoic yield 

common Dacrydium and Casuarina pollen in association. 

This indicates that kerapah or watershed peats have been 

common elements of the landscape for more than 27 million years and thus represent one of the oldest plant associations from the region. The principal examples noted 

by the author are from (1) the Oligocene of East Java (Lelono and Morley, In press), (2) the late Oligocene Talang 

Akar Formation in West Java (Morley, 2000), and (3) the 

early Miocene of the Malay Basin in Seismic Group I 

(Morley and Shamsudin, 2006); and in laterally equivalent facies, (4) the strata of infilled incised valleys from 

the West Natuna Basin (R. J. Morley, unpublished data), 

(5) the middle Miocene coals from Southeast Kalimantan 

(Demchuk and Moore, 1988), and (6) the middle Miocene “Group E” coals from the Malay Basin (Shamsudin 

and Morley, 2006). 

FIGURE 2.8. Palynological analysis of the Lawas peat swamp in Brunei. Analysis was performed by Jan Muller in 1963, but data are published 

here for the first time.
number 95 • 3 3

There is no real record of Dacrydium pollen that 

could be considered to be derived from montane environments during the Tertiary, although Dacrydium pollen has 

been found in many Quaternary montane sites. Whether 

Dacrydium descended into the lowlands or ascended into 

the mountains cannot be determined from the fossil record, although on the basis of the early arrival of clearly 

lowland Dacrydium in eastern Java, it is thought that ascent is more likely, but this theory needs to be tested by 

molecular studies.

Dacrycarpus

Dacrycarpus has a long history in Australia and New 

Zealand, first occurring in the late Paleocene (Martin, 

1994), and in Patagonia (South America), first occurring in 

the early Eocene (Wilf, 2007). It dispersed to New Guinea 

(Figure 2.7) during the late Miocene (Khan, 1976), presumably as montane environments became established with uplift of the New Guinea mountains, well after the collision 

of the Australian and Asian plates. It then dispersed to the 

Philippines (van der Kaars, 1991) and on to Borneo during the mid-Pliocene, indicated by its appearance in marine 

sediments from the offshore Brunei region from that time 

and onward, initially reported by Muller (1966). 

Dispersal probably occurred through a combination 

of global temperature decline and the creation of dispersal 

routes through uplift in the Philippine region. The appearance in northwest Borneo was within Nannofossil Zone 

NN15 between 3.4 and 4.04 mya. Dispersal was probably 

by birds, and the dispersal route was through an island 

chain.

In Central Java, Dacrycarpus pollen was already present in Nannofossil Zone NN15, contemporaneous with 

its appearance in northwest Borneo; Dacrycarpus pollen 

is well represented in the late Pliocene to basal Pleistocene 

Java Man locality near Modjokerto, dated to approximately 1.8 mya (R. J. Morley, unpublished data; Huffman, 

2001). An area offshore from northwest Sarawak yields 

Dacrycarpus pollen from the basal Pleistocene to the present day. Sediments in this area are sourced from rivers that 

flowed from Sumatra across the Sunda Shelf, suggesting 

that dispersal to Sumatra did not take place until the early 

Pleistocene (Figure 2.9). In 2005 a petroleum exploration 

well drilled in the center of the Malay Basin yielded the 

first record of regular Dacrycarpus pollen in that area in 

basal Pleistocene sediments (palynological analyses on 

previous wells from this area were undertaken only on 

the early Pliocene and older succession). Dacrycarpus pollen also ranges into the earlier Pleistocene in Myanmar 

(Morley, 2000). It is likely that Dacrycarpus is still extending its range into Indochina.

In Southeast Asian montane regions, Dacrycarpus is 

very common in upper montane forest, which according 

to Flenley (1995), only forms during interglacial periods 

from taxa recruited from lower montane forest. During 

glacial periods, upper montane taxa retreat and find refuge in lower montane forest. Deep-sea cores from the 

Makassar Straits (Figure 2.10) indicate that in the last 

30,000 years Dacrycarpus pollen is more common during 

the Holocene than during the last glacial. This occurrence 

is consistent with the Holocene expansion of upper montane forest in which Dacrycarpus was likely to have been 

a prominent member. However, Lithocarpus (Fagaceae) 

is considerably more common during the Last Glacial 

Maximum, consistent with the much greater expansion 

of lower montane forest during this time at the expense 

of lowland dipterocarp forest (Cannon et al., 2009). The 

Podocarpaceae do not appear to show increased representation in lowland forests during the Last Glacial 

FIGURE 2.9. Dispersal of Dacrycarpus imbricatus across the 

Sunda region during the Pliocene and Pleistocene, based on pollen 

records. Dates are in millions of years. The positions of the ProtoMusi, Hari, Kampar, and Pahang rivers at the time of the Last 

Glacial Maximum (and older sea level low stands) are shown following Voris (2000). These rivers carried pollen that was deposited in the Malay Basin (+) and in deltas offshore from northwest 

Sarawak (*), dating dispersal from Borneo/Java to the mountains 

of Sumatra and the Malay Peninsula (#).
3 4 • smithsonian contributions to botany

Maximum, as has been demonstrated for the Amazon 

(Colinvaux et al., 1996).

Phyllocladus

Phyllocladus pollen has a long history in Australia, with the oldest records of bisaccate pollen from the 

Paleocene (Martin, 1994). However, Phyllocladus pollen 

first appeared in northwestern Borneo just at the beginning of the Pleistocene about 1.9 mya, with the parent 

plant presumably dispersing via New Guinea. It has no 

fossil record in the Sunda region outside the northwestern Borneo area, so it currently shows its maximum extension into the area. In late Quaternary sections, such 

FIGURE 2.10. Summary palynological diagram showing occurrence of Podocarpaceae pollen from 

the Papalang-10 core, drilled in 2341 m of water at the base of the Mahakam Fan, Makassar Strait 

(Morley et al., 2004). The rare elements are Alnus (one specimen) and Pinus, probably carried by 

currents from the South China Sea.
number 95 • 3 5

as in the Makassar Straits between Borneo and Sulawesi, 

it also shows increased abundance during the Holocene 

compared to the Last Glacial Maximum (Figure 2.10), 

which may also reflect the expansion of upper montane 

forest with climatic amelioration following the Last Glacial Maximum.

Microcachrys

Microcachrys-type pollen is found throughout the 

Tertiary of Australia (Martin, 1994) and has also been 

reported from the late Oligocene to early Miocene of Patagonia (South America) by Barreda and Palazzesi (2007). 

Kahn (1976) observed pollen of Microcachrys type in the 

New Guinea Pliocene. This distribution was used by Kershaw and McGlone (1995) to suggest that Microcachrys

retracted its range during the Cenozoic. However, the 

Microcachrys specimens figured by Khan are dark colored 

and preserved poorly compared to the remainder of the 

assemblages and are most likely reworked elements from 

older sediments. Microcachrydites antarcticus is a regular 

component of palynomorph assemblages from the Bajocian (Middle Jurassic) to Early Cretaceous of Irian Jaya 

(Indonesia), and it is likely that the Pliocene specimens 

were reworked from Mesozoic sediments. Microcachrys

was, however, reported from the Paleocene (ODP 214) 

and Oligocene (ODP 254) cores of the Ninety East Ridge 

by Kemp and Harris (1975).

Africa

In West Africa, conifer pollen is absent from the Cretaceous–Tertiary boundary until the mid-Pliocene, when 

Podocarpus pollen suddenly appeared about 2.7 mya in 

the Niger Delta region (Knaap, 1972) and formed a useful 

stratigraphic marker. Podocarpus was likely to have been 

present in upland areas in East Africa through much of the 

Tertiary but dispersed to West Africa as global climates 

cooled during the late Pliocene. Maley et al. (1990) suggested that Podocarpus in West Africa dispersed from the 

East African highlands via upland areas in Angola (Figure 

2.11). Poumot (1987) shows gymnosperm pollen occurring commonly throughout the late Miocene and Pliocene 

of the Niger Delta, but this was subsequently shown to be 

in error (Morley, 2000). 

The time of dispersal into Africa is unknown, but 

Podocarpus pollen was present during the Early Cretaceous (see above), and it may have been present in upland 

areas away from the low latitudes throughout the whole 

of the Cenozoic. The timing of dispersal of podocarps into 

Africa could be investigated using a molecular approach 

of the modern remaining taxa. 

Summary of Old World Podocarp

dispersals and extinctions

Podocarpus Sensu Lato

Originating in Gondwana by the earliest Cretaceous, 

Podocarpus was present in India and Africa during the 

Early Cretaceous but became extinct in West Africa following the mid-Cretaceous denudation of uplands (which 

may not have occurred in East or South Africa) and became reduced in extent in India following its Late Cretaceous northward drift (Morley, 2000: fig. 8.1). It extended 

its range to the Ninety East Ridge by the Paleocene and 

FIGURE 2.11. Dispersal path of Podocarpus into West Africa 

according to Maley et al. (1990). West African regional mountain systems as follows: (I) West African; (II) Cameroun-Jos; 

(III) Ethiopian; (IV) Imatonga-Kenya-Usambara; (V) RuwenzoriKivu; (VI) Uluguru-Mlange; (VII Chimanimani; (VIII) Drakensberg; (IX) Angolan.
3 6 • smithsonian contributions to botany

was present at the same time in Patagonia. Subsequently, 

Podocarpus dispersed presumably from India to the Sunda 

region during the late Eocene (and possibly at later times 

from Australia by long-distance dispersal) following 

global cooling, from which it radiated to its present distribution across the Southeast Asian region. It subsequently 

expanded to East Asia and may also have extended around 

the Pacific rim to Alaska at the time of the Miocene climatic optimum. In Africa, it dispersed from East Africa to 

the West African highlands following further global cooling 2.7 mya, during the time of expansion of the Northern 

Hemisphere ice sheets (Figure 2.12).

Dacrydium

Dacrydium originated in Australasia (Figure 2.13) 

during the Late Cretaceous (Santonian, 86 mya) and 

dispersed to the Ninety East Ridge by the Paleocene 

(55 mya). It then appeared in India 50 mya during the 

early Eocene and in East Java at the basal Oligocene (33 

mya). It attained a widespread distribution in Southeast 

Asia and reached China and Vietnam by the late Oligocene (25 mya) and Japan during the Miocene thermal 

maximum (16 mya). There are also records from the midTertiary of Patagonia.

Dacrycarpus

Dacrycarpus originated in Australasia during the 

Maastrichtian (Late Cretaceous, 75 mya) and was present in Patagonia during the early Eocene. It dispersed to 

New Guinea during the late Miocene. It established itself 

in Borneo and Java during the early Pliocene but subsequently dispersed to Sumatra, the Malay Peninsula, and 

Myanmar during the early Pleistocene. 

Phyllocladus

Phyllocladus producing the typical bisaccate pollen 

with diminutive sacci first appeared at the same time in 

Australia and Patagonia during the Paleocene (Martin, 

1994; Wilf et al., 2003). It dispersed to New Guinea in the 

late Miocene and to Borneo during the earliest Pleistocene.

Microcachrys

Microcachrys was widespread across Australasia and 

the Indian subcontinent during the Jurassic and Early Cretaceous but disappeared from lower-latitude areas, including India and the New Guinea region, after the Albian (96 

mya). Its latest “low-latitude” location was on the Ninety 

East Ridge during the Paleocene and Oligocene (Kemp 

and Harris, 1975). 

Conclusions

The family Podocarpaceae first appeared in the Triassic of Gondwana and apparently spread to the Northern Hemisphere during the Jurassic. However, from the 

Early Cretaceous onward the family has had an essentially Gondwanan, or Gondwana-derived, distribution. 

Low-latitude Cretaceous wood fossils, always tentatively 

attributed to the Podocarpaceae, are thought unlikely to 

be podocarps since they are not accompanied by bi- or 

trisaccate pollen, which is ubiquitous in extant podocarps 

with the exception of the isolated genus Saxegothaea. The 

main podocarp genera diversified in Gondwana during the 

Cretaceous and earliest Tertiary, coinciding with the opening of the Southern Ocean, and by the Paleocene all the 

taxa that can be differentiated using pollen were in place. 

The Podocarpaceae is, with minor exceptions, essentially 

adapted to areas of wet, equable, mesothermal to microthermal climate, and this has been the case throughout its 

history. The availability of areas of wet climate and equable mesothermal temperatures has probably impacted on 

its pattern of dispersal or extinction during the Cenozoic. 

At the beginning of the Tertiary, the Podocarpaceae 

was an important element of the vegetation of Australasia, 

Antarctica, and southernmost South America, disappearing from Antarctica following mid-Tertiary glaciations.

Podocarpus s.l. may have been present at low latitudes 

in elevated areas of Africa during the Early Cretaceous 

and, together with Microcachrys, was an important member of the Indian and New Guinea floras (both of which 

lay south of the tropical zone at that time). Podocarps 

became of limited distribution on the Indian Plate during 

the Late Cretaceous following competition from African 

immigrant angiosperms (Morley, 2000) and possibly the 

presence of unfavorable climates as the Indian Plate drifted 

across the Southern Hemisphere high-pressure zone. Aridity and marine transgression were probably responsible 

for its disappearance from the New Guinea region. 

In Southeast Asia, Podocarpus s.l. first appeared in 

the late Eocene in Java, presumably as a result of dispersal from India but also possibly long-distance dispersal 

from Australia. This was closely followed during the early 

Oligocene by Dacrydium, which probably dispersed into 

Southeast Asia by island hopping along the Ninety East 

Ridge and via India (where it subsequently became extinct). 
number 95 • 3 7

FIGURE 2.12. Dispersal of temperate taxa into low latitudes associated with Quaternary global cooling (from Morley, 2000).
3 8 • smithsonian contributions to botany

The first members of Dacrydium to reach the Sunda region 

were probably trees of lowland forests and dispersed via 

nutrient-poor heath forests (kerangas) and peat swamps. 

Subsequently, some Dacrydium species may have found 

niches in montane forests. Podocarpus s.l. was probably a 

tree of montane forests at the time of initial dispersal, but 

its widespread occurrence in low-altitude nutrient-poor 

habitats probably reflects multiple long-distance dispersal 

events rather than descent from montane species. 

Dacrycarpus dispersed from Australia to the mountains of New Guinea as the island formed during the late 

Miocene. It spread by island hopping into Borneo and 

Java during the mid-Pliocene and then to the Sumatra and 

the Malay Peninsula at the beginning of the Pleistocene. It 

is probably still in the process of range expansion. Phyllocladus followed the same route as Dacrycarpus to New 

Guinea during the late Miocene and island hopped to Borneo at the beginning of the Pleistocene.

It is likely that Podocarpus s.l. was present in upland 

areas of the African continent during the mid-Tertiary, enabling dispersal into West Africa by island hopping between areas of montane forest during the mid-Pliocene, 

coinciding with the time of global climate cooling and the 

expansion the Northern Hemisphere ice caps.

Although not part of this review, it is intriguing that 

only Podocarpus s.l. dispersed to the neotropics, despite 

the full diversity of podocarp genera being present in 

Patagonia during the early Tertiary and the presence of an 

appropriate dispersal path in the form of the Andes. It is 

suggested that unfavorable climates within the Southern 

Hemisphere high-pressure zone may have inhibited such 

dispersals. 

Acknowledgments

I am grateful to Han Van Konijnenberg-van Cittert 

(Nationaal Natuurhistorisch Museum, Naturalis, Leiden), 

for current views on Northern Hemisphere macrofossils 

previously referred to Podocarpaceae, for improving the 

manuscript, and also for helping with Mesozoic literature. 

I am also grateful to Steve Noon and Patrice Brenac of 

CoreLab Indonesia for freely providing me with records 

of Podocarpaceae pollen from their large microfossil database from India. Vandana Prasad of the Birbal Sahni 

Institute in Lucknow, India, kindly provided information 

on Indian Paleocene pollen referred to the morphogenus 

Podocarpidites. I am also grateful to Ben Turner for inviting me to contribute to this volume.

REFERENCES

Adie, H., and M. J. Lawes. 2011 (this volume). Podocarps in Africa: 

Temperate Zone Relicts or Rainforest Survivors? In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 79–100. Smithsonian Contributions to Botany, No. 

95. Smithsonian Institution Scholarly Press, Washington, D.C.

Anderson, J. A. R. 1964. The Structure and Development of the Peat 

Swamps of Sarawak and Brunei. J. Trop. Geogr. 18: 7–16.

Anderson, J. M., H. M Anderson, and C. J. Cleal. 2007. Brief History of 

the Gymnosperms: Classification, Biodiversity, Biogeography and 

Ecology. Strelitzia 20: 1–279.

Archangelsky, S. 1966. New Gymnosperms from the Tico Flora, Santa 

Cruz Province, Argentina. Bull. Brit. Mus. (Nat. Hist.) Geol. 13: 

259–295.

Archangelsky, S., and G. Del Fueyo. 1989. Squamastrobus Gen. N., a 

Fertile Podocarp from the Early Cretaceous of Patagonia, Argentina. Rev. Palaeobot. Palynol. 59: 109–126.

Axsmith, B. J., T. N. Taylor, and E. N. Taylor. 1998. Anatomically Preserved Leaves of Notophyllum krauselii (Podocarpaceae) from the 

Triassic of Antarctica. Amer. J. Bot. 85: 704–713.

Baksi, S. K., and U. Deb. 1981. Palynology of the Upper Cretaceous of 

the Bengal Basin, India. Rev. Palaeobot. Palynol. 31: 335–365.

Baldoni, A. M., and T. N. Taylor. 1982. The Ultrastructure of Trisaccites 

Pollen from the Cretaceous of Southern Argentina. Rev. Palaeobot. 

Palynol. 38: 23–33.

Balme, B. E. 1995. Fossil In Situ Spores and Pollen Grains: An Annotated 

Catalogue. Rev. Palaeobot. Palynol. 87: 81–323.

Barreda, V., and L. Palazzesi. 2007. Patagonian Vegetation Turnovers 

during the Paleogene–Early Neogene: Origin of Arid-Adapted 

Floras. Bot. Rev. 73: 31–50.

Biffin, E., J. Conran, and A. Lowe. 2011 (this volume). Podocarp Evolution: A Molecular Phylogenetic Perspective. In Ecology of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, 

FIGURE 2.13. Dispersal of Dacrydium into Southeast and East Asia.
number 95 • 3 9

eds., pp. 1–20. Smithsonian Contributions to Botany, No. 95. 

Smithsonian Institution Scholarly Press, Washington, D.C.

Brunig, E. F. 1974. Ecological Studies in Kerangas Forests of Sarawak 

and Brunei. Borneo Literature Bureau for Sarawak Forest Department, Kuching, Malaysia.

Brunig, E. F. 1990. Oligotrophic Forested Wetlands in Borneo. In Ecosystems of the World. Volume 15, Forested Wetlands, ed. A. E. Lugo et 

al., pp. 299–344. Elsevier, Amsterdam.

Cannon, C. H., R. J. Morley, and A. B. G. Bush. 2009. The Current 

Refugial Rainforests of Sundaland Are Unrepresentative of Their 

Biogeographic Past and Highly Vulnerable to Disturbance. Proc. 

Natl. Acad. Sci. U.S.A. 106: 11,188–11,193.

Colinvaux, P. A., P. E. De Oliviera, J. E. Moreno, M. C. Miller, and 

M. B. Bush. 1996. A Long Pollen Record from Amazonia: Forest 

and Cooling in Glacial Times. Science 274: 85–88.

Cookson, I. C. 1947. Plant Microfossils from the Lignites of Kerguelen 

Archipelago. Rep. Brit. Austral. New Zealand Antarc. Exped. A2: 

127–142.

Cookson, I. C. 1953. Identification of the Sporomorph Phyllocladites

with Dacrydium and Its Distribution in Southern Tertiary Deposits. 

Austral. J. Bot. 1: 64–70.

Cookson, I. C., and K. M. Pike. 1953a. The Tertiary Occurrence and 

Distribution of Podocarpus (Sect Dacrycarpus) in Australia and 

Tasmania. Austral. J. Bot. 1: 71–82.

Cookson, I. C., and K. M. Pike. 1953b. A Contribution to the Tertiary 

Occurrence of the Genus Dacrydium in the Australian Region. Austral. J. Bot. 1: 474–484. 

Cookson, I. C., and K. M. Pike. 1954. The Fossil Occurrence of Phyllocladus and Two Other Podocarpaceous Types in Australia. Austral. 

J. Bot. 2: 60–68.

de Jersey, N. J. 1971. Early Jurassic Miospores from the Helidon Sandstone. Palaeontological Papers, No. 25. Geological Survey of 

Queensland, Brisbane, Australia.

de Laubenfels, D. J. 1988. Coniferales. Fl. Malesiana, Ser. 1, Spermatoph. 

10: 337–453.

Demchuk, T., and T. A. Moore. 1993. Palynofloral and Organic Characteristics of a Miocene Bog-Forest, Kalimantan, Indonesia. Org. 

Geochem. 20: 119–134.

Dettmann, M. E. 1994. Cretaceous Vegetation: The Microfossil Record. 

In History of Australian Vegetation, Cretaceous to Recent, R. S. Hill, 

ed., pp. 143–170. Cambridge University Press, Cambridge, UK.

Douglas, J. G. 1994. Cretaceous Vegetation, the Macrofossil Record. In 

History of Australian Vegetation, Cretaceous to Recent, R. S. Hill, 

ed., pp. 171–188. Cambridge University Press, Cambridge, UK.

Doyle, J. A., P. Biens, A. Doerenkamp, and S. Jardine. 1977. Angiosperm 

Pollen from the Pre-Albian Cretaceous of Equatorial Africa. Bull. 

Centr. Rech. Explor. Prod. Elf Aquitaine 1: 451–473.

Dupéron-Laudoueneix, M. 1991. Importance of Fossil Woods (Conifers 

and Angiosperms) Discovered in Continental Mesozoic Sediments 

of Northern Equatorial Africa. J. African Earth Sci. 12: 391–396.

Dupéron-Laudoueneix, M., and J. Dupéron. 1995. Inventory of Mesozoic and Cenozoic Woods from Equatorial and North Equatorial 

Africa. Rev. Palaeobot. Palynol. 84: 439–480

Enright, N. J., and T. Jaffré. 2011 (this volume). Ecology and Distribution of the Malesian Podocarps. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 57–77. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Erdtman, G. 1965. Pollen and Spore Morphology/Plant Taxonomy. Volume 2. Gymnospermae, Pteridophyta, Bryophyta, Illustrations. 

Hafner Publishing Company, New York.

Farjon, A. 1998. World Checklist and Bibliography of Conifers. Royal 

Botanical Gardens, Kew, Richmond, Surrey, UK.

Flenley, J. R. 1995. Problems of the Quaternary on Mountains of the 

Sunda–Sahel Region. Quatern. Sci. Rev. 15: 549–556.

Gaussen, H. 1973. Les gymnospermes actuelles et fossiles. Trav. Lab. 

Forest. Toulouse 2: 1–43.

Gnaedinger, S. 2007. Podocarpaceae Woods (Coniferales) from Middle 

Jurassic Formation, Santa Cruz Province, Argentina. Rev. Palaeobot. Palynol. 147: 77–93.

Hall, R. 1998. The Plate Tectonics of Cenozoic SE Asia and the Distribution of Land and Sea. In Biogeography and Geological Evolution 

of SE Asia, R. Hall and J. D. Holloway, eds., pp. 98–131. Backhuys 

Publishers, Leiden, Netherlands.

Harris, T. M. 1979. The Yorkshire Jurassic Flora. Volume 5. Coniferales. 

British Museum (Natural History), London.

Hill, R. S. 1994. History of Australian Vegetation, Cretaceous to Recent. 

Cambridge University Press, Cambridge, UK.

Huffman, O. F. 2001. Geological Context and Age of the Perning/

Mojokerto Homo erectus, East Java. J. Human Evol. 40: 353–362

Huffman, O. F., and Y. Zaim. 2003. Mojokerto Delta, East Jawa, Palaeoenvironment of Homo modjokertensis—First Results. J. Min. 

Technol. 10: 1–32.

Iglesias, A., P. Wilf, K. R. Johnson, A. B. Zamuner, N. R. Cúneo Museo, 

S. D. Matheos, and B. S. Singer. 2007. A Paleocene Lowland 

Macroflora from Patagonia Reveals Significantly Greater Richness 

Than North American Analogs. Geology 35: 947–950.

Jardine, S., and L. Magloire. 1965. Palynologie et stratigraphie du cretace des bassins du Senegal et de Cote d’Ivoire. Mem. Bur. Rech. 

Geol. Min. 32: 187–245.

Kar, R. K. 1985. The Fossil Floras of Kachchh—IV, Tertiary Palynostratigraphy. Palaeobotanist 34: 1–279.

Kemp, E. M., and W. K. Harris. 1975. The Vegetation of Tertiary Islands 

on the NinetyEast Ridge. Nature 258: 303–307.

Kershaw, A. P., and M. S. McGlone. 1995. The Quaternary History of 

the Southern Conifers. In Ecology of the Southern Conifers, N. J. 

Enright and R. S. Hill, eds., pp. 31–63. Melbourne University Press, 

Carlton, Australia.

Khan, A. H. 1976. Palynology of Tertiary Sediments from Papua New 

Guinea. II. Gymnosperm Pollen from Upper Tertiary Sediments. 

Austral. J. Bot. 24: 783–791.

Kimura, T., T. Ohana, and K. Mimoto. 1988. Discovery of a Podocarpaceous 

Plant from Lower Cretaceous of Kochi Prefecture, in the Outer Zone 

of Southwest Japan. Proc. Japan Acad., Ser. B 64: 213–216. 

Knaap, W. A. 1972. A Montane Pollen Species from the Upper Tertiary 

of the Niger Delta. J. Min. Geol. Metall. Soc. Nigeria 6: 23–29.

Krassilov, V. A. 1974. Podocarpus from the Upper Cretaceous of Eastern 

Asia and Its Bearing on the Theory of Conifer Evolution. Palaeontology 19: 365–370.

Lelono, E. B. 2000. Palynology of the Nanggulan Formation, Central 

Java, Indonesia. Ph.D. thesis, Department of Earth Sciences, Royal 

Holloway, University of London, London. 

Lelono, E. B. 2007. Gondwanan Palynomorphs from the Paleogene Sediment of East Java? The Evidence of Earlier Arrival. Lemigas Scientific Contributions to Petroleum Science and Technology 30(2): 

1–12. [In Indonesian.]

Lelono, E. B., and R. J. Morley. In press. Oligocene Palynological Succession from the South China Sea. In The SE Asian Gateway: 

History and Tectonics of Australia-Asia Collision, R. Hall, M. A. 

Cottam, and M. E. J. Wilson, eds. Geological Society of London 

Special Publication.

Maley, J., G. Cabale, and P. Sita. 1990. Etude d’un peuplement residuelle a basse altitude de Podocarpus latifolius sur le flank Congolaise du Massif du Chaillu. Implications palaeoclimatiques et biogeographiques. Etude de la pluie pollinique actuelle. In Paysages 

Quaternaire de l’Afrique Central Atlantique, R. La Franchini, and 

D. Shwartz, eds., pp. 336–352. ORSTROM, Paris. 

Martin, H. A. 1994. Tertiary Phytogeography: Palynological Evidence. 

In History of Australian Vegetation, Cretaceous to Recent, ed. R. S. 

Hill, pp. 104–142. Cambridge University Press, Cambridge, UK.
4 0 • smithsonian contributions to botany

Mill, R. R., and M. Stark-Schilling. 2009. Cuticle morphology of Saxegothaea. Bot. J. Linn. Soc. 159: 58–67.

Morley, R. J. 1981. Development and Vegetation Dynamics of a Lowland Ombrogenous Swamp in Kalimantan Tengah, Indonesia. 

J. Biogeogr. 8: 383–404.

Morley, R. J. 1998. Palynological Evidence for Tertiary Plant Dispersals 

in the SE Asia Region in Relation to Plate Tectonics and Climate. 

In Biogeography and Geological Evolution of SE Asia, R. Hall 

and J. Holloway, eds., pp. 177–200. Bakhuys Publishers, Leiden, 

Netherlands.

Morley, R. J. 2000. Origin and Evolution of Tropical Rain Forests. John 

Wiley and Sons, London.

Morley, R. J., H. P. Morley, A. A. H. Wonders, Sukarno, and S. van 

der Kaars. 2004. Biostratigraphy of Modern (Holocene and Late 

Pleistocene) Sediment Cores from Makassar Straits. In Proceedings 

of the Deepwater and Frontier Exploration in Asia and Australasia Symposium, pp. 201–212. Indonesian Petroleum Association, 

Jakarta.

Morley, R. J., and J. Shamsudin. 2006. The Sequence Biostratigraphy 

and Chronostratigraphy of the Malay Basin. In Proceedings of the 

Petroleum Geology Conference and Exhibition 2006, p. 77–78. 

Geological Society of Malaysia, Kuala Lumpur.

Muller, J. 1965. Palynological Study of Holocene Peat in Sarawak. In 

Symposium on Ecological Research in Humid Tropics Vegetation. 

pp. 147–156. UNESCO, Kuching, Sarawak.

Muller, J. 1966. Montane Pollen from the Tertiary of N.W. Borneo. 

Blumea 14: 231–235.

Muller, J. 1968. Palynology of the Pedawan and Plateau Sandstone Formations (Cretaceous–Eocene) in Sarawak. Micropaleontology 14: 

1–37. 

Oecipa, M. A. 1998. Current State-of-the-Art in Studies on Jurassic Flora 

from Antarctica. Tomy Jurajskie 2: 151–156. (In Polish with English abstract.)

Philippe, M., and M. K. Bamford. 2008. A Key to Morphogenera Used 

for Mesozoic Conifer-Like Woods. Rev. Palaeobot. Palynol. 148: 

184–207.

Philippe, M., G. Cuny, M. Bamford, E. Jaillard, G. Barale, B. Gomez, 

M. Ouaja, F. Thevernard, M. Theibaut, and P. Von Sengbusch. 2003. 

The Palaeoxylological Record of Metapodocarpoxylon libanoticum

(Edwards) Dupéron-Laudoueneix et Pons and the Gondwana Late 

Jurassic–Early Cretaceous Continental Biogeography. J. Biogeogr.

30: 389–400.

Pocknall, D. T. 1981. Pollen Morphology of New Zealand Species of 

Dacrydium Solander, Podocarpus L’Heritier and Dacrycarpus

Endlicher (Podocarpaceae). New Zealand J. Bot. 19: 67–95.

Poole, I., and D. J. Cantrill. 2006. Cretaceous and Cenozoic Vegetation 

of Antarctica, Integrating the Fossil Wood Record. Geol. Soc. London Special Publ. 258: 63–81.

Poumot, C. 1987. Palynological Evidence for Eustatic Events in the 

Tropical Neogene. Bull. Centr. Rech. Explor. Prod. Elf Aquitaine

13: 347–353. 

Prasad, V., A. Farooqui, S. K. M. Tripathi, R. Garg, and B. Thakier. 2009. 

Evidence of Late Palaeocene–Early Eocene Equatorial Rain Forest 

Refugia in Southern Western Ghats, India. J. Biosci. 34: 777–797.

Racey, A., and J. Goodall. 2009. Palynology and Stratigraphy of the Mesozoic Khorat Group Red Bed Sequences from Thailand. Geol. Soc. 

London Special Publ. 315: 69–83.

Racey, A., J. G. S. Goodall, M. A. Love, S. Polachan, and P. D. Jones. 

1994. New Age Data for the Mesozoic Khorat Group of Northeast Thailand. In Proceedings of the International Symposium on 

Stratigraphic Correlation of Southeast Asia, Bangkok, Thailand, 

pp. 245–252. Department of Mineral Resources, Bangkok.

Rao, A. R. 1943. Nipaniostrobus, a New Genus of Dacrydium-Like

Seed-Bearing Cones and Other Silicified Plants from the Rajmahal 

Series. Proc. Natl. Acad. Sci. India 13: 113–132.

Rao, A. R. 1947. Nipanioruha granthia gen. et sp. nov., a New Petrified 

Coniferous Shoot from the Rajmahal Hills, Bihar. J. Indian Bot. 

Soc. M. O. P. Iyengar Commemorative Volume: 389–397.

Rao, A. R. 1949. The Megastrobilus of Nipanioruha granthia Rao, A.R. 

Curr. Sci. 18: 447–448.

Regali, M. S., N. Uesugui, and A. S. Santos. 1975. Palinologia dos sedimentos meso-cenozoicos do Brazil. Bol. Tecn. Petrobras 17: 177–

191.

Reinink-Smith, L. M., and E. B. Leopold. 2005. Warm Climate in the 

Late Miocene of the South Coast of Alaska and the Occurrence of 

Podocarpaceae Pollen. Palynology, 29: 205–262.

Reymanowna, M. 1987. A Jurassic Podocarp from Poland. Rev. Palaeobot. Palynol. 51: 133–143.

Richards, P. W. 1996. The Tropical Rain Forest, 2nd ed. Cambridge University Press, Cambridge, UK.

Saxena, R. K. 1991. Stratigraphy of the Area around Matanomadh in 

Northwestern Kachchh with Special Reference to the Matanomadh 

Formation. Palaeobotanist 27: 300–313.

Shamsudin, J., and R. J. Morley. 2006. Integration of Biostratigraphy 

with Seismic for Sequence Stratigraphic Interpretation in the Malay 

Basin. In Proceedings of the Petroleum Geology Conference and 

Exhibition 2006, pp. 101–102. Geological Society of Malaysia, 

Kuala Lumpur.

Srivastava, R., and J. S. Gularia. 2006. A Catalogue of Cenozoic (Tertiary) Plant Megafossils from India (1989–2005). Birbal Sahni Institute of Palaeobotany, Lucknow, India.

Stover, L. E., and A. D. Partridge. 1973. Tertiary and Late Cretaceous 

Spores and Pollen from the Gippsland Basin, Australia. Proc. Roy. 

Soc. Victoria 85: 237–286.

Sun, X. I., M. X. Li, Y. Y. Zhang, Z. Q. Lei, Z. C. Kong, P. Li, Q. Ou, and 

Q. N. Lui. 1981. Palynology Section. In Tertiary of the Northern 

Continental Shelf of the South China Sea. Guandong Technology 

Press, Nanjing China.

Suthar, O. P., and B. D. Sharma. 1987. Petrified Fructifications of Conifers from the Jurassic of Rajmahal Hills, India. Geophytology 16: 

159–165.

Tanai, T. 1972. Tertiary History of Vegetation in Japan. In Floristics and 

Paleofloristics of Asia and Eastern North America, A. Graham, ed., 

pp. 235–255. Elsevier Scientific, Amsterdam.

Tomskaya, A. I. 1981. Palinologia Kainozoya Yakutii [Palynology of 

Yakutia’s Coenozoic]. Novosibirsk: [Publisher name unknown]. [In 

Russian.]

Townrow, J. A. 1967. On Rissikia and Mateia Podocarpaceous Conifers 

from the Lower Mesozoic of Southern Lands. Pap. Proc. Roy. Soc. 

Tasmania 101: 103–136.

Trivedi, B. S., and R. Srivastava. 1989. Gymnospermous Woods from 

Early Tertiary of Chhindwara District of Madhya Pradesh. Phytomorphology 39: 659–659.

van der Kaars, W. A. 1991. Palynological Aspects of Site 767 in the Celebes Sea. In Proceedings of the Ocean Drilling Program, Scientific 

Results, Volume 124, ed. E. A. Silver et al., pp. 369–374. Ocean 

Drilling Program, College Station, Tex.

Van Konijnenberg-van Cittert, J. H. A. 1971. In Situ Gymnosperm Pollen 

from the Middle Jurassic of Yorkshire. Acta Bot. Neerl. 20: 1–96

Vishnu-Mittre. 1959. Studies on the Fossil Flora of Nipania (Rajmahal 

Series), Bihar. Coniferales. Palaeobotanist 6: 82–112.

Voris, H. K. 2000. Maps of Pleistocene Sea Levels in Southeast Asia: 

Shorelines, River Systems and Time Durations. J. Biogeogr. 27: 

1153–1167.

Wilf, P. 2007. Biogeographic Significance of the Laguna Del Hunco 

Flora, Early Eocene of Patagonia, Argentina. Geol. Soc. Amer. Abstr. Programs, 39(6): 585.

Wilf, P., N. Ruben Cueno, K. R. Johnson, J. F. Hicks, S. L. Sing, and J. D. 

Obradovich. 2003. High Plant Diversity in Eocene South America: 

Evidence from Patagonia. Science 300: 122–125. 
number 95 • 4 1

Whitmore, T. C. 1975. Tropical Rain Forests of the Far East. Clarendon 

Press, Oxford, UK. 

Woltz, P. 1985. Place des gymnospermes endemiques des Andes Meridionales dans la vegetation du Chili. Lazaroa 8: 293–314.

Yamanoi, T. 1992. The Palynoflora of Early Middle Miocene Sediments 

in the Pohang and Yangnam Basins, Korea. In Centenary of Japanese Micropaleontology, ed. K. Ishizaki and T. Saito, pp. 473–480. 

Tokyo: Terra Scientific Publishing Company.

Zachos, J. C., M. Pagani, L. Sloan, E. Thomas, and K. Billups. 2001. 

Tends, Rhythms and Aberrations in Global Climate, 65 Ma to Present. Science 292: 686–693. 

Zhou, Z. 1983. Stalagma samara, a New Podocarpaceous Conifer with 

Monocolpate Pollen from the Upper Triassic of Hunan, China. Palaeontographica 185: 56–78.

3 Ecology and Distribution of 

Neotropical Podocarpaceae

James W. Dalling, Phoebe Barkan, Peter 

J. Bellingham, John R. Healey, and 

Edmund V. J. Tanner

ABSTRACT. Podocarps are a frequent, but rarely a dominant, component of neotropical wet forests extending from South America into central Mexico and the Greater Antilles. Although podocarps are often considered to be predominantly montane taxa, several 

species occur in lowland forest and are locally abundant on some Pacific and Atlantic 

coastal islands in Central America. Here we review literature on the origins and distribution of neotropical podocarps and highlight their apparent association with resourcepoor environments. As a consequence of forest conversion and logging, many podocarps 

that were already habitat specialists are now further restricted to small and increasingly 

fragmented populations. Unfortunately, there is little information on the regeneration 

ecology of podocarps with which to assess the recruitment potential of these populations. 

An exception is the long-term studies of the dynamics of Podocarpus urbanii, a common 

species in montane forest in Jamaica. Podocarpus urbanii is moderately shade tolerant 

and successfully regenerates beneath undisturbed forest. The low juvenile mortality rate 

of P. urbanii, coupled with relatively high diameter growth, suggests that this species 

and possibly other podocarps may have greater utility for reforestation than is currently 

recognized.

DIVERSITY OF NEOTROPICAL PODOCARPACEAE

Central and South America harbor a large fraction of global podocarp diversity and are represented by five genera: Podocarpus (31 species), Prumnopitys (5 

species), Retrophyllum (2 species), Saxegothaea (1 species), and Lepidothamnus

(1 species). Most of these podocarps (excluding the last two genera) have a 

tropical distribution; the 29 neotropical Podocarpus species account for nearly 

a third of the species currently recognized in the genus (Farjon, 2001). Malesian podocarps show a diversity of forms, including parasitic, lianescent, and 

aquatic species on New Caledonia (Enright and Jaffré, this volume), whereas 

James W. Dalling, Department of Plant Biology, 

University of Illinois at Urbana-Champaign, 265 

Morrill Hall, 505 S. Goodwin Avenue, Urbana, 

Illinois 61081, USA, and Smithsonian Tropical 

Research Institute, Apartado 0843-03092, Balboa, Republic of Panama. Phoebe Barkan, Department of Plant Biology, University of Illinois 

at Urbana-Champaign, 265 Morrill Hall, 505 S. 

Goodwin Avenue, Urbana, Illinois 61081, USA. 

Peter J. Bellingham, Landcare Research, P.O. Box 

40, Lincoln 7640, New Zealand. John R. Healey,

School of Environment, Natural Resources 

and Geography, University of Wales, Bangor, 

Gwynedd, LL57 2UW, UK. Edmund V. J. Tanner, Department of Plant Sciences, University of 

Cambridge, Cambridge CB2 3EA, UK. Correspondence: J. Dalling, dalling@illinois.edu.

Manuscript received 13 April 2010; accepted 

9 July 2010.
4 4 • smithsonian contributions to botany

neotropical taxa are all canopy trees of mature forest, although a few elfin forest species found on infertile soils 

(P. tepuiensis, P. sprucei, P. buchholzi) seldom grow more 

than a few meters tall. 

PALEOHISTORY OF NEOTROPICAL 

PODOCARPACEAE

Podocarpaceae is a monophyletic group of Gondwanan origin with a fossil record dating back to the Early 

Cretaceous (Krassilov, 1974). Neotropical fossil evidence 

indicates the presence of podocarps in northern South 

America at least since the late Eocene to Oligocene (van 

der Hammen and Hooghiemstra, 2000). The modern distribution of podocarps, however, has been most affected by 

more recent events. The rise of the Andes from the south 

to north and west to east first created montane habitats 15 

mya, culminating in the rapid uplift of the Eastern Cordillera during the Pliocene 2–5 mya (Gregory-Wodzicki, 

2000; Antonelli et al., 2009; Graham, 2009). Although 

little is known about the flora and environment of tropical 

South America during the Pliocene, sediment records indicate that the principal species in northern Andes forests 

were the montane taxa Weinmannia (Cunoniaceae) and 

Podocarpus (van der Hammen, 1974).

Concurrent with Andean uplift, formation of the Panama land bridge allowed podocarp species to migrate north 

into Central America and potentially competing species to 

migrate south into the Andes. Analysis of continuous lake 

sediments from the plain of Bogota (Eastern Cordillera of 

the Andes, 2,580 m elevation), spanning the late Pliocene 

to the Holocene, indicate that podocarps were among the 

most important taxa in northern Andean forests during interglacial periods up to 330,000 years ago, before being replaced primarily by Quercus (oak) forests (van’t Veer and 

Hooghiemstra, 2000). Quercus was one of the last immigrants to northern South America a million years ago (van 

der Hammen, 1989) and became dominant after the last 

glacial cycle at elevations of 2,000–3,000 m in the northern Andes and through Central America. Quercus, however, only extends as far south as the Colombia–Ecuador 

border (1°N; Hooghiemstra, 2006), so competitive exclusion by oaks cannot account for the rarity of podocarps in 

southern Andean forests.

Temperature fluctuations associated with glacial cycles may also have induced elevational shifts in podocarp 

populations. During the Pleistocene, podocarp pollen appears periodically at multiple low-elevation sites (Behling 

et al., 1999; Haberle and Maslin, 1999; Ledru et al., 2001; 

Niemann and Behling, 2008). The occurrence of podocarps at lowland Amazonian sites has been interpreted 

as key evidence indicating glacial cooling (e.g., Liu and 

Colinvaux, 1985; Behling, 1998). Comparisons of the presumed extant elevational distribution of podocarps in Andean forests with paleorecords of podocarp pollen has led 

to an inferred climate cooling of 4.5°C–7.0°C during the 

Wisconsin glacial maximum (Liu and Colinvaux, 1985; 

Haberle and Maslin, 1999). 

Although extensive pollen records exist for podocarps, glacial migration patterns of individual taxa cannot 

be corroborated using these data. Pollen identifications are 

limited to the generic level (Hooghiemstra et al., 2006), 

and interpretation of low-density pollen records are further 

affected by the potential for long-distance transport (e.g., 

Behling, 2001; but see van der Hammen and Hooghiemstra, 2000). However, palynological data, when combined 

with genetic analyses, provide a useful additional tool to 

infer the timing of podocarp migration patterns. Ledru 

et al. (2007) combined pollen records with molecular 

analysis of living material to infer relationships among 26 

populations of three Brazilian endemic species (P. sellowii, 

P. lambertii, and P. brasiliensis) that occur in diverse forest 

types: along rivers in Cerrado, mid-elevational Araucaria

forest, and Atlantic rainforest in southern and eastern 

Brazil. Clustering in the molecular data indicated that the 

three podocarps formed three groups: (1) a rather homogenous group consisting of P. lambertii, a species associated with Araucaria forest, suggesting recent population 

expansion in the last 3,000 years in southern Brazil; (2) a 

more heterogeneous northern group of P. sellowii (that 

also includes P. brasiliensis), associated with riverine forest that expanded earlier (~16,000 years ago); and (3) a 

montane and coastal group from eastern Brazil including 

both P. sellowii and lambertii, which are relicts from a 

population expansion over a short period during the cool 

and moist conditions of the last glaciations ~29,000 years 

ago. Combined genetic and palynological approaches 

now hold promise for understanding the distribution and 

timing of migration of northern and western Amazonian 

podocarps.

CURRENT RANGE DISTRIBUTION 

OF PODOCARPS

Neotropical podocarps have been collected extensively, with metadata available for >1,900 specimens 

accessible through the Global Biodiversity Information 

Facility (GBIF) (http://www.gbif.net, accessed 10 October 
number 95 • 4 5

2009). Broad distributional patterns at the genus level are 

therefore generally well resolved. At the species level, however, taxon boundaries remain poorly differentiated, with 

some species based on very few specimens (Farjon, 2001). 

As a consequence, disjunct populations of some taxa continue to be discovered (Neill, 2008). Below, we describe 

distribution patterns for neotropical taxa recognized by 

Farjon (2001) based on plots of locality information for 

herbarium specimens.

The northern distributional limit of podocarps is delimited by P. matudae, with an outlying population in cloud 

forest in Tamaulipas, Mexico, at 23°N (Figure 3.1a). Two 

other Central American species with broad distributional 

patterns also extend into Mexico: P. guatemalensis occurs 

at 300 m elevation at the transition between lowland and 

mesophilic montane forest in Oaxaca and may also extend into the more-mesic forests in the southern Yucatan 

Peninsula, whereas P. oleifolius occurs in lower montane 

forest at 1,000 m in Veracruz. Elsewhere in Central America podocarp taxa mostly have broad geographic ranges: 

P. oleifolius occurs through to Panama and the Andes as 

far as Venezuela and northern Peru, P. guatemalensis extends to Colombia, and P. costaricensis has a narrower 

range restricted to central Costa Rica and eastern Panama. 

Two remaining Central American Podocarpus taxa recognized by Farjon (2001) are taxonomically more doubtful. 

Podocarpus magnifolius occurs in Bolivia, Peru, and Venezuela, but several additional collections have been made 

in eastern and central Panama. Podocarpus monteverdeensis, which occurs only in central Costa Rica, has been 

considered a synonym of P. oleifolius (Merello, 2003). A 

single endemic species of Prumnopitys, P. standleyi, occurs 

in Costa Rica in high-elevation oak forests.

Two species, Podocarpus angustifolius and P. aristulatus, occur in Cuba at 20°N–21°N, whereas P. aristulatus

and P. hispaniolensis occur in Hispaniola and P. purdieanus and P. urbanii occur in Jamaica at 18°N. In contrast 

to the island endemics of the Greater Antilles, only a single species, P. coriaceus, is recognized to occur across the 

Lesser Antillean islands of Dominica, Guadeloupe, Martinique, Montserrat, and St. Kitts and Nevis, as well as 

Puerto Rico. An additional endemic species, P. trinitensis, 

occurs on Trinidad.

In South America, most tropical podocarps are distributed along the northern and western Andes or centered 

on the Guyana Shield of southern Venezuela (Figure 3.1b). 

Although some taxa have extensive distributions within 

the Andes (notably P. parlatorei in the southern Andes extending north into Bolivia and P. oleifolius through Peru, 

Ecuador, and Colombia), most species are more restricted 

in their ranges and exhibit multiple disjunct populations suggestive of habitat specialization or refugial distributions. Three species, P. magnifolius, P. celatus, and 

P. tepuiensis, maintain populations in both the Guyana 

Shield and the western Andes. In addition to Podocarpus, 

three species of Prumnopitys and one species of Retrophyllum are associated with mid-elevation (P. harmsiana) 

and high-elevation (P. montana, P. exigua, and R. rospigliosii) tropical Andean forests. 

ELEVATIONAL RANGE DISTRIBUTION 

OF PODOCARPS

Paleoclimate reconstructions for the neotropics based 

on podocarp pollen data hinge on the assumption that 

podocarps are restricted to montane forests. This assumption is clearly violated for Central American taxa, where 

Podocarpus guatemalensis, the most widespread species, 

has a primarily lowland distribution (Figure 3.2a). Podocarpus guatemalensis illustrates that under current climate 

conditions podocarps are capable of persisting at sea level; 

GBIF herbarium collection data indicate that P. guatemalensis occurs in Caribbean coastal habitat from Belize 

to Panama and along the Pacific coast from Costa Rica 

south to Isla Gorgona and the Chocó of Colombia. Elsewhere in South America, P. guatemalensis occurs primarily 

at <1,000 m elevation, with a few collections at 2,600 m 

in Zamora-Chinchipe, southern Ecuador, representing distributional outliers for this species. No occurrences of this 

species have been reported east of the Andes.

South American podocarp taxa do have a primarily 

montane or lower montane distribution, with a few exceptions (Figure 3.2b). Most notably, P. celatus occurs 

in lower montane and lowland forest across the western 

Amazon of Ecuador and Peru and the northern Amazon of 

Venezuela. The lowest elevation occurrence of this taxon 

is at 130 m in Loreto, Peru, where it occurs on infertile 

lateritic and white sand soils.

In the Greater Antilles, Podocarpus urbanii extends 

to the highest point of Jamaica (2,256 m; Asprey and 

Robbins, 1953), whereas on Hispaniola P. aristulatus 

scarcely occurs above 1,800 m in the Cordillera Central. Podocarpus aristulatus is restricted to cloud forests 

(1,550–1,800 m), where it is the third commonest tree; 

above 1,800 m forests are dominated by Pinus occidentalis (Martin et al., 2007). The absence of Podocarpus aristulatus at higher elevations may be related to fire. Above 

1,800 m fires are associated with El Niño droughts, occurring, on average, every seven years (Martin and Fahey, 
4 6 • smithsonian contributions to botany

2006). In contrast, lower-elevation cloud forests do not 

support fire (Martin et al., 2007). On Hispaniola, a constraint on the distribution of P. aristulatus imposed by fire 

is consistent with the great majority of podocarps being 

intolerant of fire (Coomes and Bellingham, this volume). 

HABITAT ASSOCIATIONS OF

NEOTROPICAL PODOCARPS

The global distribution of conifers suggests a competitive advantage over angiosperms at high latitude and in 

arid or nutrient-poor environments (Ellenberg, 1988). In 

tropical and mesic temperate forests, Bond (1989) suggested that conifers have been excluded by their relatively 

low seedling growth rates, compared with angiosperm 

competitors. Low-productivity environments may eliminate this competitive disadvantage; inherently slow growth 

and tissue turnover rates can result in greater use efficiency 

of nutrients for conifers than angiosperms (Grime, 1979). 

Recently, Coomes et al. (2005) highlighted an additional 

mechanism that might account for temperate-forest podocarp distributions. On the South Island of New Zealand, 

fertile alluvial terraces are dominated by angiosperms, 

whereas nearby older, phosphorus-impoverished terraces 

are dominated by podocarps. However, rather than nutrient availability, Coomes et al. (2005) argued that a dense 

understory fern layer leading to a thick, slowly decomposing litter layer effectively prevents seedling recruitment 

of podocarps, whereas smaller-seeded angiosperms are 

able to establish on less-shaded elevated recruitment sites 

formed by fallen logs.

Herbarium metadata unfortunately provide little 

information on the habitat associations of neotropical 

podocarps, although notes on specimens of P. celatus, 

P. coriaceus, P. ingensis, and P. oleifolius comment on the 

presence of sandy or quartzite soils, whereas the Cuban 

endemic species P. angustifolius occurs on serpentine soils 

(identified as P. ekmannii) or on lateritic soils that are more 

organic-rich than those dominated by pine (Pinus cubensis) forest (Smith, 1954; Borhidi, 1991). Ideally, evidence 

for habitat associations could be provided by plot-based 

ecological studies, but podocarps seldom seem to occur in plots. Almost all neotropical permanent plots are 

in the Amazonian lowlands, where podocarps are scarce. 

Podocarps have not been reported from any of the >250 

(i)
FIGURE 3.1. Collection locations for neotropical Podocarpus species in (i, facing page) Central America and (ii) South America based 

on specimen metadata available through the Global Biodiversity Information Facility (http://www.gbif.net). Insets A and B provide enhanced regional detail. Antillean taxa and South American taxa with 

<10 georeferenced collections are omitted. Collections are plotted on 

the WorldClim gray-scale elevation surface for the neotropics (Hijmans et al., 2005). Darker shading indicates higher elevations.

(ii)
4 8 • smithsonian contributions to botany

ha of the RAINFOR (Amazon Forest Inventory Network) 

0.1–1 ha permanent plots arrayed across lowland Amazonia (O. Phillips, University of Leeds, personal communication), nor from lowland and montane 25–50 ha forest 

plots maintained by the Center for Tropical Forest Science (http://www.ctfs.si.edu). Because of their presumably 

patchy distribution, they are also absent from a network of 

1 ha plots in the Colombian Andes (A. Duque, Universidad 

Nacional de Colombia, personal communication). When 

present in plots, they tend to occur at low relative density 

in species-rich forest. For nine Podocarpus species recorded 

in plot inventories, only in four cases did they account for 

>10% of either basal area or stem density (Table 3.1).

For four Podocarpus species, soils data accompanying plot inventories can be used to infer habitat specialization. Podocarpus oleifolius is a montane species distributed 

along the Continental Divide of Central America and the 

northern Andes. At the Fortuna Reserve in western Panama, P. oleifolius has a highly localized distribution: it is 

restricted to very wet sites with acidic humic soils underlain by a striking white soil developed from rhyolitic tuff 

(Table 3.1). It is absent from more fertile adjoining andesitic sites with similar elevation and rainfall (Andersen et 

al., 2010; J. Dalling, unpublished data). Podocarpus oleifolius also occurs on highly acidic soils in Venezuela (Kelly 

et al., 1994) and sandy acidic soils in northern Colombia 

FIGURE 3.2. Box plots showing the median, 10th, 25th, 75th, and 90th percentiles for the elevation ranges of (a) Central American, Antillean, and widespread taxa and (b) South American Podocarpus species. Values above each box indicate the sample size for each species. Taxa with less than 

three elevational records are not included. Species are ordered by median elevation.
number 95 • 4 9

(Marín, 1998) and reaches highest abundance in tanninrich swamps at Monteverde, Costa Rica (Haber, 2000). 

A striking parallel to P. oleifolius in Panama is the recent discovery of P. tepuiensis growing at 1,600 m along 

the Ecuador–Peru border (Neill, 2008). Podocarpus 

tepuiensis was previously thought to be endemic to the 

Guyana Shield of northwestern South America, where it 

occurs on sandstone mesas (tepuis). In Ecuador, P. tepuiensis is restricted to coarse quartzite outcrops dispersed along 

the Cordillera del Cóndor that consist of mid-Cretaceous 

TABLE 3.1. Site information, stem density (density, individuals ha−1), and basal area for neotropical permanent forest plots containing 

Podocarpus species. The table is sorted by latitude. See table footnotes for site, census information, and references. A dash (-) indicates 

that data are not available.

 Rain Soil Basal area Density Fisher’s

Species Site Elevation (m) (mm) pH (m2 ha-1

) (%) (ind ha-1) (%) alpha

P. matudae Mexico a 800–1,400 2,500 - 1.1 3.5 83 7.1 -

P. matudae Mexico b 1,800 1,000 - 4.1 5.5 120 5.7 15.1

P. aristulatus Hispaniola c 1,100–2,500 2,000 - 4.2 18.0 32 4.0 8.5

P. hispaniolensis Haiti d 1,280 - - 14.9 21.0 222 6.3 11.7

P. urbanii Jamaica e 1,580 3,000 4.1 10.1 29.1 420 10.3 10.2

P. urbanii Jamaica f 1,580 3,000 3.6 12.0 26.6 840 15.7 8.5

P. urbanii Jamaica g 1,580 3,000 4.3 8.5 18.0 156 3.9 7.4

P. urbanii Jamaica h 1,580 3,000 3.0 0.7 1.1 117 1.5 3.4

P. urbanii Jamaica i 1,760 3,000 3.7 5.5 9.9 225 3.0 -

P. urbanii Jamaica j 1,620 3,000 5.0 2.0 4.6 113 2.5 -

P. urbanii Jamaica k 1,660 3,000 4.1 4.4 6.4 80 1.4 -

Podocarpus spp. Colombia l 2,940 1,500 - 35.9 45.0 120 3.8 12.5

P. oleifolius Costa Rica m 2,300 3,300 - - - 20 3.5 11.1

P. oleifolius Panama n 1,240 6,200 3.6 0.2 0.4 1 0.1 21.2

P. oleifolius Panama o 1,100 4,300 3.9 2.5 7.8 6 0.6 12.6

P. oleifolius Venezuela p 2,600 2,500 3.5 0.0 0.1 5 0.1 7.3

P. guatemalensis Panama q 200 6,000 5.8 1.4 5.2 12 2.6 10.2

P. sprucei Ecuador r 1,120 - 4.4 0.9 5.2 7 1.2 25.3

P. oleifolius Ecuador r 1,120 - 4.4 0.3 1.9 4 0.7 20.1

P. tepuiensis Ecuador s 1,620 - 4.6 0.9 7.0 9 1.7 21.6

P. selowii Brazil t 10 1,875 - 0.1 0.4 3 0.4 30.3

a Puig et al. (1987), Gómez Farías, Tamaulipas, 23°3′N, 99°18′W, min dbh = 5 cm; means of nine 0.25 ha plots.

b Phillips and Miller (2002), Site 49, Sierra de Manantlan, Jalisco, 19°44′N, 104°15′W, min dbh = 2.5 cm; Gentry 0.1 ha transect plot. c Martin et al. (2007), Cordillera Central, Dominican Republic, 19°1′N, 70°60′W, min dbh = 10 cm; means of twenty-five 0.05 ha plots.

d Senterre et al. (2006), Bois Cavalier, Macaya National Park, 18°19′N, 74°9′W, min dbh = 10 cm; 0.063 ha plot. e Tanner and Bellingham (2006), wet slope forest, Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, 0.1 ha plot. f Tanner and Bellingham (2006), mull ridge forest, Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, 0.1 ha plot. g Tanner and Bellingham (2006), col forest (“gap” forest in Tanner, 1977), Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, 0.09 ha 

plot.

h Tanner and Bellingham (2006), mor ridge forest, Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, 0.06 ha plot. i Bellingham (unpublished), ridge crest forest, Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, mean of six 0.02 ha plots.

j Bellingham (unpublished), windward slope forest, Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, mean of five 0.02 ha plots. k Bellingham (unpublished), leeward slope forest, Blue Mountains National Park, 18°05′N, 76°39′W, min dbh = 3 cm, mean of five 0.02 ha plots. l Phillips and Miller (2002), Site 119, Serranía de Perijá, Cesar, 10°30′N, 72°55′W, min dbh = 2.5 cm; Gentry 0.1 ha transect plot, three Podocarpus

species occur in the plot.

m Lieberman et al. (1996), Volcan Barva elevational transect, 10°8′N, 84°6′W, min dbh = 10 cm, 1 ha plot. n Dalling (unpublished), Quebrada Honda B, Fortuna Forest Reserve, 8°45′N, 82°14′W, min dbh = 10 cm, 1 ha plot. o Dalling (unpublished), Quebrada Chorro, Fortuna Forest Reserve, 8°45′N, 82°14′W, min dbh = 10 cm, 1 ha plot. p Kelly et al. (1994), Pico Bolivar, Sierra Nevada National Park, 8°35′N, 71°07′W, min dbh = 3.2 cm, 0.22 ha plot. q Ibañez (unpublished) La Falla, Coiba Island, 7°30′N, 81°42′W, min dbh = 10 cm, 1 ha plot. r Neill (2008), lower Nangaritza plot, Cordillera del Condor, 4°14′S, 78°39′W, min dbh = 10 cm, 1 ha plot. s Neill (2008), upper Nangaritza plot, Cordillera del Condor, 4°14′S, 78°39′W, min dbh = 10 cm, 1 ha plot. t Negrelle (2002), Volta Velha Reserve, Santa Catarina, 26°4′S, 48°38′W, min dbh = 5 cm, 1 ha plot.
5 0 • smithsonian contributions to botany

Hollin Formation sandstones. The Hollin Formation is 

similar to the Guyana Shield mesa sandstones >1,500 km 

away from which they are ultimately derived. Paired plots 

established on the Hollin Formation and adjacent granitic 

substrates showed that podocarps were restricted to sites 

underlain by sandstone (Neill, 2008). 

Another widely distributed species, P. guatemalensis, 

occurs near sea level from Belize to Isla Gorgona on the 

Pacific coast of Colombia. In Panama, P. guatemalensis

occurs on numerous Pacific and Atlantic coastal islands, 

including Coiba, Bastimentos, and Escudo de Veraguas, 

and occasionally in wet lowland forest on the mainland. 

On Coiba, P. guatemalensis occurs in one of seven 1 ha 

forest plots (A. Ibañez, Smithsonian Tropical Research 

Institute, unpublished data). The distribution of P. guatemalensis on Coiba appears to be constrained to mafic 

substrates on the southern side of a geological fault line 

(A. Ibañez, unpublished data). Although available evidence therefore suggests that podocarps are associated 

with acidic, infertile soils, this is not always the case. The 

Caribbean island species P. aristulatus and P. purdieanus occur in wet forest on karst limestone in central and 

western Cuba and western Jamaica, respectively (Borhidi, 

1991; Bachman et al., 2007), where exposed rock outcrops and steep topography can result in a relatively open 

forest canopy. 

HABITAT ASSOCIATIONS, FUNCTIONAL 

TRAITS, AND DEMOGRAPHY OF

PODOCARPUS URBANII IN JAMAICAN 

MONTANE FOREST

Among the neotropical montane podocarps, our best 

understanding of relationships of distribution and abundance in relation to geology and soils is for Podocarpus urbanii, which is endemic to the Blue Mountains of 

eastern Jamaica, between 1,370 and 2,256 m (Buchholz 

and Gray, 1948). The Blue Mountains are composed of 

granodiorite, mudstones, sandstones, and conglomerates 

(Grubb and Tanner, 1976), and P. urbanii occurs on all of 

these rock types, although not on local outcrops of limestone (P. J. Bellingham, unpublished data). On the basis of 

stem density, P. urbanii is the fourth most abundant tree 

species in the upper slope and ridgetop forests of the Blue 

Mountains, accounting for 7% of stems >3 cm diameter 

at breast height (dbh) (Tanner and Bellingham, 2006), 

and the fourth highest basal area, behind three ericoid 

tree species (Cyrilla racemiflora, Vaccinium meridionale, 

and Clethra occidentalis; Bellingham et al., 2005).

Podocarpus urbanii occurs across a range of soil types 

in the Blue Mountains. For example, it occurs in four forest types within 300 m of each other at 1,580–1,600 m 

that range considerably in soil pH and concentrations of 

carbon, nitrogen, and phosphorus (Tanner, 1977; Table 

3.2). Forest stature declines from a canopy height of 18 to 

7 m as soil pH decreases and soil C:N and N:P ratios increase across the sites (Table 3.2), and forest composition 

varies considerably (Tanner, 1977). Podocarpus urbanii is 

present in all forest types, with the highest proportion of 

total basal area and stem density occurring in slope forest 

and mull ridge forests (ridgetop forest lacking a deep litter 

layer), which have intermediate fertility (Table 3.2). Podocarpus urbanii is markedly less abundant in the shortstature mor ridge forest (which has highly acidic soils with 

high soil C:N and N:P; Table 3.2). The rarity of P. urbanii

on the mor site is most likely a consequence of the high organic matter content of the mor soils (>47% carbon up to 

30 cm soil depth; Tanner, 1977). Mor soils, in turn, derive 

from nutrient-poor recalcitrant litter produced by trees in 

the Ericales that dominate the site. A competitive advantage for the Ericales may arise from symbiotic association 

with ericoid mycorrhizas, which scavenge effectively for 

organic sources of nitrogen and phosphorus (Read et al., 

2004). In the nearby mull ridge forest, bioassay experiments (Tanner, 1977; Healey, 1989), a field fertilization 

experiment (Tanner et al., 1990), and a root ingrowth experiment (Stewart, 2000) all indicate colimitation to plant 

growth by both nitrogen and phosphorus. 

A more-extensive view of relationships between P. urbanii and site and soil variables is derived from 15 permanent plots within a 250 ha portion of the western part 

of the Blue Mountains centered on the axial range (plots 

1,470–1,900 m, Bellingham et al., 2005; one plot at 1,300 

m is below the lower altitudinal limit of P. urbannii). 

Podocarpus urbanii occurred in 12 of these plots, within 

which it comprised 1%–10% of stems ≥3 cm dbh (2004 

census) and 1%–22% of stand basal area. The percentage 

of stems and basal area in the plots composed of P. urbanii

was unrelated to altitude and slope (r2

 < 0.18, p > 0.12). 

The percentage of stems and basal area had a unimodal 

response to soil pH (most frequent in plots with soil pH 

3.5–4.2 and not found in plots with soil pH > 5.0; range 

across plots: 3.1–5.7). The percentage of stems was positively related to soil C:N ratio (r2

 = 0.30, p = 0.03), but the 

percentage of basal area was not (r2 = 0.16, p = 0.14), and 

both were unrelated to soil N:P ratio or total phosphorus 

concentration (r2 < 0.09, p > 0.28).

In the Jamaican montane forests, P. urbanii has a 

specific leaf area 55 cm2 g-1, which is 32% less than the 
number 95 • 5 1

average (81 cm2 g-1) across 26 species in the forests, and 

a leaf thickness of 527 μm, which is more than double 

the average (237 μm) across 50 species in these forests 

(Tanner and Kapos, 1982). Across the four adjacent forest types described by Tanner (1977), the foliar nitrogen 

concentration of P. urbanii was consistently less than 

the average across co-occurring angiosperm species in 

each site (Table 3.2), whereas the foliar phosphorus concentration of P. urbanii was less than average in all but 

the very nutrient-poor mor ridge forest (Table 3.2). The 

lower foliar nitrogen concentration in a Jamaican montane podocarp compared to coexisting angiosperms is 

consistent with results from a temperate rainforest soil 

chronosequence (Richardson et al., 2005), although in 

that chronosequence foliar phosphorus concentrations of 

podocarps were generally not different from co-occurring 

angiosperms, in contrast to Jamaica.

The montane forests in which P. urbanii occurs are 

subject to frequent but irregular disturbance by hurricanes 

(with severe canopy damage, on average, every 25 years) 

and, locally, by landslides triggered by high-intensity rainfall and earthquakes. Comparative data for P. urbanii

and coexisting angiosperms include a 30-year record of 

growth and survivorship in permanent plots (Tanner and 

Bellingham, 2006), seedling recruitment in experimental 

tree fall gaps and undisturbed forest (Healey, 1990) and 

on a chronosequence of landslides (Dalling, 1994), and 

surveys of tree recovery from hurricane damage (Bellingham et al., 1994, 1995; Bellingham and Tanner, 2000).

Pooling data from across four forests of contrasting soils and forest composition (Tanner, 1977), the tree 

size structure of Podocarpus urbanii shows a distribution 

skewed toward smaller sizes, with more small stems than 

two coexisting angiosperm canopy dominants, Clethra occidentalis and Lyonia octandra, but fewer small stems than 

Hedyosmum arborescens (Bellingham et al., 1995). The 

size structure of P. urbanii is similar to some podocarps 

in other tropical montane rainforests (e.g., Falcatifolium 

falciforme, Aiba et al., 2004) and warm temperate rainforests (e.g., Nageia nagi, Kohyama, 1986) and suggests that 

P. urbanii is at least moderately shade tolerant, which is 

consistent with its relatively high abundance as seedlings 

under intact canopies (Figure 3.3; Sugden et al., 1985; 

Healey, 1990). However, its size structure has not been 

constant in these permanent plots over 30 years. In 1974, 

at least 23 years after the forest had last been disturbed 

by a hurricane, small stems (<10 cm dbh) were common, 

and there were few large stems (>25 cm dbh; Figure 3.4). 

Hurricane Gilbert, the most powerful North Atlantic hurricane in the twentieth century, severely disturbed these 

TABLE 3.2. Percentage of total basal area and total stem density of Podocarpus urbanii (stems ≥3 cm diameter at 1.3 m) 

in four montane rainforest types within 300 m of each other in the Blue Mountains, Jamaica (1580–1600 m elevation; 

2004 census), and canopy height and soil characteristics of each forest type. Data are from Grubb and Tanner (1976), 

Tanner (1977), and Tanner and Bellingham (2006).

Characteristic Col Slope Mull Mor

Total basal area (m2 ha−1) 58 ± 5.2 57 ± 3.7 45 ± 2.7 62 ± 6.7

P. urbanii basal area (%) 17 ± 5.3 22 ± 2.3 23 ± 3.1 2 ± 1.3

Total stem density (stems ha−1) 4320 ± 277 4490 ± 318 6220 ± 313 8180 ± 512

P. urbanii stem density (%) 4 ± 1 13 ± 1.1 9 ± 1 2 ± 1

Canopy height (m) 12–18 8–13 8–13 (4–)5–7

Soil pH 4.3 4.1 3.6 3.0

Soil total carbon (%) 11.0 ± 1.4 9.1 ± 1.5 11.6 ± 1.5 49.0 ± 1.2

Soil total nitrogen (%) 1.1 ± 0.12 0.68 ± 0.08 0.88 ± 0.10 2.0 ± 0.03

Soil total phosphorus (%) 0.07 ± 0.01 0.04 ± 0.01 0.04 ± 0.01 0.05 ± 0.00

Soil C:N ratio 10 ± 0.3 13 ± 0.8 13 ± 0.4 24 ± 0.9

Soil N:P ratio 15.7 ± 1.3 20.4 ± 8.7 23.7 ± 5.5 43.8 ± 3.5

Foliar nitrogen (%), all species (n) 1.76 (8) 1.27 (9) 1.61 (14) 1.05 (13)

Foliar nitrogen (%), P. urbanii 0.86 0.71 0.71 0.69

Foliar phosphorus (%), all species (n) 0.10 (8) 0.08 (9) 0.07 (14) 0.05 (13)

Foliar phosphorus (%), P. urbanii 0.05 0.05 0.05 0.05
5 2 • smithsonian contributions to botany

forests in 1988 (Bellingham et al., 1995). Sixteen years 

later, in 2004, there was a greater frequency of stems >20 

cm dbh, but many fewer stems <10 cm dbh than in 1974 

(Figure 3.4).

Over the past 30 years, mortality rates for P. urbanii

were between two- and sevenfold lower than co-occurring 

species on slope, mull ridge, and col forests but similar 

to co-occurring species on the infertile mor ridge site 

(Figure 3.5a). Differences in mortality rates among sites 

probably reflect spatial heterogeneity in tree mortality resulting from Hurricane Gilbert in 1988 linked to ridge and 

slope topography (Bellingham, 1991). The low mortality 

of P. urbanii relative to co-occurring species does not appear to be a consequence of structural traits. Podocarpus

urbanii has the fourth lowest wood density in the community (0.6 g cm−3; Tanner, 1977) and above-average diameter growth rates at all sites except the mor ridge (Figure 

3.5b). Recruitment rates into the 3 cm dbh class, however, 

have been exceptionally low at all sites (Figure 3.5c), and 

there is little contribution of resprouting to population 

FIGURE 3.3. (a) Basal area, (b) stem density (individuals <3.2 cm 

diameter at 1.3 m height), (c) sapling density (individuals <3.2 cm 

diameter at breast height and >3 m height), (d) seedling density, (e) 

seedling number per unit basal area for all species (solid bars), and 

P. urbanii (open bars). Adult and sapling data are from six 0.024 ha 

plots; seedling data are from ninety-six 1 m2

 plots. Data are from 

Healey (1990).

FIGURE 3.4. Frequency distribution of stems of Podocarpus urbanii ≥3 cm diameter at 1.3 m height, pooled across four forest types 

within 300 m of each other in the Blue Mountains, Jamaica (total 

area sampled = 0.35 ha) at two censuses of the same plots (1974, 

solid circles; and 2004, open circles). Data are in 2 cm interval 

classes, with averaged interval classes linked by a left-tailed horizontal bar. Curve fitting followed Kohyama (1986) and provided a better fit than the Weibull function (Bailey and Dell, 1973). Solid line 

(1974): ln(y) = 5.075 – 0.08148x – 0.6563ln(x), r2

 = 0.89; dashed 

line (2004): ln(y) = 2.684 – 0.1226x + 0.5334ln(x), r2

 = 0.85.
number 95 • 5 3

maintenance of P. urbanii, in contrast to many of the coexisting angiosperms (Bellingham et al., 1994).

Differences in adult growth and mortality rates among 

species in part reflect differences in susceptibility to hurricane damage. Podocarpus urbanii was significantly more 

resistant to hurricane damage than the community average when assessed up to four years after Hurricane Gilbert 

(Bellingham et al., 1995), but the decline in recruitment 

between 1974–1984 and 1994–2004 suggests that its 

comparative abundance may derive from periods of relatively less disturbance. Evidence to support this view derives from a study of experimental canopy gaps, similar 

to those formed during Hurricane Gilbert, in which P. urbanii was the twelfth most abundant species as seedlings 

compared with being the fourth most abundant species as 

seedlings under adjacent closed canopies (Healey, 1990; 

Figure 3.6a,b). Podocarpus urbanii may also benefit from 

other more patchy and less frequent disturbances such as 

landslides (Dalling, 1994; Figure 3.6c), although observations of recruitment on older (>50 years old) landslides 

(Dalling, 1994) suggest that they are much more important recruitment sites for ericoid canopy trees. 

In summary, Podocarpus urbanii is a moderately 

shade-tolerant tree species in Jamaican montane forest, 

FIGURE 3.6. Density of new seedling recruits per hectare of principal canopy species recorded in forty-eight 1 m2 plots distributed 

across (a) three understory plots and (b) three forest gaps simulating hurricane damage, 18 months after an initial survey. (c) Seedling 

recruits recorded on four 14-year-old landslides triggered by road 

construction. Data are from Healey (1990) and Dalling (1992).

FIGURE 3.5. Annualized (a) mortality, (b) growth, and (c) recruitment rates of Podocarpus urbanii (solid bars) and all other species 

(open bars) from 1974 to 2004 for individuals >3 cm dbh at four 

forest types in the Blue Mountains, Jamaica (see Table 3.2). Podocarpus, all sites combined, mortality (calculated from a census of 

n = 136), recruitment (n = 11), growth (n = 136). Other species, 

all sites combined, mortality (n = 1417), recruitment (n = 904), 

growth (n = 822). Mortality and recruitment rate calculations follow Burslem et al. (2000).
5 4 • smithsonian contributions to botany

capable of regenerating from seed in undisturbed forest 

more frequently than many of the other principal canopy 

species. Podocarpus urbanii leaf traits and low adult 

mortality rates are also consistent with shade tolerance. 

However, P. urbanii maintains surprisingly high diameter growth rates, which is probably attributable to its 

relatively low wood density and may help explain the frequency of this species in hurricane-prone forest. 

CONSERVATION AND MANAGEMENT 

OF NEOTROPICAL PODOCARPS

Of 31 neotropical podocarps, 11 are considered at 

risk (near-threatened to endangered), 13 are of “least 

concern,” and 5 species lack sufficient data to be evaluated (International Union for Conservation of Nature 

[IUCN], 2009). Taxa of least concern either have widespread distributions, with populations within protected 

areas (e.g., Podocarpus oleifolius, P. guatemalensis), or are 

restricted to remote, undisturbed rainforests, principally 

in the Guyana Shield or western Andes. With the exception of Podocarpus coriaceus, which occurs on multiple 

Lesser Antillean islands, all podocarp taxa that occur in 

the insular Caribbean are of conservation concern. Most 

threatened are the three Greater Antilles endemics, P. hispaniolensis, P. angustifolius, and P. purdieanus, each of 

which has restricted distributions on Hispaniola, Cuba, 

and Jamaica, respectively. Species for which data are insufficient to make a status evaluation include the Trinidad 

endemic, P. trinitensis, and taxa whose distributions are 

either restricted or scattered or in localities where logging or forest conversion may threaten populations in the 

future.

In the absence of information on population size or 

growth, IUCN designation of threatened species must rely 

heavily on criteria based on observed range size. Our review, indicating that many podocarps are associated with 

infertile soils, suggests that the large observed geographic 

ranges (Figure 3.1) of many species may support only 

small, localized, and therefore unconnected populations. 

For example, the range distribution of Prumnopitys harmsiana includes portions of Venezuela, Colombia, Ecuador, 

Peru, and Bolivia. However, in Colombia the species is 

known from only five small populations 600 km apart 

(Cogollo, 2007). The predominantly mid-elevational distribution of many podocarp taxa (Figure 3.2) has also 

meant that many populations have been drastically reduced by forest clearance for coffee cultivation, pasture, 

and row crops (Cogollo, 2007). 

In addition to land conversion, several podocarp species have been logged extensively in Colombia and probably elsewhere (Torres-Romero, 1988; Cogollo, 2007). 

Species that reportedly formed high-density stands, including Retrophyllum rospigliosii and Podocarpus guatemalensis, are now almost extinct in the Rio Magdalena 

valley (Torres-Romero, 1988). As yet, few efforts at ex 

situ conservation of neotropical podocarps have been attempted; however, several species in Antioquia, Colombia, 

including R. rospigliosii, have been promoted for watershed reforestation or have been established in arboreta 

(Velasquez-Rua, 2005). 

Attempts at propagating podocarp seedlings for reforestation have met with limited success. Marín (1998) 

notes that germination and establishment success of Podocarpus oleifolius and Prumnopitys harmsiana seedlings are 

low, whereas propagation of cuttings using plant hormone 

treatments or removal of established seedlings from wild 

populations has been more effective. Poor seedling establishment success may also account for the relative paucity 

of Podocarpus urbanii in secondary forest when compared 

to nearby old-growth forest sites (McDonald and Healey, 

2000). Growth and survival trials of seedling transplants, 

however, indicate that P. urbanii performs well above average relative to other Jamaican montane forest trees (McDonald et al., 2003), suggesting that podocarps may have 

unrealized potential for reforestation.

Acknowledgments

Authors JWD and PJB thank the ARC–NZ Research 

Network for Vegetation Function and Macquarie University for financial support and the New Zealand Foundation 

for Research, Science and Technology (Ecosystem resilience 

OBI) for additional support to PJB. We thank Ian Dickie, 

(Landcare New Zealand), Surangi Punyasena (University 

of Illinois), Alvaro Duque (National University of Colombia, Medellin), Juan Toro (Corporación Ambiental del 

Centro de Antioquia, Colombia) and David Coomes (University of Cambridge) for providing literature, comments 

on the manuscript, and assistance with species mapping.

REFERENCES

Aiba, S., K. Kitayama, and M. Takyu. 2004. Habitat Associations with Topography and Canopy Structure of Tree Species in a Tropical Montane Forest on Mount Kinabalu, Borneo. Pl. Ecol. 174: 147–161.

Andersen, K. M., B. L. Turner, and J. W. Dalling. 2010. Soil-Based Habitat Partitioning in Understory Palms in Lower Montane Tropical 

Forests. J. Biogeogr. 37: 278–292.
number 95 • 5 5

Antonelli, A., J. A. A. Nylaander, C. Persson, and I. Sanmartín. 2009. 

Tracing the Impact of the Andean Uplift on Neotropical Plant Evolution. Proc. Natl. Acad. Sci. U.S.A. 106: 9749–9754.

Asprey, G. F., and R. G. Robbins. 1953. The Vegetation of Jamaica. Ecol. 

Monogr. 23: 359–412

Bachman, S., A. Farjon, M. Gardner, P. Thomas, D. Luscombe, and 

C. Reynolds. 2007. Podocarpus purdieanus. In IUCN Red List 

of Threatened Species. Version 2009.1. http://www.iucnredlist.org

(accessed 10 October 2009).

Bailey, R. L., and T. R. Dell. 1973. Quantifying Diameter Distributions 

with the Weibull Function. Forest Sci. 19: 97–104.

Behling, H. 1998. Late Quaternary Vegetational and Climatic Changes 

in Brazil. Rev. Palaeobot. Palynol. 99: 143–156.

Behling, H. 2001. Late Quaternary Environmental Changes in the Lagoa da Curuça Region (Eastern Amazonia, Brazil) and Evidence of 

Podocarpus in the Amazon Lowland. Veg. Hist. Archaeobot. 10: 

175–183.

Behling, H., J. C. Berrio, and H. Hooghiemstra. 1999. Late Quaternary 

Pollen Records from the Middle Caquetá River Basin in Central 

Colombian Amazon. Palaeogeogr. Paleoclimatol. Palaeoecol. 145: 

193–213.

Bellingham, P. J. 1991. Landforms Influence Patterns of Hurricane Damage: Evidence from Jamaican Montane Forests. Biotropica 23: 

427–433.

Bellingham, P. J., and E. V. J. Tanner. 2000. The Influence of Topography 

on Tree Growth, Mortality and Recruitment in a Tropical Montane 

Forest. Biotropica 32: 378–384.

Bellingham, P. J., E. V. J. Tanner, and J. R. Healey. 1994. Sprouting of 

Trees in Jamaican Montane Forests after a Hurricane. J. Ecol. 82: 

747–758.

Bellingham, P. J., E. V. J. Tanner, and J. R. Healey. 1995. Damage and 

Responsiveness of Jamaican Montane Tree Species after Disturbance by a Hurricane. Ecology 76: 2562–2580.

Bellingham, P. J., E. V. J. Tanner, and J. R. Healey. 2005. Hurricane Disturbance Accelerates Invasion by the Alien Tree Pittosporum undulatum in Jamaican Montane Rain Forests. J. Veg. Sci. 16: 675–684.

Bond, W. J. 1989. The Tortoise and the Hare: Ecology of Angiosperm 

Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 

227–249.

Borhidi, A. 1991. Phytogeography and Vegetation Ecology of Cuba. 

Akadémiai Kiadó, Budapest.

Buchholz, J. T., and N. E. Gray. 1948. A Taxonomic Revision of Podocarpus. IV. The American Species of Section Eupodocarpus, Subsections C and D. J. Arnold. Arbor. 29: 123–151.

Burslem, D. F. R. P., T. C. Whitmore, and G. C. Brown. 2000. ShortTerm Effects of Cyclone Impact and Long-Term Recovery of Tropical Rain Forest on Kolombangara, Solomon Islands. J. Ecol. 88: 

1063–1078.

Cogollo, A. 2007. Las podocarpáceas. In Volume 5: Las Magnoliaceas, Las Miristicáceas y Las Podocarpáceas, N. García, ed., pp. 

189–226, Libro Rojo de Plantas de Colombia. Serie Libros Rojos 

de Especies Amenazadas de Colombia. Ministerio de Ambiente, 

Bogotá.

Coomes, D. A., R. B. Allen, W. A. Bentley, L. E. Burrows, C. D. Canham, L. Fagan, D. M. Forsyth, A. Gaxiola-Alcantar, R. L. Parfitt, 

W. A. Ruscoe, D. A. Wardle, D. J. Wilson, and E. F. Wright. 2005. 

The Hare, the Tortoise and the Crocodile: The Ecology of Angiosperm Dominance, Conifer Persistence and Fern Filtering. J. Ecol.

93: 918–935.

Coomes, D. A., and P. J. Bellingham. 2011 (this volume). Temperate 

and Tropical Podocarps: How Ecologically Alike Are They? In 

Ecology of the Podocarpaceae in Tropical Forests, B. L. Turner 

and L. A. Cernusak, eds., pp. 119–140. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Dalling, J. W. 1992. Forest Regeneration on Landslides in the Blue 

Mountains, Jamaica. Ph.D. thesis, University of Cambridge, Cambridge, UK.

Dalling, J. W. 1994. Vegetation Colonization on Landslides in the Blue 

Mountains, Jamaica. Biotropica 26: 350–361.

Ellenberg, H. 1988. The Vegetation Ecology of Europe. Cambridge University Press, Cambridge, UK.

Enright, N. J., and T. Jaffré. 2011 (this volume). Ecology and Distribution of the Malesian Podocarps. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 57–77. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution 

Scholarly Press, Washington, D.C.

Farjon, A. 2001. World Checklist and Bibliography of Conifers. Royal 

Botanic Gardens, Kew, Richmond, Surrey, UK.

Graham, A. 2009. The Andes: A Geological Overview from a Biological 

Perspective. Ann. Missouri Bot. Gard. 96: 371–385

Gregory-Wodzicki, K. M. 2000. Uplift History of the Central and Northern Andes: A Review. Geol. Soc. Amer. Bull. 112: 1091–1105

Grime, J. P. 1979. Plant Strategies and Vegetation Processes. John Wiley 

and Sons, Chichester, UK.

Grubb, P. J., and E. V. J. Tanner. 1976. The Montane Forests and Soils of 

Jamaica: A Reassessment. J. Arnold Arbor. 57: 313–368.

Haber, W. A. 2000. Plants and Vegetation. In Monteverde: Ecology and 

Conservation of a Tropical Cloud Forest, N. Nadkarni and N. Wheelwright, eds., pp. 39–90. Oxford University Press, Oxford, UK. 

Haberle, S. G., and M. A. Maslin. 1999. Late Quaternary Vegetation 

and Climate Change in the Amazon Basin Based on a 50,000 Year 

Pollen Record from the Amazon Fan ODB Site 932. Quatern. Res. 

51: 27–38.

Healey, J. R. 1989. A Bioassay Study of Soils in the Blue Mountains 

of Jamaica. In Mineral Nutrients in Tropical Forest and Savannah 

Ecosystems, J. Proctor, ed., pp. 273–288. Blackwell Scientific, Oxford, UK.

Healey, J. R. 1990. Regeneration in a Jamaican Montane Tropical Rainforest. Ph.D. thesis, University of Cambridge, Cambridge, UK.

Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. 

2005. Very High Resolution Interpolated Climate Surfaces for 

Global Land Areas. Int. J. Climatol. 25: 1965–1978.

Hooghiemstra, H. 2006. Immigration of Oak into Northern South 

America: A Paleo-ecological Document. In Ecology and Conservation of Neotropical Montane Oak Forests, M. Kapelle, ed., pp. 

17–28. Springer-Verlag, Berlin.

Hooghiemstra, H., V. M. Wijninga, and A. M. Cleef. 2006. The Paleobotanical Record of Colombia: Implications for Biogeography and 

Biodiversity. Ann. Missouri Bot. Gard. 93: 297–324.

International Union for Conservation of Nature (IUCN). 2009. The 

IUCN Red List of Threatened Species. Version 2009.1. http://www.

iucnredlist.org/ (accessed 10 October 2009).

Kelly, D. L., E. V. J. Tanner, E. M. Nic Lughadha, and V. Kapos. 1994. 

Floristics and Biogeography of a Rain Forest in the Venezuelan Andes. J. Biogeogr. 21: 421–440.

Kohyama, T. 1986. Tree Size Structure of Stands and Each Species in Primary Warm-Temperate Rain Forests of Southern Japan. Bot. Mag. 

(Tokyo) 99: 267–279

Krassilov, V. A. 1974. Podocarpus from the Upper Cretaceous of Eastern 

Asia and Its Bearing on the Theory of Conifer Evolution. Palaeontology 17: 365–370.

Ledru, M.-P., R. C. Campello, J. M. L. Dominguez, L. Martin, P. Mourguiart, A. Sifeddine, and B. Turcq. 2001. Late Glacial Cooling in 

Amazonia Inferred from Pollen at Lagoa do Caco, Northern Brazil. 

Quatern. Res. 55: 47–56

Ledru, M.-P., M. L. Ferraz Salatino, G. Ceccantini, A. Salatino, F. Pinheiro, and J.-C. Pintaud. 2007. Regional Assessment of the Impact 

of Climatic Change on the Distribution of a Tropical Conifer in the 

Lowlands of South America. Diversity Distrib. 13: 761–771.
5 6 • smithsonian contributions to botany

Lieberman, D., M. Lieberman, R. Peralta, and G. S. Hartshorn. 1996. 

Tropical Forest Structure and Composition on a Large Scale Altitudinal Gradient in Costa Rica. J. Ecol. 84: 137–152.

Liu, K.-B., and P. A. Colinvaux. 1985. Forest Changes in the Amazon 

Basin during the Last Glacial Maximum. Nature 318: 556–557.

McDonald, M. A., and J. R. Healey. 2000. Nutrient Cycling in Secondary Forests in the Blue Mountains of Jamaica. Forest Ecol. Managem. 139: 257–278.

McDonald, M. A., A. Hofny-Collins, J. R. Healey, and T. C. R. Goodland. 2003. Evaluation of Trees Indigenous to the Montane Forest 

of the Blue Mountains of Jamaica for Reforestation and Agroforestry. Forest Ecol. Managem. 175: 379–401.

Marín, A. 1998. Ecología y Silvicultura de las Podocarpáceas Andinas de 

Colombia. Smurfit Cartón, Cali, Colombia.

Martin, P. H., and T. J. Fahey. 2006. Fire History along Environmental 

Gradients in the Subtropical Pine Forests of the Cordillera Central, 

Dominican Republic. J. Trop. Ecol. 22: 289–302.

Martin, P. H., R. E. Sherman, and T. J. Fahey 2007. Tropical Montane 

Forest Ecotones: Climate Gradients, Natural Disturbance, and Vegetation Zonation in the Cordillera Central, Dominican Republic. 

J. Biogeogr. 34: 1792–1806.

Merello, M. 2003. Podocarpaceae. In Volume 2: Gimnospermas y 

Monocotiledóneas, C. V. Hollowell, A. McPherson, and D. Gunter, 

eds., pp. 11–13, Manual de Plantas de Costa Rica. Missouri Botanical Garden, St. Louis. 

Negrelle, R. R. B. 2002. The Atlantic Forest in the Volta Velha Reserve: 

A Tropical Rainforest Site Outside the Tropics. Biodivers. Conserv. 

11: 887–919.

Neill, D. 2008. Botanical Inventory of the Cordillera del Cóndor Region 

of Ecuador and Peru: Project Activities and Findings, 2004–2007. 

http://www.mobot.org/MOBOT/research/ecuador/cordillera/

welcome.shtml (accessed 10 October 2009).

Niemann, H., and H. Behling. 2008. Late Quaternary Vegetation, Climate and Fire Dynamics Inferred from the El Tiro Record in Southeastern Ecuadorian Andes. J. Quatern. Sci. 23: 203–212.

Phillips, O. L., and J. S. Miller. 2002. Global Patterns of Plant Diversity: Alwyn H. Gentry’s Forest Transect Data Set. Missouri Botanic 

Garden, St. Louis.

Puig, H., R. Bracho, and V. J. Sosa. 1987. El Bosque Mesofilo de Montaña: Composicion Floristica y Estructura. In El Bosque Mesofilo 

de Montaña de Tamaulipas, H. Puig and R. Bracho, eds., pp. 55–

79. Instituto de Ecología, Mexico City. 

Read, D. J., J. R. Leake, and J. Perez-Moreno. 2004. Mycorrhizal Fungi 

as Drivers of Ecosystem Processes in Heathland and Boreal Forest 

Biomes. Canad. J. Bot. 82: 1243–1263.

Richardson, S. J., D. A. Peltzer, R. B. Allen, and M. S. McGlone. 2005. 

Resorption Proficiency along a Chronosequence: Responses among 

Communities and within Species. Ecology 86: 20–25.

Senterre, B., J.-M. Laurent, B. Peguero. T. Clase, and J. V. Hilaire. 2006. 

Plant Diversity along Elevational Gradient and Forest Strata in 

Rainforests of Macaya National Park, Haiti. Final Report. Laboratoire de Botanique Systématique et de Phytosociologie, Université 

Libre de Bruxelles, Brussels.

Smith, E. E. 1954. The Forests of Cuba. Maria Moors Cabot Foundation 

Publication, No. 2. Harvard University Press, Cambridge, Mass.

Stewart, G. S. 2000. A Test of Nutrient Limitation in Two Tropical Montane Forests Using Root Ingrowth Cores. Biotropica 32: 369–373.

Sugden, A. M., E. V. J. Tanner, and V. Kapos. 1985. Regeneration Following Clearing in a Jamaican Montane Forest: Results of a TenYear Study. J. Trop. Ecol. 1: 329–351.

Tanner, E. V. J. 1977. Four Montane Forests of Jamaica: A Quantitative Characterization of the Floristics, the Soils and the Foliar 

Mineral Levels, and a Discussion of the Interrelations. J. Ecol. 65: 

883–918.

Tanner, E. V. J., and P. J. Bellingham. 2006. Less Diverse Forest Is More 

Resistant to Hurricane Disturbance: Evidence from Montane Rain 

Forests in Jamaica. J. Ecol. 94: 1003–1010.

Tanner, E. V. J. and V. Kapos. 1982. Leaf Structure of Jamaican Upper 

Montane Rain-Forest Trees. Biotropica 14: 16–24.

Tanner, E. V. J., V. Kapos, S. Freskos, J. R. Healey, and A. M. Theobald. 

1990. Nitrogen and Phosphorus Fertilization of Jamaican Montane 

Forest Trees. J. Trop. Ecol. 6: 231–238.

Torres-Romero, J. H. 1988. Podocarpaceae. In Flora of Colombia, Volume 5, P. Pinto and G. Lozano, eds., pp. 1–73. Universidad Nacional de Colombia, Bogotá.

van der Hammen, T. 1974. The Pleistocene Changes of Vegetation and 

Climate in Tropical South America. J. Biogeogr. 1: 3–26.

van der Hammen, T. 1989. History of Montane Forests of the Northern 

Andes. Pl. Syst. Evol. 162: 109–114

van der Hammen, T., and H. Hooghiemstra. 2000. Neogene and Quaternary History of Vegetation, Climate, and Plant Diversity in Amazonia. Quatern. Sci. Rev. 19: 725–742.

van’t Veer, R., and H. Hooghiemstra. 2000. Montane Forest Evolution 

during the Last 650 000 yr in Colombia: A Multivariate Approach 

Based on Pollen Record Funza-I. J. Quatern. Sci. 15: 329–346.

Velasquez-Rua, C. 2005. Identificación de Especies Amenazadas en la 

Jurisdicción de CORANTIOQUIA de las Familias Annonaceae, 

Fagaceae, Juglandaceae, Magnoliaceae, Myristicaceae y Podocarpaceae. Corporación Autónoma del Centro de Antioquia, Medellin, 

Colombia.
4 Ecology and Distribution of 

the Malesian Podocarps

Neal J. Enright and Tanguy Jaffré

ABSTRACT. Podocarp species and genus richness is higher in the Malesian region than 

anywhere else on earth, with maximum genus richness in New Guinea and New Caledonia and maximum species richness in New Guinea and Borneo. Members of the Podocarpaceae occur across the whole geographic and altitudinal range occupied by forests 

and shrublands in the region. There is a strong tendency for podocarp dominance of 

vegetation to be restricted either to high-altitude sites close to the limit of tree growth 

or to other sites that might restrict plant growth in terms of water relations and nutrient supply (e.g., skeletal soils on steep slopes and ridges, heath forests, ultramafic parent 

material). Although some species are widespread in lowland forests, they are generally 

present at very low density, raising questions concerning their regeneration ecology and 

competitive ability relative to co-occurring angiosperm tree species. A number of species 

in the region are narrowly distributed, being restricted to single islands or mountain 

tops, and are of conservation concern. Our current understanding of the distribution and 

ecology of Malesian podocarps is reviewed in this chapter, and areas for further research 

are identified.

INTRODUCTION

The Malesian region has the highest diversity of southern conifers (i.e., 

Podocarpaceae and Araucariaceae) in the world (Enright and Hill, 1995). It is a 

large and heterogeneous area, circumscribing tropical and subtropical lowland 

to montane forest (and some shrubland) assemblages, extending from Tonga in 

the east to India in the west and from the subtropical forests of eastern Australia 

in the south to Taiwan and Nepal in the north (Figure 4.1). As a natural entity, 

the region is best defined by the distribution of closed forests with tropical affinity (Webb and Tracey, 1981; Whitmore, 1984). The Podocarpaceae is the 

largest conifer family in the region in terms of genera and species, and the genus 

Podocarpus is both the most numerous and widespread (Table 4.1, Appendix).

The taxonomy of the Podocarpaceae in this region has been extensively 

described by de Laubenfels (1969, 1985, 1987, 1988), who continues to add 

Neal J. Enright, School of Environmental Science, 

Murdoch University, Murdoch, Western Australia 6150, Australia. Tanguy Jaffré, UMR AMAP 

Institut de Recherche pour le Développement 

(IRD), Laboratoire de Botanique et d’Ecologie 

Végétale, Nouméa, New Caledonia. Correspondence: N. Enright, N.Enright@murdoch.edu.au.

Manuscript received 13 April 2010; accepted 

9 July 2010.
5 8 • smithsonian contributions to botany

FIGURE 4.1. Malesian distribution of (top) genera and (bottom) species in the family Podocarpaceae, showing 

nodes of maximum genus diversity in New Caledonia and New Guinea, high levels in eastern Indonesia to the 

Philippines, and nodes of maximum species diversity in New Guinea and Borneo. Information for southern Australia and New Zealand is not shown. Although outside the region discussed here, data are shown for Japan to 

indicate the northern range limit for Podocarpaceae globally. (Figure prepared by H. Kobryn.)
number 95 • 5 9

new species to the group (de Laubenfels, 2003, 2005). 

New Guinea (31 species), Borneo (30 species), and New 

Caledonia (20 species), followed by the Philippines and 

Peninsular Malaysia, show the highest levels of species diversity in the region (Figure 4.1, bottom). Tropical eastern 

Australia is notable for its lower diversity of podocarps 

(six species, four genera) relative to tropical regions to 

the north and east and New Zealand and Tasmania to the 

temperate south. Even Fiji has higher diversity at the genus level (five genera). Lowest diversity is associated with 

extreme isolation, with one species each in Tonga in the 

southeast and India in the west. Low podocarp diversity 

in the Australian tropics may reflect species losses due to 

the impacts of Pleistocene climate change associated with 

TABLE 4.1. Malesian distribution of genera and species in the family Podocarpaceae, showing the total species in each genus and the 

percentage of the global total occurring within the region. Data were compiled from de Laubenfels (1969, 1985, 1987, 1988, 2003, 

2005), Silba (1986, 1987), Enright and Hill (1995), Farjon (1998, 2008), and the Gymnosperm Database (http://www.conifers.org/index

.html).

Distribution

AcmopyleDacrycarpusDacrydiumFalcatifoliumNageiaParasitaxusPhyllocladusPodocarpusPrumnopitysRetrophyllumSundacarpusTotal

Tonga 0 0 0 0 0 0 0 1 0 0 0 1

Fiji 1 1 2 0 0 0 0 2 0 1 0 7

New Caledonia 1 1 4 1 0 1 0 9 1 2 0 20

Vanuatu 0 1 0 0 0 0 0 1 0 0 0 2

Solomon Islands 0 1 4 0 0 0 0 6 0 0 0 11

NE Australia 0 0 0 0 0 0 0 4 1 0 1 6

New Guinea 0 5 7 1 1 0 1 14 0 1 1 31

Moluccas 0 2 3 0 1 0 1 6 0 1 1 15

Sulawesi 0 3 4 0 1 0 1 5 0 0 1 15

Sunda Islands 0 1 1 1 1 0 0 3 0 0 1 8

Borneo 0 4 7 2 3 0 1 12 0 0 1 30

Sumatra 0 2 4 0 2 0 0 7 0 0 1 16

Malaya 0 1 5 0 2 0 0 6 0 0 0 14

Vietnam 0 1 1 0 2 0 0 3 0 0 0 7

Laos 0 1 1 0 1 0 0 0 0 0 0 3

Thailand 0 0 0 0 2 0 0 3 0 0 0 5

Cambodia 0 0 1 0 1 0 0 1 0 0 0 3

Assam 0 0 0 0 1 0 0 1 0 0 0 2

India 0 0 0 0 1 0 0 0 0 0 0 1

Nepal 0 0 0 0 0 0 0 1 0 0 0 1

China 0 1 1 0 3 0 0 7 0 0 0 12

Philippines 0 2 3 1 1 0 1 11 0 0 1 20

Taiwan 0 0 0 0 1 0 0 5 0 0 0 6

Burma 0 1 0 0 1 0 0 2 0 0 0 4

TOTAL SPECIES 2 8 20 5 6 1 1 55 2 3 1 104

GLOBAL SPECIES 2 9 21 5 6 1 5 106 9 5 1 195

PERCENT MALESIAN 100 89 95 100 100 100 20 52 22 60 100 54
6 0 • smithsonian contributions to botany

glacial–interglacial cycles and the increased occurrence of 

fire, which has relegated closed forests to fire-protected 

moist gullies in many areas (Webb and Tracey, 1981; Kershaw, 1988). In India, low podocarp diversity is likely to 

be associated with plate tectonic and climate history since 

the Late Cretaceous, whereas in some tropical islands 

(e.g., Vanuatu) it is associated with recent geological formation (Enright and Gosden, 1992). Local radiation of 

species appears to be the major source of species diversity 

in areas characterized by high numbers of endemic species 

(e.g., New Caledonia, Borneo), especially within the genus 

Podocarpus.

Conifers are often characterized by great longevity 

and a low potential rate of population increase relative to 

angiosperm competitors (Loehle, 1988), which may place 

them at a competitive disadvantage under either lowstress or high-disturbance regimes (Grime, 1979). Bond 

(1989), Midgley and Bond (1989), and Midgley (1991) 

emphasized functional constraints on growth rate in their 

analyses of the reasons for the decline of conifers relative to angiosperms at the evolutionary timescale. They 

argued that conifers have a less-efficient vascular system 

than angiosperm trees since their tracheids are generally 

more resistant to solute flow than are angiosperm vessels 

and their leaves are not as fully vascularized. This has limited the range of possible leaf sizes and shapes in conifers 

and, they argued, helps to explain why conifers are rarely 

prominent in shaded habitats. Subsequent experimental 

studies and reviews by Brodribb and colleagues (Brodribb 

and Hill, 1998, 1999, 2004; Brodribb et al., 2005), Becker 

(2000), and others (Pammenter et al., 2004; Coomes et al., 

2005) support this contention, illustrating that conifers 

generally have lower hydraulic efficiency and so are disadvantaged under high potential productivity conditions 

(see Brodribb, this volume). However, under low-light 

conditions this competitive disadvantage relative to angiosperms declines (but is not eliminated), and under a combination of low-light and low-nutrient conditions, such as 

in some tropical forests, the disadvantage may disappear 

altogether (Becker, 2000; Pammenter et al., 2004). Given 

these constraints, the Podocarpaceae are undoubtedly the 

most successful of all conifers, with a large number of species showing a broad range of leaf adaptations, facilitating 

persistence in a range of tropical (and temperate) forests 

from sea level to altitudinal tree line and beyond.

Population size structures for conifers in both tropical and southern temperate forests are frequently discontinuous, with regeneration gaps evident in the sapling and 

small tree stages (Clayton-Greene, 1977; Veblen and Stewart, 1982; Veblen and Lorenz, 1987; Stewart and Rose, 

1989; Burns, 1991; Lara, 1991; Lusk and Ogden, 1992). 

Demographic studies have generally shown that such discontinuities in stage structures are typically local in extent 

and can be explained by differential response to disturbances at local to landscape scale, with the conifers often 

characterized as long-lived colonizers (e.g., Ogden, 1985; 

Enright, 1995; Enright et al., 1999). Although this may be 

true for podocarp species that dominate high-altitude forests in parts of tropical Malesia, the population dynamics 

of many species present at lower density in angiospermdominated lowland and lower montane tropical forests is 

less well understood. 

There have been few major ecological studies that 

focused on podocarp species in the Malesian region. The 

limited information presented here is obtained from a variety of published and unpublished sources, and it deals 

mostly with forest composition and structure in general 

or focuses on how our knowledge of podocarp ecology in 

temperate forests or of other tropical plant groups with 

some shared attributes (e.g., rarity) informs a growing understanding of their ecology.

DISTRIBUTION AND ECOLOGY

OF MALESIAN PODOCARPS

Podocarps are typically infrequent components of lowland and lower montane tropical forests, but may strongly 

dominate in upper montane forests, alpine shrublands, and 

some swamp forest associations at both low and high elevations (Paijmans, 1976; Enright and Hill, 1995). Species of 

Podocarpus, Nageia, Prumnopitys, and Sundacarpus (with 

generally flattened, broad leaves) are most common in lowland and lower montane forests in Australia, New Guinea, 

and Southeast Asia, whereas those of Dacrydium, Dacrycarpus, and Falcatifolium (with generally imbricate/small 

leaves) are most common in higher-elevation forests of New 

Guinea and the Indonesian and Philippine islands. Podocarpus and Dacrydium species are also locally common 

in lowland peat and heath forests in Sarawak and Borneo 

(Whitmore, 1984; Nishimua et al., 2007). New Caledonia 

represents such a unique set of circumstances in terms of 

its isolation history, ultramafic geology, and associated vegetation assemblages (Jaffré, 1993) that its rich and wholly 

endemic podocarp flora is treated separately here.

Widespread and Common Species

Three species stand out in terms of their distributions, both geographically and altitudinally, through the 
number 95 • 6 1

Malesian region: Dacrycarpus imbricatus is widespread 

in montane forests (500–3,000 m) from Fiji to northern 

Myanmar, Podocarpus neriifolius occurs in lowland to 

montane forests from Fiji to Nepal, and Nageia wallichiana occurs from India to New Guinea and the Philippines, 

mostly in lower montane and montane forests, but occasionally also in lowland stands close to sea level (Kuang et 

al., 2006; Thomas et al., 2007; see Appendix, Table 4.A1). 

Podocarpus neriifolius is exploited for timber and has been 

depleted in some regions, especially in low- and middlealtitude forests. Other species with wide geographic distributions include Sundacarpus amarus (northeastern 

Australia to the Philippines), Podocarpus pilgeri (Solomon 

Islands to southern China), and Dacrydium beccarii and 

D. xanthandrum (Solomon Islands to the Philippines). Although not necessarily widespread, some podocarps may 

be abundant within their geographic ranges, dominating 

the forest stands in which they occur. For example, Dacrycarpus compactus occurs only in New Guinea but is the 

principal tree line species there. It is present on almost all 

mountains of the central mountain chain, often as the tree 

line dominant. However, it is virtually absent from sandstone mountains (e.g., Mount Jaya) where Papuacedrus 

papuana (Cupressaceae) and Phyllocladus hypophyllus

dominate (Hope, 1976). A range of podocarps is locally 

abundant on poor soils associated with ultramafic geology 

(e.g., Podocarpus gibbsiae and P. confertus in Borneo) and 

other resource-limiting substrates (e.g., Dacrydium cornwallianum in montane swamp forests in New Guinea and 

D. pectinatum in lowland heath and peat forests on acid 

sands in Borneo).

Rare and Restricted Species

Among 85 species from 10 genera in the Malesian 

region outside of New Caledonia, 45 show geographic 

ranges restricted to a single country or island (Appendix). 

There are at least six endangered podocarps, and a further 

seven species are known from only one or a few collection 

sites. In Fiji, a number of narrow endemic taxa, including 

Acmopyle sahniana (critically endangered), Dacrydium 

nausoriense (endangered), and Podocarpus affinis, occur 

in small stands in cloud forest on ridgetops at 375–900 

m. Acmopyle sahniana is restricted to three small stands 

at Namosi, Viti Levu. Populations are declining, seed production is poor, and there is no recent evidence of germination and recruitment of seedlings. In Tonga, the endemic

P. pallidus occurs on steep slopes in Calophyllum- and

Garcinia-dominated montane forest at 190–300 m on 

‘Eua, one of the oldest (Eocene) and largest limestone 

islands in the Tongan island chain (Drake, 1996). These 

isolated island species are threatened by logging and associated erosion, and little detailed information is available 

about the ecology of the podocarps growing there.

Other endangered species include Dacrydium comosum in Peninsular Malaysia, Nageia fleuryi in mainland 

Southeast Asia, Podocarpus costalis in the Philippines and 

Taiwan, and P. nakaii in Taiwan (Appendix). A number of 

local endemics are restricted to one or a few localities in 

northern Borneo on or near Mount Kinabalu, including 

Dacrycarpus kinabaluensis, Podocarpus gibbsiae, P. globulus, and Falcatifolium angustum (Sarawak), or to single 

mountains in New Guinea (Dacrydium leptophyllum, 

D. spathoides) or the Philippines (Podocarpus lophatus).

Altitudinal Zonation and High-­Altitude Stands

Johns (1982) describes a generalized altitudinal forest 

zonation for New Guinea, with Podocarpus species often 

present at low density in angiosperm-dominated lowland 

(0–700 m) and lower montane rainforest (700–1,800 

m), Podocarpus and Dacrydium present in Nothofagusdominated mid-montane forests (1,800–3,000 m), and 

Dacrycarpus (with Papuacedrus; Cupressaceae) dominant 

near the tree line at altitudes of 3,000–3,900 m. Similar 

sequences can be described for other parts of Malesia, 

although mountain forest zones and altitudinal tree lines 

tend to occur at lower altitudes on smaller land masses 

and mountain ranges (the mass elevation effect), so that it 

is difficult to compare directly species’ altitudinal ranges 

among species and locations. Several podocarp species 

also occur above the tree line as shrubs in alpine scrub, including Dacrycarpus kinabaluensis on Borneo, Dacrydium 

medium in Sumatra, Podocarpus spathoides in Peninsular 

Malaysia, and Dacrycarpus imbricatus and Podocarpus 

pilgeri in central Irian Jaya (west New Guinea), where 

they form dense thickets 1–2 m high on infertile sandstone 

sites at 3,000 m (G. Hope, Australian National University, 

Canberra, Australia, personal communication).

Wade and McVean (1969) describe the high mountain forests of Mount Wilhelm, the highest peak in Papua 

New Guinea (4,510 m above sea level (asl)), in some detail: Dacrycarpus cinctus is prominent in Nothofagusdominated montane forests at 2,400–2,800 m, reaching 

a diameter at breast height (dbh) of >100 cm. In mountain “cloud” forest at 3,100–3,350 m emergent podocarps 

(Dacrycarpus compactus and Podocarpus pilgeri) form an 

open canopy at around 25 m over a diverse angiosperm 

tree canopy (containing at least 44 species) at about 18 m. 

Seedlings and saplings of the tree species are abundant 
6 2 • smithsonian contributions to botany

in the understory, which is draped in bryophytes and 

filmy ferns. Associated species are primarily derived from 

groups with tropical affinity. However, with increasing altitude, a greater number of the forest species show affinity 

with either southern or northern temperate-latitude taxa. 

Lower subalpine forest extends upward to about 

3,600 m (Wade and McVean, 1969). These forests are 

lower (9–15 m) and structurally and floristically less complex (~35 tree species). Trees are often crooked, and few 

exceed 20 cm dbh, apart from the emergent Dacrycarpus 

compactus. Gleichenia bolanica and bryophytes may form 

thickets that exclude woody plants from the forest floor. 

The upper subalpine (tree line) forests on Mount Wilhelm 

occasionally reach 3,900 m, interfingered with alpine 

grasslands. Dacrycarpus compactus and Rapanea vaccinioides are emergent above a low tree canopy (6–12 m) containing a total of only 15 tree species. Woody shrubs from 

the Ericaceae are abundant in the understory. 

Kitayama (1992) and Aiba and Kitayama (1999) 

describe altitudinal zonation of vegetation on Mount 

Kinabalu, Borneo, with patterns differing between ultramafic and nonultramafic substrates. In general, Kitayama 

(1992) identified four forest zones: lowland forests to 

1,200 m, montane forests to 2,000 m, upper montane forests to 2,850 m, and subalpine forests to the tree line at 

3,400 m. Dacrycarpus imbricatus, Dacrydium pectinatum, 

and Falcatifolium falciforme are prominent components 

of montane forest (at 1,560 m) on Tertiary sedimentary 

substrates, with densities of 20−50 trees >10 cm dbh 

per hectare (Aiba et al., 2004). Falcatifolium falciforme

shows moderate abundance of small trees and saplings 

in the shaded understory, but juveniles of Dacrycarpus

and Dacrydium are infrequent and appear to be associated with canopy openings. Forest structure and composition diverge markedly in the upper montane forest zone: 

forests on ultramafic substrate are of smaller stature and 

are dominated by Dacrycarpus kinabaluensis and the ultramafic endemic Dacrydium gibbsiae, whereas forests on 

nonultramafic substrate are dominated by angiosperm tree 

species. Podocarps (particularly D. kinabaluensis) become 

more prominent in subalpine forest on nonultramafic substrate, whereas they decline in abundance on ultramafic 

sites and are replaced there by dense, low (to 6 m) stands 

of Leptospermum recurvum (Myrtaceae). See Kitayama et 

al. (this volume) for more detailed coverage of the altitudinal vegetation sequence and factors affecting the distribution of podocarps on Mount Kinabalu. Detailed analyses 

of forest structure and composition in relation to altitude 

are lacking for many other parts of the region.

Lowland Rainforest

Podocarps are rare in the tropical lowlands. Podocarpus neriifolius, Nageia wallichiana, N. motleyi (Malaysia), N. fleuryi (Vietnam), and Sundacarpus amarus

(northeastern Australia) are large trees (to 40 m height 

and >100 cm dbh) that tend to occur as solitary canopy 

trees in angiosperm-dominated lowland and lower montane forests. Seedlings and saplings are infrequent. Extensive prelogging surveys of lower montane (700–1,500 m 

asl) rainforests in the Bulolo and Jimmi Valleys of Papua 

New Guinea conducted in the 1940s and 1950s reported 

densities of 0–2 canopy trees >50 cm dbh per hectare for P. 

neriifolius and S. amarus (Papua New Guinea Department 

of Forests, unpublished reports). In a sample of 32 halfhectare plots in lower montane forest enumerated in the 

1970s near Bulolo, Papua New Guinea, and dominated by 

either Araucaria, Castanopsis, or Lithocarpus (Fagaceae) 

species, podocarps were present in 10, mostly at densities 

of 2–4 individuals >10 cm dbh per hectare (N. Enright and 

R. Johns, Bulolo Forestry College, Papua New Guinea, 

unpublished data). A single outlier plot contained 16 individuals (32 ha-1

), evenly split between P. neriifolius and 

S. amarus, comprising ~12.5% of stand density and basal 

area. Although densities are too low to allow spatial analysis, the two species appear to occupy separate regions of 

the sample space and are not well mixed. 

In a large rainforest census plot in the Pasoh Forest Reserve, Peninsular Malaysia (80 m asl), 27 trees of N. motleyi >1 cm dbh were recorded in a 50 ha plot containing 

>300,000 trees, and in a plot in Lambir Hills National 

Park, Sarawak, three trees were recorded in a sample of 

about 350,000 individuals in the forest overall at 100–

200 m asl (http://www.ctfs.si.edu). Podocarpus neriifolius

is also listed as a “frequent” canopy tree in rainforest on 

sandstones of the McHenry Uplands of Cape York Peninsula (11°S–12°S) in far northern Queensland, Australia (Adam, 1992). These species have among the largest 

leaves of any podocarp, along with P. dispermum, a geographically restricted species growing in the understory of 

wet forests in northeast Queensland between 16°30’S and 

17°50′S.

Heath and Swamp Forests

Heath (kerangas) and peat (kerapah) forests form 

on low-nutrient acidic sands and wet peaty soils, respectively, most commonly at low altitude in Borneo, Sumatra, 

and Malaya (Bruenig, 1990). They are characterized by 
number 95 • 6 3

at least seasonal waterlogging and low levels of mineral 

nutrient availability and support high stem densities of 

small-diameter trees (typically <20 cm dbh) with smaller 

leaf size and markedly different floristic composition than 

lowland dipterocarp rainforest on nearby red-yellow clay 

soils (Oxisols and Ultisols) (Whitmore, 1984; Newbery et 

al., 1986). Drought stress is thought to be a major driver 

of forest structure and composition, with shallow root 

systems (a response to seasonal waterlogging) leading to 

increased vulnerability during dry periods. Miyamoto et 

al. (2007) reported a marked decrease in stand productivity during the El Niño drought of 1997–1998, followed by 

rapid return to much higher rates of biomass production, 

with overall rates similar to lowland dipterocarp forests. 

They concluded that a combination of high leaf mass allocation, small specific leaf area (as well as low leaf stomatal density and thicker/multiple palisade layers; Cao, 

2000), and long leaf life span relative to adjacent lowland 

dipterocarp forest stands on more-fertile soils facilitated 

the maintenance of moderate levels of stand productivity 

under conditions of recurrent drought stress. Tyree et al. 

(1998) found no evidence of increased resistance to xylem 

cavitation/embolism among heath forest tree species, so 

that adaptation to drought appears primarily through leaf 

attributes. Nutrient deficiency, antiherbivore defenses, and 

heat load have also been suggested as factors that may 

interact with drought to explain the structure and dynamics of these forest types (Whitmore, 1984; Miyamoto et 

al., 2007). Riswan and Kartawinata (1991) reported much 

higher levels of recovery through vegetative resprouting 

(rather than seedling recruitment) following canopy disturbance relative to nearby dipterocarp forest, which may 

also be linked to water- and nutrient-related stress tolerance attributes of heath forest species. 

Given these attributes, conifers might be expected to 

be generally more abundant in heath and swamp forests 

than in dipterocarp forest, and this is, indeed, the case. 

Agathis borneensis (Araucariaceae) is widespread and often dominant, and some of the highest-density stands of 

podocarps in the region also occur in heath forests. For 

example, Newbery (1991) recorded 40–72 Podocarpus 

neriifolius trees >7.6 cm dbh ha-1

 (but low basal area of 

0.12–0.40 m2 ha-1) in heath forests in Sarawak and Brunei 

codominated by the dipterocarps Shorea ovata and S. revoluta, and Nishimua et al. (2007) reported 20 trees >5 cm 

dbh (but relative basal area of only 0.19%) for N. wallichiana in a 1 ha heath forest plot near Palangkaraya, 

Kalimantan. Although there are no data on recruitment or 

mortality rates, stem diameter growth rate over two years 

was similar to or greater than that for most co-occurring 

angiosperm tree species (Nishimua et al., 2007). A number 

of other podocarps occur in heath and peat swamp forests 

in Borneo, including Dacrydium pectinatum, Nageia maxima, Podocarpus laubenfelsii, and Sundacarpus amarus. 

The higher-than-expected colonization of roots by arbuscular mycorrhizal fungi (relative to ectomycorrhizal fungi) 

in the surface organic soils of heath and swamp forests 

compared with mixed dipterocarp forest (Moyersoen et 

al., 2001) may be linked to the higher density of conifers, 

all of which have arbuscular mycorrhizal symbionts.

Podocarp dominance in swamp forest stands also occurs at some mid-montane elevations (1,400–2,300 m) in 

New Guinea. Several Dacrydium species (especially D. nidulum, but also D. cornwallianum) occur in almost pure 

stands (>95% of all trees) on swampy land in the Western 

and Southern Highlands. Associated species there include

Nothofagus grandis and Pandanus sp. (Johns, 1976). 

Members of the Podocarpaceae cover the whole geographic and altitudinal range occupied by forests in the 

Malesian region. Nevertheless, there is a strong tendency 

for dominance to be restricted either to high-altitude sites 

close to the limit of tree growth or to other sites that might 

restrict plant growth in terms of water relations or nutrient supply (e.g., steep slopes and ridges, heath and swamp 

forest formations, ultramafic geology, limestone hills, 

other infertile parent material, and skeletal soils). There 

is surprisingly little specific ecological information available for podocarps in lowland forest, probably because 

the extremely low density of trees makes field studies of 

demographic behavior difficult and unrewarding relative 

to the opportunities afforded by the many more abundant 

co-occurring (and sometimes commercially important) 

tree species. 

DISTRIBUTION AND ECOLOGY OF

NEW CALEDONIAN PODOCARPS

New Caledonia is distinctive in its podocarp flora, 

sharing no species with any other part of the region and 

with most species restricted to ultramafic substrates with 

unusual chemical properties. The Podocarpaceae of New 

Caledonia comprises 20 species in 8 genera: Podocarpus

(9 spp.), Dacrydium (4 spp.), Retrophyllum (2 spp.), Prumnopitys, Falcatifolium, Dacrycarpus, Acmopyle, and Parasitaxus (Table 4.1). All species and one genus (Parasitaxus) 

are endemic (Appendix). They include shrubs, small trees, 

and trees (Figure 4.2). Retrophyllum comptonii reaches a 
6 4 • smithsonian contributions to botany

A

B

C
number 95 • 6 5

FIGURE 4.2. Examples of podocarps endemic to New Caledonia. Facing page: (A) Parasitaxus usta, the only known parasitic gymnosperm; 

(B) Retrophyllum minus, an endangered species restricted to permanent and ephemeral stream banks in the south of the Grand Terre; (C) 

Podocarpus decumbens, a critically endangered, sometimes lianescent, species restricted to high-altitude maquis on the summit of the Montagne des Sources in the south of the Grand Terre. Above: (D) Acmopyle pancheri, a widely distributed tree species of forests from 150 to 

1000 m asl; (E) Podocarpus novae-caledoniae, a shrub species of low-altitude (0–700 m asl) ligno-herbaceous maquis in the south of the 

Grand Terre; (F) Dacrydium guillauminii, a critically endangered species restricted to a few streambank locations in the Plain of Lakes region 

in the south of the Grand Terre.

D E

F
6 6 • smithsonian contributions to botany

height of 30 m, and individuals 20–25 m high have been 

observed for Dacrydium lycopodioides, both species occurring in the canopy layer of dense evergreen rainforest. 

Acmopyle pancheri, Dacrycarpus vieillardii, Dacrydium 

balansae, Falcatifolium taxoides, Podocarpus longefoliolatus, P. polyspermus, P. lucienii, and Prumnopitys ferruginoides may reach 10–15 m but are usually shorter. Most 

occur in stunted montane rainforest at altitudes >1,000 m, 

except D. vieillardii (100–800 m), D. balansae (150–900 

m), and Podocarpus polyspermus (650–950 m). Dacrydium guillauminii and Retrophyllum minus, reaching 

heights of 1–6 m, are restricted to river and lake edges 

in the south of the main island on ultramafic substrates. 

Podocarpus novae-caledoniae, P. gnidioides, P. decumbens, and Parasitaxus usta do not exceed 2 m in height. 

Podocarpus decumbens tends to be lianescent, whereas 

P. gnidioides has a prostrate habit when growing in exposed sites (Jaffré, 1995).

The overall distribution of podocarps in New Caledonia accords less with the archaic angiosperms than with 

the more advanced angiosperms. Grandcolas et al. (2008) 

reviewed recent geological and phylogenetic work on New 

Caledonian plants and animals and concluded that many 

groups, including the podocarps, most likely arrived by 

long-distance dispersal after 37 mya, following up to 20 

million years of total submersion of the main land mass, 

with little chance of survival in situ for Gondwanan stock. 

Low gene sequence divergence rates within the New Caledonian species of Retrophyllum reported by Herbert et 

al. (2002) support this view. Further, most new, locally 

endemic species within this (and other) taxa appear to 

have arisen over the last few million years, primarily in 

response to the major climatic fluctuations associated with 

glacial-interglacial cycles. 

Vegetation Types and Species Distributions

Although only reaching a maximum elevation of 

about 1,600 m asl, the mountains of New Caledonia 

are characterized by montane cloud forest above 900 m 

similar in structure to forests at higher altitude (typically 

>2,000 m) on larger land masses such as New Guinea 

(Nasi et al., 2002). Annual rainfall exceeds 3,500 mm, 

and the vegetation is distinctly shorter than at lower altitudes, comprising a broken canopy layer of small trees 

with poorly developed trunks to 8 m high. The flora is less 

rich in angiosperms, although several species of the genera 

Metrosideros (Myrtaceae), Cunonia, and Pancheria (Cunoniaceae) are prominent, and genera with primitive features (Nemuaron, Paracryphia, Quintinia, Sphenostemon,

Trimenia, Zygogynum) are well represented, including the 

endemic family Phellinaceae. Podocarps are frequent in 

and beneath the low and discontinuous canopy, although 

many have fragmented distributions. Retrophyllum comptonii and Dacrydium lycopodioides contribute to the 

canopy of the forest or are emergent above it. Dacrydium 

lycopodioides is confined to exposed summits, whereas 

the more widespread Retrophyllum comptonii occupies a 

variety of sites. The extremely rare Podocarpus longefoliolatus (recorded from six localities on crests) is confined 

exclusively to the undergrowth of higher-altitude forests. 

Acmopyle pancheri, Falcatifolium taxoides, Parasitaxus 

usta, Podocarpus lucienii, P. sylvestris, and Prumnopitys 

ferruginoides have a wide altitudinal distribution between 

150 and >1,000 m asl. Two podocarps are restricted to 

evergreen rainforest of low altitudes, Dacrycarpus vieillardii to gallery forests on alluvium subject to flooding and 

Podocarpus polyspermus on slopes mostly above 600 m 

and, less frequently, in gallery forest at 50 m asl. Podocarpus novae-caledoniae and P. gnidioides occur in lignoherbaceous (sedge) maquis, the latter restricted to a few 

localized populations on rocky or lateritic crests. 

Podocarps are rarely dominant, but Dacrydium balansae forms an almost pure canopy layer in forest on the 

massif of Koniambo between 400 and 600 m (perhaps 

suggesting cohort recruitment after landscape-scale disturbance), and D. araucarioides is an abundant species in 

shrubby secondary maquis often codominated by Gymnostoma deplancheanum (Casuarinaceae). Dacrydium 

araucarioides is a fire-killed, small tree to 20 cm dbh in lowaltitude (mostly 100–400 m asl, but also in one locality at 

900 m at Montagne des Sources), open-maquis vegetation 

on shallow soils and lateritic boulder fields (cuirasse ferralitique) derived from ultramafic parent material. McCoy 

(1998) and McCoy et al. (1999) found that growth rings 

were clear and probably annual, with counts suggesting 

ages of up to 125 years for individuals approaching 20 cm 

dbh. Dacrydium araucarioides may recruit continuously 

in dry, open forests with G. deplancheanum prominent, 

but recruitment declines in more-mesic sites as rainforest 

tree species form a closed canopy, with disturbance (e.g., 

by fire) needed for recruitment to resume. 

Dacrydium guillauminii and Retrophyllum minus are 

confined to river margins and marshes in the southern ultramafic massif of the Grande Terre, in the Plain of Lakes 

region. The former is limited to four localities on the margins of the Rivière des Lacs and at the edge of the Lac en 

Huit. The latter grows at the margins of some other watercourses and, more rarely, on lateritic duricrust in shallow, periodically flooded depressions. Both species form 
number 95 • 6 7

populations of a few to several dozen individuals, which 

are shrinking as a result of increased fire frequency and 

other human impacts, with population size of R. minus

< 2,500 (Farjon and Page, 1999; Herbert et al., 2002) and 

considerably smaller for D. guillauminii. Although seed 

production and germination is good, seedling establishment beyond the perimeter of existing parent populations 

is very rare. Two other species, Dacrycarpus vieillardii and

Podocarpus novae-caledoniae, also grow along stream 

banks and tolerate temporary inundation. 

Parasitaxus usta is the only known parasitic conifer. 

Its foliage is red-purple, and it is always associated with 

Falcatifolium taxoides, from which it obtains nourishment 

by means of haustoria penetrating the base of the trunk or 

the roots (Köpke et al., 1981). Feild and Brodribb (2005) 

recently demonstrated that P. usta does not photosynthesize, has a strong connection of tracheids between its roots 

and those of F. taxoides, and is mycoheterotrophic—in 

combination, a unique solution to the parasitic life-form. 

It occurs around 1,000 m asl in mixed-angiosperm montane forests to 20 m high, with occasional emergent Araucaria to 30 m (and at a few locations in forests below 300 

m in the south of the Grande Terre). Seeds are produced, 

but there has been little success in ex situ germination, 

and seedlings are infrequent. There are no data on stem 

growth rates or estimates of longevity, but on average, 

longevity must be less than that of its host plant F. taxoides, so perhaps up to 200 years.

Environmental Controls

All of the New Caledonian podocarps are either restricted to ultramafic substrates (which cover about onethird of the Grand Terre, mostly in the south) or occur on 

both ultramafic and nonultramafic (mostly metamorphic) 

parent materials. Soils derived from ultramafic rocks are 

characterized by low concentrations of nitrogen, phosphorus, potassium, and calcium. Only Dacrydium balansae is 

able to grow on hypermagnesium soils, in which a deficit 

in exchangeable calcium (<2 meq 100 g-1

) is accentuated 

by the antagonistic action of magnesium (Jaffré, 1980). 

On the other hand, many conifers grow on colluvial or 

eroded soils (often covered with a thick organic horizon at 

higher altitudes) characterized by a less-marked calcium/

magnesium disequilibrium and greater concentrations of 

available nickel (>0.5%) and manganese in acidic soils. 

Analysis of mineral elements in chlorophyll tissues reveals 

a limited requirement for nitrogen, phosphorus, and potassium, as well as a capacity to selectively absorb calcium 

while limiting the absorption of manganese and nickel. 

Root nodules are present, but no research has been conducted into their form for New Caledonian species or the 

role that they might play in mediating (or restricting) element uptake from soil. 

The podocarps are mostly found in very wet environments (in dense rainforest, at higher altitudes, and at 

the margins of watercourses) and on ultramafic geology. 

They are usually light demanding, overtopping dense rainforests, or contributing to the dominant stratum of the 

maquis. They are also adapted to a wide range of habitats. 

Their affinity for ultramafic rocks probably results from 

their preadaptation to infertile soils and rocky sites, their 

apparent tolerance of sometimes toxic concentrations of 

nickel and manganese, and their light-demanding nature. 

In addition, the ultramafic substrate may limit the growth 

of some angiosperm groups, preventing the establishment 

of more rapidly growing species that have a high demand 

for nitrogen and phosphorus.

Conservation and Threats

The rarest podocarps undoubtedly formerly occupied 

much larger areas but are now restricted to sites in wet 

montane forest on ridges (Podocarpus decumbens, critically endangered, and P. longefolaliatus, endangered) or 

along the margins of watercourses (Dacrydium guillauminii, Retrophyllum minus), which have provided them with 

a refuge from fire. The main populations of Dacrydium 

guillauminii (critically endangered) and Retrophyllum minus (endangered) are now protected within botanical reserves. However, mining activities in the region, leading to 

possible dewatering of soil profiles near intermittent watercourses, continue to be a potential threat to the survival 

of some populations (Pascal et al., 2008). 

Perhaps among the most threatened species are the recently described Podocarpus beecherae (critically endangered, closely related to P. novae-caledoniae) from hilltop 

maquis in the south of the Grand Terre (de Laubenfels, 

2003) and P. colliculatus (endangered) from a single locality in moist forest on ultramafic substrate at Pic N’ga, Île 

des Pins, where tourism is developing without adequate 

control (de Laubenfels, 2005). However, the taxonomic 

status of P. colliculatus remains to be officially confirmed, 

and this collection may be synonymous with P. sylvestris (T. Jaffré, personal observations). In contrast, conifers common in dense rainforest, such as Falcatifolium 

taxoides, Prumnopitys ferruginoides, and Retrophyllum 

comptonii, as well as some less-common species with a 

wide distribution (e.g., Acmopyle pancheri) show less evidence of decline within the broad-leaved forests, although 
6 8 • smithsonian contributions to botany

post-European settlement fragmentation, logging, fire, 

and road construction (including many mining exploration and recreational tracks) have certainly had some 

impact; A. pancheri has been revised recently to nearly 

threatened. Now listed as vulnerable, Parasitaxus usta, the 

only known parasitic conifer, also seems to be disappearing from some formerly occupied sites. The potentially 

deleterious genetic consequences of fragmentation and 

population contraction in New Caledonian conifers have 

been illustrated for the rare Araucaria nemorosa, with genetic diversity lower in recent recruits than in parents and 

inbreeding becoming more common (Kettle et al., 2007). 

For the species of high-altitude, wet montane forests, 

global warming also poses a real threat that could cause 

the disappearance of their very specific ecological requirements (Nasi et al., 2002).

LIFE HISTORY ATTRIBUTES AND 

POPULATION ECOLOGY

Insights into the ecology of the Malesian podocarps 

may be gleaned from a consideration of their morphological and physiological attributes and comparison with 

those of co-occurring angiosperm tree species. For the majority of attributes little detail is known for these tropical 

podocarps relative to their temperate relatives. Nevertheless, some generalizations can be made and areas for fruitful future investigation identified.

Ecophysiology

Brodribb and Hill (1998, 1999, 2004) and Brodribb 

et al. (2005) have established a detailed understanding 

of the ecophysiological responses of podocarp seedlings 

for a mix of both temperate and tropical taxa that informs our understanding of their growth and survival 

in the understory of lowland mixed angiosperm–conifer 

forests. Most species have evolved bilaterally flattened 

leaves that mimic angiosperm leaves in shape and are efficient in the low-light environment of the forest understory. However, other than in the genus Nageia, podocarp 

leaves are single-veined, and this may set limits to leaf size 

and hydraulic conductivity that place them at a disadvantage relative to angiosperm tree species. On the basis of 

a broad survey of podocarp distributions in relation to 

climate and water availability, Brodribb and Hill (1998) 

concluded that podocarps were more constrained by 

seasonal drought than by overall patterns of rainfall, so 

that species were largely confined to moist, aseasonal or 

weakly seasonal climates. Brodribb et al. (2005) showed 

that seedlings of two tropical Malesian understory podocarps (N. fleuryi and P. grayae) had sixfold lower growth 

than comparison angiosperms under high-light conditions (1,300–1,800 mmol s-1

), whereas at low light levels 

(30 mmol s-1) growth rates were more similar but still 

significantly lower. The podocarps consistently had lower 

leaf to stem ratios (i.e., were constrained to support more 

nonphotosynthetic tissue) and were slower to respond to 

increases in light. Ultimately, the authors concluded that 

these tropical podocarps had lower rates of gas exchange 

and less-efficient production of leaf area than angiosperms 

and were best able to compete with angiosperms as stress 

tolerators under low light, where their disadvantage was 

at a minimum. Despite multiple veins per leaf, species of 

(the more recently evolved) Nageia are not clearly more 

successful than other forest podocarps.

Similar results were reported by Rundel et al. (2001), 

who found very low rates of net photosynthesis in N. wallichiana under high-light conditions in Thailand, and by 

Pammenter et al. (2004) in relation to hydraulic properties 

of angiosperms and conifers, including Podocarpus latifolius, in southern Africa. Pammenter et al. (2004) further 

concluded that the competitive advantage to angiosperms 

was maximized under high-productivity circumstances, 

with conifer competitiveness less impacted under low-soilnutrient (e.g. see Becker, 2000) and low-light conditions, 

such as in cloud forest, where both canopy and atmospheric factors contribute to low light availability. 

Population Ecology

Many podocarps, especially in the genus Podocarpus,

are dioecious, and all have wind-dispersed pollen, traits 

that may lead to the generally low tree densities reported 

for them in lowland tropical forests. Pollen dispersed by 

wind must fortuitously find its way from male to female 

plants across a landscape filled with competing species, 

whereas seeds (and seedlings recruited from them) can 

only be produced and dispersed from female adults, so 

that sex ratios and spatial distributions of adults also become important components of the species dynamics. Indeed, Haig and Westoby (1991) and Regal (1977) argued 

that the cost of rarity in angiosperms was lower than that 

in conifers because of the advantages of efficient insect and 

bird pollination relative to inefficient wind pollination. To 

what extent the combination of dioecy and wind pollination occurs in rainforest tree floras is unknown, but it may 

be infrequent; for example, Behling et al. (1997) reported 

that Podocarpus lambertii was the only wind-pollinated 
number 95 • 6 9

species among 97 tree species in a 1 ha plot in southern 

Atlantic rainforest in Brazil. Nanami et al. (2005) investigated the sex ratio in the Japanese podocarp Nageia nagi, 

finding a bias in the number of males, faster growth rate 

in males, and spatial segregation between male and female 

adults. Female trees were also more heavily impacted by 

neighbor competition. No similar studies have been conducted for podocarps in tropical forests. 

Podocarp seeds are dispersed by birds, and perhaps 

some small mammals, which are attracted by the typically 

single-seeded fleshy fruit and/or swollen bract. Fruiting 

structures range from green to red or purple in color. Seed 

production varies considerably among species, being recorded as infrequent or even rare in some cases (e.g., P. neriifolius in Vietnam). Germination of tropical podocarp 

species is usually rapid, ranging from 20 to 60 days for 

Dacrycarpus imbricatus, Nageia fleuryi, and P. neriifolius,

with seeds then losing viability so that there is no persistent soil-stored seed bank. Baskin and Baskin (2001) noted 

that the widespread and common Dacrycarpus imbricatus

and Podocarpus neriifolius exhibit morphological dormancy (underdeveloped embryos at time of dispersal) but 

that germination can occur within four weeks of dispersal, 

whereas the rare and endangered Dacrydium comosum

exhibits morphophysiological dormancy, requiring both 

growth of the embryo to critical size and breakdown of 

physiological dormancy, thus slowing germination. Delayed seed germination, sometimes exceeding one year 

(Enright and Cameron, 1988; Geldenhuys, 1993), and a 

requirement for cold stratification have been reported for 

a number of temperate podocarps (Fountain and Outred, 

1991) but are unlikely for tropical species. Seed germination ex situ has proven difficult in some other tropical 

species; for example, Doust et al. (2006) were unable to 

germinate cleaned seeds of Sundacarpus amarus in a study 

of rainforest restoration procedures in northeast Australia. This species is thought to be dispersed by the flightless 

cassowary, a tropical forest bird species now in significant 

decline due to forest fragmentation, logging, and other 

human impacts (Westcott et al., 2005). Cassowaries are 

considered to be important in the dispersal of >100 species of rainforest trees in northeast Australia and New 

Guinea, and their loss as a dispersal vector may seriously 

impact the future abundance and genetic structure of such 

species (Stocker and Irvine, 1983; Mack, 2006). Cordiero 

and Howe (2002) documented significantly lower rates 

of seedling recruitment in plant species dependent upon 

fruit-eating animals for seed dispersal (relative to wind 

and gravity dispersal species) in small versus large forest 

fragments for a tropical submontane forest in Tanzania, 

with primate and bird counts confirming frugivore species 

decline with decreasing fragment size.

Masting has been well documented for many temperate podocarps and is also likely among tropical species, especially given its occurrence in other tropical conifer taxa, 

such as Araucaria. Chalwell and Ladd (2005) suggested 

that synchronized high cone and pollen production years 

may be beneficial to dioecious understory plants (such 

as Podocarpus drouynianus in southwestern Australia; 

see Ladd and Enright, this volume), which are dependent 

upon wind dispersal of pollen in a low-wind environment. 

Although the tropical podocarps may be canopy trees, 

their low density provides a similar context within which 

one might argue that mast strobili and coning years would 

best ensure pollination of low-abundance, coning trees. 

However, parentage could be asymmetrical; female trees 

of both canopy and subcanopy size may receive pollen, 

but only canopy males may successfully disperse pollen to 

them if pollen dispersal in subcanopy males is limited by 

reduced atmospheric turbulence. Over what distances predominantly understory podocarps of closed forests successfully disperse pollen is unknown. Behling et al. (1987) 

measured pollen rain in traps distributed systematically 

through a 1 ha Atlantic rainforest plot in Brazil containing four Podocarpus lambertii trees. Pollen influx for the 

podocarps was generally low but highly variable across 

the plot, with distinctly higher values at two pollen trap 

sites (presumably close to pollen-producing trees). They 

concluded that pollen transport among rainforest trees 

can often be very limited and short distance.

In the absence of a persistent soil seed bank, potential 

recruits to the subcanopy, and eventually the canopy, of 

the forest must accumulate and persist in a seedling bank 

in the low-light environment of the forest understory. 

Data for size frequency distributions of podocarps in tropical forests are as infrequent as the species themselves and 

are generally restricted to individuals >5 cm dbh, so that 

there are no data for seedlings and small saplings. Aiba 

et al. (2004) reported size distributions (>5 cm dbh) for 

Dacrycarpus imbricatus and Falcatifolium falciforme in 

tropical montane forest at Mount Kinabalu, and in both 

cases the numbers in the smallest size class were smaller 

than those in some larger classes, suggesting relatively 

poor rates of recruitment in undisturbed forest. Elsewhere, 

Tesfaye et al. (2002) reported “hampered” regeneration in 

Afrocarpus falcatus in montane forests in Ethiopia based 

on size distribution studies, and Arriaga (2000) recorded 

P. matudae as a gap-phase species dependent upon disturbance for recruitment in tropical montane cloud forest at 

Tamaulipas, Mexico. 
7 0 • smithsonian contributions to botany

Persistence and Coexistence

Given the low density of many podocarp species in 

lowland rainforests, it is uncertain how they can persist with the large number of co-occurring tree species, 

many of which show higher levels of fecundity and faster 

growth rates under both high- and low-light conditions. 

This conundrum also applies to rare or infrequent angiosperm species. Rosetto and Kooyman (2005) found that 

persistence of the paleoendemic rainforest tree Eidothea 

hardeniana (Proteaceae) in a subtropical forest in northern New South Wales, Australia, was best explained by 

a combination of large and unpalatable fruits, on the one 

hand, and tolerance facilitated by basal resprouting, on 

the other. On the basis of a life history trait analysis of 258 

local taxa, they concluded that these traits might explain 

the restricted distribution and rarity of a number of other 

locally endemic rainforest species. 

Wright (2002) reviewed mechanisms for coexistence 

in tropical forests, identifying the lack of competition between suppressed understory plants as potentially important, and Russo et al. (2005) reported lower growth and 

mortality rates among trees on infertile soils in lowland 

Bornean rainforest, with increased cost of herbivory on 

resource-poor sites perhaps selecting for better-defended 

and slower-growing taxa, such as conifers. Indeed, among 

lowland forest sites, podocarps achieve their highest densities in low-nutrient swamp and heath forests. These 

findings suggest that podocarp populations in angiospermdominated rainforests are best viewed as stress tolerators, 

characterized by slow growth rate and low mortality rate 

(but also low levels of herbivore damage), largely avoiding competition with faster-growing species through their 

location on low-nutrient sites and in deep shade, where 

angiosperm competitiveness is reduced most strongly. 

Although the development of dense podocarp and other 

conifer species stands in montane forests may be associated 

with large-scale disturbance by storms and fire (e.g., see Enright et al., 1999, on araucarian forest stand dynamics in 

the Southwest Pacific region), the ultimate growth of lowabundance podocarps to the canopy layer in lowland tropical forests most likely depends upon canopy gaps caused 

by the death of individual trees. However, ecophysiological 

evidence suggests that angiosperm competitors should be 

greatly advantaged by any sudden increase in light availability (e.g., Brodribb et al., 2005) and would preempt such 

gaps. Thus, it may take several cycles of gap formation at 

a single location before the subcanopy podocarps are able 

to capture a canopy space, implying the need for markedly 

greater longevity than in co-occurring angiosperm species. 

Indeed, longevity is one of the most obvious differences in life history traits between conifers and comparable angiosperm woody perennial species at a global scale. 

Loehle (1988) compiled typical and maximum life spans, 

time to reproduction, growth rate, and shade tolerance 

for a sample of 44 conifer and 76 angiosperm tree species from North America. These data revealed a median 

longevity of 250 years for angiosperms and 400 years for 

conifers. A list compiled for Southern Hemisphere conifers 

by Enright and Ogden (1995) revealed a strikingly similar 

distribution of maximum longevities but a higher median 

for conifers of 525 years, although some arid-zone conifers 

(e.g., Callitris species of semiarid woodlands in Australia) 

with longevities in the 100- to 300-year range were excluded from consideration. Little additional information 

of relevance has been published since this analysis. Data 

on stem diameter growth rate and maximum recorded tree 

size for three tropical podocarps from Mount Kinabalu 

(Dacrycarpus imbricatus and Falcatifolium falciforme; 

Aiba et al., 2004) and Kalimantan (Nageia wallichiana; 

Nishimua et al., 2007) suggest life spans of 400 years or 

more. Co-occurring angiosperm tree species growth rates 

and tree sizes suggest longevities ranging from less than 

200 years to more than 400 years, so that although most 

angiosperm trees were shorter-lived, at least some were 

likely equally long-lived. Overall, data for forest podocarps suggest that tropical podocarp species of lowland 

and lower montane forests might have longevities in the 

400- to 600-year range (Table 4.2).

Southern Hemisphere conifers also show very high 

nutrient use efficiency for nitrogen and phosphorus relative to most (but not all) angiosperm tree types (Enright 

and Ogden, 1995), although there is little specific evidence for podocarps. The ability to photosynthesize over 

a longer time period per unit of nutrient use (i.e., greater 

leaf longevity) and lower mean leaf nitrogen concentration may be the primary mechanism of increased use efficiency (Chapin, 1980; Enright and Ogden, 1987; Sprugel, 

1989; Becker, 2000). Although very long leaf longevities 

have been shown for araucarians and some other conifer groups, little information is available on leaf longevity 

and nutrient levels for tropical podocarps relative to cooccurring angiosperm trees.

Another question relevant to the dynamics of some 

sparse, lower montane and lowland podocarp populations 

is the extent to which long-distance dispersal of seeds and 

pollen might operate to maintain (or rescue) populations 

that may otherwise decline and disappear. Some podocarp species of lowland forests are broadly distributed 

and are characterized by much greater population sizes 
number 95 • 7 1

and densities at higher altitudes or under specific habitat conditions (e.g., Podocarpus neriifolius occurs from 

sea level to 2,100 m, typically as scattered trees in lowland forests, but at increasing density at higher altitudes 

on dry ridgetops, on infertile soils), and it is not clear to 

what extent the dynamics of sparse lowland populations 

might be supported by inputs from higher-elevation populations or might rely upon local dynamics. The “rescue” 

hypothesis is supported by evidence from Behling et al. 

(1997), who reported pollination of a single individual of 

Araucaria angustifolia in Atlantic rainforest in Brazil from 

long-distance-transported pollen grains that must have 

come from a highland population at least 25 km away. 

This question could readily be addressed by using genetic 

methods to identify both mother (from nuclear microsatellite markers) and father (from chloroplast microsatellite 

markers) plants for each seedling/sapling/small tree encountered, so that the distribution of individuals in relation to pollen and seed dispersal could be analyzed. Such 

analyses would reveal dispersal distances and the extent to 

which pollen and seed is derived within local populations 

(e.g., see Godoy and Jordano, 2001; Dick et al., 2003). 

SYNTHESIS

The ecology of podocarps in tropical forests of New 

Caledonia and the Malesian region is massively understudied relative to that for their temperate counterparts 

in New Zealand, Tasmania, South Africa, and South 

America. This is particularly true for species present in 

low-density populations of lowland and lower montane 

angiosperm-dominated forests and reflects both the significant problems of studying low-abundance species in 

situ and the demand for scientific attention from the many 

competing (including more abundant and more economically important) species in these high-diversity ecosystems. 

Field studies of low-abundance tree species are difficult; 

trees are hard to locate (and to relocate), sample sizes are 

small, and study sites are large (and therefore often highly 

TABLE 4.2. Selected life history properties of Southern Hemisphere podocarps (modified from Enright and 

Ogden, 1995). Data are from Palmer and Pitman (1972), Ogden (1978,) Veblen et al. (1981), Ash (1985), 

Norton et al. (1988), Lusk and Ogden (1992), Enright et al. (1995), McCoy (1998), Aiba et al. (2004), and 

Nishimua et al. (2007).

Longevity Growth Shade

Species Location (years) rate a tolerance b

Afrocarpus falcatus South Africa 700 2 3

Dacrycarpus dacrydioides New Zealand 600 1 2

D. imbricatus Borneo 400 c 2 2

Dacrydium araucarioides New Caledonia 200 1 1

D. cupressinum New Zealand 1,160 2 3

D. nidulum New Guinea 363 3 3

Falcatifolium falciforme Borneo 400 c 1 3

Nageia wallichiana Borneo 400 c 2 3

Podocarpus hallii New Zealand 555 2 2

P. latifolius South Africa 500 2 4

P. lawrencei SE Australia 460 1 2

P. nubigenus South America 400 3 3

P. totara New Zealand 890 2 2

Prumnopitys ferruginea New Zealand 771 1 4

P. ladei SE Australia 600 2 3 

P. taxifolia New Zealand 1,013 1 2

Saxegothaea conspicua South America 400 3 4

a Scale: 1 = <1 mm year-1

, 2 = 1–2 mm year-1, 3 = 2–3 mm year-1. b Scale: 1 = intolerant (full light) to 4 = tolerant.

c Longevities based on growth rate and stem diameter data.
7 2 • smithsonian contributions to botany

heterogeneous), complicating data collection, analysis, 

and interpretation in relation to basic questions concerning their ecology and demography. Although some components of these species’ life histories might be explored ex 

situ, including seed viability and germination and seedling 

growth/ecophysiology in relation to key environmental 

gradients (light, nutrients), and other information might 

be obtained from analyses of wood and leaf properties, 

most parts of their life histories (particularly pollen and 

seed dispersal, recruitment, growth and survivorship) 

must be examined in situ if we are to understand how and 

why they are able to persist at low density in angiospermdominated stands. 

In this review we have sought to detail what is known 

about the distribution and ecology of podocarps in tropical and subtropical vegetation types of the Malesian region and why podocarp species are distributed in this way. 

A lack of data from field-based investigations means that 

conclusions about drivers of population dynamics often 

must be inferred using data from ex situ experiments on 

seeds and seedlings and in situ studies for other (better 

studied) conifers and some angiosperm tree species characterized by (analogous) low density in tropical forests. Our 

conclusions largely support the hypotheses proposed by 

Midgley and Bond (1989) and Wright (2002) and the conclusions of experimental studies of seedling physiology by 

Brodribb and colleagues (Brodribb and Hill, 1998, 1999, 

2004; Brodribb et al., 2005). Podocarps are often most 

abundant at sites where the growth of competing species is 

limited. However, their high species diversity in the Malesian region and the broad range of vegetation types and 

environments in which they are found suggest that they 

are a highly successful plant group that has adapted to 

a remarkably broad range of environmental conditions. 

Nevertheless, detailed field investigations of species demographies (including genetic marker studies of pollen 

and seed dispersal) are required urgently in order to establish a sound understanding of tropical podocarp ecology 

and to explain their population dynamics and the circumstances facilitating their recruitment and persistence.

APPENDIX

TABLE 4.A1. Podocarp species of the tropical and subtropical Malesian region. Data were compiled from de Laubenfels (1969, 1985, 

1987, 1988, 2003, 2005), Silba (1986, 1987), Enright and Hill (1995), Farjon (2008), and the Gymnosperm Database, http://www.conifers

.org/index.html.

Genus and speciesTongaFijiNew CaledoniaVanuatuSolomon IslandsNE AustraliaNew GuineaMoluccasSulawesiSunda IslandsBorneoSumatraMalayaVietnamLaosThailandCambodiaAssamIndiaNepalChinaPhilippinesTaiwanBurma

Acmopyle Pilg. 

A. pancheri - - 1 - - - - - - - - - - - - - - - - - - - - -

A. sahniana Buchh. & Gray - 1 - - - - - - - - - - - - - - - - - - - - - -

Dacrycarpus (Endl.) de Laub.

D. cinctus (Pilg.) de Laub. - - - - - - 1 1 1 - - - - - - - - - - - - - - -

D. compactus (Wassch.) de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

D. cumingii (Parl.) de Laub. - - - - - - - - - - 1 1 - - - - - - - - - 1 - -

D. expansus de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

D. imbricatus (Blume) de Laub. - 1 - 1 1 - 1 1 1 1 1 1 1 1 1 - - - - - 1 1 - 1

D. kinabaluensis (Wassch.) de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

D. steupii (Wassch.) de Laub. - - - - - - 1 - 1 - 1 - - - - - - - - - - - - -

D. vieillardii - - 1 - - - - - - - - - - - - - - - - - - - - -

Dacrydium Soland.

D. araucarioides - - 1 - - - - - - - - - - - - - - - - - - - - -

D. balansae - - 1 - - - - - - - - - - - - - - - - - - - - -

(continued)
number 95 • 7 3

D. beccarii Parl. - - - - 1 - 1 1 1 - 1 1 1 - - - - - - - - 1 - -

D. comosum Corner - - - - - - - - - - - - 1 - - - - - - - - - - -

D. cornwallianum de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

D. elatum (Roxb.) Wallich - - - - - - - - - - 1 1 1 1 1 - 1 - - - - - - -

D. ericoides - - - - - - - - - - 1 - - - - - - - - - - - - -

D. gibbsiae Stapf. - - - - - - - - - - 1 - - - - - - - - - - - - -

D. gracile de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

D. guillauminii - - 1 - - - - - - - - - - - - - - - - - - - - -

D. leptophyllum (Wassch.) de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

D. lycopodioides - - 1 - - - - - - - - - - - - - - - - - - - - -

D. magnum de Laub. - - - - 1 - - 1 - - - - - - - - - - - - - - - -

D. medium de Laub. - - - - - - - - - - - 1 1 - - - - - - - - - - -

D. nausoriense de Laub. - 1 - - - - - - - - - - - - - - - - - - - - - -

D. nidulum de Laub. - 1 - - 1 - 1 - 1 1 - - - - - - - - - - - - - -

D. novo-guineense Gibbs. - - - - - - 1 1 1 - - - - - - - - - - - - - - -

D. pectinatum de Laub. - - - - - - - - - - 1 - - - - - - - - - 1 1 - -

D. spathoides de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

D. xanthandrum Pilg. - - - - 1 - 1 - 1 - 1 1 1 - - - - - - - - 1 - -

Falcatifolium de Laub.

F. angustum de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

F. falciforme (Parl.) de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

F. gruezoi de Laub. - - - - - - - - - 1 - - - - - - - - - - - 1 - -

F. papuanum de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

F. taxoides - - 1 - - - - - - - - - - - - - - - - - - - - -

Nageia Gaert.

N. fleuryi (Hickel) de Laub. - - - - - - - - - - - - - 1 1 - 1 - - - 1 - - -

N. formosensis - - - - - - - - - - - - - - - - - - - - - - 1 -

N. maxima (de Laub.) de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

N. motleyi (Parl.) de Laub. - - - - - - - - - - 1 1 1 - - 1 - - - - - - - -

N. nagi (Thunb.) Kuntze - - - - - - - - - - - - - 1 - - - - - - 1 - - -

N. wallichiana (Presl.) O. Kuntze - - - - - - 1 1 1 1 1 1 1 - - 1 - 1 1 - 1 1 - 1

Parasitaxus (Veillard)

P. usta - - 1 - - - - - - - - - - - - - - - - - - - - -

Phyllocladus L. C. et A. Rich

P. hypophyllus - - - - - - 1 1 1 - 1 - - - - - - - - - - 1 - -

Podocarpus L. Herit. ex Pers.

P. affinis Seeman - 1 - - - - - - - - - - - - - - - - - - - - - -

P. annamiensis - - - - - - - - - - - - - 1 - - - - - - 1 - - -

P. archiboldii Gray - - - - - - 1 - - - - - - - - - - - - - - - - -

P. atjehensis (Wassch.) de Laub. - - - - - - 1 - - - - 1 - - - - - - - - - - - -

P. beecherae - - 1 - - - - - - - - - - - - - - - - - - - - -

TABLE 4.A1. (Continued)

Genus and speciesTongaFijiNew CaledoniaVanuatuSolomon IslandsNE AustraliaNew GuineaMoluccasSulawesiSunda IslandsBorneoSumatraMalayaVietnamLaosThailandCambodiaAssamIndiaNepalChinaPhilippinesTaiwanBurma

(continued)
7 4 • smithsonian contributions to botany

TABLE 4.A1. (Continued)

Genus and speciesTongaFijiNew CaledoniaVanuatuSolomon IslandsNE AustraliaNew GuineaMoluccasSulawesiSunda IslandsBorneoSumatraMalayaVietnamLaosThailandCambodiaAssamIndiaNepalChinaPhilippinesTaiwanBurma

P. borneensis de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

P. bracteatus Blume - - - - - - - - - 1 - 1 - - - - - - - - - - - -

P. brassii Pilg. - - - - - - 1 - - - - - - - - - - - - - - - - -

P. brevifolius (Stapf.) Foxw. - - - - - - - - 1 1 1 1 - 1 - - - - - - 1 1 - -

P. chinensis - - - - - - - - - - - - - - - - - - - - 1 - - 1

P. chingianus - - - - - - - - - - - - - - - - - - - - 1 - - -

P. colliculatus - - 1 - - - - - - - - - - - - - - - - - - - - -

P. confertus de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

P. costalis C. Presl. - - - - - - - - - - - - - - - - - - - - - 1 1 -

P. crassigemmis de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

P. decumbens - - 1 - - - - - - - - - - - - - - - - - - - - -

P. deflexus Ridley - - - - - - - - - - - 1 1 - - - - - - - - - - -

P. degeneri (Gray) de Laub. - 1 - - - - - - - - - - - - - - - - - - - - - -

P. dispermus White - - - - - 1 - - - - - - - - - - - - - - - - - -

P. elatus R. Brown ex Endl. - - - - - 1 - - - - - - - - - - - - - - - - - -

P. fasciculus de Laub. - - - - - - - - - - - - - - - - - - - - - - 1 -

P. gibbsiae Gray - - - - - - - - - - 1 - - - - - - - - - - - - -

P. glaucus Foxw. - - - - 1 - 1 1 - - - - - - - - - - - - - 1 - -

P. globulus de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

P. gnidioides - - 1 - - - - - - - - - - - - - - - - - - - - -

P. grayae de Laub. - - - - - 1 - - - - - - - - - - - - - - - - - -

P. insularis de Laub. - - - 1 1 - 1 - - - - - - - - - - - - - - - - -

P. laubenfelsii Tiong - - - - - - - - - - 1 - - - - - - - - - - - - -

P. ledermannii Pilg. - - - - - - 1 - - - - - - - - - - - - - - - - -

P. levis de Laub. - - - - - - 1 1 1 - 1 - - - - - - - - - - - - -

P. longefoliolatus - - 1 - - - - - - - - - - - - - - - - - - - - -

P. lophatus de Laub. - - - - - - - - - - - - - - - - - - - - - 1 - -

P. lucienii - - 1 - - - - - - - - - - - - - - - - - - - - -

P. macrocarpus de Laub. - - - - - - - - - - - - - - - - - - - - - 1 - -

P. macrophyllus (Thunb.) Sweet - - - - - - - - - - - - - - - - - - - - 1 - 1 1

P. micropedunculatus de Laub. - - - - - - - - - - 1 - - - - - - - - - - - - -

P. nakaii Hayata - - - - - - - - - - - - - - - - - - - - - - 1 -

P. neriifolius Don ex Lamb. - 1 - - 1 - 1 1 1 - 1 1 1 1 - 1 - 1 - 1 - 1 - -

P. novae-caledoniae - - 1 - - - - - - - - - - - - - - - - - - - - -

P. palawanensis - - - - - - - - - - - - - - - - - - - - - 1 - -

P. pallidus Gray 1 - - - - - - - - - - - - - - - - - - - - - - -

P. pilgeri Foxw. - - - - 1 - 1 1 1 - 1 - - - - 1 1 - - - 1 1 - -

P. polyspermus - - 1 - - - - - - - - - - - - - - - - - - - - -

P. polystachyus R. Brown ex Endl. - - - - - - 1 1 - - 1 - 1 - - 1 - - - - - 1 - -

P. pseudobracteatus de Laub. - - - - - - 1 - - - - - - - - - - - - - - - - -

P. ridleyi (Wassch.) Gray - - - - - - - - - - - - 1 - - - - - - - - - - -

(continued)
number 95 • 7 5

REFERENCES

Adam, P. 1992. Australian Rainforests. Oxford Monographs on Biogeography, No. 5. Clarendon Press, Oxford, UK.

Aiba, S.-I., and K. Kitayama. 1999. Structure, Composition and Species 

Diversity in an Altitude-Substrate Matrix of Rain Forest Tree Communities on Mount Kinabalu, Borneo. Pl. Ecol. 140: 139–157.

Aiba, S.-I., K. Kitayama, and M. Takyu. 2004. Habitat Associations 

with Topography and Canopy Structure of Tree Species in a Tropical Montane Forest on Mount Kinabalu, Borneo. Pl. Ecol. 174: 

147–161.

Arriaga, L. 2000. Gap-Building-Phase Regeneration in a Tropical Montane Cloud Forest of North-eastern Mexico. J. Trop. Ecol. 16: 

535–562.

Ash, J. 1985. Growth Rings and Longevity in Agathis vitiensis (Seeman) 

Benth. and Hook. f. ex Drake in Fiji. Austral. J. Bot. 33: 82–88.

Baskin, C. C., and J. M. Baskin. 2001. Seeds: Ecology, Biogeography 

and Evolution of Dormancy and Germination. Academic Press, San 

Diego. 

Becker, P. 2000. Competition in the Regeneration Niche between Conifers and Angiosperms: Bond’s Slow Seedling Hypothesis. Funct. 

Ecol. 41: 401–412.

Behling, H., R. R. B. Negrelle, and P. A. Colinvaux. 1997. Modern Pollen 

Rain Data from the Tropical Atlantic Rain Forest, Reserva Volta 

Velha, South Brazil. Rev. Palaeobot. Palynol. 97: 287–299.

Bond, W. J. 1989. The Tortoise and the Hare: Ecology of Angiosperm 

Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 

227–249.

Brodribb, T. J. 2011 (this volume). A Functional Analysis of Podocarp 

Ecology. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 165–173. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Brodribb, T., and R. S. Hill. 1998. The Photosynthetic Drought Physiology of a Diverse Group of Southern Hemisphere Conifer Species 

Is Correlated with Minimum Seasonal Rainfall. Funct. Ecol. 12: 

465–471.

Brodribb, T., and R. S. Hill. 1999. The Importance of Xylem Constraints 

in the Distribution of Conifer Species. New Phytol. 143: 365–372.

Brodribb, T., and R. S. Hill. 2004. The Rise and Fall of the Podocarpaceae in Australia. In The Evolution of Plant Physiology, A. R. 

Hemsley and I. Poole, eds., pp. 381–400. Elsevier, London.

Brodribb, T. J., N. M. Holbrook, and R. S. Hill. 2005. Seedling Growth 

in Conifers and Angiosperms: Impacts of Contrasting Xylem Structure. Austral. J. Bot. 53: 749–755.

TABLE 4.A1. (Continued)

Genus and speciesTongaFijiNew CaledoniaVanuatuSolomon IslandsNE AustraliaNew GuineaMoluccasSulawesiSunda IslandsBorneoSumatraMalayaVietnamLaosThailandCambodiaAssamIndiaNepalChinaPhilippinesTaiwanBurma

P. rotundus de Laub. - - - - - - - - - - 1 - - - - - - - - - - 1 - -

P. rubens de Laub - - - - - - 1 - 1 1 - 1 - - - - - - - - - - - -

P. rumphii Blume - - - - - - - - - - - - - - - - - - - - - 1 1 -

P. salomoniensis Wassch. - - - - 1 - - - - - - - - - - - - - - - - - - -

P. smithii de Laub. - - - - - 1 - - - - - - - - - - - - - - - - - -

P. spathoides - - - - 1 - 1 1 - - - - 1 - - - - - - - - - - -

P. subtropicalis - - - - - - - - - - - - - - - - - - - - 1 - - -

P. sylvestris - - 1 - - - - - - - - - - - - - - - - - - - - -

P. teysmannii Miquel - - - - - - - - - - - 1 1 - - - - - - - - - - -

Prumnopitys Philippi

P. ferruginoides - - 1 - - - - - - - - - - - - - - - - - - - - -

P. ladei (Bailey) de Laub. - - - - - 1 - - - - - - - - - - - - - - - - - -

Retrophyllum C. N. Page

R. comptonii - - 1 - - - - - - - - - - - - - - - - - - - - -

R. minus - - 1 - - - - - - - - - - - - - - - - - - - - -

R. vitiense (Seem.) C. N. Page - 1 - - - - 1 1 - - - - - - - - - - - - - - - -

Sundacarpus (Buchh. & Gray) C. N. Page

S. amarus (Blume) C. N. Page - - - - - 1 1 1 1 1 1 1 - - - - - - - - - 1 - -

TOTAL SPECIES 1 8 20 2 11 6 31 15 15 8 30 16 14 7 3 5 3 2 1 1 12 20 6 4

TOTAL GENERA 1 5 8 2 3 4 8 7 6 6 7 5 4 4 3 2 3 2 1 1 4 7 2 3
7 6 • smithsonian contributions to botany

Bruenig, E. F. 1990. Oligotrophic Forested Wetlands in Borneo. In Volume 

15: Forested Wetlands, A. E. Lugo, M. Brinson, and S. Brown, eds., 

pp. 299–334, Ecosystems of the World. Elsevier Science, New York. 

Burns, B. R. 1991. Regeneration Dynamics of Araucaria. Ph.D. thesis, 

Department of Geography, University of Colorado, Boulder.

Cao, K.-F. 2000. Leaf Anatomy and Chlorophyll Content of 12 Woody 

Species in Contrasting Light Conditions in a Bornean Heath Forest. 

Canad. J. Bot. 78: 1245–1253.

Chalwell, S. T. S., and P. G. Ladd. 2005. Stem Demography and Post 

Fire Recruitment of Podocarpus drouynianus: A Resprouting Nonserotinous Conifer. Bot. J. Linn. Soc. 149: 433–449.

Chapin, F. S. 1980. The Mineral Nutrition of Wild Plants. Annual Rev. 

Ecol. Syst. 11: 233–260.

Clayton-Green, K. A. 1977. Structure and Origin of Libocedrus bidwillii

Stands in the Waikato District, New Zealand. New Zealand J. Bot. 

15: 19–28.

Coomes, D. A. R. B. Allen, W. A. Bentley, L. E. Burrows, C. D. Canham, L. Fagan, D. M. Forsyth, A. Gaxiola-Alcantar, R. L. Parfitt, 

W. A. Ruscoe, D. A. Wardle, D. J. Wilson, and E. F. Wright. 2005. 

The Hare, the Tortoise and the Crocodile: The Ecology of Angiosperm Dominance, Conifer Persistence and Fern Filtering. J. Ecol.

93: 918–935.

Cordiero, N. J., and H. F. Howe. 2002. Low Recruitment of Trees Dispersed by Animals in African Forest Fragments. Conservation Biol. 

15: 1733–1741.

de Laubenfels, D. 1969. A Revision of the Malesian and Pacific Rainforest Conifers. 1. Podocarpaceae. J. Arnold Arbor. 50: 274–369.

de Laubenfels, D. 1985. A Taxonomic Revision of the Genus Podocarpus. Blumea 30: 251–278.

de Laubenfels, D. 1987. Revision of the Genus Nageia (Podocarpaceae). 

Blumea 32: 209–211.

de Laubenfels, D. 1988. Notes on Asian-Pacific Podocarpaceae: 1 (Podocarpus). Phytologia 64: 290–292.

de Laubenfels, D. J. 2003. A New Species of Podocarpus from the 

Maquis of New Caledonia. New Zealand J. Bot. 41: 715–718.

de Laubenfels, D. J. 2005. Statut du Podocarpus de l’Île des Pins 

(Nouvelle-Caledonie). Adansonia 27: 151–153.

Dick, C. W., G. Etchelecu, and F. Austerlitz. 2003. Pollen Dispersal of 

Tropical Trees (Dinizia excelsa: Fabaceae) by Native Insects and 

African Honeybees in Oristine and Fragmented Amazonian Rainforest. Molec. Ecol. 12: 753–764.

Doust, S. J., P. D. Erskine, and D. Lamb. 2006. Direct Seeding to Restore 

Rainforest Species: Microsite Effects on the Early Establishment 

and Growth of Rainforest Tree Seedlings on Degraded Land in the 

Wet Tropics of Australia. Forest Ecol. Managem. 234: 333–343.

Drake, D. 1996. Rainforest Vegetation of ‘Eua Island, Kingdom of 

Tonga. New Zealand J. Bot. 34: 65–77.

Enright, N. J. 1995. Conifers of Tropical Australasia. In Ecology of the 

Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 197–222. 

Melbourne University Press, Carlton, Australia.

Enright, N. J., and E. C. Cameron. 1988. The Soil Seed Bank of a Kauri 

(Agathis australis) Forest Remnant Near Auckland, New Zealand. 

New Zealand J. Bot. 26: 223–236. 

Enright, N. J., and C. Gosden. 1992. Unstable Archipelagos: Southwest 

Pacific Environment and Prehistory Since 30,000 Years B.P. In The 

Näive Lands: Human–Environment Interactions in Australasia, 

J. R. Dodson, ed., pp. 160–198. Longmans, Sydney, Australia. 

Enright, N. J., and R. S. Hill. 1995. Ecology of the Southern Conifers. 

Melbourne University Press, Carlton, Australia.

Enright, N. J., and J. Ogden. 1987. Decomposition of Litter from Common Woody Species in Kauri (Agathis australis) Forest in Northern 

New Zealand. Austral. J. Ecol. 12: 109–124.

Enright, N. J. and J. Ogden. 1995. The Southern Conifers—A Synthesis. 

In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, 

eds., pp. 271–287. Melbourne University Press, Carlton, Australia.

Enright, N. J., J. Ogden, and L. S. Rigg. 1999. Dynamics of Forests with 

Araucariaceae in the Western Pacific. J. Veg. Sci. 10: 793–804.

Farjon, A. 1998. World Checklist and Bibliography of Conifers. Royal 

Botanic Gardens, Kew, Richmond, Surrey, UK.

Farjon, A. 2008. A Natural History of Conifers. Timber Press, Portland, 

Oregon.

Farjon, A., and C. N. Page. 1999. Status Survey and Conservation Action 

Plan: Conifers. IUCN, Gland, Switzerland.

Field, T. S., and T. J. Brodribb. 2005. A Unique Mode of Parasitism in 

the Conifer Coral Tree Parasitaxus ustus (Podocarpaceae). Pl. Cell 

Environ. 28: 1316–1325. 

Fountain, D. W., and H. A. Outred. 1991. Germination Requirements 

of New Zealand Native Plants: A Review. New Zealand J. Bot. 29: 

311–316.

Geldenhuys, C. J. 1993. Reproductive Biology and Population Structures 

of Podocarpus falcatus and P. latifolius in the Southern Cape Forest. Bot. J. Linn. Soc. 112: 59–74.

Godoy, J. A., and P. Jordano. 2001. Seed Dispersal by Animals: Exact 

Identification of Source Trees with Endocarp DNA Microsatellites. 

Molec. Ecol. 10: 2275–2283.

Grandcolas, P., J. Murienne, T. Robillard, L. Desutter-Grandcolas, 

H. Jourdan, E. Guilbert, and L. Deharveng. 2008. New Caledonia: A Very Old Darwinian Island? Philos. Trans. Roy. Soc. B 363: 

3309–3317.

Grime, J. P. 1979. Plant Strategies and Vegetation Processes. John Wiley 

and Sons, New York. 

Haig, D., and M. Westoby. 1991. Seed Size, Pollination Costs and Angiosperm Success. Evol. Ecol. 5: 231–247.

Herbert, J., P. M. Hollingsworth, M. F. Gardner, R. R. Mill, P. I. Thomas, 

and T. Jaffré. 2002. Conservation Genetics and Phylogenetics of 

New Caledonian Retrophyllum (Podocarpaceae) species. New Zealand J. Bot. 40: 175–188.

Hope, G. S. 1976. Vegetation. In The Equatorial Glaciers of New 

Guinea, G. S. Hope, J. A. Peterson, U. Radok, and I. Allison (eds.), 

pp. 113–172. A. A. Balkema, Rotterdam.

Jaffré, T. 1980. Etude écologique du peuplemnt végétal des sols deérivés 

de roches ultrabasiques en Nouvelle-Calédonie. Travaux et Document de l’ORSTOM, No. 124. ORSTOM, Paris.

Jaffré, T. 1993. The Relationship between Ecological Diversity and Floristic Diversity in New Caledonia. Biodivers. Lett. 1: 82–87.

Jaffré, T. 1995. Distribution and Ecology of the Conifers of New Caledonia. In Ecology of the Southern Conifers, N. J. Enright and R. S. 

Hill, eds., pp. 171–196. Melbourne University Press, Carlton, 

Australia.

Johns, R. J. 1976. A Classification of the Montane Forests of Papua New 

Guinea. Sci. New Guinea 4: 105–127.

Johns, R. J. 1982. Plant Zonation. In Biogeography and Ecology of New 

Guinea, J. L. Gressitt, ed., pp. 309–330. Monographiae Biologicae, 

No. 42. W. Junk, The Hague, Netherlands. 

Kershaw, A. P. 1988. Australasia. In Vegetation History, B. Huntley and 

T. Webb III, eds., pp. 237–306. Kluwer Academic Publishers, Dordrecht, Netherlands. 

Kettle, C. J., P. M., Hollingsworth, T. Jaffre, B. Moran, and R. A. Ennos. 2007. Identifying the Early Genetic Consequences of Habitat 

Degradation in a Highly Threatened Tropical Conifer, Araucaria 

nemorosa Laubenfels. Molec. Ecol. 16: 3581–3591.

Kitayama, K. 1992. An Altitudinal Transect Study of the Vegetation on 

Mount Kinabalu, Borneo. Vegetatio 102: 149–171.

Kitayama, K., S. Aiba, M. Ushio, T. Seino, and Y. Fujiki. 2011 (this 

volume). The Ecology of Podocarps in Tropical Montane Forests 

of Borneo: Distribution, Population Dynamics, and Soil Nutrient 

Acquisition. In Ecology of the Podocarpaceae in Tropical Forests, 

B. L. Turner and L. A. Cernusak, eds., pp. 101–117. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.
number 95 • 7 7

Köpke, E., L. J. Musselman, and D. J. de Laubenfels. 1981. Studies on 

the Anatomy of Parasitaxus ustus and Its Root Connections. Phytomorphology 31: 85–92.

Kuang, S. W., H. Gillett, and S. Ferriss. 2006. Strategies for the Sustainable Use and Management of Timber Tree Species Subject to International Trade: South East Asia. Report (un-numbered). UNEP–

WCMC, Cambridge, UK. 

Ladd, P. G., and N. J. Enright. 2011 (this volume). Ecology of FireTolerant Podocarps in Temperate Australian Forests. In Ecology of 

the Podocarpaceae in Tropical Forests, ed. B. L. Turner and L. A. 

Cernusak, pp. 141–155. Smithsonian Contributions to Botany, No. 

95. Smithsonian Institution Scholarly Press, Washington, D.C.

Lara, A. 1991. The Dynamics and Disturbance Regimes of Fitzroya cupressoides Forests in the South-Central Andes of Chile. Ph.D. thesis, Department of Geography, University of Colorado, Boulder.

Loehle, C. 1988. Tree Life History Strategies: The Role of Defenses. Canad. J. Forest Res. 18: 209–222.

Lusk, C., and J. Ogden. 1992. Age Structure and Dynamics of a Podocarp–Broadleaf Forest in Tongariro National Park, New Zealand. 

J. Ecol. 80: 379–393.

Mack, A. L. 2006. Distance and Non-randomness of Seed Dispersal by 

the Dwarf Cassowary Casuarius bennetti. Ecography 18: 286–295.

McCoy, S. 1998. The Dynamics of Gymnostoma Maquis on Ultramafic 

Soils in New Caledonia. Ph.D. thesis, Department of Archaeology 

and Natural History, Australian National University, Canberra.

McCoy, S., T. Jaffré, F. Rigault, and J. E. Ash. 1999. Fire and Succession in the Ultramafic Maquis of New Caledonia. J. Biogeogr. 26: 

579–594.

Midgley, J. J. 1991. How Important is Biotic Pollination and Dispersal to 

the Success of the Angiosperms? Philos. Trans. Roy. Soc. London, 

Ser. B 333: 209–215.

Midgley, J. J., and W. J. Bond. 1989. Evidence from South African Coniferales for the Historical Decline of the Gymnosperms. S. African 

J. Sci. 85: 81–84.

Miyamoto, K., J. S. Rahajoe, and T. Kohyama. 2007. Forest Structure 

and Primary Productivity in a Bornean Heath Forest. Biotropica

39: 35–42.

Moyersoen, B., P. Becker, and I. J. Alexander. 2001. Are Ectomycorrhizas 

More Abundant Than Arbuscular Mycorrhizas in Tropical Heath 

Forests? New Phytol. 150: 591–599.

Nanami, S., H. Kawaguchi, and T. Yamakura. 2005. Sex Ratio and 

Gender-Dependent Neighbouring Effects in Podocarpus nagi, a Dioecious tree. Pl. Ecol. 177: 209–222.

Nasi, R., T. Jaffré, and J.-M. Sarrailh. 2002. Les forêts de montages de la 

Nouvelle-Calédonie. Bois Forêts Trop. 274: 5–18.

Newbery, D. McC. 1991. Floristic Variation within Kerangas (Heath) 

Forest: Re-evaluation of Data from Sarawak and Brunei. Pl. Ecol. 

96: 43–86.

Newbery, D. McC., E. Renshaw, and E.F. Brünig. 1986. Spatial Pattern 

of Trees in Kerangas Forest, Sarawak. Pl. Ecol. 65: 77–89.

Nishimua, T. B., E. Suzuki, T. Kohyama, and S. Tsuyuzaki. 2007. Mortality and Growth of Trees in Peat-Swamp and Heath Forests in 

Central Kalimantan after Severe Drought. Pl. Ecol. 188: 165–177.

Norton, D. A., J. W. Herbert, and A. E. Beveridge. 1988. The Ecology 

of Dacrydium cupressinum: A Review. New Zealand. J. Bot. 26: 

37–62.

Ogden, J. 1978. On the Dendrochronological Potential of Australian 

Trees. Austral. J. Ecol. 3: 339–356.

Ogden, J. 1985. An Introduction to Plant Demography with Special Reference to New Zealand Trees. New Zealand J. Bot. 23: 751–772.

Paijmans, K. 1976. New Guinea Vegetation. Australian National University Press, Canberra.

Palmer, E., and P. Pittman. 1972. Trees for Southern Africa, Covering All 

Known Indigenous Species in RSA, South West Africa, Botswana, 

Lesotho and Swaziland. A. A. Balkema, Cape Town, South Africa.

Pammenter, N. W., G. F. Midgley, and W. J. Bond. 2004. Xylem Hydraulics and Angiosperm Success: A Test Using Broad-Leafed Species. 

In The Evolution of Plant Physiology, A. R. Hemsley and I. Poole, 

eds., pp. 259–272. Elsevier, Amsterdam Netherlands. 

Pascal, M., B. R. De Forges, H. Le Guyader, and D. Simberloff. 2008. 

Mining and Other Threats to the New Caledonia Biodiversity 

Hotspot. Conservation Biol. 22: 498–499.

Regal, P. 1977. Ecology and the Evolution of Flowering Plant Dominance. Science 196: 622–629.

Riswan, S., and K. Kartawinata. 1991. Species Strategy in Early Stage 

of Secondary Succession Associated with Soil Properties Status in 

a Lowland Mixed Dipterocarp Forest and Kerangas Forest in East 

Kalimantan. Tropics 1: 13–34.

Rosetto, M., and R. M. Kooyman. 2005. The Tension between Dispersal 

and Persistence Regulates the Current Distribution of Rare Palaeoendemic Rainforest Flora: A Case Study. J. Ecol. 93: 906–917.

Rundel, P. W., M. Patterson, K. Boonpragob, and S. Watthana. 2001. 

Photosynthetic Capacity in Thai Conifers. Nat. Hist. Bull. Siam 

Soc. 49: 295–303.

Russo, S. A., S. J. Davies, D. A. King, and S. Tan. 2005. Soil-Related Performance Variation and Distributions of Tree Species in a Bornean 

Rain Forest. J. Ecol. 93: 879–889.

Silba, J. 1986. Encyclopedia Coniferae. Phytologia Memoirs, No. 8.

H. and A. Moldenke, Corvallis, Oregon.

Silba, J. 1987. Notes on Some Conifers Reported from Some Inaccessible 

Areas of the South Pacific. Conifer Soc. Austral. Newslett. 1: 8–10.

Sprugel, D. G. 1989. The Relationship of Evergreenness, Crown Architecture, and Leaf Size. Amer. Naturalist 133: 465–479.

Stewart, G. H., and A. B. Rose. 1989. Conifer Regeneration Failure in 

New Zealand: Dynamics of Montane Libocedrus bidwillii Stands. 

Vegetatio 79: 41–49.

Stocker, G. C., and A.K. Irvine. 1983. Seed Dispersal by Cassowaries 

(Casuarius casuarius) in North Queensland. Biotropica 15: 170–

176.

Tesfaye, G., D. Teketaye, and M. Fetene. 2002. Regeneration of Fourteen Tree Species in Harenna Forest, Southeast Ethiopia. Flora 197: 

461–474.

Thomas, P., K. Sengdala, V. Lamxay, and E. Khou. 2007. New Records 

of Conifers in Cambodia and Laos. Edinburgh J. Bot. 64: 37–44.

Tyree, M. T., S. Patiño, and P. Becker. 1998. Vulnerability to DroughtInduced Embolism of Bornean Heath and Dipterocarp Forest Trees. 

Tree Physiol. 18: 583–588.

Veblen, T. T., C. Donoso, F. M. Schlegel, and B. Escobar. 1981. Forest 

Dynamics in South-Central Chile. J. Biogeogr. 8: 211–247.

Veblen, T. T., and D. C. Lorenz. 1987. Post-Fire Stand Development 

of Austrocedrus-Nothofagus Forests in Patagonia. Vegetatio 73: 

113–126.

Veblen, T. T., and G. H. Stewart. 1982. On the Conifer Regeneration 

Gap in New Zealand: The Dynamics of Libocedrus bidwillii Stands 

on South Island. J. Ecol. 70: 413–436.

Wade, L. K., and D. N. McVean. 1969. Mt Wilhelm Studies I. The Alpine 

and Subalpine Vegetation. Department of Biogeography and Geomorphology Publication, No. BG/1. Australian National University, 

Canberra.

Webb, L. J., and J. G. Tracey. 1981. The Rainforests of Northern Australia. In Australian Vegetation, R. H. Groves, ed., pp. 67–101. Cambridge University Press, Cambridge, UK. 

Westcott, D. A., J. Bentrupperbäumer, M. G. Bradford, and A. McKeown. 2005. Incorporating Patterns of Disperser Behaviour into 

Models of Seed Dispersal and Its Effects on Estimated Dispersal 

Curves. Oecologia 146: 57–67.

Whitmore, T. C. 1984. Tropical Rainforests of the Far East. 2nd ed. 

Clarendon Press, Oxford, UK.

Wright, S. J. 2002. Plant Diversity in Tropical Forests: A Review of 

Mechanisms of Species Coexistence. Oecologia 130: 1–14.

5 Podocarps in Africa: 

Temperate Zone Relicts 

or Rainforest Survivors?

Hylton Adie and Michael J. Lawes

ABSTRACT. Podocarp distribution in Africa follows a discontinuous mountainous belt 

from Cameroon to Angola in the west and from Ethiopia in the northeast to the southern 

Cape in South Africa. Besides a relict population of Afrocarpus falcatus in coastal lowland forest in northeastern South Africa and southern Mozambique, African podocarps 

are generally limited to highland (Afrotemperate) regions. All podocarps are restricted to 

montane regions in Madagascar. Afrotemperate landscapes are characterized by a patchy 

mosaic of forest and grassland. Processes in the matrix, such as fire, are important drivers 

of forest distribution in the highland regions. Here we examine the relative performance 

of podocarps and angiosperms along an altitudinal gradient from temperate highlands 

to subtropical coastal regions in eastern South Africa. Podocarpus latifolius is a successful component of temperate highland forest, where it dominates old-growth stages. The 

success of podocarps is attributed to their greater longevity and ability to regenerate 

in shade, whereas many potential competing angiosperms are less capable of doing so. 

Regeneration by P. latifolius and associated angiosperms is less successful in high-light 

gap environments, where ferns and grasses suppress establishment. Podocarps are rare 

in coastal scarp forest, where the population is dominated by adult individuals. They 

are unable to regenerate in very deep shade (<3% daylight), which may account for the 

lack of P. latifolius regeneration beneath the dense canopy of coastal scarp forest. Lownutrient soils did not favor podocarps over angiosperms, although the fact that soil nutrients do not appear to be limiting and the scarcity of shade-tolerant angiosperms in forests 

may influence this outcome. The relative role of light and soils on angiosperm-conifer 

competition is unknown for lowland forest, although current evidence from montane 

forests suggests that under prevailing soil conditions, light is the more important axis of 

niche differentiation.

Introduction

The subtropical forests of southern Africa are characterized by a mixed 

angiosperm-Podocarpus composition that ranges along a productivity gradient 

from angiosperm dominance in coastal and mid-altitude (1,100–1,500 m above 

Hylton Adie, School of Biological and Conservation Sciences, Forest Biodiversity Research 

Unit, University of KwaZulu-Natal, Private 

Bag X01, Scottsville 3209, South Africa. Michael J. Lawes, Research Institute for the Environment and Livelihoods, Charles Darwin 

University, Darwin, Northern Territory 0909, 

Australia. Correspondence: Michael.Lawes@cdu

.edu.au.

Manuscript received 13 April 2010; accepted 

9 July 2010.
8 0 • smithsonian contributions to botany

sea level) forests to podocarp dominance in high-altitude 

montane forests. The dynamics of these main components 

are poorly understood, and mechanisms explaining their 

dominance have not been examined in detail (Adie and 

Lawes, 2009a). In temperate forests, the mechanisms 

conferring component dominance are proposed variously 

as climatic and soil nutrient constraints on angiosperm 

seedling growth rates in favor of slow-growing conifers 

at high altitudes (Bond, 1989), conifer shade tolerance 

(Midgley et al., 1990), a less-competitive reproductive 

system in terms of the ability of conifers to colonize or 

capture space relative to most angiosperms (Bond, 1989), 

competitive exclusion of podocarps by the understory vegetation, especially herbs and grasses in more productive 

environments (Midgley and Bond, 1989; Midgley et al., 

1995a), prevention of shade-tolerant conifers from escaping angiosperm competition in deep shade (Coomes et al., 

2005), and the intensity and frequency of large-scale disturbances (Ogden and Stewart, 1995; Ogden et al., 2005). 

In the Southern Hemisphere podocarps appear to have 

the competitive edge relative to associated angiosperms in 

seasonally colder temperate sites that experience periodic 

intense disturbance, and they are a successful component 

of montane forests in tropical latitudes but are rare in lowland tropical forests (Enright, 1995; Enright and Jaffré, 

this volume).

We examined the dynamics of high-altitude podocarps in the subtropics and focused on regeneration patterns of the two principal forest canopy components: 

conifers, represented by Podocarpus latifolius, and angiosperms (all other species). Angiosperms are reported 

to have poor regeneration in many inland forests (Moll, 

1972; Everard et al., 1995; West et al., 2000; Lawes et al., 

2007b), possibly due to shade intolerance (Midgley et al., 

1995b). In a landmark paper, Bond (1989) explored factors limiting the distribution of conifers. He argued that 

faster-growing and competitively superior angiosperms 

outperform conifers in the early regeneration phase, restricting conifers to edaphically or climatically suboptimal sites. Bond’s proposal continues to stimulate interest 

(Becker, 2000; Coomes et al., 2005). In this chapter we 

examine the question: What enables podocarps to persist 

in angiosperm-dominated environments? As an introduction to the African Podocarpaceae we briefly discuss the 

taxonomic status of African and Madagascan species. 

Next, we examine the historical biogeography of African 

Podocarpaceae and propose an explanation for distribution anomalies consistent with differences in dispersal 

and reproductive biology between podocarp taxa. Finally, 

we explore a case study that investigates the regeneration 

ecology in eastern South African montane forests to understand the angiosperm–conifer contest.

Taxonomy

Compared with the rest of the Southern Hemisphere, 

Africa and Madagascar are relatively depauperate in species belonging to the Podocarpaceae (Farjon, 2001; Mill, 

2003). In this review we refer collectively to members of 

African Podocarpaceae as podocarps. Two genera (Afrocarpus, Podocarpus) and 13 to 17 species are recognized 

from the continent and associated islands (Table 5.1). All 

taxa were previously placed in the genus Podocarpus (for 

a recent review see Barker et al., 2004), but recent morphological (Kelch, 1997) and molecular (Kelch, 1998; 

Conran et al., 2000; Sinclair et al., 2002; Barker et al., 

2004) data support the decision to raise the section Afrocarpus to generic level as proposed by Page (1989). 

Afrocarpus is more closely related to the podocarp genera Nageia (Southeast Asia, India, Japan, Philippines, Indonesia) and Retrophyllum (South America, Indonesia, 

New Caledonia) than to the rest of the African species incorporated into Podocarpus (Conran et al., 2000; Sinclair 

et al., 2002). The genus-level identity of podocarp pollen 

is confounded by the failure to separate Podocarpus from 

Afrocarpus in the pollen record. Where podocarps appear 

in West African pollen cores they are assumed to be Podocarpus because of the present West African distribution 

of the genus.

The present status of several podocarp taxa in Africa 

and Madagascar is uncertain. Dowsett-Lemaire and White 

(1990) adopt the view that the four podocarp species from 

South Africa (A. falcatus, P. henkelii, P. latifolius, P. elongatus) are the only true species on mainland Africa. In 

support of this notion, de Laubenfels (1985) considered 

P. ensiculus collected from the western Usambaras of 

Tanzania (Melville, 1954) to be a synonym of P. henkelii,

endemic to the midlands of southeastern South Africa. 

More recently, the henkelii-ensiculus group has been recorded from the highlands of Malawi (Dowsett-Lemaire 

and White, 1990). Farjon (2001) recognizes differences 

between temperate southern Africa and tropical Africa 

by assigning the formerly pan-African species A. falcatus and P. latifolius to southern Africa and acknowledging A. gracilior from east Africa and the central African 

P. milanjianus, respectively. Using DNA sequence data, 

Barker et al. (2004) were unable to separate P. milanjianus from P. latifolius. These authors concede, however, 

that failure to detect sequence differences does not negate 
number 95 • 8 1

species distinctness, given that morphologically distinct 

A. falcatus and A. gracilior have identical markers for the 

same region tested. In this review we consider P. milanjianus to be a synonym of P. latifolius (Drummond, 1975; 

Barker et al., 2004). In Madagascar, de Laubenfels (1985) 

proposed that P. woltzii and P. perrieri be synonymized 

within P. capuronii and P. rostratus, respectively. Stockey 

et al. (1998), however, comment that the rarity of some 

Madagascan podocarp species may have resulted in their 

incorporation into a single taxon. Using cuticle micromorphology, these authors found some evidence to split the 

P. capuronii–P. woltzii and P. rostratus–P. perrieri pairs 

into distinct species.

In Africa, all podocarp species occur in highland regions or, if coastal, then mostly at temperate latitudes 

(e.g., A. falcatus and P. latifolius in the southern Cape). 

The distribution of A. falcatus in coastal lowland forest 

at subtropical latitudes of northeastern South Africa and 

southern Mozambique is unusual and probably relictual, a 

legacy of former cooler periods during the late Pleistocene 

and Holocene (Mazus, 2000; Finch and Hill, 2008; Neumann et al., 2008). Confined to the winter rainfall region 

of the southwestern Cape, P. elongatus is unique among 

African members of the Podocarpaceae in its ability to regenerate from roots (Midgley et al., 1995a).

Biogeography

The earliest records of African taxa possibly belonging to the Podocarpaceae arise in the Jurassic in Morocco, 

followed by Egypt in the Eocene and Ethiopia in the Miocene (Dupéron-Laudoueneix and Dupéron, 1995). Miocene pollen records of Podocarpaceae associated with now 

extinct taxa in the southwestern Cape support the hypothesis of a common Gondwanan flora (Coetzee and Muller, 

1984). Consistent with this proposal are the vicariant 

distributions of A. mannii on São Tomé Island (Maley, 

1996b) in the Gulf of Guinea and podocarp genera on 

Madagascar (Schatz, 1996). With five to seven podocarp 

taxa, Madagascar has been a center of radiation and, 

given its Gondwanan distribution adjacent to East Africa, 

also a site of Afrocarpus radiation, suggesting podocarps 

have expanded their distribution from East Africa. Podocarp fossils first appear in East Africa 14 mya (Bonnefille, 

1994) and in West Africa 2.7 mya (Morley, 2000, 2003, 

this volume).

The distribution of podocarps on mainland Africa 

is reasonably well known, and the family has featured 

prominently in reconstructing paleoenvironments for the 

last 150,000 years. In general, African podocarps are restricted to highland archipelagos (sensu White, 1981) that 

TABLE 5.1. Podocarpaceae species from Africa and Madagascar (after Farjon, 2001).

Species Broad distribution

Afrocarpus dawei East African highlands (Kenya, Tanzania, Uganda, Democratic Republic of the Congo)

Afrocarpus falcatus Southern South Africa (Swellendam) eastwards through highlands of Eastern Cape, KwaZulu-Natal, 

north into Mpumalanga and Northern Province, and into southern Mozambique (coastal)

Afrocarpus gaussenii Eastern plateau of Madagascar

Afrocarpus gracilior Highland regions of Ethiopia, Kenya, Tanzania, Uganda

Afrocarpus mannii São Tomé Island in the Gulf of Guinea

Afrocarpus usambarensis Burundi, Rwanda, Congo, Tanzania

Podocarpus (section Podocarpus)

Podocarpus elongatus Winter rainfall region of Western Cape, South Africa

Podocarpus latifolius Southern South Africa (Swellendam) eastwards through highlands of Eastern Cape, KwaZulu-Natal, 

Mpumalanga, and Northern Province

Podocarpus (section Scytopodium)

Podocarpus capuronii Endemic to Madagascar, mountainous regions

Podocarpus henkelii Highland regions of Eastern Cape and KwaZulu-Natal provinces of South Africa

Podocarpus humbertii Endemic to Madagascar, mountainous regions in north

Podocarpus madagascariensis Endemic to Madagascar

Podocarpus rostratus Endemic to Madagascar, mountainous regions
8 2 • smithsonian contributions to botany

correspond with regions of high species richness and endemism that are considered refuges during extreme paleoclimatic conditions (White, 1981; Maley, 1989; Linder, 

2001; Figure 5.1). The principal Afromontane forest belt 

extends intermittently from Ethiopia southward to the 

southern Cape. Afrocarpus is distributed throughout this 

region but is absent from West Africa. Podocarpus has an 

isolated distribution in West Africa, extending from the 

Cameroon highlands as far south as central Angola, and 

occurs throughout the East African mountain chain but is 

absent from Ethiopia. At the landscape scale, Afromontane forests persist as relatively small patches within a 

grassland or fynbos/heathland matrix (Figure 5.2).

Sharing of Afromontane faunal and floral elements 

between the Cameroon highlands and East Africa has 

long been recognized (Moreau, 1966; Kingdon, 1971; 

FIGURE 5.1. Highland regions in Africa where Afromontane forest is distributed (adapted from 

White, 1981). Areas in red indicate now extinct distributions of what is assumed to be Podocarpus latifolius. Arrows indicate proposed migration route of Afromontane elements from the East 

African highland region into West Africa via the Zambezi-Congo watershed (adapted from Maley, 

1989). The West African distribution of P. latifolius was compiled from multiple sources: western 

Cameroon highlands (Maley and Brenac, 1998), Equatorial Guinea (Parmentier et al., 2001), the 

Chaillu massif in Gabon (Maley et al., 1990), west central highlands (Huambe) of Angola (Huntley 

and Matos, 1994), southeastern Congo highlands (Malaisse, 1967). Pollen cores from multiple 

marine and terrestrial sites in West Africa attest to a former distribution in the Guinean highlands 

(Maley, 1993; Dupont et al., 2000) and the Batéké Plateau of Congo (Elenga et al., 1991).
number 95 • 8 3

White, 1978, 1981; Hamilton, 1989; Dawson and Powell, 1999). An explanation for this disjunct distribution 

is that a direct dispersal corridor opened during drier 

climatic periods (Moreau, 1966; Van Zinderen Bakker, 

1967; Coetzee and Van Zinderen Bakker, 1970; Kingdon, 

1971). On the basis of montane floral elements, however, 

White (1981), and later Maley (1989, 1996a), proposed 

a more southern migration route that avoided the central Congo basin (Figure 5.1). In support of this pathway, 

Linder (2001) recently identified the Zambezi–Congo 

watershed, extending from northern Zambia to central 

Angola, as an important center of plant species diversity 

and endemism.

Determining the timing of migration between East 

and West Africa is difficult given the long history of 

podocarps in West Africa (2.7 mya; Morley, 2000, 2003, 

this volume). Repeated climatic oscillations in the last 

800,000 years, and in particular the last 150,000 years, 

for which the pollen record is well known (Maley, 1993; 

Dupont et al., 2000), provide adequate opportunity for 

biotic movement via the proposed Zambezi–Congo watershed corridor to West Africa. The significant increase 

in montane elements (particularly podocarps) in East Africa from 115,000 to 95,000 years ago reflects the expansion of montane forest taxa to lowland areas associated 

with cooler and dryer conditions (Cohen et al., 2007). At 

FIGURE 5.2. Indigenous forest in KwaZulu-Natal, South Africa, showing the patchy distribution 

at the landscape scale. Sites referred to in the text are Royal Natal (RN), Ongoye (ONG), and Kosi 

Bay (KB).
8 4 • smithsonian contributions to botany

much the same time, two phases of cool and dry conditions (115,000–105,000 and 95,000–85,000 years ago) 

resulted in maximum expansion of montane elements in 

West Africa (Fredoux, 1994; Maley, 1996a; Dupont et al., 

2000). At no stage, even during the Last Glacial Maximum (18,000 years ago), does podocarp pollen dominate 

the record as much as in that earlier time period.

Even though the taxonomy and systematics of African Podocarpaceae require further refinement, the intriguing differences in distribution between Podocarpus and 

Afrocarpus invite speculation. In West Africa, podocarp 

pollen assumed to be P. latifolius was last recorded from 

the Guinean highlands approximately 74,000 years ago 

(Fredoux, 1994; Jahns et al., 1998; Dupont et al., 2000) 

and from the Batéké Plateau in the Congo Republic just 

prior to the Holocene (Elenga et al., 1991). Apart from 

the isolated distribution of A. mannii on São Tomé Island 

in the Gulf of Guinea, Afrocarpus has not been recorded 

from West Africa. Afrocarpus is the only podocarp in 

Ethiopia but coexists with Podocarpus throughout East 

and southern Africa. The absence of Podocarpus from 

Ethiopia is unusual since many common Afromontane 

tree species occur in the region (White, 1978; Dawson 

and Powell, 1999). Regional extinction is plausible given 

the history of local extinction of Podocarpus (assumed) 

in West Africa (Elenga et al., 1991; Dupont et al., 2000). 

The relatively impoverished bird and butterfly faunas of 

Ethiopia and the high endemicity of the latter (Carcasson, 

1964; Moreau, 1966) suggest the region has long been isolated, adding support to the extinction hypothesis. However, shared bird subspecies between Ethiopia and Kenya 

imply a recent biotic exchange (Moreau, 1966), at least 

for vagile animal species, but does not explain the absence 

of P. latifolius, an otherwise widely distributed podocarp, 

from Ethiopia.

A consistent pattern from soil cores in Africa is the 

concomitant increase in podocarp and grass pollen, associated with the regression of rainforest elements (Meadows, 

1984; Fredoux, 1994; Dupont et al., 2000; Neumann et 

al., 2008). Even when an increase in podocarp pollen is associated with a simultaneous decline in grass (e.g., DeBusk, 

1998; Cohen et al., 2007), the proportion of grass in the 

pollen record is still high (20% or more). An abundance of 

grass in pollen cores is always characteristic of open habitats (Vincens et al., 2006) and is frequently associated with 

cooler conditions. In East and West Africa, temperature declines of 4°C or more were associated with the expansion of 

Afromontane elements to lower elevations and the contraction of tropical (lowland) rainforest (Van Zinderen Bakker, 1982; Bonnefille et al., 1990; Maley, 1996a). Given the 

abundance of grass during these cooler periods, Afromontane forest is unlikely to have extended its distribution as a 

continuous belt. Indeed, contemporary Afromontane landscapes are a patchy mosaic of forest and grassland, with 

forest patches usually situated on south-facing slopes or in 

valley heads (Everard, 1986; Meadows and Linder, 1993; 

Adie and Lawes, 2009b; Figure 5.2). Fire in the grassland 

matrix is the dominant process responsible for this patchy 

and isolated distribution of forest (Geldenhuys, 1994). The 

migration of Afrotropical elements during late Pleistocene 

climatic fluctuations is therefore most likely to have followed the “stepping-stone” process (DeBusk, 1998), which 

requires dispersal across an inhospitable grassland matrix. 

This proposal is consistent with the forest-grassland mosaic typical of the Drakensberg Mountains of eastern South 

Africa, where all forest tree species, and especially P. latifolius, persist in fire refugia situated in the grassland matrix 

(Adie and Lawes, 2009b; Figure 5.3). Being bird dispersed 

and capable of rapid germination (4–6 weeks, H. Adie and 

M. J. Lawes, unpublished data; Geldenhuys, 1993) in a 

variety of habitats, P. latifolius displays traits typical of a 

highly vagile species. Podocarpus latifolius, therefore, fits 

the model of a good disperser with a high probability of 

establishment within a grass-dominated environment, provided it can escape fire. However, the species appears to be 

a weak competitor at the regeneration phase when faced 

with lowland angiosperm species (Adie and Lawes, unpublished), which may account for its failure to persist in 

isolated refuges once warmer conditions return that favor 

lowland forest species.

In contrast to Podocarpus, the absence of Afrocarpus

west of the Eastern Afromontane chain suggests this taxon 

never extended farther westward. We propose that the 

westward expansion of Afrocarpus has been constrained 

by its reproductive biology. Dispersed by birds, bats, 

monkeys, and baboons (Geldenhuys, 1993; Teketay and 

Granstrom, 1997; Negash, 2003; Hitimana et al., 2004), 

the falcatus–gracilior group is unlikely to be dispersal 

limited, even across the open grass-dominated landscapes 

that characterize the Afrotemperate region. However, 

the hard sclerotesta of A. falcatus cones delays germination for a year or more and leads to high postdispersal 

damage by mammals, resulting in low recruitment rates 

(Geldenhuys, 1993). In addition, seed viability declines by 

more than 50% within 12 months of harvesting (Negash, 

2003). Loss of viability and postdispersal mortality combined with infrequent seed production (mast fruiter) all 

reduce the probability of colonizing new habitat. At the 

landscape scale, Afrocarpus appears to be a poor colonist 

but persists well once established. The minor radiation 
number 95 • 8 5

of Afrocarpus in East Africa and the discovery of distinct 

A. falcatus provenances in South Africa (Geldenhuys and 

Von dem Bussche, 1997) are consistent with the hypothesis that the genus is restricted by stepping-stone dispersal 

and imply that the distribution of Afrocarpus in Africa is 

an ancient one.

Podocarp ecophysiology

The ecophysiology of African podocarps is largely unknown. Nevertheless, explanations for conifer distribution 

in Africa have been based in large part on physiological 

differences between conifers and competing angiosperms 

(Bond, 1989). Bond argued that functional constraints 

such as tracheids and nonvascularized leaves place conifers at a competitive disadvantage at the regeneration 

phase, restricting them to edaphically or climatically suboptimal sites where they perform better than angiosperms.

The dual role of mechanical support and hydraulic 

function performed by wood leads to trade-offs in performance with important ecological implications (Chave et 

al., 2009). Angiosperms solved this problem by separating mechanical support from hydraulic function with the 

evolution of xylem vessels, multicellular conduits for water 

transport, and a matrix of fibers for support (Sperry et al., 

2006). Released from their structural function, angiosperm 

vessels achieve greater conducting efficiency by increasing 

FIGURE 5.3. Mature Podocarpus latifolius persisting in a fire-safe topographic refuge situated in a regularly burnt grassland matrix at Royal 

Natal.
8 6 • smithsonian contributions to botany

their diameter (Tyree and Ewers, 1991; Sperry et al., 2005). 

In contrast, conifer tracheids are limited by their unicellularity and the need to provide both mechanical support and 

hydraulic function to the plant (Sperry et al., 2006; Lusk, 

this volume; Brodribb, this volume). The dual role of tracheids leads to a trade-off between their two primary functions, a constraint that conifers have overcome to some 

extent with the evolution of the torus-margo pit, a membrane that joins conduit end-walls, allowing significantly 

higher conductivity compared with the longer vessels of 

angiosperms (Hacke et al., 2004; Pittermann et al., 2005). 

Nevertheless, conifers grow more slowly than angiosperms 

(Coomes and Bellingham, this volume).

Compared to angiosperms, conifer leaves are poorly 

vascularized and have low stomatal conductance and low 

specific leaf area, resulting in lower photosynthetic capacity (Lusk et al., 2003; Brodribb et al., 2005a, 2005b). 

Photosynthetic capacity increases with xylem vessel conductance (Brodribb and Feild, 2000; Hubbard et al., 

2001), but large vessels are at risk of embolism in cold 

environments (Sperry et al., 1994). Photosynthetic yield 

(measured by the leaf area to stem area ratio) has been 

shown to be much greater in angiosperms measured in 

high light, but this advantage over conifers tends to be 

neutralized in low light (Brodribb et al., 2005a). A pervasive pattern among African podocarps is superior shade 

tolerance compared with associated angiosperms, which 

demand more light (Midgley et al., 1995b; Adie and 

Lawes, 2009a). However, Coomes and Bellingham (this 

volume) point out that many shade-tolerant podocarps are 

capable of regenerating in shaded environments yet fail in 

deep shade, where light levels are ~2% of daylight. This is 

consistent with the finding that plants, in general, are substantially more responsive to nutrient supply at light levels 

of >5% of daylight compared with deep understory shade, 

where light levels are often <2% of daylight (Coomes and 

Grubb, 2000). Thus, it is not surprising that relative shade 

tolerance of podocarps is strongly implicated in the coexistence of African podocarps and angiosperms and is likely 

the dominant determinant of mixed angiosperm–conifer 

tree community structure in African forests (Adie and 

Lawes, 2009a).

Ecology

Mixed Angiosperm–Conifer Forests

Here we examine podocarp regeneration along an 

altitudinal gradient extending from the Drakensberg, 

a mountainous region situated in the northwest of 

KwaZulu-Natal province, to lowland forest on the east 

coast of South Africa (Figure 5.2). Mixed angiosperm–

conifer forests in the montane region are characteristically 

small, usually less than 5 ha and rarely exceeding 30 ha 

(Lawes et al., 2007a), and exist as an archipelago within 

a grassland matrix between 1,400 and 1,830 m above sea 

level. Forest distribution is limited by fire and is therefore 

generally restricted to moist south-facing slopes and steepsided ravines (Everard, 1986; Geldenhuys, 1994) situated 

beneath tall sandstone cliffs. Lowland forest lies on the 

plains inland of the coastal dune cordon (Mucina and 

Rutherford, 2006) and is well represented just south of 

Kosi Bay in northern Maputaland (Figure 5.2). The forests have a well-developed canopy and subcanopy, and 

the semiwoody herb Isoglossa woodii (Acanthaceae) frequently dominates the shrub layer. Intermediate between 

the inland mountains and coastal lowlands is coastal scarp 

forest, a species-rich subtropical forest type that is derived 

from, and hence owes its diversity to, tropical coastal 

forests and inland Afromontane elements (Lawes, 1990; 

Griffiths and Lawes, 2006). Situated in a mosaic of grasslands and rocky granitic outcrops, Ongoye Forest Reserve 

lies between 300 and 500 m elevation and is 2,600 ha in 

extent (Boudreau et al., 2005). 

Three species of Podocarpaceae are distributed along 

the described altitudinal gradient. Podocarpus latifolius

is an abundant and widespread species throughout the 

Drakensberg and KwaZulu-Natal midlands and extends 

toward the coast, where it is an uncommon component 

of scarp forest. Known from only one forest in the Drakensberg, P. henkelii is rare in the montane region but common in mist belt forests of the midlands (H. Adie, personal 

observation). Afrocarpus falcatus has a patchy but locally 

common distribution in the Drakensberg, is widespread 

and relatively common in the midlands, is present but uncommon in scarp forest, and is the only podocarp found 

in the subtropical lowland forests of the coastal plains, 

where it is scarce.

Biophysical Factors

Light is a critical factor determining plant growth and 

survival in forest ecosystems (Denslow, 1987), in which 

the differential response to light during the regeneration 

phase drives plant community composition and dynamics (Kobe et al., 1995; Bloor and Grubb, 2003). In mixed 

angiosperm–conifer forests of the Southern Hemisphere, 

regeneration following both autogenic and allogenic disturbance is driven by differences in plant shade tolerance 
number 95 • 8 7

(Lusk and Ogden, 1992; Ogden and Stewart, 1995; Lusk 

and Smith, 1998). Deep shade (~2% daylight) in southern 

forests tends to favor angiosperms at the expense of podocarps (Lusk, 1996; Coomes et al., 2005).

To understand regeneration patterns in Afromontane 

forest, two forest types that differed substantially in structure and, therefore, in light environment were compared. 

Angiosperm forest, as the name implies, is dominated by 

angiosperm canopy species. Tree density in this forest 

type is relatively high, and the forest canopy is moderate 

in stature (<20 m). Podocarpus latifolius is usually present in the angiosperm forest canopy, but at low density. 

Forests dominated by the conifer (>60% of canopy trees) 

differ structurally from those dominated by angiosperms 

by having a higher canopy (20–25 m) and larger trees with 

greater nearest neighbor distances, resulting in an open 

mid-story and “cathedral-like” structure. The two forest 

types differ in terms of the quality and quantity of light 

reaching the forest floor beneath the intact canopy and in 

canopy gaps (Adie and Lawes, 2009a; Figure 5.4). Photosynthetically active radiation was high (~17% irradiance) 

in canopy gaps in both forest types, but light quality (measured as the ratio of red to far red light; Capers and Chazdon, 2004) in angiosperm canopy gaps, which were small 

(84.6 ± 13.7 m2, n = 10), showed far less variation and 

was lower compared with the much larger gaps (183 m2

± 36.6, n = 10) in Podocarpus forest (Adie and Lawes, 

2009a). We also sampled forest tree regeneration outside 

true forest, in a thicket environment dominated by Rhus 

tomentosa. The thicket habitat, which had a low canopy 

of 4–6 m, was less shaded than the two forest habitats, but 

light quality was substantially lower, probably because of 

the high stem density of the habitat (Lee, 1989; Smith and 

Whitelam, 1997).

The structural conditions described above cause 

important differences in the light reaching the forest 

FIGURE 5.4. Light characteristics (percent light transmittance, red:far red) at ground level in Rhus tomentosa thicket 

and two habitats (canopy, gap) in forest dominated by angiosperms and conifers.
8 8 • smithsonian contributions to botany

understory environment, and both light and the understory vegetation act in combination to restrict regeneration by forest canopy species (Adie and Lawes, 2009a). 

Grass was the principal ground cover beneath the intact 

Podocarpus forest canopy, but was absent from both 

angiosperm forest and thicket. Bare ground or a sparse 

covering of litter dominated the thicket habitat and angiosperm forest. Gaps in both forest types were frequently 

choked by a combination of grasses, vines, ferns, and understory shrubs. With this background to the physical environment, we discuss the relative success of angiosperm 

and conifer regeneration in Afrotemperate forest.

The role of disturbance in

mixed angiosperm–conifer

forests in South Africa

Gap-Phase Dynamics

Gap-phase dynamics is an important driver of forest 

structure and dynamics in New Zealand and South America (Lusk and Ogden, 1992; Ogden and Stewart, 1995). In 

these temperate forests, the differential response to gaps 

at the juvenile stage leads to canopy species coexistence 

(Lusk and Smith, 1998; Gutierrez et al., 2004; Gutierrez et 

al., 2008). In contrast, canopy gaps have a limited role in 

the regeneration dynamics of Afromontane forests (Adie 

and Lawes, 2009b), where poor regeneration by angiosperm canopy species results from their shade intolerance 

(Midgley et al., 1995b; Adie and Lawes, 2009a). 

Gaps in angiosperm forest are created by lateral 

branch breakage and stem snapping, resulting in relatively 

small gaps. Young gaps tend to be larger than old gaps, 

suggestive of progressive canopy closure with age due to 

lateral ingrowth of adjacent canopies. Interestingly, seedling and sapling densities do not differ among gap sizes or 

from densities recorded beneath the closed canopy (Adie 

and Lawes, 2009a). Thus, in spite of elevated light levels, the gap environment offers no new regeneration opportunities for angiosperms or P. latifolius. Even though 

angiosperm seedlings were abundant, very few saplings or 

poles were recorded in gaps or beneath the canopy (Figure 5.5), suggesting that light conditions were inadequate 

for growth into larger size categories. Young conifer trees 

were abundant in these regeneration environments, but 

less so in older gaps, implying self-thinning or suppression by ground cover (Beckage et al., 2000; Coomes et al., 

2005). In addition, P. latifolius saplings (1–5 cm diameter 

at breast height [dbh]) and poles (5 cm < dbh ≤ 10 cm) 

were common in young tree fall gaps (<24 months old), 

demonstrating that successful gap fillers were drawn from 

individuals in the advanced regeneration phase that established prior to gap creation (Adie and Lawes, 2009b). 

Being shade tolerant, or more shade tolerant than associated angiosperm species, the conifer outperformed angiosperms at gap formation because it was able to establish 

profusely beneath the angiosperm canopy.

In contrast to the high rate of establishment by P. latifolius in angiosperm forest, regeneration by the conifer in 

Podocarpus-dominated forest was substantially less than 

that recorded for angiosperms (Adie and Lawes, 2009a). 

Canopy gaps in Podocarpus forest were generally created by uprooting of large-canopy individuals (Adie and 

Lawes, 2009b). Consequently, canopy gaps in Podocarpus forest were relatively large compared with angiosperm 

forest, yet they offered no new regeneration opportunities 

to angiosperms or P. latifolius. Curiously, unlike angiosperm forest, there were almost no P. latifolius seedlings 

beneath the intact canopy of Podocarpus forest. Grass, the 

dominant ground cover in Podocarpus forest, suppressed 

P. latifolius seedlings, causing high mortality (Adie and 

Lawes, 2009b). Even in gaps, the abundant grass cover 

resulted in relatively low densities of P. latifolius (0.9 ± 

0.3 per 0.01 ha) and angiosperm canopy species (1.2 ± 0.3 

per 0.01 ha). 

FIGURE 5.5. Mean density (± standard error, n = 10) of young conifer and angiosperm trees in two regeneration environments in Afromontane forest.
number 95 • 8 9

Besides grass, dense understory vegetation and vines 

may also dominate gaps. An inverse J-shaped distribution 

of angiosperm stem sizes in Podocarpus forest suggests 

that grass does not suppress angiosperm seedlings in the 

same way it does P. latifolius. Seedlings were common, 

but the scarcity of saplings implies growth suppression, 

with possibly light limitation restricting the growth of 

seedlings into larger size categories. Notwithstanding the 

low density of both angiosperms and P. latifolius in gaps, 

the contest between these two plant groups in Podocarpus forest is equivocal, with both apparently having an 

equal opportunity to occupy gaps. Tree fall gaps therefore 

offer one mechanism to maintain angiosperm diversity in 

Afrotemperate forest, but in old-growth forest only (Adie 

and Lawes, 2009a).

Catastrophic Disturbance

Large-scale natural disturbances (earthquakes, cyclones, landslides, volcanic eruptions) have had a pervasive influence on the structure and dynamics of mixed 

angiosperm–conifer forests in New Zealand (Stewart and 

Rose, 1989; Ogden and Stewart, 1995; Wells et al., 2001) 

and South America (Veblen and Ashton, 1978; Veblen et 

al., 1995). The Afromontane landscape in the subtropics is 

relatively benign in that it lacks the climatic, topographic, 

or geological extremes that cause stand-destroying disturbance in many southern temperate forest environments. 

Fire has also been reported as an important process controlling stand structure in mixed forests in South America 

(Burns, 1993), and extensive precolonization fires in New 

Zealand probably caused a mosaic of seral and mature forest communities (Ogden et al., 1998). Natural fire is also 

implicated in the total destruction of podocarp forests following drought on New Zealand’s South Island (Kershaw 

and McGlone, 1995) and in New Guinea Araucaria forest 

(Enright, 1995). In tropical environments, fires are more 

likely during drought years, when fragmented forests are 

particularly vulnerable (Cochrane and Laurance, 2002). 

South American gallery forest, a naturally fragmented 

form of tropical moist forest that exists within a savanna 

matrix (Kellman and Meave, 1997), is more prone to fire 

in the late dry season, when plant material is more ignitable (Biddulph and Kellman, 1998). Drakensberg montane 

forest is not unlike gallery forest in that it exists as small 

patches within a fire-prone grassland matrix (Everard, 

1986), yet fire has largely been de-emphasized as a process 

driving forest change in South Africa (Mucina and Rutherford, 2006), a viewpoint that is not unexpected since fire 

is unusual in South African forests (Midgley et al., 1997). 

Forests with a canopy dominated by angiosperms do not 

burn (Bond, 1997) because of low fuel loads and high leaf 

moisture levels (van Wilgen et al., 1990) or high fuel moisture content (Eriksson et al., 2003). Nevertheless, it is notable that most Afromontane forests establish and persist 

in fire refugia, where they escape the prevailing grassland 

fire direction (Geldenhuys, 1994).

Although rare under the present grassland management system in the subtropics of southern Africa, fire 

may have been a critical historical driver of inland forest 

structure and dynamics by destroying old-growth Podocarpus forest. Catastrophic disturbance provides relatively 

rare regeneration opportunities for angiosperm trees in 

the Afromontane landscape. Historical records report 

catastrophic fires devastating indigenous forest, particularly in the temperate Podocarpus forests of the southern 

Cape (Geldenhuys, 1994). In most cases fires were preceded by several days of hot berg wind conditions (van 

Wilgen, 1984; Geldenhuys, 1994; Bond, 1997). The open 

physiognomy of Podocarpus-dominated forests is highly 

susceptible to the desiccating effect of berg winds and, 

coupled with high levels of volatile compounds in longlived sclerophyllous leaves (Kershaw and McGlone, 1995) 

and the well-developed grass cover in old-growth forests, 

predisposes Podocarpus forest to fire.

Does pattern and process in

Afromontane forests conform

to other southern hemisphere

podocarp forests?

Regeneration patterns of canopy trees in montane forests are consistent with the temporal stand replacement 

model (TSRM; Ogden, 1985; Enright et al., 1999; Ogden et 

al., 2005), with important exceptions. The TSRM was proposed to explain the dominance of long-lived pioneer conifer cohorts and the widespread regeneration failure reported 

from temperate forests in New Zealand (Veblen and Stewart, 

1982; Stewart and Rose, 1989) and South America (Veblen 

et al., 1980, 1995). Under the TSRM, sites are colonized 

by a pioneer cohort, usually a long-lived conifer, following 

stand-destroying disturbance. In the absence of further disturbance, synchronous senescence by the colonizing cohort 

causes overstory mortality, creating gaps that offer diminishing regeneration opportunities for the first-generation 

conifer in favor of more shade-tolerant species, usually an 

angiosperm (Enright et al., 1999; Ogden et al., 2005).

Regeneration failure by the angiosperm canopy component is a recurrent pattern in South African inland forests 
9 0 • smithsonian contributions to botany

(Moll, 1972; Everard et al., 1995; West et al., 2000; Lawes 

et al., 2007b). Drakensberg montane forests, with a near 

absence of advanced angiosperm regeneration beneath the 

intact canopy, are no exception (Adie and Lawes, 2009b). 

However, angiosperm regeneration was recorded from 

scrub thicket sites and a grassland fire-exclusion site, leading us to propose that many angiosperm species assume a 

colonizing role and establish as a pioneer cohort following 

disturbance (Adie and Lawes, 2009b). Unlike temperate 

forests elsewhere, P. latifolius was slow to regenerate in 

these scrub environments, possibly because of slow seedling growth rates relative to angiosperms (Bond, 1989). 

The prevalence of angiosperm-dominated canopies among 

forests that were logged extensively (i.e., catastrophic disturbance) during the colonial era from the early to mid1800s to the early twentieth century (Fourcade, 1889; 

Hutchins, 1905; McCracken, 1986) is consistent with the 

proposal that angiosperms assume the colonizing role following major disturbance. Therefore, in South Africa a 

suite of angiosperm species take on the pioneer role that is 

usually filled by a long-lived gymnosperm species in New 

Zealand. The slow colonization of fire-protected grassland 

sites by angiosperm tree species demonstrates that catastrophic disturbance, another key feature of the TSRM, is 

not a necessary requirement for forest development in the 

Afrotemperate landscape.

Podocarpus latifolius regenerated continuously beneath the intact angiosperm-dominated canopy in the 

Drakensberg, confirming shade tolerance in this species. 

Age data for P. latifolius, which shows that Podocarpusdominated forest is considerably older than angiosperm 

forest, confirms the replacement of angiosperms by the 

conifer and is consistent with the TSRM as a two-phase 

system with phases separated in time (Adie and Lawes, 

2009b). Continuous regeneration by the shade-tolerant 

conifer eliminates the need for the synchronous canopy 

senescence that is a key feature of the TSRM in other 

southern temperate forests. Conifer persistence, the central 

feature of conifer–angiosperm competition, appears to be 

curtailed by more shade-tolerant angiosperms elsewhere. 

Superior angiosperm shade tolerance in Chilean temperate 

forest prevents conifer regeneration in deep shade (Lusk, 

1996), and productive alluvial forest habitats in New Zealand appear too dark for even the most shade-tolerant 

conifers (Coomes et al., 2005). Indeed, the progressive replacement of the colonizing cohort by more shade-tolerant 

angiosperm species in southern temperate forest is a key 

feature of the TSRM (Enright and Ogden, 1995; Ogden 

et al., 2005). In these temperate forests, canopy gaps favor 

recruitment by conifers, leading to their coexistence with 

angiosperms (Lusk and Smith, 1998). The differential response by tree species to varying light conditions is a critical driver of forest structure and dynamics in New Zealand 

(Ogden and Stewart, 1995). More recently, soil nutrient 

availability has been shown to have an important role in 

plant community development, with conifers performing 

better than angiosperms on nutrient-poor sites (Richardson 

et al., 2004; Coomes et al., 2005; Carswell et al., 2007).

Soil Nutrients

Superior shade tolerance of P. latifolius in the Afromontane environment relative to angiosperms weakens 

the proposition that conifers are restricted to suboptimal 

environments (climate, nutrients) by competitively superior angiosperms at the regeneration phase (Bond, 1989). 

Angiosperm shade intolerance removes competition at 

the conifer seedling phase and ultimately results in the replacement of angiosperms by the podocarp. Do depleted 

soil nutrient levels affect the tortoise–hare contest in favor of the conifer as Bond (1989) predicted? In New Zealand, soil nutrient status alters regeneration success among 

podocarps (Carswell et al., 2007), and podocarps perform 

better on infertile (phosphorus-limited) and poorly drained 

soils relative to co-occurring angiosperms (Richardson et 

al., 2004; Coomes et al., 2005). The role of soil fertility 

in altering the outcome of the angiosperm-podocarp contest has not been examined directly in African forests. At 

fynbos sites, known to be very infertile, shaded microhabitats were more important than soil organic matter content 

for germination of forest species (Cowling et al., 1997), 

and in the southern Cape, topography and aspect, rather 

than soil type, determined forest distribution (Geldenhuys, 

1994). In these regions fire was the overriding process 

determining forest distribution (van Wilgen et al., 1990; 

Geldenhuys, 1994; Cowling et al., 1997).

Compared with P. latifolius, which showed no nutrient effect, seedling growth of angiosperm canopy species 

was consistently higher at high nitrogen (half-strength 

Hoagland’s solution containing 10% of the recommended nitrogen concentration; Hewitt, 1966) compared 

with low nitrogen (1% nitrogen) levels, but there was a 

steady decline in performance with diminishing light (Figure 5.6). In Chilean temperate rainforest, shade-tolerant 

conifers were associated with nutrient-poor and climatically stressed sites, but these species were also associated 

with high-disturbance gap sites (Lusk, 1996), suggesting 

response to light is equally, if not more, important to regeneration success. Coomes et al. (2005) showed variable 

performance by conifers along a productivity gradient, 
number 95 • 9 1

the conifers performing better in lower-nutrient (yet more 

open) terrace forest, where they established in gaps. In 

contrast, shadier habitats and ferns limited regeneration 

opportunities for conifers at the upper end of the productivity gradient. In Afromontane forests of the South 

African Drakensberg Mountains we found no association 

between conifer or angiosperm community dominance 

and soil chemical composition (M. J. Lawes, unpublished 

data). Nitrogen does not appear to be a limiting soil nutrient in African forest sites. In the Munesa region of the 

Ethiopian southeastern highlands, where A. falcatus is an 

important canopy species, the soil carbon to nitrogen ratio 

was 12.6 (Solomon et al., 2002). This value is no different 

from values for Drakensberg and subtropical forest sites 

in KwaZulu-Natal (Table 5.2) but is substantially lower 

than nutrient-poor sites in New Zealand (Richardson et 

al., 2004; Coomes et al., 2005). We have no comparable 

values for total phosphorus, which has been shown to be 

a strong driver of plant community structure in New Zealand forests (Richardson et al., 2004; Coomes et al., 2005; 

Carswell et al., 2007). However, available phosphorus, the 

quantity of phosphorus that is easily extracted and directly 

available to the plant (Holford, 1997), does not seem to 

be limiting in the Drakensberg or subtropical scarp forest 

sites (Table 5.2). Concentrations of available phosphorus 

>10 mg kg-1

 (Ambic-2 method; Thibaud et al., 1994) in 

similar soils are not considered severely limiting for annual 

agricultural crops in KwaZulu-Natal; it is therefore unlikely that concentrations >5 mg kg-1

 would be limiting for 

slow-growing forest trees (A. Manson, Soil Fertility Analytical Services, KZN Department of Agriculture and Environmental Affairs, personal communication). Available 

phosphorus recorded in forests in the central Ethiopian 

highlands (31.7 mg kg-1

; Bray II method; Michelsen et al., 

1996) was similar to Ongoye forest. These data indicate 

that soils in southeastern Africa are neither nitrogen nor 

phosphorus limited, and it is possible that soil moisture 

may have an importance not recognized in other Southern 

Hemisphere locations where podocarps are present.

Arbuscular mycorrhizal fungi provide an important 

mechanism to overcome growth constraints imposed by 

nutrient-poor soils (Brundrett, 2002). Such fungi have a 

significant effect on seedling growth (Janos, 1980), particularly in soils where available phosphorus concentrations 

are low (Chen et al., 2005; Lambers et al., 2008), and have 

the potential of causing differential regeneration success 

FIGURE 5.6. Seedling mass (mean ± standard error, n = 6) of P. latifolius after three months growth 

under three light treatments (low = 2.4% photosynthetically active radiation (PAR), medium = 

8.0% PAR, and high = 13.5% PAR) and two nutrient levels (10% nitrogen and 1% nitrogen).
9 2 • smithsonian contributions to botany

and therefore affecting species diversity in forests (Kiers 

et al., 2000; Chen et al., 2005). Phosphorus uptake by 

conifer roots is stimulated by the presence of arbuscular 

mycorrhizal fungi (Morrison and English, 1967; Baylis, 

1969), and Dickie and Holdaway (this volume) propose 

that root nodules serve to increase the volume of the root 

cortex volume, resulting in greater fungal infection. Arbuscular mycorrhizas have been identified in A. falcatus

(Allsopp and Stock, 1993; Wubet et al., 2003) and P. latifolius (Hawley and Dames, 2004) and are also present 

in many associated angiosperm species in Afrotemperate 

forest (Hawley and Dames, 2004). The importance of arbuscular mycorrhizal fungi at the regeneration phase, and 

whether it affects the conifer–angiosperm contest, is unknown for Afromontane forests but is unlikely if phosphorus is not limiting.

Podocarps in Coastal Forest

The presence of podocarps in coastal forest is probably 

a legacy of climatic extremes during the Last Glacial Maximum, when inland forests are thought to have retreated 

toward the coast (Eeley et al., 1999). Podocarpus latifolius persists as large-canopy individuals in scarp forest, but 

the continuous regeneration so prevalent in montane forest is absent. Seedlings and saplings beneath the canopy 

are rare and tend to be spindly in appearance (Adie and 

Lawes, unpublished data). However, angiosperm species 

are similarly absent from the understory at Ongoye, which 

contradicts the view that direct competitive interactions 

limit the conifer beneath the forest canopy in subtropical environments (Midgley et al., 1995a). Either (1) shade 

tolerance of P. latifolius in scarp forest differs from that in 

montane forest populations, which is not an unreasonable 

hypothesis since there is evidence for distinct A. falcatus

provenances in southern Africa (Geldenhuys and Von dem 

Bussche, 1997), or (2) the response to light by P. latifolius does not differ between the two forest habitats, but 

there is a lower limit below which the conifer is unable to 

perform. Incoming photosynthetically active radiation beneath the intact canopy at Ongoye was substantially lower 

than that recorded in Afromontane forests (Figure 5.7) because of a more-productive angiosperm canopy and many 

shade-tolerant mid-canopy species in scarp forest. Deep 

shade (<2% photosynthetically active radiation) and not 

direct competition from understory angiosperms, which 

were absent beneath the canopy, seems to be a more likely 

mechanism suppressing P. latifolius regeneration in scarp 

forest. Many podocarp species persist in deep shade but 

do not regenerate continuously in these habitats (Coomes 

and Bellingham, this volume).

Conifer regeneration opportunities were similarly 

restricted in productive alluvial forest habitats in New 

Zealand (Coomes et al., 2005). Saplings of P. latifolius

growing adjacent to forest roads and on the forest edge at 

Ongoye were robust (Adie and Lawes, unpublished data), 

reflecting successful growth and supporting our contention that light, rather than direct angiosperm competition 

at the regeneration phase, ultimately suppresses growth 

of this species in scarp forest. Enhanced productivity in 

scarp forest, which may result from a combination of soil 

fertility and climate, is a proximate factor that operates 

indirectly by altering light levels that suppress P. latifolius

performance.

The differential response to light between angiosperms 

and conifers appears to be the critical factor driving lowland forest dynamics. An isolated population of A. falcatus exists in tropical coastal lowland forest at Kosi Bay 

in northern Maputaland (Figure 5.2). Afrocarpus falcatus

is a shade-tolerant tree (Fetene and Feleke, 2001; Tesfaye 

et al., 2002) that regenerates continuously in forest but 

has higher seedling growth rates in gaps compared with 

more shaded sites (Teketay, 1997). The latter point concurs with the observation of Laughton (1938), who considered A. falcatus more light demanding than P. latifolius

in southern Cape forests. 

At Kosi Bay the structure of the A. falcatus population 

is consistent with regeneration failure. Very large canopy 

individuals (>60 cm diameter at breast height) form an 

integral part of the angiosperm-dominated canopy, with 

a preponderance of young plants (including seedlings 

but few saplings) beneath the canopy (R. Kyle, personal 

communication). Intermediate-sized trees are rare or absent. Saplings and poles are a valuable resource to local 

communities because the wood is hard and the poles are 

TABLE 5.2. Soil chemical characteristics (mean ± standard 

error, n = 6) from forest sites in the Drakensberg (Monk’s Cowl, 

Royal Natal) and a subtropical site (Ongoye Forest Reserve) in 

KwaZulu-Natal. Available phosphorus was analyzed using the 

Ambic-2 method (Thibaud et al., 1994).

Total N Available P

Site C:N (%) (mg P kg-1

)

Royal Natal 12.06 ± 0.81 0.91 ± 0.045 12.89 ± 0.876

Monk’s Cowl 12.55 ± 0.62 1.21 ± 0.171 9.88 ± 1.04

Ongoye 11.77 ± 0.60 0.71 ± 0.215 27.68 ± 1.42
number 95 • 9 3

straight. Consequently, there is heavy harvesting pressure 

on juvenile plants, which presumably accounts for the 

paucity of medium-sized trees. Kyle (personal communication) reports that fruiting trees produce abundant fruit 

and that the high number of seedlings noted in the forest 

reflects good germination.

Were it not for the intense harvesting pressure on 

juvenile stages, we suggest that A. falcatus would show 

continuous regeneration in coastal forests. Their establishment beneath the canopy and the straight nature of poles 

is consistent with shade tolerance for this conifer. It is not 

clear whether the persistence of A. falcatus in subtropical lowland forest is directly associated with its ability to 

establish in shade or whether there is an interactive effect 

with soil nutrient status. Coastal forests are dominated by 

light-demanding angiosperms, with few species showing 

successful establishment beneath the shaded closed canopy and pervasive shrub layer (Griffiths et al., 2007). The 

understory herbaceous shrub Isoglossa woodii influences 

forest dynamics by suppressing tree recruitment in dune 

forest (Griffiths et al., 2007; Tsvuura et al., 2007). The 

proposition that A. falcatus persists in subtropical lowland forest through shade tolerance mirrors our finding 

for P. latifolius in Afromontane forest. However, some 

podocarp species are able to persist in lowland tropical 

forest where soil conditions are poor (Coomes and Bellingham, this volume). Soils in the Kosi Bay system are 

sandy and infertile (Maud, 1980) and may favor A. falcatus over competing angiosperms given the superior ability 

of conifers to acquire and retain nutrients (Coomes and 

Bellingham, this volume). 

The persistence of A. falcatus in coastal lowland habitats is an enigma. Several aspects of the biology of this 

species would seem to conspire against long-term success. 

First, regeneration failure is not uncommon among mastfruiting species (Blundell and Peart, 2004), and logging 

has been shown to reduce the extent and intensity of mastfruiting events, resulting in regeneration failure (Curran et 

al., 1999). Second, the threat of extinction among dioecious plants, particularly woody species, is high (Vamosi 

and Vamosi, 2005). Reduced mate assurance leads to pollination failure (Pannell and Barrett, 1998), or reduced 

seed production limits the effective size of the breeding 

population (Heilbuth et al., 2001). Third, recruitment 

rates are generally low because of delayed germination 

and high postdispersal damage by mammals (Geldenhuys, 

1993) and loss of seed viability (Negash, 2003). Finally, 

sustained harvesting of A. falcatus poles has a significant 

FIGURE 5.7. Mean light transmittance (± standard error, n = 12) in a scarp forest understory gap 

and beneath the canopy of scarp forest and angiosperm-dominated Afromontane forest. The gap in 

scarp forest was created artificially by felling eight mid-canopy tree species.
9 4 • smithsonian contributions to botany

impact on regeneration success (Tesfaye et al., 2002; 

Lawes et al., 2007b). The ability to regenerate in shaded 

environments, compared with an angiosperm component 

dominated almost entirely by light-demanding species, explains this species’ persistence in lowland coastal forest.

Cyclical regeneration

and podocarp persistence

The TSRM promotes a deterministic successional process that relies on catastrophic disturbance to initiate the 

sequence (Ogden, 1985; Ogden and Stewart, 1995). However, catastrophic disturbance is not always necessary to 

explain forest structure and the persistence of podocarps 

(Six Dijkstra et al., 1985; Lusk and Ogden, 1992). Podocarps are able to maintain their dominance, or coexistence 

with angiosperms, through cyclical regeneration driven 

principally by endogenous disturbance and the differential 

response of trees at the juvenile stage to canopy opening 

(Lusk and Smith, 1998). At the landscape scale, tree species coexistence is mediated through temporal (progressive overstory collapse) and spatial (microsite, degree of 

canopy closure) segregation (Ogden and Stewart, 1995). 

The duration of the proposed regeneration cycle may last 

650–700 years (Beveridge, 1973; Six Dijkstra et al., 1985). 

In South African Afromontane forests, it is not clear what 

follows the old-growth Podocarpus-dominated phase since 

not only is this type of forest rare, but these old-growth 

forests appear to be relatively young. Trees exceeding 600 

years in age are routinely recorded from southern temperate forests in New Zealand and Chile (e.g., Lusk and Ogden, 1992; Lusk, 1996; Smale et al., 1997), yet we dated 

the largest P. latifolius to a little over half that age (Adie 

and Lawes, 2009b).

Several lines of evidence lead to a model that proposes 

the persistence of old-growth Podocarpus forest in the 

absence of stand-destroying disturbance in South Africa. 

First, grass suppresses the establishment of P. latifolius, 

restricting regeneration to occasional episodes that may 

be associated with higher than usual rainfall (Adie and 

Lawes, 2009a). This finding, combined with the continuous regeneration of P. latifolius during the angiosperm 

phase, results in a multi-aged P. latifolius canopy at the oldgrowth phase, which eliminates synchronous canopy senescence and the associated progressive overstory collapse 

(Adie and Lawes, 2009b). Second, angiosperm canopy 

trees in Afromontane forests are relatively shade intolerant, resulting in very limited angiosperm regeneration in 

old-growth forest. Finally, gap creation, frequently caused 

by multiple tree falls, provides angiosperms with a limited 

opportunity of reaching the canopy in old-growth forest.

Summary

Members of the Podocarpaceae, especially P. latifolius, 

are exceptionally successful in South African inland forests. The genus was decimated by colonial logging, and its 

present abundance in forest throughout its range is largely 

a consequence of that disturbance. Given adequate time, 

and in the absence of further catastrophic disturbance, 

Podocarpus will dominate the angiosperm flora. Podocarpus dominance is attributed to its longevity (Lawes et al., 

2006) and ability to regenerate in shade, where all potential competing angiosperms are less capable of doing so 

(Adie and Lawes, 2009b).

To explain the geographical distribution of podocarps 

in South Africa, Midgley et al. (1995a) proposed that competitively superior angiosperms limit conifers in the more 

productive tropical environments. Indirectly, this claim 

holds in that deeply shaded habitat, resulting from higher 

angiosperm productivity, suppresses growth of P. latifolius

seedlings. However, we found no evidence for direct competitive interaction between angiosperms and podocarps 

at the regeneration phase, with angiosperms appearing 

to be equally suppressed by the shaded conditions. We 

contend that the response by P. latifolius to light is the 

dominant and ultimate factor explaining the relatively 

poor performance of the conifer in scarp forest. Thus, the 

persistence of P. latifolius in this productive subtropical 

forest type is driven by disturbance that creates elevated 

light levels. Canopy gaps, however, do not facilitate P. latifolius regeneration in coastal scarp forests (e.g., Ongoye) 

because gaps are rapidly colonized by fast-growing vines 

(e.g., Flagellaria guineensis) that suppress canopy tree 

regeneration. Catastrophic disturbance, linked with the 

general longevity of podocarps, may offer one mechanism 

driving persistence. 

We have no reason to suggest that African podocarps 

behave differently from other members of the Podocarpaceae. Rather, the prevalence of a generalist life history 

among competing angiosperms is important, and it is 

within this context that African podocarp ecology needs 

to be evaluated. African podocarps and their associated 

angiosperm flora have been shaped by Pleistocene climatic 

fluctuations. During the relatively benign interglacials that 

favored angiosperms, podocarps persisted by retreating to 
number 95 • 9 5

their ancestral temperate zone refuges in montane regions. 

The intervening cold glacial periods drove podocarp expansion into lowland habitats, where they were able to 

compete successfully with angiosperms. African podocarps are thus temperate forest relicts and are not lowland rainforest survivors. The regression of Afrotemperate 

forest is likely to have placed floras under increasing risk 

of extinction by processes associated with fragmentation 

and those operating in the grassland matrix causing widespread species filtering that left a temperate angiosperm 

flora bereft of shade-tolerant species (Adie and Lawes, 

2009b). Podocarpus latifolius is capable of establishing 

in relatively high light conditions and does not suffer the 

same constraints that place shade-tolerant species at risk 

of extinction in a fragmented landscape. The resulting 

relative difference in shade tolerance between conifers and 

angiosperms is an important determinant of forest structure and dynamics in Africa.

Future research directions

1. Palynological studies are needed to differentiate 

between Afrocarpus and Podocarpus to test the hypothesis that the present distribution of Afrocarpus is old (prePliocene) whereas the more vagile Podocarpus is more 

recent (Pleistocene), reflecting rapid colonization followed 

by local extinction. Podocarpus, the older lineage compared with Afrocarpus (Biffin et al., this volume), is widespread in Africa, perhaps because of life history traits that 

promote dispersal, but local extinctions suggest the taxon 

is susceptible to climatic upheavals. It is tempting to suggest that the variable climate associated with volcanism 

and rifting in East Africa (Pik et al., 2008) and cooling 

(Kender et al., 2009) in the early to mid-Miocene led to 

the selection of traits that reinforced persistence but compromised dispersal ability in Afrocarpus. Recent research 

on the Maputaland coastal plain (northeastern South 

Africa) documents expansion and regression of podocarp 

forest (Mazus, 2000; Finch and Hill, 2008; Neumann et 

al., 2008). It is not clear whether the species represented in 

the pollen record is A. falcatus, present in lowland forest 

on the coastal plain, or P. latifolius, found in scarp forest 

just inland of the coast. 

2. Podocarpus latifolius is the dominant species at altitude (inland mountains), where it dominates canopies. 

The mechanisms suppressing their performance in coastal 

scarp sites require examination, which will provide insight 

into why this species was unable to persist once lowland 

forest extended its distribution following relaxation of 

glacial maxima (West Africa).

3. In spite of intensive colonial logging, A. falcatus has 

persisted and continues to be successful in forest habitats 

from the coastal lowlands to temperate highlands. Understanding the persistence of this species is particularly relevant in the face of severe logging pressure elsewhere in 

Africa (Wubet et al., 2003, 2006) and also as a window 

to the potential response of podocarps to climate change. 

Superior drought resistance (cf. Brodribb and Hill, 1998) 

may explain the persistence of A. falcatus on the coast in 

place of P. latifolius. The performance of A. falcatus under 

varying light and soil moisture and nutrient conditions requires testing, as we have done for P. latifolius.

4. The proposed long-term persistence of A. falcatus

relative to P. latifolius may result from their contrasting 

reproductive biology and seed physiology. Afrocarpus falcatus is a dioecious masting species with a periodicity of six 

to seven years between reproductive events (Geldenhuys, 

1993). Podocarpus latifolius, on the other hand, is an annual seeder, resulting in less episodic recruitment and lower 

vulnerability to climatic instability compared with A. falcatus, which may partly explain the wider and more continuous distribution of P. latifolius. In addition, shade-tolerant 

species rely on seed reserves for energy and nitrogen (Kitajima, 2002), and large energy reserves enhance establishment (Kitajima and Fenner, 2000). The high lipid content 

of A. falcatus seed (20%; Wirminghaus et al., 2002) may 

contribute to the success of this species in shaded environments and in competition with grasses in old-growth 

podocarp-dominated forests. Trials testing relative germination and establishment success with competing C3

grasses are required to test the persistence hypothesis.

5. The recovery by A. falcatus and P. latifolius after 

colonial logging activities differ markedly, and understanding this relationship may offer insight into differences in their ecology and distribution. In the Drakensberg 

Mountains the response by A. falcatus was slow, resulting 

in a relatively low abundance and restricted distribution 

compared with the dominance of P. latifolius.

Acknowledgments

Scotty Kyle of Ezemvelo KZN Wildlife kindly shared 

his observations of Afrocarpus falcatus at Kosi Bay. Alan 

Manson from Soil Fertility Analytical Services, KZN Department of Agriculture and Environmental Affairs, advised on soil analyses. Zivanai Tsvuura of the School of 

Biological and Conservation Sciences, Forest Biodiversity 
9 6 • smithsonian contributions to botany

Research Unit, University of KwaZulu-Natal, provided 

the light data for dune forest.

REFERENCES

Adie, H., and M. J. Lawes. 2009a. Explaining Conifer Dominance in Afrotemperate Forests: Shade Tolerance Favours Podocarpus latifolius

over Angiosperm Species. Forest Ecol. Managem. 259: 176–186.

Adie, H., and M. J. Lawes. 2009b. Role Reversal in the Stand Dynamics 

of an Angiosperm–Conifer Forest: Colonising Angiosperms Precede 

a Shade-Tolerant Conifer in Afrotemperate Forest. Forest Ecol. 

Managem. 258: 159–168.

Allsopp, N., and W. D. Stock. 1993. Mycorrhizal Status of Plants Growing in the Cape Floristic Region, South Africa. Bothalia 23: 91–104.

Barker, N. P., E. M. Muller, and R. R. Mill. 2004. A Yellowwood by Any 

Other Name: Molecular Systematics and the Taxonomy of Podocarpus and the Podocarpaceae in Southern Africa. S. African J. Sci.

100: 629–632.

Baylis, G. T. S. 1969. Mycorrhizal Nodules and Growth of Podocarpus 

in Nitrogen-Poor Soil. Nature 223: 1385–1386.

Beckage, B., J. S. Clark, B. D. Clinton, and L. Haines. 2000. A LongTerm Study of Tree Seedling Recruitment in Southern Appalachian 

Forests: The Effects of Canopy Gaps and Shrub Understories. Canad. J. Forest Res. 30: 1617–1631.

Becker, P. 2000. Competition in the Regeneration Niche between Conifers and Angiosperms: Bond’s Slow Seedling Hypothesis. Funct. 

Ecol. 14: 401–412.

Beveridge, A. E. 1973. Regeneration of Podocarps in Central North Island Forests. Proc. New Zealand Ecol. Soc. 11: 48–55.

Biffin, E., J. Conran, and A. Lowe. 2011 (this volume). Podocarp Evolution: A Molecular Phylogenetic Perspective. In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 1–20. Smithsonian Contributions to Botany, No. 95. 

Smithsonian Institution Scholarly Press, Washington, D.C.

Biddulph, J., and M. Kellman. 1998. Fuels and Fire at Savanna–Gallery 

Forest Boundaries in Southeastern Venezuela. J. Trop. Ecol. 14: 

445–461.

Bloor, J. M. G., and P. J. Grubb. 2003. Growth and Mortality in High 

and Low Light: Trends among 15 Shade-Tolerant Tropical Rain 

Forest Tree Species. J. Ecol. 91: 77–85.

Blundell, A. G., and D. R. Peart. 2004. Seedling Recruitment Failure 

Following Dipterocarp Mast Fruiting. J. Trop. Ecol. 20: 229–231.

Bond, W. J. 1989. The Tortoise and the Hare: Ecology of Angiosperm 

Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 

227–249.

Bond, W. J. 1997. Fire. In Vegetation of Southern Africa, R. Cowling, 

D. M. Richardson, and S. M. Pierce, eds., pp. 421–446. Cambridge 

University Press, Cambridge, UK.

Bonnefille, R. 1994. Palynology and Palaeoenvironment of East African 

Hominid Sites. In Integrative Paths to the Past: Palaeoanthropological Advances in Honor of F. Clark Howell, R. S. Corruccini 

and R. L. Ciochon, eds., pp. 415–427. Prentice Hall, Englewood 

Cliffs, N.J.

Bonnefille, R., J. C. Roeland, and J. Guiot. 1990. Temperature and Rainfall Estimates for the Past 40,000 Years in Equatorial Africa. Nature 346: 347–349.

Boudreau, S., M. J. Lawes, S. E. Piper, and L. J. Phadima. 2005. Subsistence Harvesting of Pole-Size Understorey Species from Ongoye 

Forest Reserve, South Africa: Species Preference, Harvest Intensity, 

and Social Correlates. Forest Ecol. Managem. 216: 149–165.

Brodribb, T. J. 2011 (this volume). A Functional Analysis of Podocarp 

Ecology. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 165–173. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Brodribb, T. J., and T. S. Feild. 2000. Stem Hydraulic Supply Is Linked to 

Leaf Photosynthetic Capacity: Evidence from New Caledonian and 

Tasmanian Rainforests. Pl. Cell Environm. 23: 1381–1388.

Brodribb, T., and R. S. Hill. 1998. The Photosynthetic Drought Physiology of a Diverse Group of Southern Hemisphere Conifer Species 

Is Correlated with Minimum Seasonal Rainfall. Funct. Ecol. 12: 

465–471.

Brodribb, T. J., N. M. Holbrook, and R. S. Hill. 2005a. Seedling Growth 

in Conifers and Angiosperms: Impacts of Contrasting Xylem Structure. Austral. J. Bot. 53: 749–755.

Brodribb, T. J., N. M. Holbrook, M. A. Zwieniecki, and B. Palma. 2005b. 

Leaf Hydraulic Capacity in Ferns, Conifers and Angiosperms: Impacts on Photosynthetic Maxima. New Phytol. 165: 839–846.

Brundrett, M. C. 2002. Coevolution of Roots and Mycorrhizas of Land 

Plants. New Phytol. 154: 275–304.

Burns, B. R. 1993. Fire-Induced Dynamics of Araucaria araucana–

Nothofagus antarctica Forest in the Southern Andes. J. Biogeogr.

20: 669–685.

Capers, R. S., and R. L. Chazdon. 2004. Rapid Assessment of Understory Light Availability in a Wet Tropical Forest. Agric. Forest Meteorol. 123: 177–185.

Carcasson, R. H. 1964. A Preliminary Survey of the Zoogeography of 

the African Butterflies. E. African Wildlife J. 2: 122–157.

Carswell, F. E., S. J. Richardson, J. E. Doherty, R. B. Allen, and S. K. 

Wiser. 2007. Where Do Conifers Regenerate after Selective Harvest?: A Case Study from a New Zealand Conifer–Angiosperm Forest. Forest Ecol. Managem. 253: 138–147.

Chave, J., D. Coomes, S. Jansen, S. L. Lewis, N. G. Swenson, and A. E. 

Zanne. 2009. Towards a Worldwide Wood Economics Spectrum. 

Ecol. Letters 12: 351–366.

Chen, X., J. Tang, G. Zhi, and S. Hu. 2005. Arbuscular Mycorrhizal 

Colonization and Phosphorus Acquisition of Plants: Effects of Coexisting Plant Species. Appl. Soil Ecol. 28: 259–269.

Cochrane, M. A., and W. F. Laurance. 2002. Fire as a Large-Scale Edge 

Effect in Amazonian Forests. J. Trop. Ecol. 18: 311–325.

Coetzee, J. A., and J. Muller. 1984. The Phytogeographic Significance 

of Some Extinct Gondwana Pollen Types from the Tertiary of the 

Southwestern Cape (South Africa). Ann. Missouri Bot. Gard. 71: 

1088–1099.

Coetzee, J. A., and E. M. Van Zinderen Bakker. 1970. Palaeoecological 

Problems of the Quaternary of Africa. S. African J. Sci. 66: 78–84.

Cohen, A. S., J. R. Stone, K. R. M. Beuning, L. E. Park, P. N. Reinthal, 

D. Dettmar, C. A. Scholz, T. C. Johnsor, J. W. King, M. R. Talbot, E. T. Brown, and S. J. Ivory. 2007. Ecological Consequences of 

Early Late Pleistocene Megadroughts in Tropical Africa. Proc. Natl. 

Acad. Sci. U.S.A. 104: 16422–16427.

Conran, J. G., G. M. Wood, P. G. Martin, J. M. Dowd, C. J. Quinn, P. A. 

Gadek, and R. A. Price. 2000. Generic Relationships within and 

between the Gymnosperm Families Podocarpaceae and Phyllocladaceae Based on an Analysis of the Chloroplast Gene rbcL. Austral. 

J. Bot. 48: 715–724.

Coomes, D. A., R. B. Allen, W. A. Bentley, L. E. Burrows, C. D. Canham, L. Fagan, D. M. Forsyth, A. Gaxiola-Alcantar, R. L. Parfitt, 

W. A. Ruscoe, D. A. Wardle, D. J. Wilson, and E. F. Wright. 2005. 

The Hare, the Tortoise and the Crocodile: The Ecology of Angiosperm Dominance, Conifer Persistence and Fern Filtering. J. Ecol.

93: 918–935.

Coomes, D. A., and P. J. Bellingham. 2011 (this volume). Temperate and 

Tropical Podocarps: How Ecologically Alike Are They? In Ecology 

of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. 

Cernusak, eds., pp. 119–140. Smithsonian Contributions to Botany, 

No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.
number 95 • 9 7

Coomes, D. A., and P. J. Grubb. 2000. Impacts of Root Competition in 

Forests and Woodlands: A Theoretical Framework and Review of 

Experiments. Ecol. Monogr. 70: 171–207.

Cowling, R. M., D. Kirkwood, J. J. Midgley, and S. M. Pierce. 1997. Invasion and Persistence of Bird-Dispersed, Subtropical Thicket and 

Forest Species in Fire-Prone Coastal Fynbos. J. Veg. Sci. 8: 475–488.

Curran, L. M., I. Caniago, G. D. Paoli, D. Astianti, M. Kusneti, 

M. Leighton, C. E. Nirarita, and H. Haeruman. 1999. Impact of El 

Niño and Logging on Canopy Tree Recruitment in Borneo. Science

286: 2184–2188.

Dawson, I. K., and W. Powell. 1999. Genetic Variation in the Afromontane Tree Prunus africana, an Endangered Medicinal Species. 

Molec. Ecol. 8: 151–156.

de Laubenfels, D. J. 1985. A Taxonomic Revision of the Genus Podocarpus. Blumea 30: 251–278.

DeBusk, G. H. 1998. A 37,500-Year Pollen Record from Lake Malawi 

and Implications for the Biogeography of Afromontane Forests. 

J. Biogeogr. 25: 479–500.

Denslow, J. S. 1987. Tropical Rainforest Gaps and Tree Species Diversity. 

Annual Rev. Ecol. Syst. 18: 431–451.

Dickie, I. A., and R. J. Holdaway. 2011 (this volume). Podocarp Roots, 

Mycorrhizas, and Nodules. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 175–187. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Dowsett-Lemaire, F., and F. White. 1990. New and Noteworthy Plants 

from the Evergreen Forests of Malawi. Bull. Jard. Bot. Natl. Belg.

60: 73–110.

Drummond, R. B. 1975. A List of Trees, Shrubs and Woody Climbers 

Indigenous or Naturalised in Rhodesia. Kirkia 10: 229–285.

Dupéron-Laudoueneix, M., and J. Dupéron. 1995. Inventory of Mesozoic and Cenozoic Woods from Equatorial and North Equatorial 

Africa. Rev. Palaeobot. Palynol. 84: 439–480.

Dupont, L. M., S. Jahns, F. Marret, and S. Ning. 2000. Vegetation 

Change in Equatorial West Africa: Time-Slices for the Last 150 Ka. 

Palaeogeogr. Palaeoclimatol. Palaeoecol. 155: 95–122.

Eeley, H. A. C., M. J. Lawes, and S. E. P. Piper. 1999. The Influence 

of Climate Change on the Distribution of Indigenous Forest in 

Kwazulu-Natal, South Africa. J. Biogeogr. 26: 595–617.

Elenga, H., A. Vincens, and D. Schwartz. 1991. Présence d’éléments forestiers montagnards sur Les Plateaux Batéké (Congo) au Pléistocéne 

Supérieur: Nouvelles données palynologiques. Palaeoecol. Africa

22: 239–252.

Enright, N. J. 1995. Conifers of Tropical Australasia. In Ecology of the 

Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 197–222. 

Melbourne University Press, Carlton, Australia.

Enright, N. J., and T. Jaffré. 2011 (this volume). Ecology and Distribution of the Malesian Podocarps. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 57–77. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Enright, N. J., and J. Ogden. 1995. The Southern Conifers—A Synthesis. 

In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, 

eds., pp. 271–287. Melbourne University Press, Carlton, Australia.

Enright, N. J., J. Ogden, and L. S. Rigg. 1999. Dynamics of Forests with 

Araucariaceae in the Western Pacific. J. Veg. Sci. 10: 793–804.

Eriksson, I., D. Teketay, and A. Granstrom. 2003. Response of Plant 

Communities to Fire in an Acacia Woodland and a Dry Afromontane Forest, Southern Ethiopia. Forest Ecol. Managem. 177: 39–50.

Everard, D. A. 1986. The Effects of Fire on the Podocarpus latifolius

Forests of the Royal Natal National Park, Natal Drakensburg. 

S. African J. Bot. 52: 60–66.

Everard, D. A., J. J. Midgley, and G. F. van Wyk. 1995. Dynamics of 

Some Forests in Kwazulu-Natal, South Africa, Based on Ordinations and Size-Class Distributions. S. African J. Bot. 61: 283–292.

Farjon, A. 2001. World Checklist and Bibliography of Conifers. Royal 

Botanic Gardens, Kew, Richmond, Surrey, UK.

Fetene, M., and Y. Feleke. 2001. Growth and Photosynthesis of Seedlings of Four Tree Species from a Dry Tropical Afromontane Forest. 

J. Trop. Ecol. 17: 269–283.

Finch, J. M., and T. R. Hill. 2008. A Late Quaternary Pollen Sequence 

from Mfabeni Peatland, South Africa: Reconstructing Forest History in Maputaland. Quaternary Res. 70: 442–450.

Fourcade, H. G. 1889. Report on the Natal Forests. Watson, Pietermaritzburg, South Africa.

Fredoux, A. 1994. Pollen Analysis of a Deep-Sea Core in the Gulf of 

Guinea: Vegetation and Climatic Changes during the Last 225,000 

Years B.P. Palaeogeogr. Palaeoclimatol. Palaeoecol. 109: 317–330.

Geldenhuys, C. J. 1993. Reproductive Biology and Population Structures 

of Podocarpus falcatus and P. latifolius in Southern Cape Forests. 

Bot. J. Linn. Soc. 112: 59–74.

Geldenhuys, C. J. 1994. Bergwind Fires and the Location Pattern of Forest Patches in the Southern Cape Landscape, South Africa. J. Biogeogr. 21: 49–62.

Geldenhuys, C. J., and G. H. Von dem Bussche. 1997. Performance of 

Podocarpus falcatus Provenances in South Africa. S. African Forest. 

J. 178: 15–24.

Griffiths, M. E., and M. J. Lawes. 2006. Biogeographic, Environmental, 

and Phylogenetic Influences on Reproductive Traits in Subtropical 

Forest Trees, South Africa. Ecography 29: 614–622.

Griffiths, M. E., M. J. Lawes, and Z. Tsvuura. 2007. Understorey Gaps 

Influence Regeneration Dynamics in Subtropical Coastal Dune Forest. Pl. Ecol. 189: 227–236.

Gutierrez, A. G., J. J. Armesto, and J. C. Aravena. 2004. Disturbance and 

Regeneration Dynamics of an Old-Growth North Patagonian Rain 

Forest in Chiloé Island, Chile. J. Ecol. 92: 598–608.

Gutierrez, A. G., J. C. Aravena, N. V. Carrasco-Farias, D. A. Christie, 

M. Fuentes, and J. J. Armesto. 2008. Gap-Phase Dynamics and Coexistence of a Long-Lived Pioneer and Shade-Tolerant Tree Species 

in the Canopy of an Old-Growth Coastal Temperate Rain Forest of 

Chiloe Island, Chile. J. Biogeogr. 35: 1674–1687.

Hacke, U. G., J. S. Sperry, and J. Pittermann. 2004. Analysis of Circular Bordered Pit Function II. Gymnosperm Tracheids with TorusMargo Pit Membranes. Amer. J. Bot. 91: 386–400.

Hamilton, A. 1989. African Forest. In Rain Forest Ecosystems: Biogeographical and Ecological Studies, H. Leith and M. J. A. Werger, 

eds., pp. 155–181. Elsevier, Amsterdam.

Hawley, G. L., and J. F. Dames. 2004. Mycorrhizal Status of Indigenous 

Tree Species in a Forest Biome of the Eastern Cape, South Africa. 

S. African J. Sci. 100: 633–637.

Heilbuth, J. C., K. Illves, and S. P. Otto. 2001. The Consequences of 

Dioecy for Seed Dispersal: Modeling the Seed-Shadow Handicap. 

Evolution 55: 880–888.

Hewitt, E. 1966. Sand and Water Culture Methods Used in the Study 

of Plant Nutrition. Commonwealth Agricultural Bureaux, Farnham 

Royal, UK.

Hitimana, J., J. L. Kiyiapi, and J. T. Njunge. 2004. Forest Structure Characteristics in Disturbed and Undisturbed Sites of Mt. Elgon Moist 

Lower Montane Forest, Western Kenya. Forest Ecol. Managem.

194: 269–291.

Holford, I. C. R. 1997. Soil Phosphorus: Its Measurement, and Its Uptake by Plants. Austral. J. Soil Res. 35: 227–240.

Hubbard, R. M., M. G. Ryan, V. Stiller, and J. S. Sperry. 2001. Stomatal Conductance and Photosynthesis Vary Linearly with Plant 

Hydraulic Conductance in Ponderosa Pine. Pl. Cell Environm. 24: 

113–121.

Huntley, B. J. and E. M. Matos, 1994. Botanical Diversity and Its Conservation in Angola. In Botanical Diversity in Southern Africa, B. J. 

Huntley, ed., pp. 53–74, National Botanical Institute, Pretoria, 

South Africa.
9 8 • smithsonian contributions to botany

Hutchins, D. E. 1905. The Indigenous Forests of South Africa. In Joint 

Meeting of the British and South African Associations for the Advancement of Science, pp. 319–335. British Association for the Advancement of Science, Cape Town, South Africa.

Jahns, S., M. Huls, and M. Sarnthein. 1998. Vegetation and Climate 

History of West Equatorial Africa Based on a Marine Pollen Record 

off Liberia (site GIK 16776) Covering the Last 400,000 Years. Rev. 

Palaeobot. Palynol. 102: 277–288.

Janos, D. P. 1980. Vesicular-Arbuscular Mycorrhizae Affect Lowland 

Tropical Rain Forest Plant Growth. Ecology 61: 151–162.

Kelch, D. G. 1997. The Phylogeny of the Podocarpaceae Based on Morphological Evidence. Syst. Bot. 22: 113–131.

Kelch, D. G. 1998. Phylogeny of Podocarpaceae: Comparison of Evidence from Morphology and 18S rDNA. Amer. J. Bot. 85: 986–996.

Kellman, M., and J. Meave. 1997. Fire in the Tropical Gallery Forests of 

Belize. J. Biogeogr. 24: 23–34.

Kender, S., V. L. Peck, R. W. Jones, and M. A. Kaminski. 2009. Middle 

Miocene Oxygen Minimum Zone Expansion Offshore West Africa: Evidence for Global Cooling Precursor Events. Geology 37: 

699–702.

Kershaw, A. P., and M. S. McGlone. 1995. The Quaternary History of 

the Southern Conifers. In Ecology of the Southern Conifers, N. J. 

Enright and R. S. Hill, eds., pp. 30–63. Melbourne University Press, 

Carlton, Australia.

Kiers, E. T., C. E. Lovelock, E. L. Krueger, and E. A. Herre. 2000. Differential Effects of Tropical Arbuscular Mycorrhizal Fungal Inocula 

on Root Colonization and Tree Seedling Growth: Implications for 

Tropical Forest Diversity. Ecol. Letters 3: 106–113.

Kingdon, J. 1971. East African Mammals: An Atlas of Evolution in Africa. Academic Press, London.

Kitajima, K. 2002. Do Shade-Tolerant Tropical Tree Seedlings depend 

Longer on Seed Reserves? Functional Growth Analysis of Three 

Bignoniaceae Species. Funct. Ecol. 16: 433–444.

Kitajima, K., and M. Fenner. 2000. Ecology of Seedling Regeneration. In 

Seeds: The Ecology of Regeneration in Plant Communities, 2nd ed., 

M. Fenner, ed., pp. 331–359. CAB International, Wallingford, UK.

Kobe, R. K., S. W. Pacala, J. A. Silander Jr., and C. D. Canham. 1995. Juvenile Tree Survivorship as a Component of Shade Tolerance. Ecol. 

Appl. 5: 517–532.

Lambers, H., J. A. Raven, G. R. Shaver, and S. E. Smith. 2008. Plant 

Nutrient-Acquisition Strategies Change with Soil Age. Trends Ecol. 

Evol. 23: 95–103.

Laughton, F. S. 1938. The Silviculture of the Indigenous Forests of the 

Union of South Africa. Government Printer, Pretoria, South Africa.

Lawes, M. J. 1990. The Distribution of the Samango Monkey (Cercopithecus mitis erythrarchus Peters, 1852 and Cercopithecus mitis 

labiatus I. Geoffroy, 1843) and Forest History in Southern Africa. 

J. Biogeogr. 17: 669–680.

Lawes, M. J., H. Adie, H. A. C. Eeley, D. J. Kotze, and R. Wethered. 

2007a. An Assessment of the Forests of the Maloti–Drakensberg 

Transfrontier Bioregion, with Reference to Important Ecosystem 

Processes. Forest Biodiversity Research Unit, School of Biological 

and Conservation Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa.

Lawes, M. J., M. E. Griffiths, and S. Boudreau. 2007b. Colonial Logging and Recent Subsistence Harvesting Affect the Composition 

and Physiognomy of a Podocarp Dominated Afrotemperate Forest. 

Forest Ecol. Managem. 247: 48–60.

Lawes, M. J., J. J. Midgley, S. Boudreau, and M. E. Griffiths. 2006. Lack 

of Disturbance as an Explanation for the Additive Basal Area Phenomenon in a Stratified Afrotemperate Forest. Austral Ecol. 31: 

471–477.

Lee, D. W. 1989. Canopy Dynamics and Light Climates in a Tropical 

Moist Deciduous Forest in India. J. Trop. Ecol. 5: 65–79.

Linder, H. P. 2001. Plant Diversity and Endemism in Sub-Saharan Tropical Africa. J. Biogeogr. 28: 169–182.

Lusk, C. H. 1996. Stand Dynamics of the Shade-Tolerant Conifers Podocarpus nubigena and Saxegothaea conspicua in Chilean Temperate 

Rain Forest. J. Veg. Sci. 7: 549–558.

Lusk, C. H. 2011 (this volume). Conifer–Angiosperm Interactions: Physiological Ecology and Life History. In Ecology of the Podocarpaceae 

in Tropical Forests, ed. B. L. Turner and L. A. Cernusak, pp. 157–

164. Smithsonian Contributions to Botany, No. 95. Smithsonian 

Institution Scholarly Press, Washington, D.C.

Lusk, C. H., and J. Ogden. 1992. Age Structure and Dynamics of a 

Podocarp–Broadleaf Forest in Tongariro National Park, New Zealand. J. Ecol. 80: 379–393.

Lusk, C. H., and B. Smith. 1998. Life History Differences and Tree Species Coexistence in an Old-Growth New Zealand Rain Forest. 

Ecology 79: 795–806.

Lusk, C. H., I. Wright, and P. B. Reich. 2003. Photosynthetic Differences 

Contribute to Competitive Advantage of Evergreen Angiosperm 

Trees over Evergreen Conifers in Productive Habitats. New Phytol.

160: 329–336.

Malaisse, F. 1967. A propos d’une nouvelle station de Podocarpus milanjianus Rendle au Katanga. Publ. Univ. Off. du Congo à Lubumbashi 16: 79–81.

Maley, J. 1989. Late Quaternary Climatic Changes in the African Rain 

Forest: The Question of Forest Refuges and the Major Role of 

Sea Surface Temperature Variations. In Paleoclimatology and Paleometeorology: Modern and Past Patterns of Global Atmospheric 

Transport, M. Leinen and M. Sarnthein, eds., pp. 585–616. Kluwer 

Academic Publishers, Dordrecht, Netherlands.

Maley, J. 1993. The Climatic and Vegetational History of the Equatorial Regions of Africa during the Upper Quaternary. In The Archaeology of Africa. Food, Metals and Towns, T. Shaw, P. Sinclair, 

B. Andah and A. Okpoko, eds., pp. 43–52. Routledge, London.

Maley, J. 1996a. The African Rain Forest: Main Characteristics of 

Changes in Vegetation and Climate from the Upper Cretaceous to 

the Quaternary. Proc. Roy. Soc. Edinburgh, B 104: 31–73.

Maley, J. 1996b. Le cadre paléoenvironnemental des refuges forestiers 

Africains: Quelques données et hypothèses. In The Biodiversity of 

African Plants, L. J. G. van der Maesen, X. M. van der Burgt, and 

J. M. van Medenbach de Rooy, eds., pp. 519–535. Kluwer, Dordrecht, Netherlands.

Maley, J., and P. Brenac. 1998. Vegetation Dynamics, Palaeoenvironments and Climatic Changes in the Forests of Western Cameroon 

during the last 28,000 Years B.P. Rev. Palaeobot. Palynol. 99: 

157–187.

Maley, J., G. Caballé, and P. Sita. 1990. Etude d’un peuplement résiduel à basse altitude de Podocarpus latifolius sur le flanc Congolais du Massif du Chaillu. Implications paléoclimatiques et biogéographiques. Etude de la pluie pollinique actuelle. In Paysages 

Quaternaires de l’Afrique centrale Atlantique, R. Lanfranchi and 

D. Schwartz, eds., pp. 336–352. Didactiques, ORSTOM, Paris.

Maud, R. R. 1980. The Climate and Geology of Maputaland. In Studies 

on the Ecology of Maputaland, M. N. Bruton and K. H. Cooper, 

eds., pp. 1–7. Rhodes University, Grahamstown and Natal Branch 

of the Wildlife Society of Southern Africa, Durban, South Africa.

Mazus, H. 2000. Clues on the History of Podocarpus Forest in Maputaland, South Africa, during the Quaternary, Based on Pollen Analysis. Africa Geosci. Rev. 7: 75–82.

McCracken, D. P. 1986. The Indigenous Forests of Colonial Natal and 

Zululand. Natalia 16: 19–38.

Meadows, M. E. 1984. Late Quaternary Vegetation History of the Nyika 

Plateau, Malawi. J. Biogeogr. 11: 209–222.

Meadows, M. E., and H. P. Linder. 1993. A Palaeoecological Perspective 

on the Origin of Afromontane Grasslands. J. Biogeogr. 20: 345–355.
number 95 • 9 9

Melville, R. 1954. The Podocarps of East Africa. Kew Bull. 9: 563–574.

Michelsen, A., N. Lisanework, I. Friis, and N. Holst. 1996. Comparisons of Understorey Vegetation and Soil Fertility in Plantations and 

Adjacent Natural Forests in the Ethiopian Highlands. J. Appl. Ecol.

33: 627–642.

Midgley, J. J., and W. J. Bond. 1989. Evidence from Southern African 

Coniferales for the Historical Decline of the Gymnosperms. S. African J. Sci. 85: 81–84.

Midgley, J. J., W. J. Bond, and C. J. Geldenhuys. 1995a. The Ecology of 

Southern African Conifers. In Ecology of the Southern Conifers, 

N. J. Enright and R. S. Hill, eds., pp. 64–80. Melbourne University 

Press, Carlton, Australia.

Midgley, J. J., D. A. Everard, and G. van Wyk. 1995b. Relative Lack of 

Regeneration of Shade-Intolerant Canopy Species in Some South 

African Forests. S. African J. Sci. 91: 7–8.

Midgley, J. J., R. M. Cowling, A. H. W. Seydack, and G. F. van Wyk. 

1997. Forest. In Vegetation of Southern Africa, R. M. Cowling, 

D. M. Richardson, and S. M. Pierce, eds., pp. 278–299. Cambridge 

University Press, Cambridge, UK.

Midgley, J. J., A. Seydack, D. Reynell, and D. McKelly. 1990. Fine-Grain 

Pattern in Southern Cape Plateau Forests. J. Veg. Sci. 1: 539–546.

Mill, R. R. 2003. Towards a Biogeography of the Podocarpaceae. In IV 

International Conifer Conference, R. R. Mill, ed. Acta Hort. 615: 

137–147.

Moll, E. J. 1972. The Current Status of Mistbelt Mixed Podocarpus Forest in Natal. Bothalia 10: 595–598.

Moreau, R. E. 1966. The Bird Faunas of Africa and Its Islands. Academic Press, London.

Morley, R. J. 2000. Origin and Evolution of Tropical Rain Forests. John 

Wiley and Sons, Chichester, UK.

Morley, R. J. 2003. Interplate Dispersal Paths for Megathermal Angiosperms. Perspect. Plant Ecol. Evol. Syst. 6: 5–20.

Morley, R. J. 2011 (this volume). Dispersal and Paleoecology of Tropical 

Podocarps. In Ecology of the Podocarpaceae in Tropical Forests, ed. 

B. L. Turner and L. A. Cernusak, pp. 21–41. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Morrison, T. M., and D. A. English. 1967. The Significance of Mycorrhizal Nodules of Agathis australis. New Phytol. 66: 245–250.

Mucina, L., and M. C. Rutherford, eds. 2006. The Vegetation of South 

Africa, Lesotho and Swaziland. South African National Biodiversity Institute, Pretoria.

Negash, L. 2003. In Situ Fertility Decline and Provenance Differences 

in the East African Yellow Wood (Podocarpus falcatus) Measured 

through In Vitro Seed Germination. Forest Ecol. Managem. 174: 

127–138.

Neumann, F. H., J. C. Stager, L. Scott, H. J. T. Venter, and C. Weyhenmeyer. 2008. Holocene Vegetation and Climate Records from Lake 

Sibaya, Kwazulu-Natal (South Africa). Rev. Palaeobot. Palynol.

152: 113–128.

Ogden, J. 1985. An Introduction to Plant Demography with Special 

Reference to New Zealand Trees. New Zealand J. Bot. 23: 751–

772.

Ogden, J., L. Basher, and M. McGlone. 1998. Fire, Forest Regeneration 

and Links with Early Human Habitation: Evidence from New Zealand. Ann. Bot. 81: 687–696.

Ogden, J., R. A. Fordham, M. Horrocks, S. Pilkington, and R. G. Serra. 

2005. Long-Term Dynamics of the Long-Lived Conifer Libocedrus 

bidwillii after a Volcanic Eruption 2000 Years Ago. J. Veg. Sci. 16: 

321–330.

Ogden, J., and G. H. Stewart. 1995. Community Dynamics of the New 

Zealand Conifers. In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 81–119. Melbourne University Press, 

Carlton, Australia.

Page, C. N. 1989. New and Maintained Genera in the Conifer Families 

Podocarpaceae and Pinaceae. Notes Roy. Bot. Gard. Edinburgh 45: 

377–395.

Pannell, J. R., and S. C. H. Barrett. 1998. Baker’s Law Revisited: Reproductive Assurance in a Metapopulation. Evolution 52: 657–668.

Parmentier, I., J. Lejoly, and N. Nguema. 2001. Inselbergs Vegetation 

of the Piedra Nzas Natural Monument (Continental Equatorial 

Guinea). Acta Bot. Gallica 148: 341–365.

Pik, R., B. Marty, J. Carignan, G. Yirgu, and T. Ayalew. 2008. Timing of 

East African Rift Development in Southern Ethiopia: Implication 

for Mantle Plume Activity and Evolution of Topography. Geology

36: 167–170.

Pittermann, J., J. S. Sperry, U. G. Hacke, J. K. Wheeler, and E. H. Sikkema. 2005. Torus-Margo Pits Help Conifers Compete with Angiosperms. Science 310: 1924.

Richardson, S. J., D. A. Peltzer, R. B. Allen, M. S. McGlone, and R. L. 

Parfitt. 2004. Rapid Development of Phosphorus Limitation in 

Temperate Rainforest along the Franz Josef Soil Chronosequence. 

Oecologia 139: 267–276.

Schatz, G. E. 1996. Malagasy/Indo-Australo-Malesian Phytogeographic 

Connections. In Biogeography of Madagascar, W. R. Lourenço, ed. 

ORSTOM, Paris.

Sinclair, W. T., R. R. Mill, M. F. Gardner, P. Woltz, T. Jaffre, J. Preston, 

M. L. Hollingsworth, A. Ponge, and M. Moller. 2002. Evolutionary 

Relationships of the New Caledonian Heterotrophic Conifer, Parasitaxus usta (Podocarpaceae), Inferred from Chloroplast trnL-F 

Intron/Spacer and Nuclear rDNA ITS2 Sequences. Pl. Syst. Evol.

233: 79–104.

Six Dijkstra, H. G., D. J. Mead, and I. L. James. 1985. Forest Architecture in Terrace Forest of Saltwater Forest, South Westland, and Its 

Implications for Management. New Zealand J. Forest. Sci. 15: 3–22.

Smale, M. C., B. R. Burns, P. N. Smale, and P. T. Whaley. 1997. Dynamics of Upland Podocarp/Broadleaved Forest on Mamaku Plateau, 

Central North Island, New Zealand. J. Roy. Soc. New Zealand 27: 

513–532.

Smith, H., and G. C. Whitelam. 1997. The Shade Avoidance Syndrome: 

Multiple Responses Mediated by Multiple Phytochromes. Pl. Cell 

Environm. 20: 840–844.

Solomon, D., F. Fritzsche, M. Tekalign, J. Lehmann, and W. Zech. 2002. 

Soil Organic Matter Composition in the Subhumid Ethiopian Highlands as Influenced by Deforestation and Agricultural Management. 

Soil Sci. Soc. Amer. J. 66: 68–82.

Sperry, J. S., U. G. Hacke, and J. Pittermann. 2006. Size and Function 

in Conifer Tracheids and Angiosperm Vessels. Amer. J. Bot. 93: 

1490–1500.

Sperry, J. S., U. G. Hacke, and J. K. Wheeler. 2005. Comparative Analysis of End Wall Resistivity in Xylem Conduits. Pl. Cell Environm.

28: 456–465.

Sperry, J. S., K. L. Nichols, J. E. M. Sullivan, and S. E. Eastlack. 1994. 

Xylem Embolism in Ring-Porous, Diffuse-Porous, and Coniferous 

Trees of Northern Utah and Interior Alaska. Ecology 75: 1736–

1752.

Stewart, G. H., and A. B. Rose. 1989. Conifer Regeneration Failure in 

New Zealand: Dynamics of Montane Libocedrus bidwillii Stands. 

Pl. Ecol. 79: 41–49.

Stockey, R. A., B. J. Frevel, and P. Woltz. 1998. Cuticle Micromorphology of Podocarpus, Subgenus Podocarpus, Section Scytopodium 

(Podocarpaceae) of Madagascar and South Africa. Int. J. Pl. Sci.

159: 923–940.

Teketay, D. 1997. Seedling Populations and Regeneration of Woody Species in Dry Afromontane Forests of Ethiopia. Forest Ecol. Managem. 98: 149–165.

Teketay, D., and A. Granstrom. 1997. Germination Ecology of Forest 

Species from the Highlands of Ethiopia. J. Trop. Ecol. 13: 805–831.
100 • smithsonian contributions to botany

Tesfaye, G., D. Teketay, and M. Fetene. 2002. Regeneration of Fourteen 

Tree Species in Harenna Forest, Southeastern Ethiopia. Flora 197: 

461–474.

Thibaud, G. R., M. P. W. Farina, J. C. Hughes, and M. A. Johnston. 

1994. Assessment of Phosphorus Availability in Soils Fertilized with 

Langebaan Rock Phosphate or Superphosphate. S. African J. Pl. 

Soil 11: 178–185.

Tsvuura, Z., M. E. Griffiths, and M. J. Lawes. 2007. The Effect of Herbaceous Understory Cover on Fruit Removal and Seedling Survival in 

Coastal Dune Forest Trees in South Africa. Biotropica 39: 428–432.

Tyree, M. T., and F. W. Ewers. 1991. The Hydraulic Architecture of Trees 

and Other Woody Plants. New Phytol. 119: 345–360.

Vamosi, J. C., and S. M. Vamosi. 2005. Present Day Risk of Extinction 

May Exacerbate the Lower Species Richness of Dioecious Clades. 

Diversity Distrib. 11: 25–32.

van Wilgen, B. W. 1984. Fire Climates in the Southern and Western Cape 

Province and Their Potential Use in Fire Control and Management. 

S. African J. Sci. 80: 358–362.

van Wilgen, B. W., K. B. Higgins, and D. U. Bellstedt. 1990. The Role 

of Vegetation Structure and Fuel Chemistry in Excluding Fire from 

Forest Patches in the Fire-Prone Fynbos Shrublands of South Africa. 

J. Ecol. 78: 210–222.

Van Zinderen Bakker, E. M. 1967. Upper Pleistocene and Holocene 

Stratigraphy and Ecology on the Basis of Vegetation Changes in 

Sub-Saharan Africa. In Background of Evolution in Africa, W. W. 

Bishop and J. Desmond-Clark, eds., pp. 125–147. University of 

Chicago Press, Chicago.

Van Zinderen Bakker, E. M. 1982. African Palaeoenvironments 18000 

yrs BP. Palaeoecol. Africa 15: 77–99.

Veblen, T. T., and D. H. Ashton. 1978. Catastrophic Influences on the 

Vegetation of the Valdivian Andes, Chile. Vegetatio 36: 149–167.

Veblen, T. T., B. R. Burns, A. L. Kitzberger, and R. Villalba. 1995. The 

Ecology of the Conifers of Southern South America. In Ecology 

of the Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 

120–155. Melbourne University Press, Carlton, Australia.

Veblen, T. T., F. M. Schlegel, and B. Escobar R. 1980. Structure and Dynamics of Old-Growth Nothofagus Forests in the Valdivian Andes, 

Chile. J. Ecol. 68: 1–31.

Veblen, T. T., and G. H. Stewart. 1982. On the Conifer Regeneration 

Gap in New Zealand: The Dynamics of Libocedrus bidwillii Stands 

on South Island. J. Ecol. 70: 413–436.

Vincens, A., J.-J. Tiercelin, and G. Buchet. 2006. New Oligocene–Early 

Miocene Microflora from the Southwestern Turkana Basin: Palaeoenvironmental Implications in the Northern Kenya Rift. Palaeogeogr. Palaeoclimatol. Palaeoecol. 239: 470–486.

Wells, A., R. P. Duncan, and G. H. Stewart. 2001. Forest Dynamics 

in Westland, New Zealand: The Importance of Large, Infrequent 

Earthquake-Induced Disturbance. J. Ecol. 89: 1006–1018.

West, A. G., J. J. Midgley, and W. J. Bond. 2000. Regeneration Failure 

and the Potential Importance of Human Disturbance in a Subtropical Forest. Appl. Veg. Sci. 3: 223–232.

White, F. 1978. The Afromontane Region. In Biogeography and Ecology 

of Southern Africa, M. J. A. Werger, ed., pp. 465–513. Dr W. Junk, 

The Hague Netherlands.

White, F. 1981. The History of the Afromontane Archipelago and the 

Scientific Need for Its Conservation. African J. Ecol. 19: 33–54.

Wirminghaus, J. O., C. T. Downs, C. T. Symes, and M. R. Perrin. 2002. 

Diet of the Cape Parrot, Poicephalus robustus, in Afromontane 

Forests in Kwazulu-Natal, South Africa. Ostrich 73: 20–25.

Wubet, T., I. Kottke, D. Teketay, and F. Oberwinkler. 2003. Mycorrhizal 

Status of Indigenous Trees in Dry Afromontane Forests of Ethiopia. 

Forest Ecol. Managem. 179: 387–399.

Wubet, T., M. Weiss, I. Kottke, and F. Oberwinkler. 2006. Two Threatened Coexisting Indigenous Conifer Species in the Dry Afromontane Forests of Ethiopia Are Associated with Distinct Arbuscular 

Mycorrhizal Fungal Communities. Canad. J. Bot. 84: 1617–1627.
6 The Ecology of Podocarps 

in Tropical Montane Forests 

of Borneo: Distribution, 

Population Dynamics, and 

Soil Nutrient Acquisition

Kanehiro Kitayama, Shin-ichiro Aiba, 

Masayuki Ushio, Tatsuyuki Seino, 

and Yasuto Fujiki

ABSTRACT. We review the ecology of podocarps on various soil types in Borneo, 

largely relying on our studies conducted on Mount Kinabalu. Podocarps are generally 

abundant in montane forests, but their abundance varies with soil nutrient status, and 

they can occur in lowland forests where soil nutrients are scarce. These patterns suggest 

control by soil nutrients rather than by temperature. Analyses of population structure, 

growth rate, and crown light conditions in montane forests indicate that podocarps are 

generally shade intolerant and require canopy gaps or sparse canopy for regeneration. 

Podocarps have greater maximum tree sizes than most co-occurring angiosperm species 

in Mount Kinabalu forests. Once they reach the upper canopy layer, they persist for a 

long time because of their long life span, allowing them to regenerate in rare events of 

canopy disturbance. The roots of two podocarp species (Dacrycarpus imbricatus and 

Dacrydium gracile) showed a greater acid phosphatase activity when compared with angiosperm roots within the same lower montane forest. Moreover, an analysis using lipid 

biomarkers indicated that saprophytic fungi are more abundant in the soils beneath the 

two podocarps than beneath angiosperms, and a fungal biomarker lipid correlated with 

soil acid phosphatase activity. The dominance of saprophytic fungi appears to be related 

to high soil acid phosphatase activity, suggesting feedback effects between the podocarps 

and soil microbial communities. These results indicate that podocarps are efficient in 

the acquisition of phosphorus from the acidic montane soils and decomposing litter. We 

suggest that the architectural and life history advantages and physiological adaptations 

to nutrient limitation are essential for the persistence of podocarps, despite their lower 

shade tolerance as compared to angiosperms.

Kanehiro Kitayama, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan. 

Shin-ichiro Aiba, Graduate School of Science and 

Engineering, Kagoshima University, Kagoshima 

890-0065, Japan. Masayuki Ushio and Yasuto 

Fujiki, Center for Ecological Research, Kyoto 

University, 509-3 Hirano 2-chome, Otsu, Shiga 

520-2113, Japan. Tatsuyuki Seino, Yatsugatake 

Forest, University of Tsukuba, Minamimaki, Nagano 384-1305, Japan. Correspondence: Kanehiro Kitayama, kanehiro@kais.kyoto-u.ac.jp.

Manuscript received 13 April 2010; accepted 

9 July 2010.
102 • smithsonian contributions to botany

INTRODUCTION

The contemporary landscapes of Borneo are characterized by towering, evergreen broad-leaved tropical 

rainforests. Because the family Dipterocarpaceae is the 

dominant element, they are called mixed dipterocarp forest (Richards, 1996). The Gnetaceae, usually lianas, is 

the only gymnosperm family that is relatively common 

in such mixed dipterocarp forests. Because families in the 

Coniferales are virtually absent in mixed dipterocarp forests, plant ecologists may have the false impression that 

conifers are not physiologically adaptive to hot tropical 

climates. Richards (1996) illustrated that the Coniferales, 

including the Podocarpaceae, increases in abundance with 

increasing altitude in the paleotropics (Africa and Southeast Asia, including New Guinea). Similarly, Veblen et al. 

(2005) stated that podocarps were generally restricted to 

montane cloud forests in tropical South America.

Although the patterns illustrated by Richards (1996) 

and Veblen et al. (2005) are real, they do not necessarily 

mean that the Podocarpaceae is a cool-climate element in 

the tropics, because soil nutrients may affect its distribution. There is a general trend in the tropics that lowland 

forests are limited by phosphorus availability and montane 

forests by nitrogen availability; in particular, soil nitrogen 

availability declines with increasing altitude, reflecting 

slower rates of mineralization (Tanner et al., 1998). Thus, 

it is not obvious that temperature, rather than nutrients, 

most strongly limits the distribution of the Podocarpaceae. 

In this review we illustrate the distribution patterns of 

the Podocarpaceae (and associated taxa) on various soil 

types in Borneo and suggest that they are controlled by 

soil nutrients more than by temperature. Our model site is 

Mount Kinabalu (Figure 6.1) in Sabah, a Malaysian state 

found in the north tip of Borneo.

Mount Kinabalu (4,095 m, 06°05'N, 116°33'E) is 

nonvolcanic and is the highest mountain in Southeast Asia 

between the Himalayas and New Guinea. The summit and 

adjacent areas are protected within the Kinabalu Park. 

Diverse pristine rainforests, which are all evergreen, occur from 300 m to the forest limit at 3,700 m (Kitayama, 

1992a). The climate is humid tropical, with a weak influence of the Asiatic monsoon. Mean annual air temperature 

is 18.3°C at 1,560 m and decreases linearly with increasing altitude, with a mean lapse rate of 0.55°C per 100 m 

(Kitayama, 1992a). Month-to-month thermal seasonality 

is generally <2°C. Mean atmospheric saturation deficits 

become less negative upslope as a function of decreasing 

air temperature. Mean annual rainfall during 1994–1997 

was approximately 2,300 mm at all altitudes. Longer-term 

measurements may, however, demonstrate a much greater 

year-to-year variation in rainfall. 

The geological substrates below 3,000 m consist of 

large areas of Tertiary sedimentary rocks with mosaics of 

ultramafic rocks (Jacobson, 1970). The folding of the sedimentary rocks occurred in the middle Miocene (15 mya), 

and the ultramafic rocks were probably up-faulted into the 

sedimentary rocks at that time. The summit area above 

3,000 m consists of granitic (adamellite) rocks. The intrusion of the batholithic granite through sedimentary rocks 

started in the upper Miocene (7–9 mya), and the summit 

is still being uplifted. The ultramafic rocks are remarkably 

high in magnesium and low in phosphorus compared with 

sedimentary and granitic rocks found in the area. 

Forest ecosystems of Mount Kinabalu were recently 

investigated intensively with permanent plots at various 

altitudes on different surface geologies (Kitayama et al., 

1998, 2004; Aiba and Kitayama, 1999; Kitayama and 

Aiba, 2002; Takyu et al., 2002; Aiba et al., 2004, 2005, 

2006, 2007; T. Seino and K. Kitayama, unpublished). Forest function, nutrient dynamics, and the populations of all 

trees >5 cm in diameter at breast height (dbh) were investigated (Table 6.1). In this paper, we review the results 

pertinent to the Podocarpaceae on Mount Kinabalu. 

The genus Phyllocladus is included in Podocarpaceae 

in this paper (see Biffin et al., this volume), although it has 

been elevated to family level in some of the literature (Page, 

1990; Bobrov et al., 1999). Podocarpaceae forms a monophyletic lineage with Araucariaceae within extant conifer 

families in the molecular phylogeny; both families possess 

nodulelike structures on roots and show a geographic distribution biased to the Southern Hemisphere, probably reflecting their Gondwanan origins (Quinn et al., 2002). All 

coniferous species occurring on Mount Kinabalu belong 

to these two families. We therefore include Araucariaceae 

(only the genus Agathis occurs in Borneo) in places because the two families are likely to share some common 

ecological characteristics owing to their common ancestry. 

DISTRIBUTIONAL PATTERN

General Altitudinal Distribution

In the lower montane tropical rainforest at park 

headquarters (1,560 m) of Kinabalu Park, one can easily recognize slightly overtopping crowns of conifers by 

their fine texture (Figure 6.2). These conifers are likely to 

be either of the two abundant podocarps, Dacrycarpus 

imbricatus and Dacrydium gracile. The other dominant 
number 95 • 103

species include angiosperm trees of the genera Tristaniopsis, Syzygium (both Myrtaceae), and Lithocarpus (Fagaceae). Similar forests characterized by the dominance of 

conifers (especially podocarps) are seen in montane forests 

(subalpine, upper montane, and lower montane forests; 

Kitayama, 1992a) on Mount Kinabalu above the upper 

limit (1,200 m) of mixed dipterocarp forest. A total of 20 

species of conifer (three Araucariaceae and 17 Podocarpaceae, including one Phyllocladus) have been recorded 

on Mount Kinabalu (Beaman and Beaman, 1998).

Conifers have long been considered an important 

“montane” floristic element on Mount Kinabalu (van 

Steenis, 1964; Meijer, 1965). Quantitative analysis of the 

vegetation on zonal soils from the lowlands to the upper limit of forest (600–3,400 m) supported this general 

pattern: podocarps and other conifers were recorded only 

at ≥1,400 m (Kitayama, 1992a). Podocarps were notably 

dominant from 2,800 to 3,400 m (Kitayama, 1992b), although the number of podocarp species peaked at 1,500–

1,600 m (Beaman and Beaman, 1998). Therefore, at first 

glance, the distribution of podocarps appears to be controlled by climate (primarily by temperature). 

Analyses of the altitudinal distribution patterns of 

trees on different geological substrates on Mount Kinabalu 

(Aiba and Kitayama, 1999), however, suggest that the occurrence of podocarps is, in reality, controlled by a more 

complex interaction of climate and soil conditions (Figure 6.3). The abundance of podocarps at a site generally increases with altitude, but it can vary from site to 

site depending on geology. As has been stated, on zonal 

FIGURE 6.1. Mount Kinabalu viewed from the park headquarters (1,560 m) on the south slope.
104 • smithsonian contributions to botany

soils derived from sedimentary or granitic rocks, the genera Dacrycarpus and Dacrydium are the dominant podocarps in the most developed forests on gentle slopes in the 

montane zone or above. Podocarps, which are otherwise 

exclusively montane, occur at a lower altitude of 700 m 

on soils derived from ultramafic rock, suggesting that soil 

conditions can strongly influence their distribution. The 

phylogenetically associated family Araucariaceae (Agathis 

borneensis in lowland forests and A. kinabaluensis in montane forests) also demonstrates a staggered, lowered altitudinal distribution on soils derived from ultramafic rock. 

Podocarps and Agathis borneensis can occur at sea 

level in Borneo on sandy or swampy soils (de Laubenfels, 

1988; Miyamoto et al., 2003; Nishimura et al., 2007). A 

low-stature evergreen forest, consisting of slender gnarled 

trees, occurs on nutrient-impoverished, sandy Spodosols 

(Soil Survey Staff, 1999), and the forest is termed “heath 

forest.” In the southwestern lowlands of interior Sabah, 

Dacrydium pectinatum is among the dominant species 

of heath forest at 500 m (Figure 6.4). The relative basal 

area of Dacrydium can exceed 40%, and Myrtaceae and 

Dipterocarpaceae compose the bulk of the rest in this forest (K. Takahashi and K. Kitayama, Kyoto University, 

unpublished data). This again suggests that the altitudinal distribution of podocarps is “lowered” on nutrientimpoverished soils. 

All of the podocarp species (as well as Agathis species) 

have broad altitudinal ranges on Mount Kinabalu. Dacrycarpus imbricatus was once believed to occur from 1,400 

up to 4,000 m. After a taxonomic revision, however, the 

TABLE 6.1. Description of sample plots established on different geological substrates on Mount Kinabalu.

Exact Tree

elevation Area density Altitudinal Surface Census

(m) (ha) (ha−1) a zone b geology c Topography d year Reference

Nonultramafic rock (zonal soil)

 650 1.00 1,055 e L T S 1996 Aiba and Kitayama (1999)

1,560 1.50 f 1,921 LM T L 1997, 2002 Takyu et al. (2002), Kitayama et al. (2004), 

Aiba et al. (2006)

1,560 0.10 3,030 LM T M 1997 Takyu et al. (2002)

1,560 0.05 3,300 LM T R 1997 Takyu et al. (2002)

1,860 1.00 1,951 LM Q L 1996 Takyu et al. (2002), Kitayama et al. (2004)

1,860 0.10 2,450 LM Q M 1997 Takyu et al. (2002)

1,860 0.05 3,180 LM Q R 1997 Takyu et al. (2002)

1,950 0.50 1,624 LM T g V 2000 T. Seino and K. Kitayama (unpublished)

2,590 0.25 2,116 UM T S 1995 Aiba and Kitayama (1999)

3,080 0.20 3,665 SA G S 1995 Aiba and Kitayama (1999)

Ultramafic rock (azonal soil)

 700 1.00 1,195 e L S S 1996 Aiba and Kitayama (1999)

1,860 0.20 3,445 LM S L 1995 Aiba and Kitayama (1999), Takyu et al. 

(2002)

1,860 0.10 4,190 LM S M 1997 Takyu et al. (2002)

1,860 0.05 4,100 LM S R 1997 Takyu et al. (2002)

2,700 0.20 3,775 UM S S 1995 Aiba and Kitayama (1999)

3,050 0.06 4,383 SA S S 1995 Aiba and Kitayama (1999)

a Stems ≥5 cm diameter at breast height. 

b L, lowland; LM, lower montane; UM, upper montane; SA, subalpine zones (Kitayama, 1992a). 

c T, Tertiary sedimentary rock; Q, Quaternary sediment; G, granite; S, serpentine rock.

d L, lower slope; M, middle slope; R, ridge top; S, side slope; V, valley bottom.

e Estimates based on the entire plot (1 ha) for stems 10 cm diameter at breast height and subsamples (0.20 ha) for stems <10 cm diameter at breast 

height. 

f A single 1-ha plot censused in 1997 and two 0.25-ha plots censused in 2002.

g The surface geology of this site appears to include various rock types (Quaternary sediment and ultramafic rock), although the site is mapped within an 

area of Tertiary sedimentary rock in Jacobson (1970).
number 95 • 105

plants at the upper slope were split as an endemic species, 

D. kinabaluensis. The latter species occurs most abundantly (with 5% relative basal area or greater) at altitudes 

higher than 2,800 m on both ultramafic and sedimentary 

rocks (Kitayama, 1992a; Aiba and Kitayama, 1999). Five 

species of Dacrydium occur between 800 and 3,700 m 

(Beaman and Beaman, 1998; although occurrence of one 

species is questionable). Phyllocladus hypophyllus also 

occurs widely from 1,200 up to 4,000 m. These distribution patterns suggest that podocarps have potentially wide 

physiological ranges. Three species of Agathis (Araucariaceae) are recorded from the somewhat narrower range 

from 800 to 2,200 m. 

Although podocarps (the genera Dacrycarpus and 

Dacrydium in particular) have a potentially wide altitudinal range, there is a distribution gap between 2,000 

and 2,800 m on gentle slopes on sedimentary soils (corresponding to the upper montane tropical rainforest) where 

Dacrycarpus does not occur (Kitayama, 1992a). Aiba and 

Kitayama (1999) also found only one podocarp species 

(Phyllocladus hypophyllus) in an upper montane cloud 

forest on sedimentary soils at 2,590 m. The soils in the upper montane forest are commonly waterlogged and chemically reduced because of persistent cloud and rainfall and 

may be too wet for the other conifers. Indeed, podocarps 

can frequently occur on steep ridges on sedimentary rock 

FIGURE 6.2. The canopy of lower montane tropical rainforest on Mount Kinabalu at 1,560 m, where several of the studies described in this 

chapter were conducted. This forest is dominated by Dacrycarpus imbricatus and Dacrydium gracile.
106 • smithsonian contributions to botany

or gentle slopes on ultramafic rock in this zone (Kitayama, 

1995). At these sites, water permeability is high because 

of steep topography and, on ultramafic soils, the presence 

of iron oxides, which have a low affinity with water. Dacrycarpus gains dominance in the slightly drier subalpine 

zone (2,800 m), which is above the persistent cloud. 

Dacrydium occurs in low abundance in the lower montane zone but does not occur in the upper zone except on 

ridgetops and ultramafic soils. As explained above, podocarps do occur on waterlogged soils elsewhere in Borneo, 

and we do not know why they are absent from such soils 

on Mount Kinabalu.

Although conifers co-occur with angiosperms, the 

“additive basal area phenomenon” (Enright and Ogden, 1995; Aiba et al., 2007) is not evident on Mount 

Kinabalu. This phenomenon is often reported for mixed 

conifer–angiosperm forests in the Southern Hemisphere, 

in which the high basal area of conifers does not cause the 

reduction of basal area of angiosperms. 

Response to Variation in Soil Nutrients

The above description suggests that soil conditions rather than climate may impose the main control 

FIGURE 6.3. (top) Basal area and (bottom) number of species of conifer families (Podocarpaceae 

and Araucariaceae) for trees ≥5 cm diameter at breast height in sample plots on side slopes (including lower slopes and valley bottom) established on two geological substrates along elevational 

gradients on Mount Kinabalu. The basal area of angiosperm trees combined is also shown. Rock 

types are indicated for nonultramafic series as follows: S = Tertiary sedimentary rock, Q = Quaternary sediments, G = granite. The surface geology of the site indicated by an asterisk (*) may include 

various rock types; see footnote g of Table 6.1. The number of species for the plot at 700 m on 

ultramafic rock [indicated by a dagger (†)] includes one podocarp species that occurs just outside 

the plot (Dacrycarpus imbricatus).
number 95 • 107

on the occurrence of podocarps and other conifers on 

Mount Kinabalu. Variation in podocarp abundance appears to be correlated with net soil nitrogen mineralization rate (Figure 6.5). Takyu et al. (2002) investigated 

tree species composition in nine lower montane forests 

at 1,560–1,860 m on Mount Kinabalu, including ridge, 

middle-slope, and lower-slope forests, each occurring on 

unconsolidated Quaternary sediment (colluvial deposits 

of sedimentary rocks), Tertiary sedimentary rock, and ultramafic rock (Table 6.1). Soil nitrogen availability generally decreases from Quaternary to Tertiary to ultramafic 

(most nutrient deficient) and from lower slope to middle 

slope to ridge (most nutrient deficient) on each substrate. 

With this combination of site conditions, the abundance 

of podocarps generally decreases with increasing nitrogen 

availability (r = -0.47, p = 0.203), significantly so when 

all conifers (including Agathis) were included (r = -0.67, 

p = 0.049). It has been demonstrated that soil phosphorus 

availability also changes with geological substrate and topography in a manner similar to soil nitrogen (Kitayama 

and Aiba, 2002; Kitayama et al., 2004). Therefore, nitrogen in concert with phosphorus may be important in determining the abundance of podocarps and other conifers 

in the lower montane zone of Mount Kinabalu.

Kitayama et al. (2004) compared soil phosphorus 

availability in two lower montane tropical rainforests with 

FIGURE 6.4. Heath forest on white silica 

sands in the interior of Sabah, north Borneo, 

at 500 m. Dacrydium pectinatum is the dominant species in this nutrient-impoverished 

forest.
108 • smithsonian contributions to botany

similar air temperature regimes but on different geological 

substrates: highly weathered soils on stable, old Tertiary 

sedimentary rocks and undeveloped soils on unconsolidated Quaternary sediment (Table 6.1). Concentrations of 

labile and total phosphorus were much lower in the old 

soils and appeared to control primary productivity. Podocarps are among the dominant trees in forests growing on 

old soils but are very rare in the forest growing on young 

soils, suggesting that phosphorus availability alone or in 

concert with nitrogen availability controlled the occurrence of podocarps at these sites. 

POPULATION ECOLOGY IN 

MONTANE FORESTS

Diameter Distribution

In the montane (and subalpine) forests on Mount 

Kinabalu, podocarps and the associated conifer Agathis 

kinabaluensis do not necessarily appear to be competitive 

with angiosperm trees in terms of aboveground competition for light. Figure 6.6 demonstrates the diameter size 

class distribution of conifers (podocarps and A. kinabaluensis) and angiosperm trees in three upland forests on 

zonal soils derived from sedimentary or granitic rocks 

and two forests on soils derived from ultramafic rocks. 

Conifers are minor elements in terms of the number of 

stems, but they constitute a substantial fraction of largesized stems, resulting in a relatively large basal area (Figure 6.3). Individual conifer species usually show flat or 

monomodal diameter distributions with few small trees, 

which indicates that they are shade intolerant (Figure 6.7). 

Occasionally, some conifers show an L-shaped diameter 

distribution with abundant small trees. However, the canopy layers in such forests are sparse, which allows smaller 

conifer trees to persist in the understory layer. These cases 

are rather rare. Dacrycarpus kinabaluensis found at 3,080 

m on granite showed extremely unimodal diameter distribution, which might reflect an episodic recruitment 

following large-scale disturbance (e.g., El Niño–related 

drought or landslides). Falcatifolium falciforme at 1,560 

m on sedimentary rock is exceptional in that it shows 

clearly an L-shaped diameter distribution and saplings 

grow abundantly in shaded conditions of the forest understory (see below). 

Diameter Growth Rate and

Crown Light Condition

A detailed study of growth and crown conditions for 

42 abundant tree species was conducted for stems 10 cm 

dbh in the lower montane forest at 1,560 m on sedimentary rock (Aiba et al., 2004, 2006). These species include 

four conifers (all podocarps) and 38 angiosperms. The 

study involved the investigation of overshading of each 

individual and its growth rate. The condition of overshading was expressed as a crown position index, which ranges 

from 1 (fully lit condition without any portion of neighboring crowns above that tree) to 4 (fully shaded by neighboring crowns above that tree). Podocarps other than 

Falcatifolium falciforme were characterized by well-lit 

crowns and high trunk diameter growth rates (Figure 6.8). 

These characteristics suggests that in this forest podocarps 

are light-demanding, relatively fast-growing species that 

require canopy gaps (e.g., by tree fall and slope failure) 

for regeneration and that in closed-canopy forests they are 

competitively inferior to angiosperms that are generally 

more shade tolerant. It is expected that podocarps would 

be eliminated from the forest in the absence of canopy 

disturbance. 

Frequent disturbance might allow podocarps to persist in montane forest on Mount Kinabalu despite their 

FIGURE 6.5. The relationships between net soil nitrogen mineralization rate and the relative basal areas of podocarp and conifer species 

in nine tropical rainforests of the lower montane zone on Mount 

Kinabalu. Net soil nitrogen mineralization rate was determined by 

10-day incubation of forest soils in polyethylene bags (Takyu et al., 

2002).
number 95 • 109

inferiority to angiosperms in shade tolerance. However, 

montane (and subalpine) forests are generally less dynamic than lowland forests on Mount Kinabalu in terms 

of population turnover rate (Aiba et al., 2005), suggesting 

less-frequent disturbance at higher elevations. This characteristic seems to be true even when irregular droughts 

associated with El Niño, which have inflated tree mortality, especially at higher elevations, are taken into account. 

Podocarps grow slowly because of light limitation in the 

forest understory. They can successfully regenerate only in 

well-lit conditions, but angiosperm pioneers of such genera as Macaranga and Ficus presumably outcompete podocarps on nutrient-rich soils. Only on the nutrient-deficient 

soils in the montane forest where angiosperms grow slowly 

because of nutrient limitation can podocarps outcompete 

angiosperm pioneers. 

ADVANTAGES AND ADAPTATIONS

In the above two sections, we described the distribution patterns, population structure, and growth rate of 

podocarps in the mixed evergreen conifer–broad-leaved 

tropical rainforests on Mount Kinabalu. Evidence suggests 

that podocarps have a wide temperature range (physiological niche) but are competitively inferior to co-occurring 

FIGURE 6.6. Diameter distribution of conifers (Podocarpaceae and Araucariaceae) and angiosperm trees in the sample plots where conifers attain dominance at various altitudes on different 

geological substrates. Note that the scales of the vertical axis differ among plots. The site indicated 

by an asterisk (*) appears to include various rock types; see footnote g of Table 6.1.
110 • smithsonian contributions to botany

angiosperms, particularly in competition for light. It seems 

that when the availability of soil nutrients (nitrogen and/

or phosphorus) is limited, podocarps can outcompete cooccurring angiosperms. In the following section, we discuss the architectural and life history advantages and the 

physiological adaptations to such nutrient limitation that 

allow podocarps to persist in the contemporary landscapes 

of the Bornean tropics.

Architectural and Life History Advantages

Podocarps consistently form an uppermost canopy 

layer in the lower montane forest of Mount Kinabalu, giving an impression of their predominance. The formation of 

such an upper layer is not a transient process but contributes to a persistent forest structure based on their architectural traits. Figure 6.9 shows dbh–height relationships 

FIGURE 6.7. Diameter distribution of abundant conifers (sample size ≥15) in the sample plots where 

conifers attain dominance. All species belong to Podocarpaceae except for Agathis kinabaluensis

(Araucariaceae). Note that the scales of the vertical axis differ among plots. The site indicated by an 

asterisk (*) appears to include various rock types; see footnote g of Table 6.1.
number 95 • 111

among co-occurring podocarps (Dacrycarpus kinabaluensis, Dacrydium gibbsiae, and Phyllocladus hypophyllus), associated Agathis kinabaluensis, and angiosperms in 

the lower montane forest at 1,950 m on “sedimentary” 

rock (see footnote g of Table 6.1). Two dominant conifers 

(Dacrycarpus and Agathis) attained a greater size in terms 

of both diameter and height than angiosperm trees. Moreover, when dbh–height relationships (log-transformed) 

were analyzed by analysis of covariance, the intercepts differed between conifers and angiosperms, and conifers were 

taller than angiosperm trees at a given diameter (Aiba et 

al., 2007). Thus, shade-intolerant conifers can survive in 

the forest by occupying an upper canopy layer where they 

can receive much sunlight.

For the above forest, we also estimated turnover time 

of the two dominant conifers Dacrycarpus kinabaluensis

and Agathis kinabaluensis from the increase in basal area 

of surviving trees over nine years (2000–2009), assuming 

that basal areas of individual species are in equilibrium 

(i.e., an increase in growth is balanced by a decrease in 

death if a sufficiently long period is considered). The turnover times of conifers were 168 years for Dacrycarpus 

and 364 years for Agathis, which were substantially longer than those of angiosperm trees (mean of 105 years for 

all species combined). Bornean conifers can therefore be 

regarded as long-lived trees that have many opportunities 

to regenerate during their life spans.

Acquisition of Phosphorus: 

Acid Phosphatase Activity of Podocarp Roots

The soils of the tropical lower montane forests on sedimentary rock on Mount Kinabalu (where podocarps often 

become dominant) are broadly categorized as Spodosols, 

which are highly acidic (pH 3.1–4.0 in the surface horizon) 

and impoverished in soluble inorganic forms of phosphorus 

and nitrogen (Kitayama et al., 1998; Kitayama and Aiba, 

2002). Kitayama et al. (2004) demonstrated that soils in 

the lower montane zone where podocarps were abundant 

were characterized by much lower total phosphorus concentrations than areas in the same zone where podocarps 

were rare. Further, phosphorus fractionation revealed that 

soil phosphorus at sites where podocarps were abundant 

consisted of a high proportion of physically occluded inorganic phosphate and refractory organic phosphorus, with 

low concentrations of labile organic phosphorus. On such 

soils, tree species that can acquire phosphorus from fresh 

litter or can scavenge labile organic phosphorus from the 

surface horizon may have a competitive advantage because 

the solubility of inorganic phosphorus fractions is extremely low. Phosphatase enzymes are required to hydrolyze phosphate from organic phosphorus in litter or soil. 

Phosphatases are excreted by tree roots and, in plants such 

as the Fagaceae, by symbiotic ectomycorrhizal fungi.

Y. Fujiki and K. Kitayama (unpublished) investigated 

acid phosphatase activity on roots systematically for all 

top to middle dominant species across three forests with 

differing soil phosphorus availability in the lower montane 

zone (1,560–1,860 m) on Mount Kinabalu. The analysis 

was conducted on fresh roots of seedlings of podocarps 

and 23 angiosperm species (Fagaceae, Myrtaceae, and 

other families). It should be noted that in the Fagaceae the 

phosphatase activity of symbiotic ectomycorrhizas is also 

likely to have been included in the root measurements. 

Roots were excavated, transported to the laboratory in 

a cooler box, rinsed with pure water, and assayed with 

para-nitrophenyl phosphate (a chromogenic phosphatase substrate) in acetate buffer (pH 5.0). The activity of 

FIGURE 6.8. The relationship between median crown position 

index (CPI) and mean diameter growth rate at 10–40 cm diameter at breast height among 42 abundant tree species in a tropical 

montane forest plot at 1,560 m on sedimentary rock. Triangles indicate conifers (all Podocarpaceae), and dots indicate angiosperms. 

Low median CPI indicates that species are characterized by well-lit 

crowns in heterogeneous canopy structure. Modified from Aiba 

et al. (2004, 2006).
112 • smithsonian contributions to botany

phosphatase is expressed as the amount of product (paranitrophenol) released per surface root area per unit time. 

The mean acid phosphatase activity on roots of Podocarpaceae (Dacrycarpus imbricatus, Dacrydium gibbsiae, 

Dacrydium gracile, Phyllocladus hypophyllus, and Podocarpus gibbsiae) was significantly greater than that of angiosperms (Figure 6.10, linear mixed model, p = 0.03).

The greater ability of podocarp roots to release phosphate from phosphomonoesters in organic matter may 

contribute to the efficient acquisition of phosphorus from 

litter and/or labile organic soil phosphorus fraction. This 

is potentially an important adaptation facilitating the persistence of podocarps on acidic montane Spodosols and is 

consistent with the depletion of inositol phosphate, a common phosphomonoester, as the abundance of podocarps 

increases in old soils along a temperate rainforest chronosequence in New Zealand (Turner et al., 2007). The same 

mechanism is also advantageous on soils derived from ultramafic rocks, in which inorganic phosphate is depleted 

and, consequently, the contribution of organic phosphorus to plant nutrition is relatively important (Kitayama et 

al., 1998; Kitayama and Aiba, 2002)

Symbiotic Nitrogen Fixation

Earlier researchers speculated that podocarp roots 

had the ability to fix nitrogen because of the occurrence of nodule-like structures on the root surface (van 

Tieghem, 1870; Becking, 1965; Silvester and Bennett, 

1973; Dickie and Holdaway, this volume). Roots of podocarp species (Dacrycarpus imbricatus, Dacrydium gracile, 

Falcatifolium falciforme, Podocarpus gibbsiae, and Phyllocladus hypophyllus) from the lower montane tropical 

rainforest at 1,560 m on sedimentary rock were assayed 

FIGURE 6.9. The relationship between diameter at breast height and tree height for conifers and angiosperms at 1,950 m on sedimentary rock (see footnote g of Table 6.1), measured in a 10 × 100 m 

transect laid in a sample plot. Dacrycarpus kinabaluensis (squares), Podocarpus gibbsiae (triangles), 

and Phyllocladus hypophyllus (diamonds) belong to Podocarpaceae, and Agathis kinabaluensis

(circles) belongs to Araucariaceae. Black dots represent angiosperm trees.
number 95 • 113

for nitrogen-fixing ability by following the standard acetylene reduction assay of Hardy et al. (1973) (M. Ushio 

and K. Kitayama, unpublished). Agathis kinabaluensis

was also included in the analysis. Significant ethylene production was not detected in all of these samples (data not 

shown); therefore, podocarps and Agathis kinabaluensis

on Mount Kinabalu did not have nitrogen fixation ability 

(see also Dickie and Holdaway, this volume).

Influences of Podocarps on Saprotrophic

Microbial Communities

The abundance and composition of the soil microbial 

community can be affected by plant species through the 

chemical quality and quantity of their litter (Porazinska 

et al., 2003; Bartelt-Ryser et al., 2005; Kao-Kniffin and 

Balser, 2008). The two podocarp species (Dacrycarpus 

imbricatus and Dacrydium gracile) on Mount Kinabalu 

produce leaves in which the concentration of condensed 

tannins is relatively high compared to co-occurring broadleaved species (S. Suzuki, Institute for Environmental 

Sciences, unpublished data). Condensed tannins can affect 

the composition and abundance of the soil microbial community (Kraus et al., 2003). Therefore, it is possible that 

the podocarp species have impact through the effects of 

foliar condensed tannins on soil microbial communities, 

which in turn affect soil nutrient acquisition by podocarps. 

Ushio et al. (2008) investigated the influences of 

podocarp litter on soil microbial communities in the lower 

montane forest on sedimentary rock at 1,560 m on Mount 

Kinabalu. Two podocarp species (Dacrycarpus imbricatus and Dacrydium gracile) had a distinct impact on the 

abundance and composition of soil microbial community 

(Table 6.2, Figure 6.11). Ushio et al. (2008) collected soil 

samples beneath five tree species (the two podocarps plus 

three angiosperms: Lithocarpus clementianus, Palaquium 

rioense, and Tristaniopsis sp.) that were dominant in this 

forest. The total lipid abundance (a proxy for microbial 

biomass) was greater in soils underneath Dacrydium than 

soils underneath Tristaniopsis (p < 0.05), and the abundance of specific indicator lipids also differed among some 

combinations of tree species (Table 6.2). The ratio of fungi 

to bacteria differed significantly between Dacrycarpus and 

Lithocarpus, between Dacrydium and Lithocarpus, and 

between Dacrydium and Tristaniopsis (p < 0.05). The ratio of Gram+ to Gram– bacteria was significantly higher 

in the soils underneath Dacrydium than in the soils underneath Tristaniopsis (p < 0.05). 

A principal components analysis (the analysis of overall microbial composition) also indicated distinct speciesspecific effects of podocarps (Figure 6.11). Dacrycarpus

and Tristaniopsis (p < 0.05) and Dacrydium and Tristaniopsis (p < 0.01) differed along PC1, whereas Dacrycarpus

and Lithocarpus (p < 0.01) and Dacrycarpus and Palaquium (p < 0.05) differed along the PC2 axis. Thus, mean 

coordinates of Dacrycarpus and Dacrydium (both podocarp species) were not significantly different from each 

other, and they were different from the mean coordinates 

of Tristaniopsis, Lithocarpus, and Palaquium (angiosperms). These results suggest that the primary difference 

in composition of soil microbial communities exist between conifer and angiosperm species, especially in terms 

of the relative dominance of saprophytic fungi.

In addition to the microbial compositions, Ushio et 

al. (2010) investigated the activity of acid phosphatase in 

soils. Since plant roots were carefully removed from soil 

before the measurements of soil enzyme activity, the results 

were thought to reflect the effects of the saprophytic microbial community. They found greater activity of acid phosphatase in the soils beneath Dacrydium than Lithocarpus. 

They also found a significant correlation between acid 

phosphatase and a fungal biomarker lipid (Ushio et al., 

FIGURE 6.10. Mean (± standard deviation) acid phosphatase activity of the roots of podocarp species versus angiosperm species 

in the lower montane forests of Mount Kinabalu. Acid phosphatase activity is expressed as product (para-nitrophenol) released per 

root surface area per unit time. The effects of tree species taxa (i.e., 

podocarps versus angiosperms) on acid phosphatase activity were 

evaluated by a linear mixed model (acid phosphatase activity ~ taxa 

(podocarps or angiosperms), random effects = plant individuals).
114 • smithsonian contributions to botany

2010). Therefore, the dominance of saprophytic fungi may 

be associated with high acid phosphatase activity in the 

soils beneath Dacrydium. However, whether the greater 

acid phosphatase activity feeds back to the performance of 

seedlings underneath a Dacrydium canopy is not known. 

SYNTHESIS

Our review of studies conducted on Mount Kinabalu 

suggests that podocarps regenerate successfully primarily 

under well-lit conditions like canopy gaps. Fast-growing 

angiosperm pioneers (e.g., Macaranga and Ficus species) 

generally outcompete podocarps under well-lit conditions in Bornean tropical rainforests. However, such fastgrowing pioneer species generally have a greater demand 

for nutrients (particularly nitrogen) and thus are considered inefficient in photosynthetic nitrogen use. Such 

nutrient-demanding pioneer species cannot grow well on 

nutrient-limited soils. Furthermore, the montane zone appears to be too cool for angiosperm pioneers, whereas 

podocarps are well adapted to a wide thermal range. 

Podocarps have a greater maximum tree size than 

most co-occurring angiosperm species. Once they reach 

the upper canopy layer, they will persist for a long time 

because of their longer life span, which will allow them 

to regenerate in rare events of canopy gap formation that 

are unpredictable in both space and time. Where canopy 

structure is sparse because of poor tree growth on extremely infertile soils derived from ultramafic rocks, however, some conifer species seem to regenerate continuously.

Our studies also suggest that podocarps (Dacrycarpus imbricatus and Dacrydium gracile) in lower montane tropical rainforest may have a superior ability over 

co-occurring angiosperms in acquiring phosphate from 

organic forms of phosphorus. This ability is consistent 

with the dominance of podocarps on acidic Spodosols 

and soils derived from ultramafic rocks; in both cases labile phosphorus occurs primarily as organic phosphorus, 

and consequently, the dependence of trees (as well as soil 

microbes) on organic phosphorus increases. Because soil 

phosphorus is critical in these ecosystems (Spodosols and 

ultramafic soils), a slight difference in the ability to acquire 

soil phosphorus may explain the difference in photosynthetic ability and growth rate of podocarps compared to 

angiosperms. Angiosperms in these systems possibly cannot outcompete podocarps under conditions where phosphorus availability limits productivity. 

TABLE 6.2. Mean abundance of indicator lipids in soils beneath dominant podocarp and angiosperm tree species in a lower montane 

forest at 1,560 m on Mount Kinabalu. Values within rows having the same superscripted lowercase letter are not significantly different by the Tukey–Kramer honestly significant difference test (for equal variance data) or the Games–Howell test (for unequal variance 

data) (p < 0.05). Gram+ bacteria are the sum of iso-branched and saturated lipids (i14:0, 15:0, i15:0, a15:0, i16:0, 17:0, i17:0, and 

a17:0), actinomycetes are the sum of methyl branched lipids (17:0 10Me and 19:0 10Me), and Gram− bacteria are the sum of monounsaturated and cyclopropyl lipids (16:1ω7, cy17:0, and cy19:0). Saprophytic fungi, ectomycorrhizas/saprophytic fungi, arbuscular 

mycorrhizas, and protozoa are indicated by the lipid abundance of 18:2ω6,9, 18:1ω9, 16:1ω5, and 18:3ω6,9,12, respectively. The 

fungi : bacteria ratio is the sum of abundance of fungal lipids (18:2ω6,9, 18:1ω9) to the sum of Gram+ and Gram– lipids shown here. 

The Gram+ : Gram− ratio is the ratio of the sum of iso- and methyl-branched lipids to the sum of monounsaturated and cyclopropyl 

lipids. Values in parentheses are the standard error of the mean. Data were modified from Ushio et al. (2008).

Measurement

Lipid abundance (nmol g−1)

Dacrycarpus Dacrydium Lithocarpus Palaquium Tristaniopsis

Total lipid 1,617ab (307) 2,309a (240) 1,799ab (336) 1,566ab (346) 1,118b (63)

Gram+ bacteria 170 (39.5) 231 (16.1) 213 (39.0) 185 (42.7) 139 (12.1)

Actinomycetes 24.1a (2.7) 59.7a (9.4) 52.9a (13.2) 42.7ab (16.7) 7.5b (3.2)

Gram− bacteria 90.1 (15.9) 129 (6.4) 128 (22.6) 114 (21.2) 97.6 (8.7)

Saprophytic fungi 112ab (17.0) 157a (15.7) 99.5ab (16.9) 93.9ab (15.7) 76.6b (5.9)

Ectomycorrhizas/saprophytic fungi 141ab (30.8) 181a (11.2) 144ab (17.6) 119ab (13.6) 101b (8.9)

Arbuscular mycorrhizas 69.7ab (13.5) 97.2a (8.6) 69.9ab (15.2) 63.8ab (5.8) 47.5b (4.2)

Protozoa 107 (19.3) 52.8 (6.3) 42.9 (19.5) 46.6 (4.7) 27.3 (5.6)

Fungi : bacteria ratio 0.99ab (0.05) 0.93b (0.04) 0.74c (0.04) 0.75abc (0.06) 0.75ac (0.01)

Gram+ : Gram− ratio 2.11ab (0.13) 2.28a (0.17) 2.06ab (0.17) 1.96ab (0.17) 1.53b (0.14)
number 95 • 115

However, phosphatase synthesis is a nitrogendemanding process because phosphatase enzymes consist of proteins, yet we found no evidence that podocarps 

are superior in soil nitrogen acquisition to angiosperms. 

Kitayama et al. (1998, 2004) suggest that soil nitrogen 

mineralization is down-regulated by a decline in phosphorus availability in these systems, so soil microbes and 

soil nitrogen mineralization appear to be controlled by 

phosphorus availability. Therefore, the mechanisms of soil 

nitrogen acquisition must be resolved before the adaptation of podocarps to the nutrient-limited soils on Mount 

Kinabalu can be fully understood. 

Finally, the phylogenetically associated genus Agathis

(Araucariaceae) seems to share many traits with the podocarps. Comparison with Agathis would be useful to elucidate the unique ecological characteristics of podocarps in 

tropical forests.

Acknowledgments

We thank Sabah Parks for their support of our studies. This study was supported by a Grant-in-Aid from 

the Japanese Ministry of Education, Science, Culture and 

Sports to KK (18255003, 19370010) and by the JSPS AA 

FIGURE 6.11. Principal components analysis (PCA) of soil lipids biomarkers. Lipid abundance 

was converted to mole percent values (each lipid abundance/total lipid abundance). The lipids 

with average mole percent < 0.5% were not included in the analysis. The mole percent values are 

not normally distributed, so the negative arcsine of the square root of each fatty acid mole percentage was used. Each point represents the mean of all soil samples for each species. Dacrycarpus imbricatus (solid circle) and Dacrydium gracile (solid triangle) are podocarps. Lithocarpus

clementianus (solid square), Palaquium rioense (open circle), and Tristaniopsis sp. (open triangle) are angiosperms. Bars indicate the standard error of the mean and the percentages of variance explained by each axis are indicated in parentheses. Reproduced from Ushio et al. (2008).
116 • smithsonian contributions to botany

Science Platform Program to KK. We also thank Neal Enright, Ian Dickie, and Ben Turner for their comments on 

the manuscript.

REFERENCES

Aiba, S., G. Hanya, R. Tsujino, M. Takyu, T. Seino, K. Kimura, and 

K. Kitayama. 2007. Comparative Study of Additive Basal Area of 

Conifers in Forest Ecosystems along Elevational Gradients. Ecol. 

Res. 22: 439–450.

Aiba, S., and K. Kitayama. 1999. Structure, Composition and Species 

Diversity in an Altitude-Substrate Matrix of Rain Forest Tree Communities on Mount Kinabalu, Borneo. Pl. Ecol. 140: 139–157.

Aiba, S., K. Kitayama, and M. Takyu. 2004. Habitat Associations with Topography and Canopy Structure of Tree Species in a Tropical Montane Forest on Mount Kinabalu, Borneo. Pl. Ecol. 174: 147–161.

Aiba, S., E. Suzuki, and K. Kitayama. 2006. Structural and Floristic Variation among Small Replicate Plots of a Tropical Montane Forest on 

Mount Kinabalu, Sabah, Malaysia. Tropics 15: 219–236.

Aiba, S., M. Takyu, and K. Kitayama. 2005. Dynamics, Productivity 

and Species Richness of Tropical Rainforests along Elevational and 

Edaphic Gradients on Mount Kinabalu, Borneo. Ecol. Res. 20: 

279–286.

Bartelt-Ryser, J., J. Joshi, B. Schmid, H. Brandl, and T. Balser. 2005. Soil 

Feedbacks of Plant Diversity on Soil Microbial Communities and 

Subsequent Plant Growth. Perspect. Pl. Ecol. Evol. Syst. 7: 27–49

Beaman, J. H., and R. S. Beaman. 1998. The Plants of Mount Kinabalu. 

Volume 3. Gymnosperms and Non-Orchid Monocotyledons. Natural History Publications, Kota Kinabalu, Malaysia.

Becking, J. H. 1965. Nitrogen Fixation and Mycorrhiza in Podocarpus 

Root Nodules. Pl. Soil 23: 213–226.

Biffin, E., J. Conran, and A. Lowe. 2011 (this volume). Podocarp Evolution: A Molecular Phylogenetic Perspective. In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 1–20. Smithsonian Contributions to Botany, No. 95. 

Smithsonian Institution Scholarly Press, Washington, D.C.

Bobrov, A. V., A. P. Melikian, and E. Y. Yembaturova. 1999. Seed Morphology, Anatomy and Ultrastructure of Phyllocladus L.C. & 

A. Rich. ex Mirb. (Phyllocladaceae (Pilg.) Bessey) in Connection with 

the Generic System and Phylogeny. Ann. Bot. (London) 83: 601–618.

de Laubenfels, D. J. 1988. Coniferales. Fl. Malesiana, Ser. 1, Spermatoph.

10: 337–453.

Dickie, I. A., and R. J. Holdaway. 2011 (this volume). Podocarp Roots, 

Mycorrhizas, and Nodules. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 175–

187. Smithsonian Contributions to Botany, No. 95. Smithsonian 

Institution Scholarly Press, Washington, D.C.

Enright, N. J., and J. Ogden. 1995. The Southern Conifers—A Synthesis. 

In Ecology of the Southern Conifers, N. J. Enright and H. S. Hill, 

eds., pp. 271–287. Melbourne University Press, Carlton, Australia.

Hardy, R. W. F., R. C. Burns, and R. D. Holsten. 1973. Applications of 

the Acetylene-Ethylene Assay for Measurement of Nitrogen Fixation. Soil Biol. Biochem. 5: 47–81.

Jacobson, G. 1970. Gunong Kinabalu Area, Sabah, Malaysia. Report 8.

Geological Survey of Malaysia, Kuching, Malaysia.

Kao-Kniffin, J., and T. C. Balser. 2008. Soil Fertility and the Impact of 

Exotic Invasion on Microbial Communities in Hawaiian Forests. 

Microbial Ecol. 56: 55–63

Kitayama, K. 1992a. An Altitudinal Transect Study of the Vegetation on 

Mount Kinabalu, Borneo. Vegetatio 102: 149–171.

Kitayama, K. 1992b. Comparative Vegetation Analysis on the Wet 

Slopes of Two Tropical Mountains: Mt. Haleakala, Hawaii and Mt. 

Kinabalu, Borneo. Ph.D. thesis, Botany Department, University of 

Hawaii, Honolulu.

Kitayama, K. 1995. Biophysical Conditions of the Montane Cloud Forests of Mount Kinabalu, Sabah, Malaysia. In Tropical Montane 

Cloud Forests, L. S. Hamilton, J. O. Juvik, and F. N. Scatena, eds., 

pp. 183–197. Springer-Verlag, New York.

Kitayama, K., and S. Aiba. 2002. Ecosystem Structure and Productivity 

of Tropical Rain Forests along Altitudinal Gradients with Contrasting Soil Phosphorus Pools on Mount Kinabalu, Borneo. J. Ecol.

90: 37–51.

Kitayama, K., S. Aiba, N. Majalap-Lee, and M. Ohsawa. 1998. Soil Nitrogen Mineralization Rates of Rainforests in a Matrix of Elevations and Geological Substrates on Mount Kinabalu, Borneo. Ecol. 

Res. 13: 301–312.

Kitayama, K., S. Aiba, M. Takyu, N. Majalap, and R. Wagai. 2004. Soil 

Phosphorus Fractionation and Phosphorus-Use Efficiency of a Bornean Tropical Montane Rain Forest during Soil Aging with Podozolization. Ecosystems 7: 259–274.

Kraus, T. E. C., R. A. Dahlgren, and R. J. Zasoski. 2003. Tannins in 

Nutrient Dynamics of Forest Ecosystems—A Review. Pl. Soil 256: 

41–66.

Meijer, W. 1965. A Botanical Guide to the Flora of Mount Kinabalu. In 

Symposium on Ecological Research in Humid Tropics Vegetation, 

pp. 325–364. Government of Sarawak, Kuching, Malaysia.

Miyamoto, K., E. Suzuki, T. Kohyama, T. Seino, E. Mirmanto, and 

H. Simbolon. 2003. Habitat Differentiation among Tree Species 

with Small-Scale Variation of Humus Depth and Topography in a 

Tropical Heath Forest of Central Kalimantan, Indonesia. J. Trop. 

Ecol. 19: 43–54.

Nishimura, T. B., E. Suzuki, T. Kohyama, and S. Tsuyuzaki. 2007. Mortality and Growth of Trees in Peat-Swamp and Heath Forests in 

Central Kalimantan after Severe Drought. Pl. Ecol. 188: 165-177.

Page, C. N. 1990. Phyllocladaceae. In Volume 1: Pteridophytes and 

Gymnosperms, K. Kubitzki, ed., pp. 317–319, The Families and 

Genera of Vascular Plants. Springer-Verlag, Berlin.

Porazinska, D. L., R. D. Bardgett, M. B. Blaauw, H. W. Hunt, A. N. 

Parsons, T. R. Seastedt, and D. H. Wall. 2003. Relationships at the 

Aboveground-Belowground Interface: Plants, Soil Biota, and Soil 

Processes. Ecol. Monogr. 73: 377–395.

Quinn, C. J., R. A. Price, and P. A. Gadek. 2002. Familial Concepts and 

Relationships in the Conifers Based on rbcL and matK Sequence 

Comparisons. Kew Bull. 57: 513–531.

Richards, P. W. 1996. The Tropical Rain Forest. 2nd ed. Cambridge University Press, Cambridge.

Silvester, W. B., and K. J. Bennett. 1973. Acetylene Reduction by Roots 

and Associated Soil of New Zealand Conifers. Soil Biol. Biochem. 

5: 171–179.

Soil Survey Staff. 1999. Soil Taxonomy, A Basic System of Soil Classification for Making and Interpreting Soil Surveys, 2nd ed. U.S. 

Department of Agriculture, Washington, D.C.

Takyu, M., S. Aiba, and K. Kitayama. 2002. Effects of Topography on 

Tropical Lower Montane Forests under Different Geological Conditions on Mount Kinabalu, Borneo. Pl. Ecol. 159: 35–49.

Tanner, E. V. J., P. M. Vitousek, and E. Cuevas. 1998. Experimental Investigation of Nutrient Limitation of Forest Growth on Wet Tropical Mountains. Ecology 79: 10–22.

Turner, B. L., L. M. Condron, S. J. Richardson, D. A. Peltzer, and V. J. 

Allison. 2007. Soil Organic Phosphorus Transformations during 

Pedogenesis. Ecosystems 10: 1166–1181.

Ushio, M., R. Wagai, T. C. Balser, and K. Kitayama. 2008. Variations in 

the Soil Microbial Community Composition of a Tropical Montane 

Forest Ecosystem: Does Tree Species Matter? Soil Biol. Biochem. 

40: 2699–2702.

Ushio, M., K. Kitayama, and T. C. Balser. 2010. Tree Species Effects 

on Soil Enzyme Activities Through Effects on Soil Physicochemi-
number 95 • 117

cal and Microbial Properties in a Tropical Montane Forest on Mt. 

Kinabalu, Borneo. Pedobiologia 53: 227–233.

van Steenis, C. G. G. J. 1964. Plant Geography of the Mountain Flora of 

Mt Kinabalu. Proc. Roy. Soc. London, Ser. B, Biol. Sci. 161: 7–38.

van Tieghem, P. 1870. Recherches sur la symétrie de structure des plantes 

vasculaires. Ann. Sci. Nat. Bot. 5: 5–314.

Veblen, T. T., J. J. Armesto, B. R. Burns, T. Kitzberger, A. Lara, B. Leon, 

and K. R. Young. 2005. The Coniferous Forests of South America. 

In Volume 6: Coniferous Forests, F. Andersson, ed., pp. 293–317, 

Ecosystems of the World. Elsevier, Amsterdam.

7 Temperate and Tropical 

Podocarps: How Ecologically 

Alike Are They?

David A. Coomes and 

Peter J. Bellingham

ABSTRACT. With few exceptions, podocarps are specialists of nutrient-poor soils 

within temperate and tropical rainforests. They are locally abundant in some tropical 

mountains, especially near the tree line, and in the lowland tropics most are confined to 

heathlands and impoverished habitats, although some can persist in forest understories. 

The ecology of tropical podocarps is not well understood, so here we draw on literature 

from temperate regions to help characterize their niches. Temperate podocarps are effective at capturing and retaining nutrients at the expense of competitors. They are universally slow growing, but this is not necessarily an encumbrance on poor soils because 

competition for light is relatively weak. Temperate podocarps are often outcompeted on 

richer soils because several factors stack against them: they are ill equipped to compete 

with angiosperms in the race to occupy canopy gaps, there may be few sites for their 

establishment on the forest floors, and continuous regeneration by podocarps is seldom 

found in the forest understory because their growth is severely hampered by shading. We 

suggest that competition excludes imbricate-leaved podocarps from most lowland tropical forests, whereas broad-leaved species with anastomosing veins (Nageia and some 

Podocarpus) are so shade tolerant that they regenerate beneath closed canopies.

INTRODUCTION

In 1989, Bond revisited an old but unresolved question: why were conifers pushed out of the lowland tropics and mesic temperate regions by angiosperms as they diversified and expanded in range during the Late Cretaceous? 

Previously, the leading hypothesis was that the evolution of flowers had given 

angiosperms overwhelming reproductive superiority over conifers: the wasteful process of wind pollination was usurped by directed pollination by animals 

(Raven, 1977). Bond (1989) and Midgley and Bond (1991) challenged the prevailing view, hypothesizing instead that the physiological traits of conifers made 

David A. Coomes, Forest Conservation and 

Ecology Group, Department of Plant Sciences, 

University of Cambridge, Cambridge CB2 3EA, 

UK. Peter J. Bellingham, Landcare Research, PO 

Box 40, Lincoln 7640, New Zealand. Correspondence: David A. Coomes, dac18@cam.ac.uk.

Manuscipt received 13 April 2010; accepted 

9 July 2010.
120 • smithsonian contributions to botany

them inherently slow growing as seedlings. These traits 

place them at a competitive disadvantage during the regeneration phase of the life cycle but help them survive in 

extreme environments, including cold, droughts, nutrientpoor soils, poorly drained soils, and deep shade. 

Two decades after Bond’s “slow seedling” hypothesis, 

the latest physiological evidence indicates that podocarps 

are universally slow growing. Podocarps have long-lived 

leaves and low specific leaf areas, traits always associated with low photosynthetic capacity per unit leaf mass 

(Wright et al., 2004). They have lower photosynthetic capacity than angiosperms of comparable specific leaf area 

(Lusk, this volume). Using a global database of wood densities, we find that podocarps have denser wood than other 

conifers (Figure 7.1); this trait is associated with podocarps having narrower tracheids (Pittermann et al., 2006a; 

Lusk, this volume) and results in high hydraulic resistivity 

and low photosynthetic capacity per unit leaf area (Feild 

and Brodribb, 2001). In lowland cool temperate forests, 

diameter growth of podocarp trees is approximately half 

that of angiosperm trees under similar conditions (Ogden 

and Stewart, 1995; Bentley, 2007). In subalpine shrublands, podocarps grow more slowly than several angiosperms (P. Wardle, 1963a). Podocarps are slower growing 

than other commercially valuable timber species (Bergin, 

2000). For example, Podocarpus totara seedlings with 

an initial mean height of 0.85 m reached just 2.9 m after 6 years and 5.5 m after 11 years in a provenance trial 

on fertile soils under frost-free conditions (Bergin et al., 

2008), whereas Pinus radiata reaches heights up to 30 m 

after 17 years (Beets and Kimberley, 1993). Seedlings of 

Lagarostrobos franklinii in Tasmania grow at just 2.3 cm 

yr-1

, approximately a third of the rate of the angiosperm 

tree Eucryphia milliganii, which grows in nearby forests 

(Jennings et al., 2005). Podocarp seedlings are outpaced 

by angiosperms and even by tree ferns when growing on 

rich soils in southern New Zealand: height growth under 

optimal conditions is 3–7 cm yr-1 versus 11–17 cm yr-1

for subcanopy angiosperms and ~10 cm yr-1 for tree ferns 

(Gaxiola et al., 2008; Coomes et al., 2009). We found no 

examples of fast-growing podocarps.

The notion that conifers are well equipped to cope 

with extreme environments remains unchallenged, but the 

mechanisms by which conifers are competitively disadvantaged in “productive” habitats are still a topic of debate. 

In the case of podocarps, there is considerable doubt over 

whether they can even be described as disadvantaged in 

lowland tropical habitats since a considerable number of 

shade-tolerant podocarps grow in the shade of tropical 

forests (e.g., Hill and Brodribb, 1999). The ~30 species of 

podocarps found in cool temperate forests have received 

much more attention from ecologists than the ~150 species of tropical and warm temperate forests. Can our understanding of the ecology of these temperate podocarps 

inform us about the distribution and dynamics of their 

tropical cousins? We start by discussing what types of 

habitats are occupied by temperate podocarps and why 

they are not observed in the full range of high-stress habitats occupied by conifers as a whole. We then explore the 

reasons why temperate podocarps often achieve dominance on nutrient-poor soils and why the exceptions prove 

the rule. We look at the regeneration strategies of temperate podocarps in shaded habitats and how these help 

explain the presence and persistence of some species in 

more nutrient-rich forests. These analyses lead us back to 

FIGURE 7.1. Wood density (oven-dry mass/fresh volume) of 

podocarp species from temperate and tropical regions (extracted 

from a global database; Chave et al., 2009). The Podocarpaceae 

have a greater mean wood density than six other conifer families (0.50 g cm-3

 vs. mean of 0.45 g cm-3; F7,260 = 9.7, P < 0.001) 

and a similar mean density to the Taxaceae (0.53 g cm-3

). 

Tropical podocarps have a significantly lower wood density than 

their temperate relatives (0.48 ± 0.01 vs. 0.54 ± 0.02 g cm-3

; t = 2.1, 

P = 0.03).
number 95 • 121

a discussion of the ecology of tropical podocarps and why 

they are relatively uncommon in the lowlands. 

LIMITS TO GEOGRAPHIC DISTRIBUTION: 

INTOLERANCE OF COLD AND DROUGHT

Podocarps prevail mostly in climates that are cool 

and wet. However, they do not tolerate extreme cold as 

well as Northern Hemisphere conifers: none can withstand temperatures below -20°C, whereas 88% of 117 

Northern Hemisphere conifer species can do so (Figure 

7.2; Bannister, 2007). Podocarps seldom form the tree line 

in temperate mountains but do so in tropical mountains. 

Instead, Nothofagus species often form tree lines in cool 

temperate South America, New Zealand, and Tasmania; 

podocarps are present but seldom form significant components of these forests (Wardle, 2008). Some temperate 

podocarps occur almost exclusively above tree lines as 

shrubs or prostrate woody plants in alpine ecosystems in 

New Zealand (Wardle, 1991) and Tasmania (Kirkpatrick, 

1997). Perhaps differences in present and past climate 

have reduced the need and opportunity for the evolution 

of traits conferring tolerance of extreme cold. Southern 

Hemisphere oceans act as vast heat buffers that moderate land temperatures, resulting in milder climates than 

in the Northern Hemisphere. The Southern Hemisphere 

was also less extensively glaciated during the Pleistocene 

(Sakai et al., 1981). Mild climates throughout much of 

the evolutionary history of the Southern Hemisphere may 

be responsible for its paucity of cold-tolerant trees: New 

Zealand’s tree lines, at 1,200–1,300 m, are about 500 m 

lower than continental tree lines at equivalent continental 

latitudes (Körner and Paulsen, 2004). 

Although podocarps are ill equipped to survive in extreme cold, they are relatively well protected against moderate frosts experienced in their current ranges. Frosts in 

New Zealand’s North Island damage the dominant shadetolerant angiosperm (Beilschmiedia tawa) but have no 

apparent effect on co-occurring podocarps (Kelly, 1987). 

Pot-grown podocarp seedlings are more tolerant of subzero temperatures than angiosperms taken from the same 

region (Bannister and Lord, 2006). Hardiness of Podocarpus totara in New Zealand has a strong genetic basis, 

with genotypes from the coldest regions being most hardy, 

suggesting that populations have evolved in response to 

FIGURE 7.2. Frost resistance of conifers from the Northern (light gray) and Southern 

(dark gray) hemispheres, redrawn from Bannister (2007). Frost resistance was quantified by calculating the temperature at which half of the leaves are damaged by the 

effects of cold.
122 • smithsonian contributions to botany

environmental pressures (Hawkins et al., 1991). Their 

frost hardiness appears to come at a cost, in that maximum 

growth rates of high-latitude genotypes are slower (Bergin 

et al., 2008). Angiosperms in Tasmanian montane heaths 

suffer much greater loss in xylem conductivity after being 

frozen and thawed (17%–83%) than do conifers (<12%), 

primarily, it seems, because bubbles in the xylem conduits 

formed during the freeze-thaw cycle are more easily redissolved in the narrow tracheids of conifers than in the wider 

vessels of angiosperms (Feild and Brodribb, 2001). 

Few temperate podocarps grow in dry regions, in contrast to other conifers, and this intolerance can be traced 

to their vascular systems (see also Brodbribb, this volume). 

Exceptions include Afrocarpus falcatus in drier regions of 

southern Africa (Adie and Lawes, this volume), Podocarpus drouynianus in Western Australia (Ladd and Enright, 

this volume), and Halocarpus bidwillii, Phyllocladus alpinus, and Podocarpus hallii in the dry lowland forests 

of New Zealand (~400 mm yr-1

; Bergin, 2000; McGlone, 

2001). Drought damages plants if the tension within water columns of the vascular system gets so large (i.e., the 

water potential gets so low) that cavitation occurs or if 

conduits implode (Tyree and Sperry, 1989). Plants from 

dry regions, such as conifers in the Pinaceae and Cupressaceae, withstand high tensions within their vascular systems by having thick tracheid walls that prevent implosion 

and “plugs” (torus margo) within pit membranes that prevent air bubbles from moving through the vascular system (Pittermann et al., 2006b). However, podocarps are 

peculiar among conifers in being susceptible to embolism 

at relatively low tensions, despite having thick tracheid 

walls (Pittermann et al., 2006b) and having relatively high 

hydraulic resistance across pit membranes (Pittermann et 

al., 2006a). It may also be the case that sclereids in podocarp leaves are vulnerable to implosion under tension 

(Brodribb, this volume). Plants can avoid damage by early 

closure of stomata, but we found no studies of stomatal 

responses in podocarps. Podocarps have long-lived leaves, 

so they are unable to drop all their leaves during dry periods in the way that many drought-deciduous angiosperms 

do. In one example, Podocarpus totara lost many leaves 

during a drought year, produced shorter leaves, and maintained high internal water potential but fared less well than 

drought-tolerant angiosperms (Innes and Kelly, 1992). 

TOLERANCE OF NUTRIENT-POOR SOILS

With a few important exceptions, podocarps in the 

cool temperate regions achieve greatest abundance on the 

poorer soils and/or in open habitats. In the coastal range of 

Chile, two podocarps are most common on shallow mica 

schists and poorly drained sites (Lusk, 1996), and Lepidothamnus fonkii has a dwarf habit and grows in Sphagnum

bogs (Gardner et al., 2006). In Japan, Nageia nagi occurs 

on thin soils derived from granite on Yakushima (Kohyama 

and Grubb, 1994), but it is not restricted to poor soils. In 

southeastern Australia, Podocarpus lawrencei occurs on 

acidic soils on granite and weathered sedimentary rocks, 

achieving greatest abundance on skeletal soils (Barker, 

1991). In New Zealand, podocarps often achieve greatest 

abundance on poor soils, as shown by investigations on 

two soil chronosequences: a series of deglaciated terraces 

near the Franz Josef Glacier and a series of uplifted marine 

terraces in southern Fiordland. On both chronosequences, 

plant-available phosphorus becomes depleted on the 

older sites, and podocarps become increasingly abundant 

on these impoverished soils, with some species restricted 

to them (Richardson et al., 2004; Coomes et al., 2005). 

Bond (1989) proposed that conifers are successful on poor 

soils because they are almost unrivalled in their tolerance 

of extreme environments and because competition for 

resources is neither intense nor important; conifers are 

stereotyped as “stress tolerators” in the competitor–stress 

tolerator–ruderal triangle of Grime (1977). Here we argue 

that podocarps possess traits that allow them not only to 

tolerate poor soils but also to be successful competitors for 

belowground resources.

Efficient Capture of Nutrients

Fungal hyphae have high area to mass ratios, making them more efficient than roots at foraging for immobile nutrients. Podocarps rely heavily on endomycorrhizal 

symbionts for nutrient uptake (Baylis, 1969; Russell et al., 

2002). Fine roots have low specific root length (Gaxiola et 

al., 2010) and are heavily infected by mycorrhizal fungi (up 

to nearly 100% of root length; Dickie and Holdaway, this 

volume). Podocarps on the Franz Josef chronosequence 

had lower foliar nitrogen to phosphorus ratios than ferns 

or angiosperms on the phosphorus-impoverished soils, 

suggesting that they were better able to extract soil phosphorus (Richardson et al., 2005). Angiosperm species 

from podocarp-rich forests are also heavily infected by arbuscular mycorrhizas (Hurst et al., 2002), but very little is 

known about the comparative efficiency of these groups. 

Slow-growing conifers from the Northern Hemisphere allocate a large proportion of their net primary productivity 

to roots and ectomycorrhizal fungi, particularly when nutrients are in short supply (Hobbie, 2006). The same may 
number 95 • 123

be true of podocarps: Whitehead et al. (2004) concluded 

that Dacrydium cupressinum in New Zealand swamp 

forests allocate a high proportion of total carbon belowground, on the basis of the predictions of a process-based 

simulation model. New Zealand podocarp seedlings have 

a higher root to shoot ratio that many angiosperm trees, 

particularly when grown in nutrient-poor soils. 

Increased Nutrient Retention of Long-­Lived Leaves

Species associated with nutrient-poor soils often have 

long-lived leaves (Grime, 1977; Chapin, 1980; McGlone 

et al., 2004) because a long life span reduces the annual 

rate of mineral nutrient loss via abscission (Monk, 1966). 

Plants salvage only about 50% of nitrogen and 60% of 

phosphorus from leaves during abscission (although there 

is great variability among species), so retaining leaves is 

strongly advantageous in situations where recapturing nutrients is costly (Aerts, 1995). Podocarp leaves have long 

life spans compared with angiosperm associates; Gaxiola (2006) observed that four podocarps species from the 

Waitutu chronosequence in southern New Zealand had a 

mean leaf life span of 3.1 years, compared with 1.5 years 

for 11 angiosperm species (nine of which were evergreen). 

Lusk (2001) measured leaf life spans of several Chilean 

species, including the following podocarps: Podocarpus 

nubigenus (7.3 years), Podocarpus salignus (3.2 years), 

and Saxegothaea conspicua (4.2 years). Podocarp leaves 

contain significant quantities of terpenes (Brophy et al., 

2000), which are known to deter herbivores. However, 

whether podocarps are better defended than angiosperm 

is difficult to judge objectively because terpenes are just 

one of the armory of defenses that plants deploy.

Longevity and Nutrient Retention

Some temperate conifers, including podocarps, have 

much longer life spans than co-occurring angiosperm trees 

(Wardle, 1991; Enright and Ogden, 1995). This is especially the case for some New Zealand podocarps (Lusk and 

Ogden, 1992; Bentley, 2007) and Lagarostrobos franklinii 

in Tasmania (Gibson and Brown, 1991). However, great 

longevity is not a feature of podocarps, whereas it is of 

other conifers in the same forests (e.g., Cryptomeria japonica and Tsuga sieboldii in Japan, Fitzroya cupressoides

in Chile, and Picea balfouriana in China). A tree releases 

nutrients back to the soil upon its death, so a long life span 

is advantageous in situations where regaining those nutrients requires intense competition with neighbors (Ogden 

and Stewart, 1995; Coomes et al., 2005). A long life span 

requires wood that is strong and resistant to boring insects 

and rot. Podocarps have denser wood than other conifers 

(Figure 7.1), indicating that the wood is likely to be mechanically strong (Chave et al., 2009). Many podocarp 

species are prized for their timbers because they are resistant to rot, and powerful antimicrobial chemicals have 

been isolated from the bark of several Podocarpus species 

(Abdillahi et al., 2008). An array of diterpenoids within 

bark (Cox et al., 2007), as well as the deposition of phenolics in specialized parenchyma cells (Hudgins et al., 2004), 

provides robust defense against insects.

Ecosystem Engineers That Starve

Neighbors of Nutrients

The tough fibrous leaves of New Zealand’s podocarps are slow to decompose (Wardle et al., 2008; Hoorens et al., 2010), resulting in the accumulation of organic 

matter within soils, an increase in the ratios of carbon to 

phosphorus and nitrogen to phosphorus in soil, and effects on community structure of soil microflora (Wardle 

et al., 2008). Nutrients are sequestered within the recalcitrant organic matter. Locking up nutrients in this way is 

an effective means of competing for nutrients if competitors are relatively intolerant of extreme nutrient shortage 

or less able to access organic nutrients. In effect, podocarps may engineer their local environment to their own 

advantage. 

Tolerators of Soil Anoxia

Nutrient-poor soils in high rainfall regions are often 

poorly drained as a result of subsoil cementation. Species that tolerate low concentrations of soil oxygen and 

mobilization of toxic ions are advantaged under these 

conditions. A pot experiment with three New Zealand 

podocarps showed them to survive well, with much reduced growth, under waterlogged conditions (Gaxiola et 

al., 2010). The prevalence of conifers in waterlogged sites, 

both in New Zealand and in other temperate forests, appears to result from various morphological and biochemical adaptations (Crawford, 1987). One New Zealand 

podocarp, Manoao colensoi, produces aerenchyma in its 

roots that carries air down to submerged fine roots (Molloy, 1995), but no other examples of this in podocarps are 

known. The reduced stature of podocarps associated with 

bogs (e.g., Lepidothamnus intermedius and Halocarpus 

biformis in New Zealand) may result from a lack of deep 

anchoring roots in anoxic soils, without which woody 

plants are unable to grow tall (Crawford et al., 2003). 
124 • smithsonian contributions to botany

Reduced Impact from Asymmetric

Competition for Light

Podocarps are slow growing, which is not necessarily disadvantageous on poor soils, where resource limitations reduce the potential for fast growth regardless 

of a species’ genetic potential. Forests on nutrient poor 

and waterlogged soils often have comparatively low leaf 

area indices and intercept less light (Coomes and Grubb, 

2000). For example, 1.5% of incoming photosynthetically active radiation makes its way to the forest floor 

of phosphorus-rich soils in southern New Zealand, 4.6% 

gets through on phosphorus-depleted soils, and 16% 

gets through on even poorer sites (Coomes et al., 2005). 

The growth of podocarps is hardly influenced by competition from taller neighbors on the poor soils (e.g., Figure 7.3a). As long as competition for light is not intense, 

podocarps may exclude other plants from nutrient-poor 

soils through belowground competition (see Coomes and 

Grubb, 2000).

Canopy Architecture Suited to

Growth in the Open

Genera of podocarps associated with poor soils often have small, scalelike leaves held on upright or pendent stems (Dacrydium, Halocarpus, Lepidothamnus, 

Manoao, Microcachrys, and Microstrobos) or have 

whorls of leaves that overlap. Steeply inclined or clustered leaves reduce light interception at the top of the 

canopy, allowing light to “trickle down” to lower leaves. 

This increases whole-plant photosynthesis because the 

uppermost leaves receive near-optimal rather than excessive light levels, while leaves at the bottom of the canopy 

get a greater share of resources (Horn, 1971). The world’s 

fastest-growing trees (Betula, Casuarina, and some Pinus

and Eucalyptus) have this canopy architecture, at least 

once past the seedling stage. However, clumped and pendent leaves are inefficient at scavenging light in deeply 

shaded understories and ineffective when competing for 

light against fast-growing neighbors (Leverenz et al., 

FIGURE 7.3. Height growth of podocarp (dashed line) and angiosperm (solid line) tree seedlings in response to light on (a) phosphorus-depleted terraces versus (b) alluvial terraces in southern New Zealand. 

The gray bars indicate the percentage daylight typically found at 1.35 m above ground under the canopy, 

based on the 20th and 80th percentiles of light measurements (redrawn from Coomes et al., 2009).
number 95 • 125

2000; Pickup et al., 2005). Therefore, these architectures 

are uncommon in infrequently disturbed communities 

growing on nutrient-rich soils where competition for light 

is intense (Horn, 1971). 

Efficient Use of Light

The efficient use of whole-canopy light has been investigated in detail for Dacrydium cupressinum, which 

has scalelike leaves positioned on pendent shoots; closed 

stands have a leaf area index of only 2.0 m2

 m-2 and intercept only 79% of available photosynthetically active 

radiation when growing on acidic, poorly drained soil 

(Whitehead et al., 2002). Clumping of leaves within the 

canopy of Dacrydium-dominated forest reduces canopy 

light interception by 5% but increases canopy photosynthesis by 8% through increased light use efficiency (Walcroft et al., 2005). Even though leaves in the upper crown 

of Dacrydium on poor soils have a maximum rate of carboxylation activity (half-surface leaf area basis) that is 

only 24% of that of similarly positioned leaves within an 

oak woodland on nitrogen-enriched soils in summer, the 

annual carbon uptake rate of the podocarp forest was only 

14% lower than that of oak because of its canopy organization (Whitehead et al., 2004). The canopy architecture 

and evergreen leaves, which continued to take up carbon 

in winter, contributed to a higher-than-expected carbon 

uptake rate. 

Summary

Podocarps are successful on poor soils because they 

are well adapted to acquiring and retaining nutrients. It 

may be that podocarps function similarly to slow-growing 

conifers from the Northern Hemisphere, allocating a large 

percentage of net primary productivity belowground and 

thereby enabling their roots systems (and associated mycorrhizas) to forage exhaustively for soil nutrients. In addition, their long-lived leaves, durable wood, and slowly 

decomposing litter ensure that hard-earned nutrients are 

not relinquished to competitors. Inherently slow stem 

growth may not be a serious encumbrance when nutrients are in short supply because asymmetric competition 

for light is weak, so outgrowing neighbors is not strongly 

advantageous. Any disadvantages that accrue from slow 

growth are offset by effective nutrient recovery and retention, longevity, and strength to resist catastrophic disturbance. Scalelike leaves are advantageous in terms of 

whole-plant photosynthesis in open habitats. 

REGENERATION PROCESSES

Responses to Forest Disturbance

Much attention has been given to the role of disturbances in allowing species with differing regeneration 

niches to coexist within forests (Poorter and Bongers, 

2006). In the context of Southern Hemisphere conifers, 

Ogden and Stewart (1995) recognized three categories of 

regeneration response to disturbance: (1) “Catastrophic 

regeneration” occurs in the aftermath of infrequent massive disturbances (e.g., earthquakes, floods, fires, and 

cyclones) and is characterized by a pulse of establishment after which no further establishment is possible; at 

the landscape scale, catastrophic regeneration gives rise 

to large patches (>1,000 m2

) of similarly aged trees and 

strong discontinuities in age structure within and among 

patches. (2) “Gap-phase regeneration” occurs in smaller 

gaps (<1,000 m2) created by the death a single tree or a 

few trees; it is characterized by smaller patches and fewer 

discontinuities in age. (3) “Continuous regeneration” occurs when seedlings and saplings are capable of growing 

and surviving in the shade of an intact canopy. Typically, 

these shade-tolerant trees edge slowly upward in the shade, 

growing more quickly if openings appear in the canopy 

above them (e.g., Uhl et al., 1988); near-continuous regeneration gives rise to all-aged population structures, composed of many small stems and successively fewer stem in 

larger age classes. 

Temperate podocarps vary greatly in shade tolerance. 

Some have developed flattened leaves arranged within 

planes, a shade adaptation that may have arisen in response to changes in light transmissions brought about by 

the evolution of shade-bearing angiosperms in the early 

Cenozoic (Hill and Brodribb, 1999; Brodribb and Hill, 

2003a, 2003b). Podocarps with shade-tolerant leaf morphology also have shade-tolerant physiology (Brodribb, 

this volume) and are sometimes capable of continuous regeneration. For example, Nageia nagi has large, flattened 

leaves and regenerates nearly continuously within Japanese 

warm temperate rainforests (Kohyama, 1986), and Prumnopitys ferruginea has shade-tolerant morphology and is 

quite capable of establishing without multiple-tree gaps in 

New Zealand (Figure 7.4; Duncan, 1993; Lusk and Smith, 

1998; Bentley, 2007). Other species have tiny, scalelike 

leaves held on upright stems and are unable to tolerate prolonged shade: when adult, Halocarpus biformis, a small 

tree with imbricate scale leaves, is most frequent in open 

habitats, such as the margins of bogs (Figure 7.4).
126 • smithsonian contributions to botany

Regeneration Processes in

Relation to Soil Fertility

Regeneration response depends not only on a species’ inherent shade tolerance but also on the light conditions in the understory of the forest. A species capable 

of regenerating continuously under open forests on poor 

soils may struggle to regenerate under dense forests on 

richer soils. For example, two podocarps that grow in the 

Chilean coastal range, Podocarpus nubigenus and Saxegothaea conspicua, are considered the most shade tolerant of all conifers in temperate South America (Donoso, 

1989). They attain greatest abundance on shallow soils 

(poorly drained sites in the lowlands, ridges, and shallow 

mica schist at higher altitudes). The main angiosperms at 

these sites (Nothofagus nitida and Weinmannia trichosperma) have open canopies under which the podocarps 

regenerate: there are many seedlings and saplings in the 

FIGURE 7.4. Juvenile and adult foliage of contrasting podocarps from New Zealand. Drawings modified from 

Wilson (1982) and reproduced with kind permission of the author and publisher.
number 95 • 127

forest understory, and the tree populations have reverse-J 

age distributions (Lusk, 1996; Gutiérrez et al., 2004). 

However, at sites where shade-casting angiosperms such 

as Dasyphyllum diacanthoides and Laureliopsis philippiana are common, the podocarps are less abundant and 

regeneration discontinuous (Lusk, 1996). At sites where 

shade-tolerant angiosperms are dominant, the podocarps 

are excluded altogether (e.g., Armesto and Fuentes, 1988). 

In Tasmania, Lagarostrobos franklinii appears to regenerate along rivers that frequently flood but rarely penetrates 

into closed rainforest (Gibson and Brown, 1991). In South 

Africa, Podocarpus latifolius grows and survives well in 

the understory of angiosperm-dominated warm temperate 

forest in the Drakensberg Mountains (5.5% light transmission to forest floor; Adie and Lawes, 2009a) but is 

unable to regenerate beneath coastal subtropical forest in 

KwaZulu-Natal, through which only ~1% light is transmitted (Adie and Lawes, 2009b). However, the regeneration success of P. latifolius is not simply determined by 

competition for light: seedlings are unable to establish under mature podocarp forest, even though 7.5% light penetrates to the forest floor, apparently because grasses and/

or mature trees exclude seedlings by belowground competition (Adie and Lawes, 2009a). Various other studies 

indicate that that temperate podocarps fail to regenerate 

beneath parent trees (e.g., Norton, 1991; Cameron, 1960; 

Ogden and Stewart, 1995).

Why Shade-­Tolerant Podocarps Fail

to Regenerate in the Shade

Many podocarps persist in deep shade (e.g., mortality 

rates in New Zealand lowland forest were just 1% per 

year; Smale and Kimberley, 1986), but survival counts 

for little unless accompanied by height growth. Height 

growth of New Zealand podocarps is strongly suppressed 

by shading (e.g., Smale and Kimberley, 1986; Ebbett and 

Ogden, 1998; Coomes et al., 2009; Figure 7.3), limiting 

opportunities for continuous regeneration in forest understories. For instance, Podocarpus hallii seedlings in a 

cool montane rainforest in New Zealand have an annual 

mortality rate of just 2.7%, meaning that about 5% of 

seedlings live for at least 100 years, but height growth is 

so slow that virtually no individuals get past the seedling 

stage in the shade; consequently, most regeneration is restricted to landslides (Bellingham and Richardson, 2006). 

Similarly, Dacrydium cupressinum seedlings had an annual mortality rate of 10% and a height growth of 1.5–

2.5 cm yr-1

 in a lowland New Zealand forest on highly 

leached soils, indicating that height growth is insufficient 

for seedlings to regenerate continuously in these forests 

(Coomes et al., 2009; Kunstler et al., 2009). Instead, Dacrydium cupressinum requires progressive overstory mortality (Six Dijkstra et al., 1985; Lusk and Ogden, 1992; 

Lusk and Smith, 1998; Bentley, 2007) or catastrophic disturbance (e.g., Duncan, 1993; Smale et al., 1997) in order 

to regenerate. Even highly shade-tolerant podocarps such 

as Prumnopitys ferruginea can struggle to get beyond the 

seedling stage in lowland forests (Smale et al., 1997), and 

stands of this species have a discontinuous age structure 

at some sites (e.g., Lusk and Ogden, 1992). The important implication is that shade tolerance assessed from leaf 

physiology does not necessarily equate with ability to regenerate continuously within a particular habitat. The latter depends upon the degree of shade cast by the forest as 

well as the physiological shade tolerance of the species and 

is affected by changes in shade tolerance with size (Kunstler et al., 2009). 

Reliance on Catastrophic Disturbance

in Nutrient-­Rich Habitats

Three species of podocarps dominate the alluvial 

floodplain forests of New Zealand, apparently contradicting the theory that podocarps are competitively excluded 

from nutrient-rich sites. Dacrycarpus dacrydioides is a 

dominant tree on poorly drained soils (Smale, 1984; Duncan, 1993; Norton, 1995), and Prumnopitys taxifolia and 

Podocarpus totara are dominant on better-drained soils 

(Esler, 1978; McSweeney, 1982). Establishment opportunities can be limited by near-continuous fern cover at some 

sites (Coomes et al., 2005), and although smaller-seeded 

angiosperms are able to take advantage of elevated sites 

such as fallen trunks and tree fern stems, the larger-seeded 

podocarps seldom establish in such niches (Lusk, 1995; 

Christie and Armesto, 2003; Lusk and Kelly, 2003; Gaxiola et al., 2008). Indeed, none of these podocarps can regenerate continuously beneath mature rainforest canopies 

(e.g., Urlich et al., 2005). Neither is gap-phase regeneration possible because tree fall gaps are colonized rapidly 

by fast-growing woody angiosperms, ferns, and herbaceous plants, leaving few opportunities for slow-growing 

trees (Coomes et al., 2005, 2009). Instead, slow-growing 

podocarps are able to persist in the floodplain forests in 

western South Island rainforests by regenerating after catastrophic disturbances, such as those resulting from debris 

triggered by major movements of faults in the Southern 

Alps and associated floods (Wells et al., 2001; Cullen et 

al., 2003). The long life span of these podocarps allows 

them to persist from one rare catastrophic disturbance to 
128 • smithsonian contributions to botany

the next (Enright and Ogden, 1995; Veblen et al., 1995; 

Lusk and Smith, 1998). Currently, regeneration failure 

and ageing populations are observed over most of their 

range (Holloway, 1954; Wardle, 1963b), and in some regions this could be because the last major movement of the 

Alpine fault was nearly 300 years ago (ad 1717; Wells et 

al., 1999). An event every few hundred years is sufficient 

to maintain conifers as dominant elements (i.e., a “storage 

effect” sensu Chesson, 2000). However, catastrophic regeneration of podocarps may be uncommon outside New 

Zealand. Other species, such as the two Japanese species 

in typhoon-affected forests, may benefit from disturbance 

events by being relatively resistant to damage (see Dalling 

et al., this volume). 

Floodplain podocarps grow well in bare mineral soil 

(e.g., Wardle, 1974) and presumably benefit from reduced 

competition with angiosperms on fresh alluvium. However, they are not pioneer species, as they arrive after an 

initial wave of colonization by early successional plants 

(e.g., Reif and Allen, 1988). Woody plants such as Aristotelia serrata and Melicytus ramiflorus grow quickly and 

form an open canopy; birds feed on the pseudo-arils of 

podocarps and disperse the seeds into these early successional communities (Beveridge, 1964; Wardle, 1991). The 

podocarps grow up beneath the open-crowned bushes 

and trees and eventually overtop them (Beveridge, 1973), 

continuing to colonize sites for many decades after disturbance (e.g., Wells et al., 2001). Interestingly, Dacrycarpus 

dacrydioides and Prumnopitys taxifolia undergo a major 

switch in leaf morphology at this stage, from having relatively broad leaves held in planes to having small leaves 

on pendant branches (Atkinson and Greenwood, 1989). 

These changes may be responses to increased light and 

exposure once the trees have overtopped the early successional community (McGlone and Webb, 1981). New 

Zealand has a disproportionate number of long-lived 

podocarps that rely on flooding, although they are also 

represented in Tasmania and mainland Australia (Barker, 

1991; Gibson and Brown, 1991).

Intolerance of Fire

Fire disturbance is usually fatal for podocarps, although two Australian podocarps (Podocarpus drouynianus and P. spinulosus) resist fire by sprouting from 

belowground reserves (Chalwell and Ladd, 2005; Ladd 

and Enright, this volume) and Halocarpus bidwillii can 

regenerate after fire in New Zealand heathlands (Wardle, 

1991). The increased frequency of fire since the arrival of 

humans is thought to be the major factor of range contraction of podocarps in Australia (Hill and Brodribb, 1999), 

and it all but annihilated forests formerly dominated by 

podocarps in eastern New Zealand (McGlone, 2001). 

Podocarps lack traits found in fire-adapted coniferous 

lineages, such as serotinous cones, an ability to resprout 

from the roots, and highly flammable leaves and litter. Several Podocarpus species have thin bark, suggesting that 

their vascular cambium could be susceptible to damage 

during fire. Highly flammable myrtaceous shrubs are the 

early colonizers of burnt areas in the North Island of New 

Zealand; the shrublands are soon colonized by podocarps, 

but fire must be excluded for several decades in order for 

the trees to overtop the shrubland and form a dense forest 

(McKelvey, 1963; Ogden and Stewart, 1995; Wilmshurst 

and McGlone, 1996).

Resprouting

Tall podocarp species do not, in general, resprout following damage (Martin and Ogden, 2006). For example, 

in New Zealand forests there was no resprouting of Dacrydium cupressinum after logging, and regeneration was 

dominated by resprouts of the angiosperm tree Weinmannia racemosa, to the disadvantage of D. cupressinum (Baxter and Norton, 1989). Saplings of D. cupressinum were 

unable to recover after experimental clipping to simulate 

deer browse because they resprouted poorly (Bee et al., 

2007). Typhoon-damaged trees of the podocarp Nageia 

nagi in southern Japan were also ineffective at resprouting, in contrast to many co-occurring angiosperm trees 

(Bellingham et al., 1996). Resprouting is more apparent 

for temperate podocarps from poor sites, which are often 

shrubs or small trees and exhibit multistemmed architecture. These include Halocarpus bidwillii, Lepidothamnus 

intermedius, and Lagarostrobos franklinii, all of which 

spread vegetatively in open habitats. By doing so, patches 

of L. franklinii may have persisted for 10,000 years, and 

trees within remnant populations are genetically homogenous (Clark and Carbone, 2008). Another tree of open 

habitats, Phyllocladus alpinus, resprouts after wind damage (Martin and Ogden, 2006). A taller podocarp in 

Chilean rainforests, Saxegothaea conspicua, exhibits vegetative regeneration, which is crucial for its maintenance 

under shade-tolerant angiosperms in undisturbed stands 

(Veblen et al., 1980; Lusk, 1996). 

Summary

Podocarps are ill equipped to compete with angiosperms in the race for light in canopy gaps. Some species 

have evolved to tolerate prolonged shade, and these may 

regenerate continuously under relatively open-canopied 
number 95 • 129

forest on poorer soils. However, few species can regenerate continuously under forests that are rich in shadetolerant trees, tree ferns, bamboos, or ground plants 

because establishment sites are limited in these forests and 

onward growth is severely hampered. In New Zealand, 

three podocarp species dominate forests on rich alluvial 

soils—they do this by escaping competitors when fresh 

mineral surfaces are created by catastrophic disturbance 

events. These events may occur every few hundred years, 

and the long life spans of conifers allow them to persist 

from one event to the next. 

ECOLOGY OF TROPICAL PODOCARPS

The biogeography of tropical podocarps is dealt with 

in other chapters but can be summarized as follows: podocarps are dominant elements of forests on a variety of soils 

in the mountains of Papua New Guinea, Southeast Asia, 

and subtropical and tropical Africa but are not dominant 

in the mountains of northern Australia, New Caledonia, 

and Madagascar and are only locally dominant in South 

America. There are a few lowland species in Australasia, 

the Pacific Islands, India, Africa, and the Americas; these 

can dominate poor soils but are rare in other lowland forest types (P. J. Grubb, University of Cambridge, personal 

communication; Wade and McVean, 1969; Enright, 1995).

Tolerance of Cold and Heat

Tropical podocarps differ from those in temperate regions in being a major alpine element of tree lines 

over a wide area (e.g., New Guinea; Grubb and Stevens, 

1985), indicating that they are among the least warmthdemanding trees in the tropics. They are also among the 

most tolerant, forming dense, almost pure stands immediately around frost hollow grassland (Grubb and Stevens, 

1985). Like most temperate podocarps, they are excluded 

from dry regions: although Afrocarpus falcatus is common in relatively dry forests of Africa, the overwhelming majority of species are restricted to the wet tropics. 

Podocarps have easily distinguishable pollen, and the 

observation that tropical podocarps prevail mostly in climates that are cool and wet is frequently used by palynologists to reconstruct paleoclimates. Thus, the spread 

of podocarps into lowland Amazonia during Pleistocene 

glaciations suggests cooler conditions in the basin (Colinvaux et al., 1996), whereas the upward migration of 

podocarps into the páramo grasslands suggests a period of 

warmer climate in the Peruvian Andes between 8900 and 

3300 bp. As a further example, the waxing and waning 

of podocarp-rich rainforests across southeastern Australia during the late Pliocene and Pleistocene (Brodribb and 

Hill, 2003b; Sniderman et al., 2007) and the Late Cretaceous (Gallagher et al., 2008) is interpreted in terms of 

shifts in rainfall patterns driven by Milankovitch cycles 

(greater summer insolation resulting in warmer tropical 

seas, bringing greater rainfall to the continent). 

Success on Poor Soils

Many tropical podocarps are restricted to poor soils. 

In the appendix we provide brief descriptions of 96 species 

of tropical, subtropical, and warm temperate podocarps, 

taken mostly from Earle (1997–2009). We categorized each 

species as either (1) restricted to outstandingly poor soils, 

(2) restricted to rich soils, or (3) found on both rich and 

poor soils. “Outstandingly poor soils” included ultramafic 

soils, podzolized sands, peats, and shallow soils associated 

with limestone, sandstone, coastal bluffs, and ridgetops. We 

also included species associated with tree lines in the outstandingly poor soils category, the soils being highly organic 

and probably with markedly low rates of nitrogen mineralization (P. J. Grubb, pers. comm.). We subdivided their 

habitats into montane and lowland rainforest species (montane is defined here as >1,000 m elevation in the tropics and 

>800 m in the subtropics and warm temperate regions). 

Most tropical podocarps in Earle’s database are found 

in mountains (56%), so the majority of the species occupy 

cool climates. Several of these species (21) are described 

as locally common, dominant, or forming pure stands at 

high altitude, on ridges and sometimes in peats. They include Dacrycarpus (3), Dacrydium (7), and Podocarpus 

(9). Half of the montane species are also found in “normal” montane forests as well as on poor soils, but they are 

often less common when off the poorest soils: this group 

includes all seven species of Dacrycarpus. Nine species appear to be restricted to “normal” montane forests (i.e., 

they are not mentioned as growing on poor soils in their 

ecological descriptions). 

In the lowlands, 11 species are restricted to extremely 

poor soils, 12 are common on poor soils but venture into 

forest on better soils, and 9 are found in “typical” lowland 

rainforest. The last group comprises three genera: Nageia

(3), Podocarpus (5), and Parasitaxus (1). The Nageia species 

are shade-tolerant trees of warm temperate and subtropical 

forests (Kohyama, 1986) and are canopy species that are 

“scattered” and “often common” in the forest understory. 

The Podocarpus species are described as “scattered” and 

“locally common,” and all are subcanopy (~25 m tall), except P. spinulosus, which is a shrub restricted to sheltered 

coastal sites and gullies. Finally, Parasitaxus usta (New 
130 • smithsonian contributions to botany

Caledonia) is the only parasitic gymnosperm and never 

grows taller than 2 m; it persists in shade by virtue of the 

carbon it gains by parasitism on the roots of Falcatifolium 

taxoides. The 11 species restricted to poor soils are found 

on peat swamps, kerangas, and ultramafics; they include 

Dacrydium (3), Falcatifolium (2), and Podocarpus (6). Six 

of these species are small trees (<12 m tall). 

Presumably, podocarps are successful on the poorest 

tropical soils for the same reasons as in temperate regions. 

The species restricted to the poorest soils are significantly 

shorter and have much smaller leaves than species of better soils (e.g., Aiba and Kitayama, 1999), with species associated with both soil types having intermediate height 

and leaf area (Table 7.1; significance based on analysis of 

variance). These patterns are observed in both lowland 

and montane forests. The trend is precisely as anticipated, 

given that asymmetric competition for light is less intense 

among plants growing on poor soils, so height growth is 

not as strongly advantageous, and small leaves held on 

upright stems are effective for whole-plant photosynthesis 

within open forest. In lowland and lower montane forests, the heights achieved by podocarps are unremarkable, 

but at high altitude the species are often emergent. The 

area of shade leaves (as a ratio of the area of sun leaves) 

was 2.4 ± 0.10 (r2

 = 0.85), with no evidence of variation 

among forest or soil types (Table 7.1). A shift from big, 

shade-tolerant juvenile foliage to smaller adult foliage is 

observed in many tropical podocarps, especially canopy 

emergents, just as seen in temperate species.

Success in Mountain Environments

It is not surprising that podocarps are prominent in 

tropical montane forests: these are the environments most 

similar to temperate environments in which they evolved 

as a group (Morley, this volume). Nitrogen and phosphorus are likely to be increasingly limiting in the mountains 

(Grubb, 1977), to the benefit of podocarps. Podocarps may 

be particularly effective at photosynthesis in the persistently 

cloudy conditions often encountered on tropical mountains. Using a physiological modeling approach, Whitehead 

et al. (2004) found that carbon uptake by Dacrydium cupressinum in lowland New Zealand is greater than that of 

oak trees in the United States when conditions are overcast 

and the diffuse fraction of incoming radiation is high. 

There is little published information on regeneration 

processes and size structure of tropical montane podocarp populations (but see other chapters in this volume). 

Podocarpus urbanii in Jamaican montane rainforests is 

most common on less-fertile soils, although not on highly 

acidic mor soils (Tanner, 1977). It exhibits continuous regeneration in these forests but does not have a reverse-J 

distribution (Bellingham et al., 1995). Jamaican forests are 

frequently affected by hurricanes, but P. urbanii, like the 

two podocarp species in typhoon-affected Japanese forests, is resistant to hurricane disturbance (Bellingham et 

al., 1995). Following hurricanes, the growth rate of P. urbanii is faster than that of angiosperm trees, possibly because it survives storms relatively unscathed (Dalling et 

al., this volume; E. V. J. Tanner, University of Cambridge, 

personal communication). In addition, abundant seedlings 

and saplings of podocarps are found in the understory of 

high-altitude forests in New Guinea (Wade and McVean, 

1969), suggesting that the species are sufficiently shade 

tolerant to regenerate under the canopy. Aiba et al. (2004) 

compared 42 common species, including four podocarps, 

in a plot at 1,560 m altitude in Kinabalu Park, Borneo. 

Two podocarp species were most common on ridges 

(Phyllocladus hypophyllus and Dacrydium pectinatum), 

whereas the other two were less restricted by topography 

TABLE 7.1. Relationship of mean height and mean leaf area of canopy of leaves to forest and soil type. All data were extracted from 

descriptions provided by Earle (1997–2009); N is the number of species contributing to each mean. Leaf areas were estimated from 

mean widths and lengths assuming an elliptical shape, and the largest height was used whenever a range was given.

Height Leaf area Understory to canopy

Forest type Soil N (m) (cm2

) tree leaf area ratio

Tropical lowland Poor soils 9 14.9 ± 2.8 4.7 ± 1.7 3.2 ± 0.8

Mostly poor 11 25.5 ± 5.1 5.1 ± 3.5 3.1 ± 0.8

Better soils 8 27.5 ± 4.8 9.0 ± 3.4 3.3 ± 1.3

Tropical montane and warm temperate Poor soils 17 19.2 ± 2.7 1.9 ± 0.8 4.1 ± 0.6

Mostly poor 14 24.6 ± 3.8 4.7 ± 1.6 2.3 ± 0.3

Better soils 9 26.2 ± 3.6 4.1 ± 1.5 3.1 ± 1.0

Cool temperate All soils 25 14.9 ± 2.8 1.1 ± 0.5 4.3 ± 0.9
number 95 • 131

(Dacrycarpus imbricatus and Falcatifolium falciforme). 

All podocarp species except Falcatifolium falciforme had 

a greater proportion of their crowns in exposed positions 

within the canopy than predicted by chance, suggesting 

that they were light demanding. In contrast, Falcatifolium 

falciforme had a greater proportion of its crowns in shaded 

positions and a population structure indicating that the 

species was shade tolerant (Kitayama et al., this volume). 

Rarity in Lowland Tropical

Sites on Better Soils

Podocarps are absent from much of the lowland tropics, 

except on poor soils, although they are rare components 

of Australasian tropical lowland and lower montane forests (Enright, 1995). Two widespread species, Podocarpus 

neriifolius and Nageia wallichiana, reach densities of only 

1–2 per hectare within the 700–1,500 m elevation band of 

New Guinean mountains and are usually observed as solitary trees with few seedlings nearby (Enright, 1995). We 

reason that three factors conspire to exclude podocarps: 

(1) The high leaf area index of the lowland tropical forests 

means that the understory is too deeply shaded to allow 

even the most shade tolerant of podocarps to regenerate, 

the exception being Nageia species, which have large, multiveined leaves (mean for lowland species = 48 cm2

) similar to those of Gnetum (another gymnosperm of rainforest 

understories). (2) Podocarps are outcompeted in the race 

for light in tree fall gaps. Tropical podocarps may well 

grow faster than temperate relatives—their wood contains 

wider tracheids (Lusk, this volume) and is significantly less 

dense (Figure 7.1)—but it is inconceivable that they could 

compete with the growth of light-demanding angiosperms, 

which can reach upward of 1 m a year (e.g., Richards and 

Williamson, 1975). For example, a gap-demanding angiosperm, Toona australis, was found to have greater stomatal 

conductance and leaf-specific stem hydraulic conductivity 

than two tropical podocarps (Nageia fleuryi and Podocarpus grayii) and grew much more rapidly than the podocarps in full sun (1,300–1,800 μmol m-2

 s-1) (Brodribb 

et al., 2005). Finally, (3) opportunities for catastrophic regeneration are taken by angiosperms. Among the lowland 

tropical podocarps, two New Caledonian trees, Dacrycarpus vieillardii and Podocarpus polyspermus, appear to be 

exceptions and are maintained by disturbance, colonizing 

floodplains in a way similar to D. dacrydioides and P. totara in New Zealand (Jaffré, 1995). For most of the lowland tropics this niche is taken by angiosperm trees, some 

of which are long-lived (e.g., Ceiba pentandra). Other regeneration niches associated with disturbance seem to be 

taken by angiosperms. For example, the “shade-persistent 

pioneer” strategy of the long-lived angiosperm tree Alseis 

blackiana in lowland rainforests in Panama (Dalling et al., 

2001) is analogous to some long-lived podocarps (e.g., 

Podocarpus totara) in New Zealand rainforests. 

Most tropical podocarp species are intolerant of fire, 

like their temperate cousins. In the Dominican Republic, 

fire virtually excludes Podocarpus aristulatus from forests 

above 1,800 m, which are dominated by Pinus occidentalis. 

Fires are prevalent during El Niño droughts in these forests 

(every seven years or so), and they also have lower temperatures and precipitation than the cloud forests at lower 

altitude (1,550–1,800 m), which do not support fire and 

in which P. aristulatus is the third commonest tree (Martin and Fahey, 2006; Martin et al., 2007). Similarly, the 

páramo grasslands of the Andes have spread in response 

to frequent burning during the last 8,000 years, and podocarps are now restricted to montane forests well away from 

the grasslands (Niemann and Behling, 2008). Increased 

fire frequency since the arrival of humans is thought to be 

the major driver of podocarp extinction in Australia (e.g., 

Dacrydium from tropical north Queensland; Lynch et al., 

2007). A few tropical podocarp species are capable of persisting in habitats that burn. Dacrycarpus compactus, Dacrycarpus expansus, and Dacrydium novo-guineense are all 

locally prominent components of tree fern grasslands and 

thickets that occur near tree lines on tropical mountains, 

even though indigenous peoples burn these areas. Corlett 

(1984) noted that Dacrycarpus compactus has thick bark, 

which might afford it some protection. 

CONCLUDING THOUGHTS

Tropical and temperate podocarps function much as 

Bond envisaged: they are slow-growing tortoises. Most 

tropical species are restricted to montane forests with low 

total leaf area or lowland sites with exceptionally poor 

soils. Competition for light is less intense in such forests, 

and podocarps compete effectively by efficient capture 

and retention of nutrients. In addition, genera with small 

leaves held on erect/pendent stems may also achieve high 

rates of whole-plant photosynthesis in open canopied forests that prevail on poor soils. On richer soils in the tropics, slow-growing podocarps are incapable of competing 

with angiosperms in the battle for light in tree fall gaps. 

Some species may be capable of tolerating deep shade and 

surviving for many years in forest understories, but regeneration is not possible unless there is significant height 

growth, and that is severely hampered by shading. The 

simplest hypothesis is that the leaf area indices of lowland 

tropical forests are simply too high to allow regeneration 
132 • smithsonian contributions to botany

of imbricate-leaved podocarps, whereas broad-leaved species with anastomosing veins (Nageia and some Podocarpus) are so shade tolerant that they regenerate beneath 

closed canopies. Measurement of growth and survival of 

podocarps in contrasting tropical forest types, in conjunction with demographic models (e.g., Kunstler et al., 2009), 

would help resolve this issue. 

Acknowledgments

We are grateful to Macarena Cardenas, Neal Enright, Martin Gardner, Will Gosling, Peter Grubb, Chris 

Lusk, and Ed Tanner for sharing some of their thoughts 

on tropical podocarp ecology and to Will Simonson for 

proofreading the manuscript. We thank Chris Earle for 

compiling the Gymnosperm Database, quoted extensively 

in the appendix, and for providing many suggestions on 

the manuscript. PJB was funded by the New Zealand 

Foundation for Research, Science, and Technology (Ecosystem resilience OBI).

APPENDIX: 

DESCRIPTIVE ACCOUNTS OF

PODOCARPS FROM TROPICAL, 

SUBTROPICAL, AND WARM 

TEMPERATE REGIONS

Descriptions are taken primarily from Earle (1997–

2009), who sourced his data from various primary references, and also from personal communications with P. J. 

Grubb. Information on Andean and Amazonian species 

in the last section was sourced from Jorgensen and LeonYanez (1999). Tree heights (H) are given after each description; where a range of heights for different habitats is 

published, the largest is quoted. 

Lowland Tropical Rainforests

Common on Poor Soils but Not Restricted to Them

Dacrycarpus vieillardii. New Caledonia. Grows 

throughout the main island on serpentine soils along riverbanks, in moist depressions, and in frequently flooded 

areas from sea level to 900 m above sea level. Similar in 

ecology to D. dacrydioides of New Zealand. H = 25 m. 

Dacrydium balansae. New Caledonia. Occurs in the 

drier parts of forests, normally on serpentine soils from 

sea level to 1,000 m. A few specimens from ombrophilous 

forest were 20 m tall trees. H = 12 m. 

Dacrydium guillauminii. New Caledonia. Found 

within a few kilometers along two rivers. H = 2 m.

Dacrydium magnum. Solomon Islands, Moluccas. 

Locally common in the canopy of moist tropical forest between 60 and 1,200 m. Often along ridge crests, where it 

has a somewhat reduced stature. H = 30 m.

Dacrydium nidulum. Fiji, New Guinea, Moluccas, Celebes, Lesser Sunda Islands. Common in the western parts 

of New Guinea, but elsewhere populations are mostly 

rather isolated. A canopy tree of primary and sometimes 

secondary rainforest from sea level to 1,200 m, but mostly 

under 600 m. In Fiji it forms open, low-growing, monodominant stands of stunted trees and is also a component 

of mesic forests (Keppel et al., 2006). H = 30 m. 

Dacrydium pectinatum. Hainan, China, Malesia, Borneo, Philippines. Scattered large individuals are found in 

primary rainforest other than dipterocarp forest from sea 

level to 1,500 m, but mostly below 600 m. Dense stands 

are found in boggy areas, and nearly pure stands of stunted 

trees occur in shallow sandy soils, especially on degraded 

heath forests (“padangs”) and on kerangas in heath forest. 

In Sabah it grows on ultramafic soils; in Brunei it grows in 

pure stands in the center of peat swamps. H = 40 m.

Nageia maxima. Borneo (Sarawak). Locally common 

in the understory of rainforest on ridges in Bako National 

Park and in the peat swamp forest, from ~0 to 120 m. 

H = 10 m. 

Nageia motleyi. Southern Thailand, Malesia (Malaya, Sumatra, Borneo). Scattered in primary and secondary rainforest, from very low altitude (15 m) to ~500 m. 

Occurs not only on slopes and hills on dry soil but also 

in Borneo in other situations: in Sarawak on deep peat 

in a mixed ramin-peat swamp, on ridges and hillsides in 

bindang-dipterocarp forest, and at 1,000 m on podsolic 

sandy loam. H = 54 m.

Podocarpus confertus. Malesia. Subdominant in 

somewhat open and sometimes stunted forest. Found in 

dense local populations on various poor soils, some or 

most of which are ultrabasic. H = 36 m. 

Podocarpus insularis. New Hebrides, Solomon Islands, New Britain, New Guinea and adjacent islands. 

Scattered and locally common in wet rainforest, also in 

Nothofagus forest with undergrowth of Nastus from near 

sea level to 1,680 m, and as smaller trees in low ridge habitats. H = 39 m.

Podocarpus neriifolius. Nepal, Sikkim, India, Thailand, Vietnam, Malaysia, Indonesia, Philippines, Celebes, 

Lesser Sunda Islands, Moluccas, New Guinea, New Britain, Solomon and Fiji islands. Scattered and locally common in primary rainforests from near sea level to ~2,100 
number 95 • 133

m. In most areas it appears as an understory tree with occasionally much larger, emergent specimens in the canopy, 

but in other areas it is normally a canopy tree. Various 

habitats (often on rocky hilltops, in mossy forest, and 

swampy forests but rarely riverine) and on various soils 

(limestone, kerangas in heath forest, sandstone ridges, and 

laterites, sandy clay, ultrabasic). H = 30 m.

Retrophyllum minus. New Caledonia. Southern part 

of island on ultramafic soils, at elevations of up to 200 

m above sea level. A water-dependent plant (rheophyte) 

inhabiting riparian habitats, in this case lakes and riverbanks in shallow water. H = 3 m.

Restricted to Poor Soils or Open Forest

Dacrydium araucarioides. New Caledonia. Locally, 

a dominant species in the vegetation on serpentine soils, 

from sea level to 1,150 m. H = 6 m. 

Dacrydium elatum. Vietnam, Laos, Cambodia, Thailand, Malaya, Sumatra, Borneo. Scattered in moist rainforest, from sea level but mostly above several hundred 

meters to 1,700 m. Grows most abundantly in open situations, indicating a preference for disturbed conditions. It 

also appears to prosper on difficult soils (sandstone, granite, kerangas). Does not enter into high mountain scrub. 

H = 40 m.

Dacrydium nausoriense. Fiji. In slightly open forest 

on the leeward sides of the large islands of Fiji and apparently of limited extent. H = ?

Falcatifolium angustum. Borneo. Found at 90–240 m 

on podsolized sands and kerangas. H = 20 m.

Falcatifolium falciforme. Malaya, Borneo. Locally 

common along ridges as a bushy tree or in the subcanopy 

of primary rainforest, often on podsolic sands and kerangas, but occasionally on deeper fertile soils. Somewhat 

emergent forest giant, from 400–2,100 m. H = 12 m?

Podocarpus beecherae. Southern New Caledonia. 

Maquis vegetation on ultrabasic soil (generally toxic to 

plants and the reason for the stunted plants of the maquis) 

at low elevation. H = 6 m. 

Podocarpus costalis. Philippines and other islands between Luzon and Taiwan. On coastal bluffs from sea level 

to at least 300 m elevation. H = 5 m. 

Podocarpus globulus. Borneo. Found in primary rainforest or moss forest on ridges and peak at 300–1,500 m 

elevation in areas where the forest is not dominated by 

dipterocarps. Adapted to ultramafic soils. H = 27 m. 

Podocarpus micropedunculatus. Borneo. From 0 to 

500 m elevation scattered in Agathis forest understory 

or in thickets at the edges of clearings. Mostly on sandy, 

podzolic soils, kerangas, sandstone, humic peaty podzols 

of raised beaches, and peat swamp forests. H = 7 m. 

Podocarpus polystachyus. Thailand, Malaysia (Malay Peninsula), Borneo, Philippines, Moluccas, west New 

Guinea. Mainly at low altitudes in three distinct habitats: (1) sandy beaches, often gregariously bordering the 

sea at high-tide mark, sandy coastal bluffs and low outcrops, and also sandy ridges in mangroves; (2) on lowland 

coastal kerangas and sandy pandangs (degraded heath 

forest) and sandy heath forest; and (3) on limestone hills 

inland. H = 20 m. 

Podocarpus teysmannii. Malaysia, Indonesia. An understory tree in primary or secondary rainforest at elevations up to 1,140 m. In Banka it grows on granite sands. 

H = 12 m. 

Apparently Associated with Rainforests 

on Relatively Fertile/Deep Soils 

(No Mention of Poor Soil in Description)

Nageia fleuryi. China (Guangdong, Guangxi, and 

Yunnan), Cambodia, Laos, Vietnam (mountainous provinces). Occurs sparsely in primary and slightly disturbed 

evergreen rainforests at elevations of 200–1,000 m. At 

Cuc Phuong and Cat Ba National Parks, the species occurs 

in groups and is the main species in some stands. A lightdemanding species thriving well on good sites with deep, 

well-drained soils developed from limestone. H = 25 m. 

Nageia nagi. Japan, China, Vietnam. Grows in tropical evergreen broad-leaved forest, on hills or mountains 

below 1,000 m elevation. Neutral, shade-demanding tree 

when young. When mature, may become a canopy dominant. Associated with ferralitic, deep and fertile, loamysandy soils. H = 30 m. 

Nageia wallichiana. India (Assam), Burma, Thailand, 

Indochina, China (Yunnan), Malesia (Sumatra, Malaya, 

Banka Island, western Java, Lesser Sunda Islands, Borneo, Philippines, north and central Celebes, Moluccas), 

New Guinea. Scattered and often common (but nowhere 

reported as gregarious or dominant) in primary rainforests from very low elevation (5 m), ascending occasionally as high as 2,100 m. Widely distributed in southern 

China, growing on neutral or slightly acidic soils, tolerating shade. One of the tallest trees in the forest, but perhaps 

barely emergent. H = 54 m. 

Parasitaxus usta. New Caledonia. Found at 400–

1,100 m elevation. This is the only known parasitic gymnosperm. H = 1.8 m. 

Podocarpus ledermannii. New Guinea, New Britain. Scattered and locally common in the understory of 
134 • smithsonian contributions to botany

primary rainforest from low elevation to at least 1,800 m. 

H = 26 m. 

Podocarpus levis. Eastern Borneo, Celebes, Moluccas, 

New Guinea. Scattered and locally common in primary 

rainforest, from sea level to 1,650 m. In eastern Borneo on 

limestone. H = 25 m.

Podocarpus nakaii. Taiwan. Scattered as a subcanopy 

tree in broad-leaved forests in the northern and central 

parts of the island. H = ? 

Podocarpus spathoides. Solomon Islands, eastern 

New Guinea, northern Moluccas, Malaya. Scattered and 

locally common at 1,000–1,200 m in the two western 

stands and near sea level in the east. Recent field work indicates that “P. spathoides” in the Solomon Islands (which 

occurs at sea level) is sufficiently distinct to be described as 

a new species (M. Gardner, Royal Botanic Garden Edinburgh, personal communication). H = 30 m. 

Podocarpus spinulosus. Australia (New South Wales 

and Queensland). A shrub in sheltered coastal sites and 

gullies on the adjacent ranges. H = 3 m.

Montane Tropical Rainforests

Common on Poor Soils but Not Restricted to Them

Dacrycarpus cinctus. Central Celebes, Moluccas, 

New Guinea. In New Guinea extremely common and often dominant or codominant with Nothofagus, Libocedrus, Elaeocarpus, and Podocarpus, in mountain forest 

and mossy forest. On Mount Binaja in orchard-like pure 

stands with a mossy ground cover. Rarely in muddy parts 

of swamps. A canopy tree or sometimes emergent, often 

thick trunked at 1,800–2,850 m. Occasionally reaches 

3,600 m; in Ceram occurs at 1,300–3,000 m. H = 33 m. 

Dacrycarpus compactus. New Guinea. In subalpine 

shrubberies and alpine grasslands, 3,200–3,800 m. Common on the higher peaks near the tree line, sometimes 

forming pure stands, emerging above a subalpine shrubbery, or scattered in alpine grassland often as isolated 

specimens and obviously fire resistant. A component of 

Podocarpus–Libocedrus forest, rarely on wet peaty soil, 

at 2,800–3,950 m, but mostly above 3,400 m. H = 20 m.

Dacrydium beccarii. Solomon Islands, New Guinea, 

Moluccas, Philippines, Borneo, Malaya, northern Sumatra. In the eastern part of the range there are only widely 

separated occurrences, and even in the western part they 

are somewhat discontinuous. Most common as a shrub or 

small tree on mossy ridges where it is often dominant, but 

also found rising above a low, mixed mountain scrub at 

600–2,500 m. A variety of soils have been indicated. H = ?

Dacrydium gibbsiae. Borneo. Common on the slopes, 

being codominant on ultrabasic soils in the mountain 

mossy forest at 1,500–3,600 m. H = 12 m. 

Dacrydium gracile. Borneo, Sarawak. Rows scattered 

in the canopy of mountain rainforest. In Sarawak also in 

heath forest on sandstone. Rare. H = 30 m.

Dacrydium xanthandrum. Solomon Islands, New 

Guinea, Celebes, Philippines, Borneo, northern Sumatra. 

Locally discontinuous. Locally common or even dominant 

and shrubby on mossy ridges with peaty soils over clay, 

sand, granite, sandstone, or dacite. Also scattered as trees 

in nearby primary forest from (500–)1,000–2,700 m. H = ?

Falcatifolium taxoides. New Caledonia. An understory tree in the wet forests on ultramafic soils of the main 

island. H = 15 m. 

Phyllocladus hypophyllus. Philippines, Borneo, Celebes, Moluccas, New Guinea. Moist mountain forests 

sometimes as low as 900 m up to the tree line at 3,200–

4,000 m. Scattered in the forest at lower elevation where 

trees may be quite large. More common but of reduced 

stature at higher elevations. In New Guinea it is a widespread and common species from the upper lowland forests to the subalpine shrubberies, rarely as a solitary tree in 

the alpine grasslands (900–3,600 m). H = 30 m. 

Podocarpus laubenfelsii. Borneo, Sabah, eastern Kalimantan. Scattered in primary rainforest and moss forest, 

growing as a large emergent on rocky ridges on kerangas. 

Dominant in heath forests and on waterlogged acid soils 

of Agathis forests. H = 35 m.

Podocarpus pseudobracteatus. New Guinea. Scattered and locally common in the understory of mossy 

Castanopsis-Nothofagus forest and Dacrydium swamp 

forest, sometimes entering the alpine shrubbery. H = 15 m.

Podocarpus rotundus. Eastern Borneo, Philippines. 

Found in dwarf mossy forest, at about 1,000–2,200 m. 

H = 15 m. 

Podocarpus rubens. Sumatra, Celebes, Lesser Sunda 

Islands, New Guinea. Scattered as a medium-sized tree in 

primary rainforest, mostly above 1,500 m but as low as 

800 m on smaller islands. Otherwise locally common to 

dominant as a small tree on ridges at 2,000–3,000 m or 

occasionally higher. Mostly on latosols. In New Guinea in 

fagaceous mossy forest, rarely in swampy forest on peaty 

soils with Dacrydium. H = 30 m. 

Podocarpus smithii. Australia (Queensland). Endemic 

and highly local in montane rainforests on the eastern 

Atherton Tableland. Usually grows along creeks at mid 

elevations (900–1,200 m), often on granitic soils. H = 30.

Podocarpus urbanii. Jamaica. Montane rainforests 

of the Blue Mountains (1,370–2,250 m) across most soil 
number 95 • 135

types, but most abundant on those of low, but not lowest, 

available nitrogen and phosphorus. H = 15 m.

Sundacarpus amarus. Australia (northeastern coastal 

Queensland), New Guinea, Moluccas, Lesser Sunda Islands, Java, central and southwestern Celebes, Philippines, 

Borneo, Sumatra. In Queensland primarily in the Atherton Tableland on basaltic soils at 600–1,200 m. Scattered 

and often common in primary and secondary rainforest. 

Very common in New Guinea, often in fagaceous forest, 

sometimes in mossy forest or submontane forest at ~900 

m (with Dysoxylum, Macaranga, and Ficus), where it can 

be emergent as a colossal tree. Often on latosols, rarely on 

sandy soils or on marshy ground. Occurs from sea level 

but mainly at 500–2,000(–2,300) m. H = 60 m.

Restricted to Poor Soils or Open Forest

Dacrydium comosum. Malaya. On exposed ridges as 

a local dominant in stunted mossy forest at 1,440–2,200 

m. H = 4 m. 

Dacrydium ericoides. Malesia. Locally common in 

primary forest on exposed mossy ridges at 1,000–1,500 

m. H = 17 m.

Dacrydium lycopodioides. New Caledonia. At elevations of 900–1,400 m in ombrophilous forests on the 

southern part of the main island. H = 25 m.

Dacrydium medium. Malaya, northern Sumatra. Shrub 

or small tree rising above and often dominant in low mountain scrub on what appears to be rather poor soils at 960–

2,100 m in Malaya and 1,800–2,600 m in Sumatra. H = ?

Dacrydium novo-guineense. Celebes, Moluccas, New 

Guinea. Long, mossy crests and in open areas at 700–3,000 m, 

but mostly 1,500–2,200 m. Rising above the mid-mountain 

canopy or a common small tree at higher elevations rising 

above ferns and other scrub often after fire. Sometimes dominant. On different soil types: clay, stony sand. H = 29 m. 

Falcatifolium gruezoi. Philippines, Celebes, Moluccas. 

In exposed locations along ridges or on the borders of open 

areas. At 1,600–2,200 m in the Philippines, 1,200–1,400 

m in Celebes, and 700 m in Obi (Moluccas). H = 12 m.

Podocarpus archboldii. New Guinea. Mainly found 

in upper lowland regions to upper montane areas and occasionally in the subalpine shrubberies (800–3,100 m). 

H = 40 m. 

Podocarpus brassii. New Guinea. Usually found in upper montane and subalpine regions, sometimes venturing 

out into the alpine grasslands. Also as a survivor of burned 

subalpine shrubberies replaced by grassland. H = 15 m. 

Podocarpus crassigemmis. New Guinea. Common or 

subdominant in the canopy of high-mountain mossy forest 

or emergent. Often in Nothofagus and Phyllocladus forest, rarely in secondary forest, and occasionally in grassland. H = 38 m. 

Podocarpus deflexus. Malaysia (northern Sumatra, 

Malaya). Rising above and locally dominant in dwarf 

mountain scrub at 1,500–2,100 m. H = 10 m. 

Podocarpus gibbsiae. Borneo. At 1,200–2,400 m elevation, typically on moss forest ridges. Mostly or always 

on ultramafic soils. H = 20 m. 

Podocarpus glaucus. Solomon Islands, New Guinea, 

Moluccas, Philippines. A medium-sized tree in the forest 

or more often dwarfed or even decumbent on mountain 

crests in stunted mossy forests. Often locally common, 

(500–)1,000–2,800 m. Recorded from stony, sandy clay 

and from a limestone ridge associated with Gymnostoma 

and Rhododendron on peaty soil. H = 15 m. 

Podocarpus gnidioides. New Caledonia. Above 600 

m elevation on rocky ridges in the mountains. H = 2 m. 

Podocarpus ridleyi. Malaysia. Localized and more or 

less dominant on several isolated peaks with poor soils in 

a somewhat stunted rainforest, at 480–1,300 m. On ridges 

over sandstone and on granite. H = 24 m.

Retrophyllum comptonii. New Caledonia. Ombrophilous forests on ultramafic soils throughout the main island at 750–1,450 m. H = 30 m. 

Apparently Associated with Rainforests 

on Relatively Fertile/Deep Soils

(No Mention of Poor Soil in Description)

Dacrycarpus imbricatus. Northern Burma, far southern China, Vietnam, Laos, Malaya, Philippines, Sumatra, 

Borneo, Java, Celebes, Moluccas, Lesser Sunda Islands, 

New Guinea, New Hebrides, Fiji. Mostly scattered and 

common in primary and secondary rainforest. In West 

Java codominant with Podocarpus neriifolius and Altingia noronhae, on the south slope of Mount Tjeremai 

volcano characterizing the zone between 2,400–2,700 

m, unexplainably without other codominants. In Timor 

found under more or less seasonal conditions as isolated 

specimens laden with Usnea in grassland after deforestation, mostly at 1,000–2,500 m. In Lombok reported at 

as low as 200 m, and in Celebes ascending to 3,000 m. 

Probably exterminated at lower elevations by deforestation. In China in mixed forests or pure stands on slightly 

acidic yellow earth soils in valleys of montane streams at 

400–1,500 m. H = 50 m.

Dacrydium spathoides. New Guinea. Growing as a 

canopy tree at 2,150–2,200 m in moist, mossy mountain 

rainforest. H = 34 m. 
136 • smithsonian contributions to botany

Falcatifolium papuanum. New Guinea. Grows in the 

understory of moist mountain forests at 1,500–2,400 m. 

Typical associates include Nothofagus, Myrtaceae, and 

other Podocarpaceae. H = 22 m. 

Podocarpus dispermus. Australia (Atherton Tableland). In rainforest, not plentiful. H = 20 m. 

Podocarpus macrocarpus. Philippines. Scattered and 

sometimes common in cloud forests, ~2,000–2,100 m. 

H = 20 m. 

Podocarpus macrophyllus. Southern Japan, Burma, 

China, Taiwan. Virgin broad-leaved forest dominated by 

over 20 m tall trees of Lauraceae and Fagaceae. H = 15 m.

Podocarpus magnifolius. Eastern Venezuela to Bolivia. Widely distributed in cloud forest at 800–1,600 m. 

H = 25 m. 

Podocarpus neriifolius. Vietnam. Occurs as scattered 

individuals in remaining primary forests in remote areas, 

growing sparsely along water courses, usually mixed with 

broad-leaved species, such as Fokienia hodginsii, Celtis 

australis, Altingia siamensis, Cinnamomum spp., Gironniera subaequalis, Mallotus yunnanensis, Castanopsis, 

and Lithocarpus spp. It chiefly appears on humid, fertile, especially sandy soils, but also on clayey-stony soils. 

H = 25 m.

Podocarpus rumphii. Philippines, Taiwan. Scattered 

in broad-leaved forests at medium altitudes. H = 30 m. 

Prumnopitys ladei. Australia (Atherton Tableland, 

Queensland). Rainforests on granite-derived soils at 

1,000–1,200 m. H = 25 m. 

Retrophyllum rospigliosii. Western Venezuela, Eastern Colombia, central Peru. Native to the wet forests of 

the Andes, it grows best at 500–3,500 m, needing constant 

humidity and cloudiness. Develops best on gentle slopes, 

fertile river lowlands, plateaus, and small depressions. 

Grows in wet, clay or clay-sand, deep, relatively fertile 

soils with good to slow drainage and acidic pH. H = 30 m.

Insufficient Information Available

Dacrycarpus cumingii. Widespread in Philippines, 

northern Sumatra; rare in Borneo. Locally common at 

elevations of (1,000–)1,850–2,650(3,314) m in primary 

moss forest. H = 25 m. 

Dacrycarpus expansus. Papua New Guinea (Central 

Highlands). Locally common or even in pure stands or 

codominant, sometimes emergent. Often in (human) disturbed situations, such as on edges of tree fern grassland, 

1,300–2,750 m. H = 25 m. 

Dacrycarpus kinabaluensis. Borneo. Common, growing in sometimes pure stands in dwarf mountain scrub at 

elevations from about 2,700 m to the tree line at about 

4,000 m. H = 13 m.

Dacrycarpus steupii. Central eastern Borneo, central 

Celebes, New Guinea. Locally common, particularly in 

disturbed forests, or in poorly drained areas where it may 

form nearly pure stands. In boggy grasslands and reed 

swamps, on sandy clay, once on a rocky riverbank, once 

on a limestone hillock in mossy forest (Mount Beratus). 

Elevations of 860–3,420 m, but mostly ~1,500–2,000 m. 

H = 35 m. 

Dacrydium cornwallianum. New Guinea. Dominant 

to nearly pure stands in swamp forests and perhaps also 

mossy heath forests at 1,450–2,300 m. H = 30 m. 

Dacrydium leptophyllum. Western New Guinea. 

Known only from the top of Mount Goliath at 3,000–

3,600 m. H = ?

Prumnopitys standleyi. Costa Rica. At 2,000–

3,200 m, in areas with 2,000–4,000 mm annual rainfall 

and temperature range of 3°C–25°C. H = 25 m.

Podocarpus sellowii. Brazil. Extremely broad and 

scattered range, occurring in montane vegetation. Typical 

of montane areas in the tropical coastal range rainforest 

(Mata Atlántica) and rarely occurs within Araucaria angustifolia forests. H = ?.

Podocarpus acuminatus. Brazil. H = 4.5. 

Podocarpus atjehensis. Northwestern Sumatra, New 

Guinea. H = 15 m.

Podocarpus borneensis. Borneo. Locally common 

or even dominant on mossy rocky ridges or scattered in 

nearby forest, in high kerangas forest and on white, sandy 

soils. Elevations of 700–2,070 m; one collection from a 

swamp at 360 m. H = 12 m.

Podocarpus bracteatus. Indonesia, Java, Lesser Sunda 

Islands. H = 40 m.

Podocarpus brasiliensis. Brazil, Venezuela. Mountains 

and in few hectares of wetland in the middle of the massive Cerrado. H = 15 m.

Podocarpus brevifolius. Philippines, Indonesia, China 

(Guangxi and Guangdong), Vietnam. Usually growing on 

limestone. H = 15 m.

Podocarpus buchholzii. Venezuela. H = 7 m.

Podocarpus glomeratus. Andes. Elevations of 2,500–

4,000 m. H = ?

Podocarpus ingensis. Andes. Elevations of 1,000–

3,000 m. H = ?

Podocarpus lambertii. Argentina, Brazil. H = ?

Podocarpus lophatus. Philippines. Mossy forest at 

1,800 m elevation. H = ?

Podocarpus matudae. Mexico, Guatemala. Large 

tree. H = ?
number 95 • 137

Podocarpus roraimae. Mountains bordering Venezuela and Guyana. Endemic. Elevations of 1,800–2,400 m. 

H = ?

Podocarpus sprucei. Andes. Elevations of 2,000–

4,000 m. H = ?

Podocarpus steyermarkii. Venezuela, Guyana. H = 25 m.

Podocarpus tepuiensis. Eastern Venezuela. Endemic 

shrub or small tree. H = ?

Podocarpus woltzii. Madagascar. H = 20 m.

Prumnopitys montana. Andes. Elevations of 1,500–

4,000 m. H = ?

REFERENCES

Abdillahi, H. S., G. I. Stafford, J. F. Finnie, and J. Van Staden. 2008. 

Antimicrobial Activity of South African Podocarpus species. J. Ethnopharmacol. 119: 191–194.

Adie, H., and M. J. Lawes. 2009a. Role reversal in the Stand Dynamics 

of an Angiosperm–Conifer Forest: Colonising Angiosperms Precede 

a Shade-Tolerant Conifer in Afrotemperate Forest. Forest Ecol. 

Managem. 258: 159–168.

Adie, H., and M. J. Lawes. 2009b. Explaining Conifer Dominance in Afrotemperate Forests: Shade Tolerance Favours Podocarpus latifolius

over Angiosperm Species. Forest Ecol. Managem. 259: 176–186.

Adie, H., and M. J. Lawes. 2011 (this volume). Podocarps in Africa: 

Temperate Zone Relicts or Rainforest Survivors? In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 79–100. Smithsonian Contributions to Botany, 

No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Aerts, R. 1995. The Advantages of Being Evergreen. Trends Ecol. Evol.

10: 402–407.

Aiba, S., and K. Kitayama. 1999. Structure, Composition and Species 

Diversity in an Altitude-Substrate Matrix of Rain Forest Tree Communities on Mount Kinabalu, Borneo. Pl. Ecol. 140: 139–157. 

Aiba, S., K. Kitayama, and M. Takyu. 2004. Habitat Associations with Topography and Canopy Structure of Tree Species in a Tropical Montane Forest on Mount Kinabalu, Borneo. Pl. Ecol. 174: 147–161.

Armesto, J. J., and E. R. Fuentes. 1988. Tree Species Regeneration in 

a Mid-elevation, Temperate Rain Forest in Isla de Chiloé, Chile. 

Vegetatio 74: 151–159.

Atkinson, I. A. E., and R. M. Greenwood. 1989. Relationship between 

Moas and Plants. New Zealand. J. Ecol. 12(suppl.): 67–96.

Bannister, P. 2007. A Touch of Frost? Cold Hardiness of Plants in the 

Southern Hemisphere. New Zealand J. Bot. 45:1–33.

Bannister, P., and J. M. Lord. 2006. Comparative Winter Frost Resistance 

of Plant Species from Southern Africa, Australia, New Zealand, and 

South America Grown in a Common Environment (Dunedin, New 

Zealand). New Zealand J. Bot. 44: 109–119.

Barker, P. C. J. 1991. Podocarpus lawrencei (Hook. f.): Population Structure and Fire History at Goonmirk Rocks, Victoria. Austral. J. Ecol.

16: 149–158.

Baxter, W. A., and D. A. Norton. 1989. Forest Recovery after Logging in 

Lowland Dense Rimu Forest, Westland, New Zealand. New Zealand J. Bot. 27: 391–399.

Baylis, G. T. S. 1969. Mycorrhizal Nodules and Growth of Podocarpus 

in Nitrogen-Poor Soil. Nature 223: 1385–1386.

Bee, J. N., G. Kunstler, and D. A. Coomes. 2007. Resistance and Resilience of New Zealand Tree Species to Browsing. J. Ecol. 95: 

1014–1026.

Beets, P. N., and M. O. Kimberley. 1993. Genotype × Stocking Interactions in Pinus radiata: Productivity and Yield Implications. In Management of Structure and Productivity of Boreal and Subalpine Forests, S. Linder and S. Kellomäki, eds. Stud. For. Suec. 191: 11–19.

Bellingham, P. J., T. Kohyama, and S. Aiba. 1996. The Effects of a Typhoon 

on Japanese Warm Temperate Rainforests. Ecol. Res. 11: 229–247.

Bellingham, P. J., and S. J. Richardson. 2006. Tree Seedling Growth and 

Survival over 6 Years across Different Microsites in a Temperate 

Rain Forest. Canad. J. Forest Res. 36: 910–918.

Bellingham, P. J., E. V. J. Tanner, and J. R. Healey. 1995. Damage and 

Responsiveness of Jamaican Montane Tree Species after Disturbance by a Hurricane. Ecology 76: 2562–2580.

Bentley, W. A. 2007. Influences of Soils Nutrients, Waterlogging, and 

Disturbance Factors on Forest Processes along a New Zealand Soil 

Chronosequence. Ph.D. thesis, University of Cambridge, Cambridge, UK.

Bergin, D. O. 2000. Current Knowledge Relevant to Management of 

Podocarpus totara for timber. New Zealand J. Bot. 38: 343–359.

Bergin, D. O., M. O. Kimberley, and C. B. Low. 2008. Provenance Variation in Podocarpus totara (D. Don): Growth, Tree Form and Wood 

Density on a Coastal Site in the North of the Natural Range, New 

Zealand. Forest Ecol. Managem. 255: 1367–1378.

Beveridge, A. E. 1964. Dispersal and Destruction of Seed in Central 

North Island Podocarp Forests. Proc. New Zealand Ecol. Soc. 11: 

48–55.

Beveridge, A. E. 1973. Regeneration of Podocarps in a Central North 

Island Forest. New Zealand J. Forest. 18: 23– 35.

Bond, W. J. 1989. The Tortoise and the Hare—Ecology of Angiosperm 

Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 

227–249.

Brodribb, T. J. 2011 (this volume). A Functional Analysis of Podocarp 

Ecology. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 165–173. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Brodribb, T. J., and R. S. Hill. 2003a. Implications for Leaf and Shoot 

Physiology in Podocarpaceae. Acta Hort. 615: 173–174.

Brodribb, T. J., and R. S. Hill. 2003b. The Rise and Fall of the Podocarpaceae in Australia—A Physiological Explanation. In Evolution 

of Plant Physiology, A. Hemsley and I. Poole, eds., pp. 381–399. 

Elsevier Academic Press, London.

Brodribb, T. J., N. M. Holbrook, and R. S. Hill. 2005. Seedling Growth 

in Conifers and Angiosperms: Impacts of Contrasting Xylem Structure. Austral. J. Bot. 53: 749–755.

Brophy, J. J., R. J. Goldsack, C. J. R. Fookes, and P. I. Forster. 2000. 

Essential Oils of Australian Gymnosperms. Part 1. The Leaf Oil of 

Sundacarpus amarus (Blume) C.N. Page (Podocarpaceae). J. Essential Oil Res. 12: 421–423. 

Cameron, R. J. 1960. The Indigenous Forests of New Zealand: Intensive 

and Extensive Management. Empire Forest. Rev. 39: 185–194.

Chalwell, S. T. S., and P. G. Ladd. 2005. Stem Demography and Post 

Fire Recruitment of Podocarpus drouynianus: A Resprouting Nonserotinous Conifer. Bot. J. Linn. Soc. 149: 433–449.

Chapin, F. S., III. 1980. The Mineral Nutrition of Wild Plants. Annual 

Rev. Ecol. Syst. 11: 233–260.

Chave, J., D. Coomes, S. Jansen, S. L. Lewis, N. G. Swenson, and 

A. E. Zanne. 2009. Towards a Worldwide Wood Economics Spectrum. Ecol. Letters 12: 351–366; and Dryad Digital Repository. 

doi:10.5061/dryad.234. http://hdl.handle.net/10255/dryad.235 

(accessed 1 May 2009).

Chesson, P. 2000. Mechanisms of Maintenance of Species Diversity. Annual Rev. Ecol. Syst 31: 343–366.

Christie, D. A., and J. J. Armesto. 2003. Regeneration Microsites and 

Tree Species Coexistence in Temperate Rain Forest of Chiloé Island, 

Chile. J. Ecol. 91: 776–784.
138 • smithsonian contributions to botany

Clark, C. M., and I. Carbone. 2008. Chloroplast DNA Phylogeography 

in Long-Lived Huon Pine, a Tasmanian Rain Forest Conifer. Canad. 

J. Forest Res. 38: 1576–1589.

Coomes, D. A., R. B. Allen, W. Bentley, L. E. Burrows, C. D. Canham, 

L. Fagan, D. M. Forsyth, A. Gaxiola-Alcantar, R. L. Parfitt, W. A. 

Ruscoe, D. A. Wardle, D. J. Wilson, and E. F. Wright. 2005. The Hare, 

the Tortoise and the Crocodile: The Ecology of Angiosperm Dominance, Conifer Persistence and Fern Filtering. J. Ecol. 93: 918–935.

Coomes, D. A., and P. J. Grubb. 2000. Impacts of Root Competition in 

Forests and Woodlands: A Theoretical Framework and Review of 

Experiments. Ecol. Monogr. 70: 171–207.

Coomes, D. A., G. Kunstler, C. D. Canham, and E. Wright. 2009. A 

Greater Range of Shade-Tolerance Niches in Nutrient-Rich Forests: 

An Explanation for Positive Richness–Productivity Relationships? 

J. Ecol. 97: 705–717.

Corlett, R. T. 1984. Human Impact on the Subalpine Vegetation of Mt 

Wilhelm, Papua New Guinea. J. Ecol. 72: 841–854.

Colinvaux, P. A., P. E. De Oliveira, J. E. Moreno, M. C. Miller, and M. B. 

Bush. 1996. A Long Pollen Record from Lowland Amazonia: Forest and Cooling in Glacial Times. Science 274: 85–88.

Cox, R. E., S. Yamamoto, A. Otto, and B. R. T. Simoneit. 2007. Oxygenated Di- and Tricyclic Diterpenoids of Southern Hemisphere Conifers. Biochem. Syst. Ecol. 35: 342–362.

Crawford, R. M. M. 1987. Studies in Plant Survival. Blackwell Scientific 

Publications, Oxford, UK.

Crawford, R. M. M., C. E. Jeffree, and W. G. Rees. 2003. Paludification 

and Forest Retreat in Northern Oceanic Environments. Ann. Bot.

91: 213–226.

Cullen, L. E., R. P. Duncan, A. Wells, and G. H. Stewart. 2003. Floodplain and Regional Scale Variation in Earthquake Effects on Forests, 

Westland, New Zealand. J. Roy. Soc. New Zealand 33: 693–701.

Dalling, J. W., P. Barkan, P. J. Bellingham, J. R. Healey, and E. V. J. Tanner. 2011 (this volume). Ecology and Distribution of Neotropical 

Podocarpaceae. In Ecology of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 43–56. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Dalling, J. W., K. Winter, J. D. Nason, S. P. Hubbell, D. A. Murawski, 

and J. L. Hamrick. 2001. The Unusual Life History of Alseis blackiana: A Shade-Persistent Pioneer Tree? Ecology 82: 933–945.

Dickie, I. A., and R. J. Holdaway. 2011 (this volume). Podocarp Roots, 

Mycorrhizas, and Nodules. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 175–

187. Smithsonian Contributions to Botany, No. 95. Smithsonian 

Institution Scholarly Press, Washington, D.C.

Donoso, C. 1989. Antecedentes para la silvicultura del tipo forestal siempreverde. Bosque 10: 37–53.

Duncan, R. P. 1993. Flood Disturbance and the Coexistence of Species 

in a Lowland Podocarp Forest, South Westland, New Zealand. 

J. Ecol. 81: 403–416.

Earle, C. J. 1997–2009. Gymnosperm Database. http://www.conifers.org

(accessed 1 May 2009).

Ebbett, R. L., and J. Ogden. 1998. Comparative Seedling Growth of Five 

Endemic New Zealand Podocarp Species under Different Light Regimes. New Zealand J. Bot. 36: 189–201.

Enright, N., 1995. Conifers of Tropical Australasia. In Ecology of the 

Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 197–222. 

Melbourne University Press, Carlton, Australia.

Enright, N., and J. Ogden. 1995. The Southern Conifers—A Synthesis. In Ecology of the Southern Conifers, N. J. Enright and R. S. 

Hill, eds., pp. 271–287. Melbourne University Press, Carlton, 

Australia.

Esler, A. E. 1978. Botany of the Manawatu District, New Zealand. Government Printer, Wellington, New Zealand.

Feild, T. S., and T. Brodribb. 2001. Stem Water Transport and FreezeThaw Xylem Embolism in Conifers and Angiosperms in a Tasmanian Treeline Heath. Oecologia 127: 314–320.

Gallagher, S. J., B. E. Wagstaff, J. G. Baird, M. W. Wallace, and C. L. Li. 

2008. Southern High Latitude Climate Variability in the Late Cretaceous Greenhouse World. Global Planet. Change 60: 351–364.

Gardner, M. F., V. Hechenleitner, P. Thomas, C. Echeverría, B. Escobar, 

P. Brownless, and A. C. Martínez. 2006. Threatened Plants of Central and South Chile: Distribution, Conservation and Propagation. 

Universidad Austral de Chile, Valdivia, and Royal Botanic Garden 

Edinburgh, Edinburgh. 

Gaxiola, A. 2006. Limitations to Photosynthesis, Growth and Survival 

of Plants Associated with a Soil Chronosequence in New Zealand. 

Ph.D. thesis, University of Cambridge, Cambridge, UK.

Gaxiola, A., L. E. Burrows, and D. A. Coomes. 2008. Tree Fern Trunks 

Facilitate Seedling Regeneration in a Productive Lowland Temperate Rain Forest. Oecologia 155: 325–335.

Gaxiola, A., S. M. McNeill, and D. A. Coomes. 2010. What Drives 

Retrogressive Succession? Plant Strategies to Tolerate Infertile and 

Poorly Drained Soils. Funct. Ecol, 24: 714–722.

Gibson, N., and M. J. Brown. 1991. The Ecology of Lagarostrobos 

franklinii (Hook. f.) Quinn in Tasmania. 2. Population Structure 

and Spatial Pattern. Austral. J. Ecol. 16: 223–229.

Grime, J. P. 1977. Evidence for the Existence of Three Primary Strategies 

in Plants and Its Relevance to Ecological and Evolutionary Theory. 

Amer. Naturalist 111: 1169–1194.

Grubb, P. J. 1977. Control of Forest Growth and Distribution on Wet 

Tropical Mountains with Special Reference to Mineral Nutrition. 

Annual Rev. Ecol. Syst. 8: 83–107.

Grubb, P. J., and P. F. Stevens. 1985. The Forests of the Fatima Basin and 

Mt. Kerigomna, Papua New Guinea, with a Review of Montane 

and Subalpine Rainforests in Papuasia. Australian National University, Canberra.

Gutiérrez, A. G., J. J. Armesto, and J. C. Aravena. 2004. Disturbance and 

Regeneration Dynamics of an Old-Growth North Patagonian Rain 

Forest in Chiloé Island, Chile. J. Ecol. 92: 598–608.

Hawkins, B. J., G. B. Sweet, D. H. Greer, and D. O. Bergin. 1991. Genetic Variation in the Frost Hardiness of Podocarpus totara. New 

Zealand J. Bot. 29: 455–458.

Hill, R. S., and T. J. Brodribb. 1999. Southern Conifers in Time and 

Space. Austral. J. Bot. 47: 639–696.

Hobbie, E. A. 2006. Carbon Allocation to Ectomycorrhizal Fungi Correlates with Belowground Allocation in Culture Studies. Ecology

87: 563–569.

Holloway, J. T. 1954. Forests and Climate in the South Island of New 

Zealand. Trans. Roy. Soc. New Zealand 82: 329–410.

Hoorens, B., D. Coomes, and R. Aerts. 2010. Neighbour Identity Hardly 

Affects Litter-Mixture Effects on Decomposition Rates of New 

Zealand Forest Species. Oecologia 162: 479–489.

Horn, H. S. 1971. The Adaptive Geometry of Trees. Princeton University 

Press, Princeton, N.J.

Hudgins, J. W., E. Christiansen, and V. R. Franceschi. 2004. Induction 

of Anatomically Based Defense Responses in Stems of Diverse 

Conifers by Methyl Jasmonate: A Phylogenetic Perspective. Tree 

Physiol. 24: 251–264.

Hurst, S. E., M. H. Turnbull, and D. A. Norton. 2002. The Effect of 

Plant Light Environment on Mycorrhizal Colonisation in FieldGrown Seedlings of Podocarp–Angiosperm Forest Tree Species. 

New Zealand J. Bot. 40: 65–72.

Innes, K. P. C., and D. Kelly. 1992. Water Potentials in Native Woody 

Vegetation during and after a Drought in Canterbury. New Zealand 

J. Bot. 30: 81–94.

Jaffré, T. 1995. Distribution and Ecology of the Conifers of New Caledonia. In Ecology of the Southern Conifers, N. J. Enright and R. S. 
number 95 • 139

Hill, eds., pp. 171–196. Melbourne University Press, Carlton, 

Australia.

Jennings, S. M., L. G. Edwards, and J. E. Hickey. 2005. Natural and 

Planted Regeneration after Harvesting of Huon Pine (Lagarostrobos franklinii) at Traveller Creek, Western Tasmania. Tasforests 16: 

61–70.

Jorgensen, P. M., and S. Leon-Yanez. 1999. Catalogue of the Vascular 

Plants of Ecuador. Missouri Botanical Gardens Press, St. Louis, 

Missouri.

Kelly, D. 1987. Slow Recovery of Beilschmiedia tawa after Severe Frosts in 

Inland Taranaki, New Zealand. New Zealand J. Ecol. 10: 137–140.

Keppel, G., I. H. Rounds, and N. T. Thomas. 2006. The Flora, Vegetation, and Conservation Value of Mesic Forest at Dogotuki, Vanua 

Levu, Fiji Islands. New Zealand J. Bot. 44: 273–292.

Kirkpatrick, J. 1997. Alpine Tasmania. Oxford University Press, Melbourne, Australia.

Kitayama, K., S. Aiba, M. Ushio, T. Seino, and Y. Fujiki. 2011 (this 

volume). The Ecology of Podocarps in Tropical Montane Forests 

of Borneo: Distribution, Population Dynamics, and Soil Nutrient 

Acquisition. In Ecology of the Podocarpaceae in Tropical Forests, 

B. L. Turner and L. A. Cernusak, eds., pp. 101–117. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Kohyama, T. 1986. Tree Size Structure of Stands and Each Species in Primary Warm-Temperate Rain-Forests of Southern Japan. Bot. Mag. 

(Tokyo) 99: 267–279.

Kohyama, T., and P. J. Grubb. 1994. Below- and Above-Ground Allometries of Shade-Tolerant Seedlings in a Japanese Warm-Temperate 

Rain Forest. Funct. Ecol. 8: 229–236.

Körner, C., and J. Paulsen. 2004. A World-Wide Study of High Altitude 

Treeline Temperatures. J. Biogeogr. 31: 713–732.

Kunstler, G., D. A. Coomes, and C. D. Canham. 2009. Size-Dependence 

of Growth and Mortality Influence the Shade Tolerance of Trees in 

a Lowland Temperate Rain Forest. J. Ecol. 97: 685–695.

Ladd, P. G., and N. J. Enright. 2011 (this volume). Ecology of FireTolerant Podocarps in Temperate Australian Forests. In Ecology of 

the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 141–155. Smithsonian Contributions to Botany, 

No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Leverenz, J. W., D. Whitehead, and G. H. Stewart. 2000. Quantitative 

Analyses of Shade-Shoot Architecture of Conifers Native to New 

Zealand. Trees Struct. Funct. 15: 42–49.

Lusk, C. H. 1995. Seed Size, Establishment Sites and Species Coexistence 

in a Chilean Rain-Forest. J. Veg. Sci. 6: 249–256.

Lusk, C. H. 1996. Stand Dynamics of the Shade-Tolerant Conifers Podocarpus nubigena and Saxegothaea conspicua in Chilean Temperate 

Rain Forest. J. Veg. Sci. 7: 549–558.

Lusk, C. H. 2001. Leaf Life Spans of Some Conifers of the Temperate 

Forests of South America. Revista Chilena Hist. Nat. 74: 711–718.

Lusk, C. H. 2011 (this volume). Conifer-Angiosperm Interactions: Physiological Ecology and Life History. In Ecology of the Podocarpaceae 

in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 157–

164. Smithsonian Contributions to Botany, No. 95. Smithsonian 

Institution Scholarly Press, Washington, D.C.

Lusk, C. H., and C. K. Kelly. 2003. Interspecific Variation in Seed Size and 

Safe Sites in a Temperate Rain Forest. New Phytol. 158: 535–541.

Lusk, C., and J. Ogden. 1992. Age Structure and Dynamics of a Podocarp Broadleaf Forest in Tongariro National Park, New Zealand. 

J. Ecol. 80: 379–393.

Lusk, C. H., and B. Smith. 1998. Life History Differences and Tree Species Coexistence in an Old-Growth New Zealand Rain Forest. 

Ecology 79: 795–806.

Lynch, A. H., J. Beringer, P. Kershaw, A. Marshall, S. Mooney, N. Tapper, C. Turney, and S. Van Der Kaar. 2007. Using the Paleorecord 

to Evaluate Climate and Fire Interactions in Australia. Annual Rev. 

Earth Planet. Sci. 35: 215–239.

Martin, P. H., and T. J. Fahey. 2006. Fire History along Environmental 

Gradients in the Subtropical Pine Forests of the Cordillera Central, 

Dominican Republic. J. Trop. Ecol. 22: 289–302.

Martin, P. H., R. E. Sherman, and T. J. Fahey. 2007. Tropical Montane 

Forest Ecotones: Climate Gradients, Natural Disturbance, and Vegetation Zonation in the Cordillera Central, Dominican Republic. 

J. Biogeogr. 34: 1792–1806.

Martin, T. J., and J. Ogden. 2006. Wind Damage and Response in New 

Zealand Forests: A Review. New Zealand J. Ecol. 30: 295–310.

McGlone, M. S. 2001. The Origin of the Indigenous Grasslands of 

Southeastern South Island in Relation to Pre-human Woody Ecosystems. New Zealand J. Ecol. 25: 1–15.

McGlone, M. S., and C. J. Webb. 1981. Selective Forces Influencing the 

Evolution of Divaricating Plants. New Zealand J. Ecol. 4: 20–28.

McGlone, M. S., R. J. Dungan, G. M. J. Hall, and R. B. Allen. 2004. 

Winter Leaf Loss in the New Zealand Woody Flora. New Zealand 

J. Bot. 42: 1–19.

McKelvey, P. J. 1963. The Synecology of the West Taupo Indigenous Forest. New Zealand Forest Serv. Bull. 14: 1–127.

McSweeney, G. D. 1982. Matai/Totara Flood-Plain Forests in South 

Westland. New Zealand J. Ecol. 5: 121–128.

Midgley, J. J., and W. J. Bond. 1991. Ecological Aspects of the Rise of 

Angiosperms—A Challenge to the Reproductive Superiority Hypotheses. Biol. J. Linn. Soc. 44: 81–92.

Molloy, B. P. J. 1995. Manoao (Podocarpaceae), a New Monotypic Conifer Genus Endemic to New Zealand. New Zealand J. Bot. 33: 

183–201.

Monk, C. D. 1966. An Ecological Significance of Evergreenness. Ecology

47: 504–505.

Morley, R. J. 2011 (this volume). Dispersal and Paleoecology of Tropical Podocarps. In Ecology of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 21–41. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Niemann, H., and H. Behling. 2008. Late Quaternary Vegetation, Climate and Fire Dynamics Inferred from the El Tiro Record in the 

Southeastern Ecuadorian Andes. J. Quaternary Sci. 23: 203–212.

Norton, D. A. 1991. Seedling and Sapling Distribution Patterns in a 

Coastal Podocarp Forest, Hokitika Ecological District, New Zealand. New Zealand J. Bot. 29: 463–466.

Norton, D. A. 1995. Forest Structure and Processes. In Riccarton Bush: 

Putaringamotu, B. Molloy, ed., pp. 116–127. Riccarton Bush Trust, 

Christchurch, New Zealand.

Ogden, J., and G. H. Stewart. 1995. Community Dynamics of the New 

Zealand Conifers. In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 64–80. Melbourne University Press, 

Carlton, Australia.

Pickup, M., M. Westoby, and A. Basden. 2005. Dry Mass Costs of 

Deploying Leaf Area in Relation to Leaf Size. Funct. Ecol. 19: 

88–97.

Pittermann, J., J. S. Sperry, U. G. Hacke, J. K. Wheeler, and E. H. Sikkema. 2006a. Inter-tracheid Pitting and the Hydraulic Efficiency of 

Conifer Wood: The Role of Tracheid Allometry and Cavitation Protection. Amer. J. Bot. 93: 1265–1273.

Pittermann, J., J. S. Sperry, J. K. Wheeler, U. G. Hacke, and E. H. Sikkema. 2006b. Mechanical Reinforcement of Tracheids Compromises the Hydraulic Efficiency of Conifer Xylem. Pl. Cell Environm. 29: 1618–1628.

Poorter, L., and F. Bongers. 2006. Leaf Traits Are Good Predictors of Plant 

Performance across 53 Rain Forest Species. Ecology 87: 1733–1743.

Raven, P. H. 1977. Suggestion Concerning Cretaceous Rise to Dominance of Angiosperms. Evolution 31: 451–452.
140 • smithsonian contributions to botany

Reif, A., and R. B. Allen. 1988. Plant Communities of the Steepland 

Conifer-Broadleaved Hardwood Forests of Central Westland, South 

Island, New Zealand. Phytocoenologia 16: 145–224.

Richards, P., and G. B. Williamson. 1975. Treefalls and Patterns of Understory Species in a Wet Lowland Tropical Forest. Ecology 56: 

1226–1229.

Richardson, S. J., D. A. Peltzer, R. B. Allen, and M. S. McGlone. 2005. 

Resorption Proficiency along a Chronosequence: Responses among 

Communities and within Species. Ecology 86: 20–25.

Richardson, S. J., D. A. Peltzer, R. B. Allen, M. S. McGlone, and R. L. 

Parfitt. 2004. Rapid Development of Phosphorus Limitation in 

Temperate Rainforest along the Franz Josef Soil Chronosequence. 

Oecologia 139: 267–276.

Russell, A. J., M. I. Bidartondo, and B. G. Butterfield. 2002. The Root 

Nodules of Podocarpaceae Harbour Arbuscular Mycorrhizal Fungi. 

New Phytol. 156: 283–295.

Sakai, A., D. M. Paton, and P. Wardle. 1981. Freezing Resistance of Trees 

of the South Temperate Zone, Especially Subalpine Species of Australasia. Ecology 62: 563–570.

Six Dijkstra, H. G., D. J. Mead, and I. L. James. 1985. Forest Architecture 

in Terrace Rimu Forest of Saltwater Forest, South Westland, and Its 

Implications for Management. New Zealand J. Forest. Sci. 15: 3-22.

Smale, M. C. 1984. White-Pine Bush—An Alluvial Kahikatea (Dacrycarpus dacrydioides) Forest Remnant, Eastern Bay of Plenty, New 

Zealand. New Zealand J. Bot. 22: 201–206.

Smale, M. C., B. R. Burns, P. N. Smale, and P. T. Whaley. 1997. Dynamics 

of Upland Podocarp/Broadleaved Forest on Mamaku Plateau, Central 

North Island, New Zealand. J. Roy. Soc. New Zealand 27: 513–532.

Smale, M. C., and M. O. Kimberley. 1986. Growth of Naturally Regenerating Beilschmiedia and Podocarps in Unlogged and Selectively 

Logged Podocarp/Tawa Forest, Pureora. New Zealand J. Forest. 

Sci. 16: 131–141.

Sniderman, J. M. K., B. Pillans, P. B. O’Sullivan, and A. P. Kershaw. 

2007. Climate and Vegetation in Southeastern Australia Respond to 

Southern Hemisphere Insolation Forcing in the Late Pliocene–Early 

Pleistocene. Geology 35: 41–44.

Tanner, E. V. J. 1977. Four Montane Rain Forests of Jamaica: A Quantitative Characterization of the Floristics, the Soils and the Foliar 

Nutrient Levels, and a Discussion of the Interrelations. J. Ecol. 65: 

883–918.

Tyree, M. T., and J. S. Sperry. 1989. Vulnerability of Xylem to Cavitation 

and Embolism. Annual Rev. Pl. Physiol. Pl. Molec. Biol. 40: 19–38.

Uhl, C., K. Clark, N. Dezzeo, and P. Maquirino. 1988. Vegetation Dynamics in Amazonian Treefall Gaps. Ecology 69: 751–763.

Urlich, S. C., G. H. Stewart, R. P. Duncan, and P. C. Almond. 2005. Tree 

Regeneration in a New Zealand Rain Forest Influenced by Disturbance and Drainage Interactions. J. Veg. Sci. 16: 423–432.

Veblen, T. T., B. R. Burns, T. Kitzberger, A. Lara, and R. Villalba. 1995. 

The Ecology of the Conifers of Southern South America. In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 

120–155. Melbourne University Press, Carlton, Australia.

Veblen, T. T., F. M. Schlegel, and B. Escobar R. 1980. Structure and Dynamics of Old-Growth Nothofagus Forests in the Valdivian Andes, 

Chile. J. Ecol. 68: 1–31.

Wade, L. K., and D. N. McVean. 1969. Mt Wilhelm Studies 1. The Alpine and Subalpine Vegetation. Research School of Pacific Studies, Department of Biogeography and Geomorphology Publication 

BG/1. Australian National University Press, Canberra.

Walcroft, A. S., K. J. Brown, W. S. F. Schuster, D. T. Tissue, M. H. Turnbull, K. L. Griffin, and D. Whitehead. 2005. Radiative Transfer and 

Carbon Assimilation in Relation to Canopy Architecture, Foliage 

Area Distribution and Clumping in a Mature Temperate Rainforest 

Canopy in New Zealand. Agric. Forest Meteorol. 135: 326–339.

Wardle, D. A., S. K. Wiser, R. B. Allen, J. E. Doherty, K. I. Bonner, and 

W. M. Williamson. 2008. Aboveground and Belowground Effects 

of Single-Tree Removals in New Zealand Rain Forest. Ecology 89: 

1232–1245.

Wardle, P. 1963a. Growth Habits of New Zealand Subalpine Shrubs and 

Trees. New Zealand J. Bot. 1: 18–47.

Wardle, P. 1963b. Evolution and Distribution of the New Zealand Flora, 

as Affected by Quaternary Climates. New Zealand J. Bot. 1: 3–17.

Wardle, P. 1974. The Kahikatea (Dacrycarpus dacrydioides) Forest of 

South Westland. Proc. New Zealand Ecol. Soc. 21: 62–71.

Wardle, P. 1991. Vegetation of New Zealand. Cambridge University 

Press, Cambridge, UK.

Wardle, P. 2008. New Zealand Forest to Alpine Transitions in Global 

Context. Arctic Antarc. Alpine Res. 40: 240–249.

Wells, A., R. P. Duncan, and G. H. Stewart. 2001. Forest Dynamics 

in Westland, New Zealand: The Importance of Large, Infrequent 

Earthquake-Induced Disturbance. J. Ecol. 89: 1006–1018.

Wells, A., M. D. Yetton, R. P. Duncan, and G. H. Stewart. 1999. Prehistoric Dates of the Most Recent Alpine Fault Earthquakes, New 

Zealand. Geology 27: 995–998.

Whitehead, D., G. M. J. Hall, A. S. Walcroft, K. J. Brown, J. J. Landsberg, D. T. Tissue, M. H. Turnbull, K. L. Griffin, W. S. F. Schuster, 

F. E. Carswell, C. M. Trotter, I. L. James, and D. A. Norton. 2002. 

Analysis of the Growth of Rimu (Dacrydium cupressinum) in South 

Westland, New Zealand, Using Process-Based Simulation Models. 

Int. J. Biometeorol. 46: 66–75.

Whitehead, D., A. Walcroft, K. Griffin, D. Tissue, M. Turnbull, V. Engel, K. Brown, and W. Schuster. 2004. Scaling Carbon Uptake from 

Leaves to Canopies: Insights from Two Forests with Contrasting 

Properties. In Forests at the Land–Atmosphere Interface, M. Mencuccini, J. Grace, J. Moncrieff, and K. G. McNaughton, eds., pp. 

231–254. CAB International, Wallingford, UK.

Wilmshurst, J. M., and M. S. McGlone. 1996. Forest Disturbance in the 

Central North Island, New Zealand, Following the 1850 BP Taupo 

Eruption. Holocene 6: 399–411.

Wilson, H. D. 1982. Field Guide: Stewart Island Plants. Field Guide Publications, Christchurch, New Zealand.

Wright, I. J., P. B. Reich, M. Westoby, D. D. Ackerly, Z. Baruch, 

F. Bongers, J. Cavender-Bares, T. Chapin, J. H. C. Cornelissen, 

M. Diemer, J. Flexas, E. Garnier, P. K. Groom, J. Gulias, K. Hikosaka, B. B. Lamont, T. Lee, W. Lee, C. Lusk, J. J. Midgley, M. L. 

Navas, U. Niinemets, J. Oleksyn, N. Osada, H. Poorter, P. Poot, 

L. Prior, V. I. Pyankov, C. Roumet, S. C. Thomas, M. G. Tjoelker, 

E. J. Veneklaas, and R. Villar. 2004. The Worldwide Leaf Economics 

Spectrum. Nature 428: 821–827.
8 Ecology of Fire-Tolerant 

Podocarps in Temperate 

Australian Forests

Philip G. Ladd and Neal J. Enright

ABSTRACT. Podocarpus drouynianus and P. spinulosus are two unusual conifers restricted to southwestern and eastern Australia, respectively. The species are morphologically similar and genetically closely related to each other but rather distant from 

other members of the subgenus Foliolatus. Both species have retained ancestral podocarp 

characteristics such as dioecy, wind pollination, and large, animal-dispersed seeds with 

recalcitrant germination. They also thrive on soils with generally low nutrient content. 

However, they have several innovations that ensure their success in an environment that 

would generally be considered unsuitable for podocarps. Both species have much higher 

leaf length to width ratios than other Podocarpus species: this presumably aids their 

survival on low- to moderate-rainfall sites. They both resprout strongly after fires, and 

at least for P. drouynianus, seed production is cued by defoliation, and sporophylls are 

produced most prolifically on new growth one year after fire. The species are unique in 

the genus as being successfully adapted to a relatively dry, fire-prone environment.

INTRODUCTION

In almost all parts of the world where the genus occurs, the archetypical 

Podocarpus is a single-stemmed rainforest or riparian tree that is fire sensitive. 

However, in temperate mainland Australia two fire-tolerant shrub podocarps 

represent radical departures from this model. In Ecology of the Southern Conifers (Enright and Hill, 1995), a chapter on conifers of southern Australia (Gibson et al., 1995) noted that little was known about the ecology of several of the 

temperate Australian conifers, particularly P. drouynianus from southwestern 

Australia, and the eastern equivalent species (P. spinulosus) is not even mentioned. Only P. drouynianus has any commercial importance and is used as a 

“background foliage filler” in the cut flower industry in Western Australia. Since 

1995, little has changed concerning our knowledge of the ecology of these two 

species, although one paper has been published on seed production and recruitment of P. drouynianus (Chalwell and Ladd, 2005). 

Philip G. Ladd and Neal J. Enright, School of 

Environmental Science, Murdoch University, 

Murdoch, Western Australia 6150, Australia. 

Correspondence: P. Ladd, P.Ladd@Murdoch

.edu.au.

Manuscript received 13 April 2010; accepted 

9 July 2010.
142 • smithsonian contributions to botany

The two species are classified in Podocarpus subgenus 

Foliolatus and in cladistic analyses are found in a clade 

sister to the remaining members of the subgenus (Biffin et 

al., this volume). Almost all other species in the subgenus 

are tall forest trees, although there are a few species of 

lower stature that grow at high altitudes in Asia. Both species grow in lowland eucalypt forest rather than rainforest 

and retain many of the normal attributes of Podocarpus, 

including seed, leaf, and root morphology. However, in 

other respects they are similar to the much more widespread sclerophyllous Australian flora with which they 

co-occur. This chapter describes the ecology of these firetolerant species and highlights the adaptations that have 

enabled them to survive in environments that at first impression would not be expected to support podocarps.

METHODS

Herbarium records and personal observations of plant 

locations for P. drouynianus and P. spinulosus were used 

to produce distribution maps and BIOCLIM analyses. 

BIOCLIM is a computer modeling system that uses bioclimatic parameters derived from mean monthly climatic estimates to predict climatic conditions at any specified location 

(Busby, 1986). Using a digital elevation model and parameters such as latitude, longitude, and altitude, the climatic 

envelope of a species can be predicted. BIOCLIM was used 

to examine the climatic envelope of these two podocarp species. Mean bioclimatic details for the two species were statistically compared with a t test (or Mann Whitney U test if the 

data failed to satisfy requirements for parametric testing). 

Population size and structure were measured in the field in 

plots of various sizes, depending on the density of plants 

and in order to obtain a sufficient number of plants to gain 

a representative sample. Since these species are lignotuberous multi-stemmed shrubs, size class structures were based 

on number of stems for plants up to 10 stems and then the 

circumference of the lignotuber for larger plants. This was 

considered the most appropriate procedure because stem 

number varies with time since fire and also because longest 

diameter often did not reliably represent the size of the lignotuber if its outline was irregular.

Seed Mass, Seed Production, 

and Germination Rate

Seed mass was determined for seeds collected from 

populations of P. drouynianus at Jalbarragup and Nannup, 

south of Perth, and from a population of P. spinulosus at 

Pearl Beach, near Sydney. Seed production was examined 

for populations of P. drouynianus at Jalbarragup and Sawyers Valley, east of Perth. 

Seed from natural populations at Jalbarragup and 

collected from garden-cultivated plants of P. spinulosus

was germinated on the surface of soil in seed trays in 

controlled-temperature cabinets at 5°C temperature intervals between 15°C and 35°C and, for seeds subject to cold 

stratification, at 4°C (20 seeds × 5 replicates). Large seed 

size prevented good contact with the moist surface of filter 

paper, and being partially impressed into the soil surface 

provided a better moisture contact with the seed, so that 

germination on soil was the preferred method for germination testing. Whereas seed germination for many species 

in the fire-prone sclerophyll forests of southern Australia 

is enhanced by the effects of heat and/or smoke associated 

with fire relative to rates in the absence of these cues (Enright et al., 1997), the postfire pattern of seed production 

in P. drouynianus suggested that no fire-related stimulus is 

required for germination, and initial germination testing 

assumed no such requirement.

Stem and Leaf Measurements

The timing and extent of lignotuber development was 

examined in seedlings from seed collected at Pearl Beach and 

Jalbarragup. Stem outgrowths in P. spinulosus were studied 

by microscopic examination of stem sections fixed in a mixture of formalin, acetic acid, and alcohol, then embedded in 

plastic for sectioning and stained with toluene blue.

Leaf dimensions of P. drouynianus and P. spinulosus

were compared with published measurements from other 

species in the subgenus Foliolatus. Our hypothesis was that 

as the two Australian species grow at the arid end of the 

podocarp climatic spectrum, they should have narrower 

leaves than most of the other species, which generally occur 

in much wetter environments. Leaf measurements were derived from the mean value on the basis of dimensions given 

for species listed on the Gymnosperm Database Web site 

(http://www.conifers.org/po/po/index.htm; accessed 7 July 

2009) for P. spinulosus plants grown in Perth and P. drouynianus from plants collected in the field near Nannup.

Population Structure

Size structure in P. drouynianus is reported for two 

populations (Jalbarragup and Sawyers Valley; see Chalwell and Ladd, 2005, for full details of populations and 

sampling methods) and in P. spinulosus for four populations, two at Pearl Beach (Crommelin 1 and 4), plus single 
number 95 • 143

populations at Lake Burrill and Yalwal (Table 8.1). Plants 

were divided into classes by size: the first two categories 

were by number of stems (1–2 and 3–10), and plants with 

more than 10 stems were then divided into 20 cm (P. spinulosus) or 50 cm classes (P. drouynianus).

RESULTS

Species Distribution

Podocarpus spinulosus and P. drouynianus are endemic to eastern and southwestern Australia, respectively, 

in areas relatively close to the coast, where rainfall is generally higher and risk of frosts lower than for sites farther inland at the same latitude. Podocarpus spinulosus

extends over a much greater latitudinal range (approximately 24°S–36°S) than P. drouynianus (32°S–35°S; Figure 8.1), and although the overall climate profiles of the 

two species are similar (e.g., no significant difference in 

mean annual rainfall between habitats: P. drouynianus, 

1039 ± 26 mm; P. spinulosus, 1115 ± 59 mm), there are 

several significant differences between them in other bioclimatic details (Table 8.2). Mean annual temperature is 

significantly lower for P. drouynianus than for P. spinulosus, and precipitation in the warmest quarter is significantly lower for P. drouynianus but is the reverse for the 

coolest quarter, reflecting the strong Mediterranean-type 

climate experienced by P. drouynianus.

Seed Production and Germination

Plants of both species are dioecious. The seeds are 

borne on a “podocarpium,” colored deep purple when 

ripe. Seed mean fresh mass for P. spinulosus is significantly 

lower (0.24 ± 0.01 g, Pearl Beach population; U = 625, n = 

25, p < 0.001) than for P. drouynianus (1.74 ± 0.19 g, Jalbarragup population). However, for P. drouynianus there 

was also a difference in seed mass between nearby populations (~15 km), with seeds from the Nannup population 

significantly heavier (2.30 ± 0.11 g; t = 3.89, p < 0.001) 

than seeds from Jalbarragup. 

The seed is recalcitrant and germinates several months 

after it is shed from the plant in summer. In southwestern Australia this coincides with the onset of winter rains. 

In eastern Australia rainfall is more evenly distributed 

through the year, but lower-temperature and higherhumidity conditions toward winter are likely to be more 

suitable for seedling establishment than hotter conditions 

earlier in the year.

Incubation of seeds at higher temperatures reduces the 

time to germination. For both species germination is fastest at 35°C and begins later at lower temperatures, being 

slowest at 15°C (Figure 8.2). However, final germination 

success is similar at all temperatures. Seed kept at 4°C 

failed to germinate during the time of the trial but did germinate once it was shifted to room temperature (~20°C). 

There was no germination requirement for fire-related 

cues such as heat or smoke in either species.

In natural forest populations, P. drouynianus produces 

major crops of seeds one year after a summer fire (Chalwell 

and Ladd, 2005). Both male and female plants produce 

sporophylls on the new shoots arising from the lignotuber. 

Plants that are partially burnt only produce sporophylls 

on new shoots, with none on any surviving unburnt stems. 

In the second year after fire sporophyll production is less 

prolific and seed is rarely produced, and three years or 

more after fire no sporophylls occur. However, there is no 

TABLE 8.1. Location, details, and attributes for the sites mentioned in the text. Abbreviations: NSW, New South Wales; WA, Western 

Australia.

 Elevation

Site name Location (m) Geology Soil Vegetation

Pearl Beach NSW, 33°32′S, 151°18′E 20 Sedimentary sands Sand Eucalypt open forest

Sydney Botanic Gardens NSW, 33°33′S,151°13′E 20 Sandstone Skeletal sandy soil Cultivated garden

Yalwal NSW, 34°11′S,150°37′E 200 Sandstone Skeletal sandy soil Eucalypt open forest

Burrill Lake NSW, 35°22′S, 150°26′E 20 Sedimentary sands Sand Eucalypt open forest

Sawyers Valley WA, 31°55′S, 116°13′E 250 Lateritized granite Red brown earth Eucalypt open forest

Nannup WA, 33°59′S, 115°45′E 210 Lateritized granite Red brown earth Eucalypt open forest

Jalbarragup WA, 34°03′S, 115°37′E 150 Lateritized granite Red brown earth Eucalypt open forest
144 • smithsonian contributions to botany

TABLE 8.2. Bioclimatic details of Podocarpus drouynianus and P. spinulosus. Abbreviations: MWU, 

Mann Whitney U test; NS, not significant. Values in parentheses are the standard error of the mean.

P. drouynianus P. spinulosus

Climatic measure (n = 46) (n = 22) Significance

Mean annual rainfall (mm) 1,039 (26) 1,115 (59) NS

Mean annual temperature (°C) 15.6 (0.1) 17.3 (0.1) MWU = 893, 

 p < 0.001

Mean precipitation, warmest quarter (mm) 73 (3) 375 (26) MWU = 1,012, 

 p < 0.001

Mean precipitation, coolest quarter (mm) 478 (13) 231 (70) t test, p < 0.001

FIGURE 8.1. Map showing the location of records for Podocarpus spinulosus and P. drouynianus.
number 95 • 145

simple obligate relationship between fire, new shoots, and 

seed production as plants that have persisted for many 

years without fire in paddocks after forest clearing may 

produce seeds on the new growth from established stems. 

Thus, the reproductive response to fire appears to break 

down if aboveground stems grow undisturbed by fire for 

long intervals. Seed production of P. spinulosus in natural 

populations has not been followed for sequential years after a fire. However, circumstantial evidence suggests that 

P. spinulosus produces sporophylls in most years. A population assessed at Pearl Beach two years after a fire was 

producing copious seed, and plants grown from this seed 

FIGURE 8.2. Seed germination at various temperatures for (A) P. drouynianus and (B) 

P. spinulosus. Bars are standard error of the mean (n = 4).
146 • smithsonian contributions to botany

in cultivation produced sporophylls each year once plants 

were 10 years old. Experimentally burnt cultivated plants 

did not produce sporophylls until two years after the fire. 

Occasional seeds were also observed on long-unburnt individuals in the Sydney Botanical Gardens. Thus, fire stimulates seed production in P. drouynianus, but it is not clear 

if this is true for P. spinulosus.

The transition from ovules to seeds was examined on 

randomly selected large plants (>30 stems >1 m tall) of 

P. drouynianus at Sawyers Valley, near Perth, in 2004 and 

2005. Mean ovule production in 2004 was approximately 

10 ovules per stem (3.9 seeds per stem), whereas in the following year the same stems produced only a mean of 0.8 

ovules and no seed was matured (Figure 8.3).

Randomly selected plants at Jalbarragup had a mean 

of 0.43 seeds m-2

, whereas at Sawyers Valley mean seed 

production from three 100 m2 quadrats was 0.58 m-2 in 

1994 but only 0.10 m-2 following a patchy fuel reduction 

burn at the site in 2004 (Figure 8.3). At both sites the 95% 

confidence intervals were large, indicating high variability 

of seed production among plants. 

At Jalbarragup only eight seedlings were produced 

from 6,652 seeds that were followed for six months from 

seed fall (Chalwell, 1994). In a 1998 census of seedlings 

at Sawyers Valley, establishment was patchy, with 19 seedlings growing from the 1994 seed event in one 100 m2

 plot 

but no seedlings in the two other plots. Seeds are eaten 

by emus, parrots, and mammals (including rodents and 

possums) but depend mainly on emus for dispersal. The 

passage of podocarp seeds through the gut of the emu has 

no effect on germinability (Chalwell, 1994). However, the 

concentration of seeds in emu droppings provides a focus 

for mammal predation on the seed, especially if feces are 

deposited in the open in burnt areas, where most are destroyed by secondary predation (Chalwell, 1994).

Vegetative Growth and Regrowth After Fire

Seedlings of P. spinulosus and P. drouynianus begin 

development of a lignotuber very soon after germination. A swelling mass of stem tissue, and soon afterward 

buds, begins to develop in the axils of the cotyledons in 

both species (Figure 8.4a,b). In P. drouynianus cotyledonary axillary buds appear within three months of the 

plumule emerging from between the cotyledons. In P. spinulosus lignotuber development is slower, with development of a swelling at the cotyledonary node taking up 

to 22 months. In both species, the swelling expands and 

shoots are produced within five months. In P. spinulosus

there may be asymmetrical development of the lignotuber 

with expansion on the lower side if the stem is bent, until the swelling contacts the soil. The lignotubers of these 

podocarps have more obvious buds than seen in lignotubers on most other Australian species. The lignotuber of 

P. drouynianus develops by extending lobes downward 

into the soil. With time, the underground structure may 

branch (Figure 8.4c), and in older plants the extent of the 

genet may be >1 m long (Figure 8.5f).

FIGURE 8.3. Reproduction in Podocarpus drouynianus, showing 

(A) ovules and seeds from marked plants over two years, produced 

after a fire at Sawyers Valley, east of Perth, in 2003; (B) seed production (seeds m-2

) from plants on a transect at Jalbarragup (Jal, south 

of Perth) after a fire in 1993 and from 100 m2

 quadrats at Sawyers 

Valley after fires in two different years (1993 and 2003). Bars are 

95% confidence intervals.
number 95 • 147

Lignotubers develop quickly in both species. In cultivated P. spinulosus, six-year-old plants that were burnt 

produced new shoots from the lignotuber. Although it 

is not known how old the lignotuber of P. drouynianus

needs to be before it can survive fire, its faster early development (described above) suggests that juveniles may 

become tolerant to fire even more quickly.

Swellings may develop in higher leaf axils of P. spinulosus (Lacey and Johnson, 1990) and may also occur 

along the stems in mature plants (Figure 8.5a), usually 

with a geotropic development. Although they are not in 

the position of a lignotuber, they are identical to the lignotuber in their morphology and bud development. There 

may be many outgrowths on arching stems, and if these 

FIGURE 8.4. Lignotubers of Podocarpus, showing (a) very young lignotuber buds 

in the cotyledon axils of P. drouynianus (lower scale in mm); (b) new shoot on a 

young stem burl of P. spinulosus (upper scale in mm); (c) excavated adult plant of 

P. drouynianus; (d) lignotuber of P. drouynianus for a plant approximately seven 

years old (scale in cm).
148 • smithsonian contributions to botany

touch the ground, roots develop from the base of the structure. If the stem is severed from the parent plant or burnt, 

shoots are produced, and an independent plant develops. 

The fate of the buds on the stem swelling is undetermined, 

and buds may develop into roots or shoots. Shoots may 

develop distally from roots but then grow upward (Figure 

8.5b). Sections through a young stem swelling show that 

the xylem grows out from the main axis of the stem (Figure 8.5c), but the buds on the surface of the swelling develop in proliferated cortical tissue (Figure 8.5d) and have 

a vascular trace extending through the xylem of the stem 

toward what was the primary stem tissue as the initial 

FIGURE 8.5. Podocarpus stem structures and growth form, showing (a) a young stem burl of P. spinulosus, 

with the arrow pointing to a bud apex covered by a bract (scale bar = 2 mm); (b) shoots and roots growing 

from a P. spinulosus stem burl that had been buried in the soil, with a large shoot originating below many of 

the roots (scale bar in cm); (c) transverse hand section of a stem burl of P. spinulosus, with the arrow pointing 

to a bud apex (scale bar = 10 mm); (d) light micrograph of a transverse section through a P. spinulosus stem 

burl, with the arrows pointing to bud scales (scale bar = 0.5 mm); (e) excavated prostrate stems (arrow) of 

P.spinulosus, showing shoots produced from a number of stem burls; (f) clumps of P. drouynianus in cleared 

vegetation, with each clump likely to be a genet.
number 95 • 149

stem developed. As the stem swellings increase in size, they 

develop a woody core and seem to be a condensed and 

thickened shoot with abundant superficial buds that can 

develop into roots or shoots.

Adult leaves of both P. spinulosus (length 5.7 ± 0.1 

cm, width 3.4 ± 0.1 mm, length:width ratio 16.9 ± 0.4) 

and P. drouynianus (length 8.2 ± 0.3 cm, width 3.4 ± 0.1 

mm, length:width ratio 24.5 ± 1.1) are significantly narrower (Kruskal Wallis test, p < 0.001) and have a significantly greater length:width ratio (Kruskal Wallis test, p < 

0.001) than the mean for other species in the subgenus 

Foliolatus (length 8.8 ± 1.1 cm, width 10.1 ± 1.1 mm, 

length:width ratio 9.1 ± 0.9 ).

Population Structure

The few populations of P. spinulosus that have 

been measured contain more small plants than occur in 

P. drouynianus populations (Figure 8.6). Of the four populations measured at three sites, three had a relatively high 

proportion of plants in the smallest size class (Crommelin 

4 is the exception, Figure 8.6B). In addition, there were 

few individuals with lignotubers >50 cm in circumference, 

whereas P. drouynianus populations had a much higher 

proportion of large individuals. 

Only two population structures are shown for 

P. drouynianus (Figure 8.6C), although others are presented in Chalwell and Ladd (2005). The plants of this 

species generally grow much larger than those of P. spinulosus. Plot data from Sawyers Valley (sampled in 2003) 

show a high proportion of small (young) individuals, reflecting survival of recruited seedlings after a fire in 1994. 

In this species the population structure (ignoring seedlings 

recruited after the last fire) approximates a normal curve, 

although skewed to smaller individuals in the Jalbarragup 

and larger individuals in the Sawyers Valley populations 

(Figure 8.7), respectively.

The population structure of P. spinulosus is difficult 

to interpret in terms of recruitment of new genets to the 

population. Plant stems tend to be low and spreading 

in contrast to the upright growth of P. drouynianus, so 

that ramet proliferation by layering may be common. In 

the Pearl Beach Crommelin 1 population (Figure 8.6B) 

many apparent individuals were suckers from procumbent stems, either from stem burls or from parts of the 

stem without swellings (Figure 8.5e). Pearl Beach Crommelin 4 plants were generally larger. The Yalwal population seemed to consist mostly of shoots produced from 

stem swellings that had touched the ground and produced 

roots and shoots; most had only one or two shoots (Figure 

FIGURE 8.6. Size class structures for populations of Podocarpus

drouynianus in southwestern Australia and P. spinulosus in eastern Australia. The first two classes are shoots per plant, and the 

subsequent categories are the circumference of the lignotuber. (A) 

Podocarpus spinulosus population at Burrill Lake (plot size 100 m2

, 

measured 14 July 1994) and at Yalwal (plot size 100 m2

, measured 

15 July 1994); (B) P. spinulosus population at Crommelin Reserve, 

Pearl Beach (quadrat sizes: site 1 = 30 m2

, site 4 = 10 m2; measured 

22 January 1994); (C) P. drouynianus population at Sawyers Valley 

(plot size 100 m2

, measured on 30 December 2003) and at Jalbarragup (measured January 1994, plants enumerated from 15 plots 

totaling 375 m2

).
150 • smithsonian contributions to botany

FIGURE 8.7. Sawyers Valley population of P. drouynianus, showing the size of the plants to 1.5 m in the understory of the 

Eucalyptus marginata open forest (photo by B. L. Turner).
number 95 • 151

8.6A). It was not possible to determine the original number of genets in this population.

DISCUSSION

Podocarpus spinulosus and P. drouynianus are both 

in the subgenus Foliolatus and are phylogenetically closely 

related to each other but relatively distant from the rest 

of the species in the genus (Conran et al., 2000; Biffin et 

al., this volume). Although there is abundant evidence 

of podocarps in the Australian fossil record, there is no 

evidence of podocarps in dry environments. Analyses by 

Brodribb and Hill (1998) concluded that modern podocarp distribution was constrained by seasonal drought, 

with species largely confined to moist, aseasonal or weakly 

seasonal climates. The occurrence of these two species on 

the opposite sides of the Australian continent and their 

adaptation to fire-prone, moderately to strongly seasonal 

environments that cannot have been in contact for at least 

20 million years suggest early evolution of the fire-tolerant 

life-form in Podocarpus and a long history of stasis in the 

species. It seems more likely that these two species are a 

result of vicariant speciation rather than the result of longdistance dispersal.

In Australia there has been radiation of a number of 

angiosperm groups concomitant with the drying of the 

continent through the Tertiary. However, in many cases 

only a small number of genera within a group (such as 

a family) have developed the required attributes to allow 

persistence under conditions more arid than those under which the parental group evolved. The groups that 

achieved arid adaptive changes have become spectacularly 

successful in speciation, whereas their generic relatives in 

the rainforest are usually species poor (e.g., Proteaceae; 

Johnson and Briggs, 1981; Jordan et al., 2008). Groups 

that are principally represented in rainforests but have a 

few species in dry forests are less common. In Australia 

the family Meliaceae may be an example, with Synoum

common in some eucalypt forests of the east coast but 

the majority of genera found in rainforests of Australia 

or overseas. However, Podocarpus fits into this category, 

with the two southern Australian species the only ones 

to make an evolutionary excursion into drier forests. To 

do this, they had to undergo a number of morphological 

changes in their typical podocarp plant form.

Both species have narrower leaves and a much greater 

length to width ratio than the mean dimensions for other 

species in the subgenus Foliolatus. In the podocarps (and 

conifers in general), water is distributed from the main leaf 

vein to the photosynthetic tissue via tracheids in accessory 

transfusion tissue rather than from a ramified network of 

veins as in angiosperms. This seems to be a less-efficient 

water distribution system than a network of veins. Under 

drought stress it has been shown that the tracheids of the 

accessory transfusion tissue in P. grayi, a rainforest species 

with broad leaves, collapse and therefore cease to transfer water to the mesophyll cells (Brodribb and Holbrook, 

2005). The narrow leaves of P. spinulosus and P. drouynianus ensure there is only a short distance to transport 

water to the mesophyll from the primary leaf vein, which 

benefits the plant in terms of drought resistance. Brodribb 

and Hill (1998) showed that P. drouynianus had the greatest water use efficiency when compared to the other 12 

species studied, five of which were podocarps from areas 

with greater than 1,500 mm rainfall per annum.

Both fire-tolerant podocarp species have retained their 

ancestral reproductive characteristics of dioecy, wind pollination, vertebrate dispersal, and recalcitrant seed germination. Podocarpus drouynianus has retained a form of 

synchronized cone formation and seeding, which occurs 

in at least some other podocarps (Geldenhuys, 1993), but 

this is cued by fire rather than other environmental signals. The benefits of this equate to masting and include 

increased effectiveness in a wind-pollinated species (Smith 

et al., 1990), seed predator satiation (Donaldson, 1993), 

and increased propagule visibility for a species that relies 

on animals for seed dispersal. Pyrogenic reproduction in 

P. drouynianus makes it a member of a relatively small 

group of Australian woody and herbaceous plants that 

flower almost exclusively in the first year or first few years 

after fire (Burrows and Wardell-Johnson, 2003); these 

include Angophora hispida (Auld, 1986), Doryanthes 

excelsa, Telopea speciossima (Denham and Auld, 2002), 

and the wind-pollinated Stirlingia latifolia (Ladd and 

Wooller, 1997). Podocarpus drouynianus has likely been 

constrained to this reproductive solution in a fire-prone 

environment by its ancestral characteristics, including the 

absence of a cone structure for on-plant seed storage and 

having a seed too large to survive in the soil seed bank. 

Seed maturity of P. drouynianus occurs in winter (following dispersal in late summer), allowing germination at a 

time when conditions are most likely to be reliably moist 

in the Mediterranean-type climate of southwestern Australia. The embryo in the seed is immature when the podocarpium is “ripe” (i.e., fully colored) and continues to 

grow when the seed is initially dispersed. The more rapid 

germination with increased incubation temperature indicates that the rate of embryo development increased with 

higher temperature, so the embryo matured and forced its 
152 • smithsonian contributions to botany

way out of the seed coat earlier than in seeds incubated at 

lower temperature.

Animal dispersal is common in podocarps, although 

it is not universal (Nanami et al., 1999). Geldenhuys 

(1993) identified birds and bats as important dispersers of 

South African podocarp seed, and this certainly occurs in 

a number of New Zealand podocarps (Ogden and Stewart, 1995). The emu is the most important disperser of 

P. drouynianus; other animals may move the seed, primarily as predators rather than dispersers. The emu is a large 

and wide-ranging bird. It consumes gravel that lodges in 

the gizzard, where it serves to grind food. However, seeds 

of many species pass the digestive tract unharmed and may 

take from 3 to 50 hours to pass through (Davies, 2002). 

In this time an emu may traverse several kilometers, so 

podocarp seeds may be deposited in feces far from the location where they were consumed. The large seed size (in 

the upper range of seed sizes in southwestern Australian 

plants) should allow seedlings to establish even in unburnt 

vegetation and, after a subsequent fire, to resprout in the 

relatively competition-free environment, so long as at least 

a few years are available for lignotuber development before fire (Chalwell and Ladd, 2005). Nevertheless, most 

recruitment probably occurs in newly burned areas relatively close to parent plants, and there seedlings have the 

maximum possible time to establish before fire recurs (i.e., 

approximately equal to the mean fire interval). The large 

seed size is still an advantage in an environment where 

most species have much smaller seeds. There are no records of dispersal of P. spinulosus seed, but the propagule 

structure is similar to P. drouynianus, and emus also occur 

along the east coast of Australia and are likely dispersers. 

The apparent absence of fire-stimulated fruiting in P. spinulosus may indicate that recruitment in this species occurs in unburned sites, but further research is needed on 

patterns of recruitment in this species.

Adie and Lawes (this volume) highlight podocarp regeneration failure in grassy podocarp forests in South Africa, presumably due to competition between grasses and 

podocarp seedlings. Western Australian eucalypt forests 

tend to have a relatively open ground layer, so that postfire 

competition with podocarp seedlings is not likely to be as 

severe as in the South African wet forests.

There has been some consideration in this volume of 

the idea that podocarps tend to occur on nutrient-poor 

soils. Podocarpus drouynianus, in particular, is found on 

deep sands and old lateritic soils in southwestern Australia that have been considered as among the most nutrient 

poor in the world and are particularly low in phosphorus 

(Lambers et al., 2008). Podocarpus spinulosus also grows 

on impoverished, thin soils over Permian sandstones in 

eastern Australia, but it may also extend into gullies on 

colluvial material, where nutrient status would be better 

because of a relatively high organic content in the soil. 

However, both species, in common with many other podocarps, survive well on nutrient-poor substrates.

The most obvious innovation in the Australian podocarp species is the ability to resprout from buried stem 

tissue after fire. This is rare in conifers, being found in 

only a few species, including Widdringtonia nodiflora in 

South African fynbos (Keeley et al., 1998) and Actinostrobus acuminatus in southwestern Australian kwongan (personal observation by the authors), both Cupressaceae. The 

proliferation of buds at the cotyledonary node is similar to 

that described for “basal chichi” in Ginkgo biloba seedlings (Del Tredici, 1992) and for eucalypts. Although this 

is not an essential requirement for growing in a fire-prone 

environment, it does ensure that the plant is resilient to 

burning over a range of fire frequencies. A few podocarp 

trees have epicormic sprouts that occur after defoliation by disturbances such as fires (P. elongatus; Midgley 

et al., 1995) or hurricanes, but this is not a particularly 

widespread trait in conifers (Bellingham et al., 1994). 

The lignotuber in both species develops in the axils of the 

cotyledons as in Eucalyptus and seems most similar to the 

“Group C” type of Carr et al. (1984). Del Tredici (1992) 

described the basal chichi of Ginkgo, which seem morphologically similar to the lignotuber of the podocarps and the 

eucalypts. Basal chichi are considered anatomically identical to the aerial chichi but are considered to develop from 

a bud, whereas aerial chichi develop in association with 

wounds to the trunk (Del Tredici, 1992). The aerial stem 

outgrowths of P. spinulosus develop in association with an 

axillary bud and thus differ ontogenetically from the aerial 

chichi of Ginkgo. However, the aerial chichi of Ginkgo, 

like the P. spinulosus form, can produce both shoots and 

roots. Lacey and Johnson (1990) called the woody outgrowths of P. spinulosus as lignotubers, but clearly, ontogenetically they are not strictly equivalent, as lignotubers 

should originate in association with the cotyledonary 

node. In terms of overall attributes the term chichi for the 

P. spinulosus stem outgrowths is appropriate.

Podocarpus drouynianus is a strong resprouter after 

defoliation. However, unlike many other lignotuberous 

species with which it co-occurs, the bud bank is completely 

depleted after each fire (Chalwell and Ladd, 2005), so it 

might not be well served by its bud bank under a regime of 

increasingly frequent fires, as projected for southwestern 

Australia as climate becomes hotter and drier (Williams 

et al., 2009). In P. drouynianus the root stock/lignotuber 
number 95 • 153

may produce short lateral shoots that lead to a relatively 

compact plant form with many stems that rarely grow 

>3 m tall, whereas in P. spinulosus the lignotuber tends 

to be smaller and the stems more spreading. Stems frequently become buried under leaf litter and debris, which 

allows rooting from the chichi and subsequent shoot development. Initial connection to the parent plant would 

be beneficial, allowing the ramet to develop even though 

it may be heavily shaded or covered with litter. However, 

after fire the connection to the parent may be severed, and 

the ramet can resprout in the more open, postfire environment. Similar asexual plant expansion is seen in other 

conifers and is important in their population maintenance 

(Hayakawa et al., 2004), although these species do not 

occur in fire-prone environments.

The contrasting growth forms of these two species 

can be considered similar to the phalanx (P. drouynianus) 

and guerilla (P. spinulosus) strategies of clonal growth (Begon et al., 2006). The guerilla strategy is considered to be 

advantageous in locating resources (light, nutrients) in a 

patchy environment (de Kroons and Hutchings, 1995), but 

it has not been considered in relation to fire and the tradeoff between sexual and asexual reproduction. The guerilla strategy can access more sites more quickly than the 

phalanx strategy, whereas vegetative reproduction may be 

more secure than sexual reproduction in a fire-prone environment when seedlings have limited fire resistance in the 

early years of growth. Fire frequency is difficult to summarize for the Australian forests where these species occur 

and has varied from the Aboriginal period to the present 

(Abbott, 2003). Indeed, there is considerable controversy 

about fire frequency in Western Australian forests. It has 

been deduced that jarrah forest in the Mundaring area 

(close to Sawyers Valley) could carry a fire every three to 

five years and that the frequency of fires lit in jarrah forest 

by Aborigines in summer was two to four years (Abbott, 

2003). In contrast, using fire scars on tree stems, Burrows et al. (1995) estimated an average interval between 

tree-scarring fires of about 80 years before European settlement and about 17 years afterward. However, they suggested that lower-intensity fires of greater frequency might 

not scar large trees. A fire map in Fox (1999) shows that 

fire return times for southwestern Australia are about 10 

years, whereas for much of the area occupied by P. spinulosus fire return times are three to five years and thus 

equally or more frequent than in Western Australia.

Slower lignotuber development in P. spinulosus than 

in P. drouynianus seedlings may be related to the greater 

ability of guerilla development in the former. The guerilla 

strategy involves the lax branches contacting the soil and 

the chichi structures developing roots to produce ramets 

that eventually become independent plants. In the Crommelin Reserve the plants censused in site 1 were predominantly of 1–2 shoots and were mostly produced from a 

network of formerly continuous procumbent stems (covered with plant litter) connecting chichi that had produced 

roots and a few shoots at sporadic points. A similar situation applied at Yalwal, but at that site the stems were 

aerial and mostly still intact. This species seems to rely 

heavily on asexual reproduction to maintain the population, in contrast to P. drouynianus, which has a much 

more compact growth form and can only slowly extend 

the area occupied by a genet. Colonization of new sites by 

this species will be mainly dependent on seeds, so strong 

postfire reproduction (masting) will be beneficial to this 

species in maintaining population numbers.

In frequently (and predictably) disturbed environments 

there has been a dichotomous selection for a seeder plant 

functional trait and refinement of what is often a generalized trait for resprouting. Seeder species need to develop a 

seed bank in preparation for the next stand-destroying fire, 

whereas sprouter species rely heavily on vegetative regeneration. The ancestral reproductive trait of podocarps is 

as a seeder rather than a sprouter. The seeds are large and 

not contained in fire- or desiccation-resistant cones; they 

are unsuitable for storage in soil because of their large size 

and lack of dormancy. Thus, the ancestral podocarp did 

not have a suitable strategy for surviving in a fire-prone 

environment. The development of the ability to resprout 

laid the foundation for the success of P. drouynianus and

P. spinulosus, and the other modifications they display 

are incremental, not radical. By being able to resprout, 

P. drouynianus can emulate a suite of angiosperms that 

are cued to reproduce after fire on newly produced stems 

and thus distribute seeds into a relatively competition-free 

and nutrient-rich environment. Bellingham and Sparrow 

(2000) note that there are trade-offs between vegetative 

resprouting and seeding. The reproductive trade-off for 

sprouters is that they normally do not produce as many 

seeds as seeder species. In most podocarps, adult plants 

produce seeds in all years, although there may be mast 

years (Geldenhuys, 1993), and they may have a variable 

but low investment in buds for resprouting. Podocarpus 

drouynianus has an extreme form of masting, with seeds 

produced only after fire. In years between fires (with fire 

intervals ranging from 10 to 30 years) the plants can accumulate resources to fuel resprouting and reproduction 

after the next fire occurs. However, it is unknown whether 

very long intervals without fire lead to decline in the bud 

bank and an increased susceptibility to mortality from fire, 
154 • smithsonian contributions to botany

as has been described for some other fire-tolerant lignotuberous species (Wellington and Noble, 1985; Enright et 

al., 1998). Alternatively, the time since the last fire may 

become so long that some level of annual fruiting commences, as identified for plants in paddocks that have been 

isolated from fire for many decades. More work is also 

needed on reproduction in P. spinulosus to determine its 

pattern of seed production in relation to fire.

As predicted by Midgley (1996), the development 

of resprouting has meant that both P. drouynianus and 

P. spinulosus have to relinquish the tall monopodial form 

characteristic of most podocarps in wet forests. The species have become subdominants in their communities. 

Nevertheless, they are resilient to both stress (i.e., seasonal 

drought) and disturbance (i.e., fire), and if persistence at a 

site is any indication of evolutionary success, P. drouynianus has certainly achieved this (as demonstrated in Figure 

8.5f), being one of the few native species to survive in the 

predominantly cleared area. These species clearly represent podocarps “on the edge” in terms of their adaptations 

to a set of environmental circumstances beyond those associated with any other members of this large, and typically conservative, plant family.

Acknowledgments

We thank M. Barson (Australian Government Land 

and Coasts Division) and B. Millington (Australian National University) for assisting with population data collection for P. spinulosus, S. Connell (Azimuth Consulting) 

for producing the BIOCLIM analyses, J. Fontaine (Murdoch University) for preparing the graphs, and G. Thomson (Murdoch University) for cutting the stem sections. 

The Sydney and Perth Herbaria kindly provided location 

data for P. drouynianus and P. spinulosus.

REFERENCES

Abbott, I. 2003. Aboriginal Fire Regimes in South-west Western Australia: Evidence from Historical Documents. In Fire in Ecosystems of 

South-west Western Australia: Impacts and Management, I. Abbott 

and N. Burrows, eds., pp. 119–146. Backhuys, Leiden, Netherlands.

Adie, H., and M. J. Lawes. 2011 (this volume). Podocarps in Africa: 

Temperate Zone Relicts or Rainforest Survivors? In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 79–100. Smithsonian Contributions to Botany, No. 

95. Smithsonian Institution Scholarly Press, Washington, D.C.

Auld, T. D. 1986. Post-fire Demography in the Resprouting Shrub Angophora hispida (Sm.) Blaxell: Flowering, Seed Production, Dispersal, Seedling Establishment and Survival. Proc. Linn. Soc. New 

South Wales 109: 259–269.

Begon, M., C. R. Townsend, and J. L. Harper. 2006. Ecology: From Individuals to Ecosystems 4th ed. Blackwell Publishing, Oxford, UK.

Bellingham, P. J., and A. D. Sparrow. 2000. Resprouting as a Life History 

Strategy in Woody Plant Communities. Oikos 89: 409–416.

Bellingham, P. J., E. V. J. Tanner, and J. R. Healey. 1994. Sprouting of 

Trees in Jamaican Montane Forests after a Hurricane. J. Ecol. 82: 

747–758.

Biffin, E., J. Conran, and A. Lowe. 2011 (this volume). Podocarp Evolution: A Molecular Phylogenetic Perspective. In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 1–20. Smithsonian Contributions to Botany, No. 95. 

Smithsonian Institution Scholarly Press, Washington, D.C.

Brodribb, T. J., and R. S. Hill. 1998. The Photosynthetic Drought Physiology of a Diverse Group of Southern Hemisphere Conifer Species 

Is Correlated with Minimum Seasonal Rainfall. Funct. Ecol. 12: 

465–471.

Brodribb, T. J., and N. M. Holbrook. 2005. Water Stress Deforms Tracheids Peripheral to the Leaf Vein of a Tropical Conifer. Pl. Physiol.

137: 1139–1146.

Burrows, N. D., B. Ward, and A. D. Robinson. 1995. Jarrah Forest Fire 

History from Stem Analysis and Anthropological Evidence. Austral. Forest. 58: 7–16.

Burrows, N., and G. Wardell-Johnson. 2003. Fire and Plant Interactions 

in Forested Ecosystems of South-west Western Australia. In Fire in 

Ecosystems of South-west Western Australia: Impacts and Management, I. Abbott and N. Burrows, eds., pp. 225–268. Backhuys, 

Leiden, Netherlands.

Busby, J. R. 1986. Bioclimatic Prediction System (BIOCLIM) User’s 

Manual Version 2.0. Australian Biological Resources Study Leaflet.

Carr, D. J., R. Jahnke, and S. G. M. Carr. 1984. Initiation, Development 

and Anatomy of Lignotubers in Some Species of Eucalyptus. Austral. J. Bot. 32: 415–437.

Chalwell, S. 1994. Population Biology and Vegetative Regeneration of

Podocarpus drouynianus. B.Sc. thesis, School of Environmental Science, Murdoch University, Murdoch, Australia.

Chalwell, S. T. S., and P. G. Ladd. 2005. Stem Demography and Post 

Fire Recruitment of Podocarpus drouynianus: A Resprouting Nonserotinous Conifer. Bot. J. Linn. Soc. 149: 433–449.

Conran, J. G., G. M. Wood, P. G. Martin, J. M. Dowd, C. J. Quinn, P. A. 

Gadek, and R. A. Price. 2000. Generic Relationships within and 

between the Gymnosperm Families Podocarpaceae and Phyllocladaceae Based on an Analysis of the Chloroplast Gene rbcL. Austral. 

J. Bot. 48: 715–724.

Davies, S. J. J. F. 2002. Ratites and Tinamous. Oxford University Press, 

Oxford, UK.

de Kroons, H., and M. J. Hutchings. 1995. Morphological Plasticity in 

Clonal Plants: The Foraging Concept Reconsidered. J. Ecol. 83: 

143–152.

Del Tredici, P. 1992. Natural Regeneration of Ginkgo biloba from 

Downward Growing Cotyledonary Buds (Basal Chichi). Amer. J. 

Bot. 79: 522–530.

Denham, A. J., and T. D. Auld. 2002. Flowering, Seed Dispersal, Seed 

Predation and Seedling Recruitment in Two Pyrogenic Flowering 

Resprouters. Austral. J. Bot. 50: 543–557.

Donaldson, J. S. 1993. Mast Seeding in the Cycad Genus Encephalartos: A Test of the Predator Satiation Hypothesis. Oecologia 95: 

262–271.

Enright, N. J., D. Goldblum, P. Ata, and D. H. Ashton. 1997. The Independent Effects of Heat, Smoke and Ash on Emergence of Seedlings from the Soil Seed Bank of a Heathy Eucalyptus Woodland in 

Grampians National Park, Western Victoria. Austral. J. Ecol. 22: 

81–88.

Enright, N. J., and R. S. Hill. 1995. Ecology of the Southern Conifers.

Melbourne University Press, Carlton, Australia.
number 95 • 155

Enright, N. J., R. Marsula, B. B. Lamont, and C. Wissel. 1998. The Ecological Significance of Canopy Seed Storage in Fire-Prone Environments: A Model for Resprouting Shrubs. J. Ecol. 86: 960–973.

Fox, M. D. 1999. Present Environmental Influences on the Australian 

Flora. In Volume 1: Introduction, 2nd ed., pp. 205–220, Flora of 

Australia. ABRS/CSIRO, Melbourne, Australia.

Geldenhuys, C. J. 1993. Reproductive Biology and Population Structures 

of Podocarpus falcatus and P. latifolius in Southern Cape Forests. 

Bot. J. Linn. Soc. 112: 59–74.

Gibson, N., P. C. J. Barker, P. J. Cullen, and A. Shapcott. 1995. Conifers 

of Southern Australia. In Ecology of the Southern Conifers, N. J. 

Enright and R. S. Hill, eds., pp. 223–252. Melbourne University 

Press, Carlton, Australia.

Hayakawa, T., N. Tomaru, and S. Yamamoto. 2004. Stem Structure and 

Clonal Growth of Chamaecyparis pisifera Growing in Old-Growth 

Beech-Conifer Forest. Ecol. Res. 19: 411–420.

Johnson, L., and B. Briggs. 1981. Three Old Southern Families—Myrtaceae, Proteaceae and Restionaceae. In Ecological Biogeography of 

Australia, A. Keast, ed., pp. 427–469. Junk, The Hague, Netherlands. 

Jordan, G. J., P. H. Weston, R. J. Carpenter, R. A. Dillon, and T. J. Brodribb. 2008. The Evolutionary Relationships of Sunken, Covered, 

and Encrypted Stomata to Dry Habitats in the Proteaceae. Amer. J. 

Bot. 95: 521–530.

Keeley, J. E., M. B. Keeley, and W. J. Bond. 1998. Stem Demography and 

Post-fire Recruitment of a Resprouting Serotinous Conifer. J. Veg. 

Sci. 10: 69–76.

Lacey, C. J., and R. D. Johnson. 1990. Woody Clumps and Clumpwoods. 

Austral. J. Bot. 39: 299–334.

Ladd, P. G., and S. J. Wooller. 1997. Explaining Variation in Pollination 

and Seed Set in an Andromonoecious Genus of the Proteaceae. Acta 

Hort. 437: 115–120.

Lambers, H., J. A. Raven, G. R. Shaver, and S. E. Smith 2008. Plant 

Nutrient Acquisition Strategies Change with Soil Age. Trends Ecol. 

Evol. 23: 95–103.

Midgley, J. J. 1996. Why the World’s Vegetation Is Not Totally Dominated by Resprouting Plants: Because Resprouters Are Shorter 

Than Reseeders. Ecography 19: 92–95.

Midgley, J. J., W. J. Bond, and C. J. Geldenhuys. 1995. The Ecology of 

the Southern African Conifers. In Ecology of the Southern Conifers, 

N. J. Enright and R.S. Hill, eds., pp. 64–80. Melbourne University 

Press, Carlton, Australia.

Nanami, S., H. Kawaguchi, and T. Yamakura. 1999. Dioecy-Induced 

Spatial Patterns of Two Codominant Tree Species, Podocarpus nagi

and Neolitsea aciculata. J. Ecol. 87: 678–687.

Ogden, J., and G. H. Stewart. 1995. Community Dynamics of the New 

Zealand Conifers. In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, eds., pp. 81–119. Melbourne University Press, 

Carlton, Australia.

Smith, C. C., J. L. Hamrick, and C. L. Kramer. 1990. The Advantage of 

Mast Years for Wind Pollination. Amer. Naturalist 136: 154–166.

Wellington, A. B., and I. R. Noble. 1985. Post-fire Recruitment and Mortality in a Population of the Mallee, Eucalyptus incrassata, in Semiarid South-eastern Australia. J. Ecol. 73: 645–656.

Williams, R.J., R. A. Bradstock, G. J. Cary, N. J. Enright, A. M. Gill, 

A. Liedloff, C. Lucas, R. J. Whelan, A. N. Andersen, D. M. J. S. 

Bowman, P. J. Clarke, G. D. Cook, K. Hennessy, and A. York. 

2009. The Impact of Climate Change on Fire Regimes and Biodiversity in Australia—A Preliminary Assessment. Report to Department of Climate Change and Department of Environment Heritage 

and the Arts, Canberra, Australia.

9 Conifer–Angiosperm 

Interactions: Physiological 

Ecology and Life History

Christopher H. Lusk

ABSTRACT. Worldwide, conifers are most successful on sites subject to chronic stresses 

that limit productivity (low temperatures, nutrient poverty, poor drainage). They are 

poorly represented in the lowland tropics but are often important in montane tropical 

forests. Here I explore some functional differences between leaf and xylem traits of conifer and angiosperm trees and their implications for the distributions of these two groups 

on environmental gradients. Analysis of a global data set shows that compared with 

angiosperm trees, conifers tend to have longer-lived leaves with greater mass per area 

(LMA) and lower mass-based photosynthetic capacity. As leaf life span is thought to be 

the main determinant of nutrient retention time, the prominence of conifers on infertile 

soils worldwide is at least partly attributable to thrifty use of nutrients through long leaf 

life spans. Furthermore, because leaf life span correlates with litter decomposition rates, 

these leaf trait differences could potentially influence the competitive balance between 

conifers and angiosperms via positive feedbacks on nutrient cycling. Although scaling of 

leaf life span with LMA is similar in the two groups, angiosperms achieve slightly longer 

leaf life spans than conifers of similar photosynthetic capacity. This might be caused 

by less-efficient leaf display in conifers, resulting in the useful life span of leaves being 

curtailed by self-shading. Representatives of both lineages have narrower conduits in the 

temperate zone than in the lowland tropics/subtropics, reflecting selection for resistance 

to freeze-thaw embolism in cold climates. However, conduit diameters of conifers and 

angiosperm trees differ more in tropical and subtropical forests than at higher latitudes. 

This probably reflects mechanical constraints on maximum tracheid diameters in the homoxylous wood of conifers, preventing this group from producing the highly conductive 

wood typical of fast-growing angiosperm pioneers in tropical forests. This pattern might 

explain why coexistence of conifers and angiosperms is more common in temperate forests and on tropical mountains than in the lowland tropics. Impairment of angiosperm 

carbon gain by freeze-thaw embolism during cold weather may further narrow performance differences between the two lineages on temperate sites. Differences in canopy 

residence time probably deserve more attention as a determinant of conifer-angiosperm 

coexistence in many temperate forests, the longer life span of conifers compensating for 

infrequent recruitment.

Christopher H. Lusk, Department of Biological 

Sciences, Macquarie University, Sydney, New 

South Wales 2109, Australia. Correspondence:

christopher.lusk@mq.edu.

Manuscript received 13 April 2010; accepted 

9 July 2010.
158 • smithsonian contributions to botany

Introduction

Conifers were dominant in forests worldwide during 

the Triassic and Jurassic (Florin, 1963; Miller, 1977) but 

have since been largely replaced by angiosperm trees in the 

lowland tropics, as well as losing much ground in temperate forests. Conifer dominance is now restricted mainly to 

cold or infertile sites (Bond, 1989), although they coexist 

with angiosperms in a variety of forest types (Enright and 

Hill, 1995; Becker, 2000). The advance of angiosperms 

at the expense of conifers and other lineages may have 

significantly altered ecosystem processes in forests. It has 

been suggested, controversially, that rainforests as we 

know them are a product of changes in ecosystem water 

fluxes resulting from angiosperm innovations in anatomy 

and physiology (Boyce et al., 2009). Accelerated nutrient 

cycling is another possible consequence of the angiosperm 

revolution at the end of the Cretaceous (Berendse and 

Scheffer, 2009).

Angiosperm success was initially attributed to reproductive innovations (Raven, 1977; Regal, 1977). Biotic 

pollination, used by many angiosperms, might require less 

investment in pollen than wind pollination and might be 

more effective at achieving sexual recombination in lowdensity populations. Vertebrate seed vectors might have 

dispersed seeds further and to safer sites. After reviewing fossil and contemporary evidence, Midgley and Bond 

(1991) concluded there was little support for the reproductive hypothesis. For example, isolated female trees of windpollinated Podocarpus in South African forests sometimes 

set appreciable quantities of seed (Midgley, 1989), calling 

into question the supposed inefficiency of wind pollination 

in dense, species-rich forests. Furthermore, vertebratedispersed fruits, far from being a uniquely angiosperm innovation, are also found in many conifers such as Taxus, 

Podocarpus, and Dacrydium.

In contrast, Bond (1989) argued that the outcome of 

competition between angiosperms and conifers could be 

determined during the juvenile phase, as a result of vegetative differences between these two groups. Tracheids, 

being limited to relatively small diameters, are usually less 

conductive than angiosperm vessels. This is likely to limit 

the ability of conifer seedlings to supply leaves with water 

and hence constrain carbon gain and growth. Bond (1989) 

further contended that very small initial leaf areas restrict 

the growth rates of young conifer seedlings; although some 

conifers can attain high productivity in later life by accumulating many leaf cohorts, their seedlings are likely to be 

outcompeted by angiosperms on productive sites that permit rapid growth. The more sophisticated vascularization 

of angiosperm leaves also enables them to produce a wider 

variety of leaf sizes and shapes (Bond, 1989), giving them 

advantages in light interception efficiency (C. H. Lusk, unpublished data). Bond (1989) famously applied the “tortoise and hare” metaphor to competition between conifers 

and angiosperms. In essence, conifers are relegated mainly 

to cold or infertile sites because these adverse environments nullify or reduce the potential growth advantages 

of the angiosperm “hares,” preventing them from outpacing the “tortoises.” 

Bond’s landmark paper is first and foremost a synthesis of ideas, and relatively few data were then available to test or explore the mechanisms involved. The 

intervening 20 years have witnessed tremendous growth 

of plant physiological ecology; although only a handful 

of empirical papers have directly addressed the issue of 

conifer-angiosperm interactions (e.g., Becker et al., 1999; 

Lusk et al., 2003; Brodribb et al., 2005), a good deal of 

relevant data and ideas have nevertheless been published. 

Although both lineages encompass a wide range of maximum growth rates, comparative studies of seedlings confirm that even relatively “harelike” conifers such as Pinus

species are unable to match the performance of the fastestgrowing early successional angiosperm trees (e.g., Cornelissen et al., 1996; Reich et al., 1998). Differences between 

maximum seedling growth rates of late successional conifers and angiosperms have also been reported in some 

studies (e.g., Hattenschwiler and Korner, 2000) but not in 

others (e.g., Shipley, 2002), suggesting that some angiosperms are also rather “tortoiselike.” 

Developments in plant physiological ecology have 

also given us a better understanding of the traits underlying variation in plant growth and survival in different 

habitats (e.g., Lambers et al., 1998). Of particular relevance here is our increased understanding of the traits 

that enable conifers to dominate many forests on cold or 

infertile sites despite slow seedling growth rates (Sperry

et al., 2006). This chapter examines data on some stem 

and leaf traits relevant to carbon gain and growth of juvenile conifers and angiosperms and, therefore, likely to 

influence the outcome of competition between them. I also 

briefly consider evidence that differences in adult longevity 

contribute to the coexistence of conifers and angiosperms 

in some temperate forests.

Conduit diameters

It has long been recognized that vessels tend to be 

more conductive than tracheids, as their diameters are 
number 95 • 159

usually larger (Zimmerman and Brown, 1971). According 

to the Hagen-Poiseuille law, conductivity of a conduit is 

proportional to the fourth power of its diameter. All else 

being equal, a conduit with a diameter of 60 μm should 

thus conduct about 16 times more water than one with a 

30 μm diameter. 

More recently, there has been a better understanding of the trade-offs associated with variation in xylem 

anatomy and how small conduits can be advantageous in 

certain situations. Conduit diameter is strongly correlated 

with susceptibility to freeze-thaw embolism (Davis et al., 

1999). When xylem sap freezes, air bubbles form inside 

conduits; when the ice thaws, these bubbles can either dissolve back into the sap solution or expand to fill the entire 

conduit, blocking water transport to the subtended leaves. 

There is less risk of freeze-thaw cavitation in small conduits because the bubbles formed therein are small and 

easily redissolved during thawing, unless xylem tensions 

are very high (Hammel, 1967; Feild and Brodribb, 2001). 

As a result, species with narrow conduits suffer much less 

loss of hydraulic conductivity after freeze-thaw events. 

This is probably one of the main factors underlying the 

prominence of conifers in cold climates worldwide. 

Some angiosperms in tropical forests have very large 

vessel diameters (e.g., Ewers et al., 1990). This presumably reflects a lack of selection for resistance to freeze-thaw 

embolism in tropical climates and the advantages of heteroxylous wood: as fibers do most of the job of supporting 

the tree’s weight, vessel diameters are not subject to strong 

mechanical constraints. On the other hand, the dual role 

of tracheids in homoxylous wood probably means that 

conifers are not as well placed to take advantage of the 

relaxed climatic constraints on conduit diameters in the 

tropics. Wood made up of very large diameter tracheids 

would have a very low density and so might be too weak to 

support a large tree. Tracheid dimensions may thus be limited more by unicellularity and their structural role than by 

the need to protect against cavitation (Sperry et al., 2006). 

If constraints on conduit diameters differ between conifers and angiosperms, this points to one possible explanation for the scarcity of conifers in the lowland tropics. 

On sites subject to freezing temperatures during the growing season (e.g., temperate maritime climates, tropical 

mountains), angiosperm vessels will likely be constrained 

to relatively small diameters, not too different from those 

of tracheids. On frost-free sites, in contrast, angiosperms 

could potentially develop vessel diameters far in excess of 

anything achievable by plants with homoxylous wood, 

giving them a considerable advantage over conifers in 

terms of stem conductivity (Sperry et al., 2006). This will 

influence the economics of hydraulic supply to leaves: for 

a given investment in stem tissue, angiosperms will be 

able to irrigate a larger leaf area and/or develop higher 

leaf conductances, permitting higher potential carbon gain 

and growth. 

Data collated from the literature support the proposal 

that conifer and angiosperm conduit diameters differ most 

at low latitudes (Figure 9.1). Reported conduit diameters 

of evergreen conifers and angiosperms were compared at 

high versus low latitudes. As data on lowland tropical conifers were scarce, the low-latitude category was broadened to include data from lowland subtropical sites (<30° 

latitude). Conifers growing at >2000 m elevation in the 

montane tropics were excluded, as were vesselless angiosperms. Conifer and angiosperm conduit diameters differed only about twofold on average at >30° latitude, and 

the range of diameters overlapped considerably between 

the two lineages. In the lowland tropics and subtropics, 

conifer and angiosperm conduits differed more than fourfold on average, and there was minimal overlap between 

the two lineages (Figure 9.1). In the tropics, conifers will 

therefore be at an overwhelming disadvantage in terms of 

maximum stem conductivity. This is one obstacle to the 

evolution of fast-growing early successional conifers capable of competing with tropical angiosperms such as Cecropia and Macaranga (Lusk, 2008). Most conifer species in 

the lowland tropics are shade-tolerant podocarps, which 

although never dominant on productive sites, are able to 

persist in competition with angiosperms by harvesting understory light efficiently (see Brodribb, this volume). 

In temperate regions, any angiosperm advantage in 

stem conductivity will be reduced as the smaller difference in conduit diameters will be compensated to some 

extent by the high conduit density of homoxylous conifer 

wood (Sperry et al., 2006). This is one factor contributing 

to the frequent coexistence of conifers and angiosperms 

in temperate evergreen forests, although even within 

this biome, conifer distributions tend to favor relatively 

cold and/or infertile sites (Enright and Hill, 1995). Even 

though co-occurring evergreen conifers and angiosperms 

tend to differ in maximum hydraulic capacity (Feild and 

Brodribb, 2001; Lusk et al., 2007), this difference will not 

necessarily translate into higher net carbon gain under all 

conditions. Feild and Brodribb (2001) found that vesselbearing angiosperms growing at the timberline in Tasmania were severely affected by freeze-thaw embolism, losing 

17%–83% of stem conductivity after a single freeze-thaw 

cycle. In contrast, none of their coniferous associates lost 

more than 12% of stem conductivity, as was also true of 

the vesselless angiosperm Tasmannia lanceolata. Even if 
160 • smithsonian contributions to botany

temperate evergreen angiosperms gain much more carbon 

than their coniferous associates during frost-free periods, 

this could conceivably be reversed during winter, when 

vessel-bearing angiosperms are likely to be partly embolized much of the time. 

Leaf traits

Recent reviews have highlighted coordinated scaling of a suite of structural and functional traits of leaves 

across species and ecosystems (Reich et al., 1999; Wright

et al., 2004). Most leaves worldwide can be ordinated on a 

single axis of trait variation, reflecting a trade-off between 

persistence and performance. It must be stressed that this 

“leaf economics spectrum” represents a general principle 

of leaf evolution, not a unique law, because the exact nature of bivariate relationships among the traits involved 

varies geographically (Wright et al., 2005), depending 

on climate, soils, and which resources are most limiting 

to plants. It might be asked whether habitat partitioning between conifers and angiosperms reflects different 

trait-scaling relationships in these two groups (Lusk et al., 

2003). For example, conifer leaves have a reputation for 

FIGURE 9.1. Conduit diameters of aboveground material from evergreen angiosperms and conifers growing at low latitude (<30°) and high latitude (>30°). Data are taken from sources in the appendix. Box 

plots show the 10th, 25th, 50th, 75th, and 90th percentiles. Species growing at high elevations (>2,000 m 

above sea level) were excluded from the low-latitude categories. Values in parentheses show the number of 

species in each category. Means of categories sharing the same letter do not differ significantly at p = 0.05 

(Tukey–Kramer honestly significant difference tests). Diameter data were collated by searching BIOSIS 

previews, obtaining a total of 233 entries from 54 references, representing 166 species. Multiple entries for 

a species were averaged. Stem diameters in which conduits were measured ranged from 1 to >1,000 mm, 

indicating that the means presented above include unquantified effects of stem diameter on conduit taper.

 Angiosperms Conifers Angiosperms Conifers

Mean conduit diameter (microns)

10

100

a

b

b

c

(n = 67) (n = 8) (n = 60) (n = 42)

 Angiosperms Conifers Angiosperms Conifers

Low latitude High latitude

Mean conduit diameter (microns)

10

100

a

b

b

c

(n = 67) (n = 8) (n = 60) (n = 42)
number 95 • 161

longevity (Chabot and Hicks, 1982; Lusk, 2001): does this 

reflect an ability to achieve longer life spans for a given 

investment in leaf mass per area (LMA), and might this 

explain the success of conifers on nutrient-poor soils? Or 

does the slope of the relationship between LMA and leaf 

life span differ between conifers and angiosperms? 

A global data set (Wright et al., 2004) was used to 

compare scaling of leaf life span with LMA in conifers 

and angiosperm trees. The two groups showed no significant difference in the slope of this relationship or in its 

elevation (Figure 9.2). Despite differences in leaf anatomy, 

the two groups achieved similar leaf life spans for a given 

investment of dry matter in leaf tissue per unit area. However, there was a significant shift along the common slope 

of this relationship: notwithstanding considerable overlap, extant conifer and angiosperm trees are essentially 

specialized on different regions of the continuum of leaf 

life spans. Conifers live up to their “tortoise” epithet by 

mainly occupying the “slow” end, with most having leaf 

life spans of >2 years. As leaf life span is the strongest 

influence on variation in nutrient residence time in woody 

plants (Escudero et al., 1992), the prominence of conifers on poor soils in many regions (Escudero et al., 1992; 

Read, 1995; Burns and Leathwick, 1996; Lusk and Matus, 2000) is therefore at least partly attributable to thrifty 

use of nutrients through long leaf life spans. Angiosperm 

trees are concentrated in the middle region of the spectrum, with most, but by no means all, species holding their 

leaves for between 4 months and 2 years. The “fast” end 

of the spectrum is dominated by herbaceous plants. 

It was also found that the relationship between photosynthetic capacity and leaf life span differs significantly between angiosperms and conifers (Figure 9.3). The slope 

was very similar in the two groups, although angiosperms 

leaves achieved slightly longer life spans at a given photosynthetic capacity. One possible explanation lies in the 

FIGURE 9.2. Relationships of leaf life span with leaf mass per area 

of evergreen angiosperms (white circles, dashed line) and conifers 

(solid line; gray circles show podocarps, and black circles represent 

all other conifers). Major axis tests (Falster et al., 2006) showed no 

difference in slope or elevation but showed a shift along a common 

slope (p < 0.0001). Data are from Wright et al. (2004).

FIGURE 9.3. Relationships of leaf life span with photosynthetic 

capacity of evergreen angiosperms (white circles, dashed line) and 

conifers (solid line; gray circles show podocarps, and black circles 

represent all other conifers). Major axis tests (Falster et al., 2006) 

showed no difference in slope but showed a significant difference 

in elevation (p = 0.003) as well as a shift along a common slope 

(p < 0.0001). Angiosperm leaves therefore had significantly higher 

photosynthetic capacity, on average, than conifers, as well as living 

longer than conifer leaves of comparable photosynthetic capacity. 

Data are from Wright et al. (2004).
162 • smithsonian contributions to botany

fact that large-leaved angiosperms often have more efficient leaf display than conifers (C. H. Lusk, unpublished 

data); the resulting differences in self-shading may influence the useful life span of leaves. 

In view of the subject of this book, an analysis focused specifically on podocarp leaf traits would be advantageous. However, podocarps are not well represented in 

the global data set. The few data that are available suggest 

that leaf mass per area, leaf life spans, and photosynthetic 

capacity of podocarps are unremarkable, falling toward 

the middle of the range of values encompassed by conifers 

as a whole (Figures 9.2 and 9.3).

Canopy residence time and

coexistence of angiosperms 

and conifers

Bond’s (1989) paper focused mainly on the likely impact of leaf and stem traits on relative performance of juvenile conifers and angiosperms, in an attempt to explain 

past and present habitat partitioning. One point not covered in his synthesis was the likely role of longevity differences in the coexistence of conifers and angiosperms in 

some forests. Chesson and Warner (1981) proposed that 

differences in adult longevity underlie persistence mixtures 

in many communities, including forests. The essence of this 

general hypothesis is that mixtures can persist if environmental fluctuation permits periodic recruitment of weak 

competitors that usually survive poorly as juveniles and if 

their adults are able to survive over long periods of poor 

recruitment. This “storage effect” is embodied by the dynamics of temperate conifer-angiosperm mixtures. Long 

canopy residence times enable conifers to coexist with angiosperms in many temperate forests, despite infrequent 

recruitment (Read and Hill, 1988; Lusk and Ogden, 1992; 

Carleton et al., 1996; Lusk and Smith, 1998). Data reviews 

have confirmed that conifers are appreciably longer-lived, 

on average, than angiosperm canopy trees in temperate forests of both Northern and Southern hemispheres (Loehle, 

1988; Enright and Ogden, 1995). These poorly understood 

differences in longevity might ultimately prove at least as 

important as light environment partitioning (Lusk et al., 

2009) in explaining the dynamics of tree species coexistence in these communities. Much less information on tree 

longevities is available from tropical forests, although radiocarbon dates suggest that some tropical Agathis species 

can attain ages of up to 1,000 years (Ogden, 1981). The 

role of longevity differences in explaining the dynamics of 

tropical forest communities is therefore unclear.

Conclusions

Developments during the last two decades shed light 

on several aspects of habitat partitioning between conifer 

and angiosperm trees. Bond’s (1989) emphasis on vegetative traits and competitive ability of juveniles is largely 

vindicated by evidence of the constraints imposed by xylem and leaf traits on the performance of conifer seedlings. 

The present state of knowledge permits the generalization 

that conifers do best in habitats where fitness is more a 

function of nutrient conservation or cold resistance than 

of juvenile carbon gain potential and enables us to specify 

some of the mechanisms involved. More attention could 

be paid to the mechanisms underlying coexistence of conifer and angiosperm trees in some forests, despite the apparent competitive advantages of angiosperm juveniles. 

Likely mechanisms include differences in canopy residence 

time and impairment of angiosperm carbon gain by freezethaw embolism during cold weather. 

APPENDIX: 

SOURCES OF CONDUIT DIAMETER 

DATA IN FIGURE 9.1

Barajas-Morales, J. 1985. Wood Structural Differences between Trees of 

Two Tropical Forests in Mexico. IAWA Bull. 6: 355–364.

Davis, S. D., J. S. Sperry, and U. G. Hacke. 1999. The Relationship between Xylem Conduit Diameter and Cavitation Caused by Freezing. Amer. J. Bot. 86: 1367–1372.

Drew, A. P. 1998. Growth Rings, Phenology, Hurricane Disturbance and 

Climate in Cyrilla racemiflora L., a Rain Forest Tree of the Luquillo 

Mountains, Puerto Rico. Biotropica 30: 35–49.

Ewers, F. W., J. B. Fisher, and S.-T. Chiu. 1990. A Survey of Vessel Dimensions in Stems of Tropical Lianas and Other Growth Forms. 

Oecologia 84: 544–552.

Ewers, F. W., and M. H. Zimmermann. 1984. The Hydraulic Architecture 

of Eastern Hemlock (Tsuga canadensis). Canad. J. Bot. 62: 940–946.

Feild, T. S., and T. Brodribb. 2001. Stem Water Transport and FreezeThaw Xylem Embolism in Conifers and Angiosperms in a Tasmanian Treeline Heath. Oecologia 127: 314–320.

Feild, T. S., T. Brodribb, and N. M. Holbrook. 2002. Hardly a Relict: 

Freezing and the Evolution of Vesselless Wood in Winteraceae. Evolution 56: 464–478.

Gartner, B. L., S. H. Bullock, H. A. Mooney, V. B. Brown, and J. L. Whitbeck. 1990. Water Transport Properties of Vine and Tree Stems in a 

Tropical Deciduous Forest. Amer. J. Bot. 77: 742–749.

Gillespie, R. D., S. D. Sym, and K. H. Rogers. 1998. A Preliminary Investigation of the Potential to Determine the Age of Individual Trees of 

Breonadia salicina (Rubiaceae) by Relating Xylem Vessel Diameter 

and Area to Rainfall and Temperature Data. S. African J. Bot. 64: 

316–321.

Hacke, U. G., J. S. Sperry, J. K. Wheeler, and L. Castro. 2006. Scaling 

of Angiosperm Xylem Structure with Safety and Efficiency. Tree 

Physiol. 26: 689–701.

Heady, R. D., J. G. Banks, and P. D. Evans. 2002. Wood Anatomy of Wollemi Pine (Wollemia nobilis, Araucariaceae). IAWA Bull. 23: 339–357.
number 95 • 163

Hennan, P. B. 1997. Wood Anatomy of the Carmichaelia (Fabaceae) 

Complex in New Zealand. New Zealand J. Bot. 35: 395–415.

Ilic, J. 1995. Distinguishing the Woods of Araucaria cunninghamii

(Hoop Pine) and Araucaria bidwilli (Bunya Pine). IAWA Bull. 16: 

255–260.

James, S. A., F. C. Meinzer, G. Goldstein, D. Woodruff, T. Jones, T. Restom, M. Mejia, M. Clearwater, and P. Campanello. 2003. Axial 

and Radial Water Transport and Internal Water Storage in Tropical 

Forest Canopy Trees. Oecologia 134: 37–45.

Kienholz, R. 1931. Effect of Environmental Factors on the Wood Structure of Lodgepole Pine, Pinus contorta Loudon. Ecology 12: 354–

379.

Leitch, M. A. 2001. Vessel-Element Dimensions and Frequency within 

the Most Current Growth Increment along the Length of Eucalyptus globulus Stems. Trees 15: 353–357.

Lindorf, H. 1994 Eco-anatomical Wood Features of Species from a Very 

Dry Tropical Forest. IAWA Bull. 15: 361–376.

Lusk, C. H., M. Jiménez-Castillo, and N. Salazar-Ortega. 2007. Evidence 

That Branches of Evergreen Angiosperm and Coniferous Trees Differ in Hydraulic Conductance but Not in Huber Values. Can J. Bot.

85: 141–147.

Maranho, L. T., F. Galvã, G. I. B. de Muñiz, Y. S. Kuniyoshi, and K. H. 

Preussler. 2006. Variação dimensional das traqueídes ao longo do 

caule de Podocarpus lambertii Klotzsch ex Endl., Podocarpaceae. 

Acta Bot. Brasil. 20: 633–640.

Mayr, S., and H. Cochard. 2003. A New Method for Vulnerability 

Analysis of Small Xylem Areas Reveals That Compression Wood of 

Norway Spruce Has Lower Hydraulic Safety Than Opposite Wood. 

Pl. Cell Environm. 26: 1365–1371.

McCulloh, K. A., J. S. Sperry, and F. R. Adler. 2004. Murray’s Law and 

the Hydraulic vs Mechanical Functioning of Wood. Funct. Ecol.

18: 931–938.

Okoegwale, E. E., and J. E. Idialu. 1998. Trends in Histomorphological Features of Leguminous Woods in Rain Forest and Derived Savanna Areas of Edo State, Nigeria. Acta Bot. Hung. 41: 159–169.

Patel, R. N. 1967a. Wood Anatomy of Podocarpaceae Indigenous to 

New Zealand: 1. Dacrydium. New Zealand J. Bot. 5: 171–184.

Patel, R. N. 1967b. Wood Anatomy of Podocarpaceae Indigenous to 

New Zealand: 2. Podocarpus. New Zealand J. Bot. 5: 307–321.

Patel, R. N. 1968a. Wood Anatomy of Cupressaceae and Araucariaceae 

Indigenous to New Zealand. New Zealand J. Bot. 6: 9–18.

Patel, R. N. 1968b. Wood Anatomy of Podocarpaceae Indigenous to 

New Zealand: 3. Phyllocladus. New Zealand J. Bot. 6: 3–8.

Patel, R. N. 1973a. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 1. Cornaceae. New Zealand J. Bot. 11: 3–22.

Patel, R. N. 1973b. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 2. Escalloniaceae. New Zealand J. Bot. 11: 421–434.

Patel, R. N. 1973c. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 3. Monimiaceae and Atherospermataceae. New Zealand J. Bot. 11: 587–598.

Patel, R. N. 1974a. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 5. Verbenaceae. New Zealand J. Bot. 12: 33–44.

Patel, R. N. 1974b. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 6. Meliaceae. New Zealand J. Bot. 12: 159–166.

Patel, R. N. 1974c. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 7. Santalaceae. New Zealand J. Bot. 12: 431–444.

Patel, R. N. 1975a. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 9. Sapindaceae. New Zealand J. Bot. 13: 131–140.

Patel, R. N. 1975b. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 10. Chloranthaceae. New Zealand J. Bot. 13: 141–

148.

Patel, R. N. 1978a. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 11. Oleaceae. New Zealand J. Bot. 16: 1–6.

Patel, R. N. 1978b. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 12. Icacinaceae. New Zealand J. Bot. 16: 7–12.

Patel, R. N. 1978c. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 13. Moraceae. New Zealand J. Bot. 16: 13–19.

Patel, R. N. 1986. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 15. Fagaceae. New Zealand J. Bot. 24: 189–202.

Patel, R. N. 1987. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 16. Lauraceae. New Zealand J. Bot. 25: 477–488.

Patel, R. N. 1988. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 17. Tiliaceae. New Zealand J. Bot. 26: 337–343.

Patel, R. N. 1989. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 18. Elaeocarpaceae. New Zealand J. Bot. 27: 325–

335.

Patel, R. N. 1990. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 20. Cunoniaceae. New Zealand J. Bot. 28: 349–356.

Patel, R. N. 1992. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 22. Proteaceae. New Zealand J. Bot. 30: 415–428.

Patel, R. N. 1994. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 23. Myrtaceae—Subfam. Leptospermoideae (Part I). 

New Zealand J. Bot. 32: 95–112.

Patel, R. N. 1995. Wood Anatomy of the Dicotyledons Indigenous to 

New Zealand: 25. Myrtaceae—Subfam. Myrtoideae (Part I). New 

Zealand J. Bot. 33: 541–555.

Pittermann, J., and J. S. Sperry. 2003. Tracheid Diameter Determines 

the Extent of Freeze-Thaw Induced Cavitation in Conifers. Tree 

Physiol. 23: 907–914.

Pittermann, J., and J. S. Sperry. 2006. Analysis of Freeze-Thaw Embolism in Conifers: The Interaction between Cavitation Pressure and 

Tracheid Size. Pl. Physiol. 140: 374–382.

Pittermann, J., J. S. Sperry, U. G. Hacke, J. K. Wheeler, and E. H. Sikkema. 2006. Inter-tracheid Pitting and the Hydraulic Efficiency of 

Conifer Wood: The Role of Tracheid Allometry and Cavitation Protection. Amer. J. Bot. 93: 1105–1113.

Sahri, M. H., F. H. Ibrahim, and N. A. A. Shikor. 1993. Anatomy of Acacia mangium Grown in Malaysia. IAWA Bull. 14: 245–251.

Schulte, P. J., and A. C. Gibson. 1988. Hydraulic Conductance and Tracheid Anatomy in Six Species of Extant Seed Plants. Canad. J. Bot.

66: 1073–1079.

Vander Willigen, C., H. W. Sherwin, and N. W. Pammenter. 2000. Xylem 

Hydraulic Characteristics of Subtropical Trees from Contrasting 

Habitats Grown under Identical Environmental Conditions. New 

Phytol. 145: 51–59.

Verheyden, A., F. De Ridder, N. Schmitz, H. Beeckman, and N. Koedam. 

2005. High-Resolution Time Series of Vessel Density in Kenyan 

Mangrove Trees Reveal a Link with Climate. New Phytol. 167: 

425–435.

Wheeler, J. K., J. S. Sperry, U. G. Hacke, and N. Hoang. 2005. Intervessel Pitting and Cavitation in Woody Rosaceae and Other Vesselled Plants: A Basis for a Safety versus Efficiency Trade-off in Xylem Transport. Pl. Cell Environm. 28: 800–812.

REFERENCES

Becker, P. 2000. Competition in the Regeneration Niche between Conifers and Angiosperms: Bond’s Slow Seedling Hypothesis. Funct. 

Ecol. 14: 401–412.

Becker, P., M. T. Tyree, and M. Tsuda. 1999. Hydraulic Conductances of 

Angiosperms versus Conifers: Similar Transport Sufficiency at the 

Whole-Plant Level. Tree Physiol. 19: 445–452.

Berendse, F., and M. Scheffer. 2009. The Angiosperm Radiation Revisited, an Ecological Explanation for Darwin’s ‘Abominable Mystery.’ Ecol. Letters 12: 865–872.

Bond, W. J. 1989. The Tortoise and Hare: Ecology of Angiosperm 

Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 

227–249.
164 • smithsonian contributions to botany

Boyce, C. K., T. J. Brodribb, T. S. Feild, and M. A. Zwieniecki. 2009. 

Angiosperm Leaf Vein Evolution Was Physiologically and Environmentally Transformative. Proc. Roy. Soc. B 276: 1771–1776.

Brodribb, T. J. 2011 (this volume). A Functional Analysis of Podocarp 

Ecology. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 165–173. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Brodribb, T. J., N. M. Holbrook, and R. S. Hill. 2005. Seedling Growth 

in Conifers and Angiosperms: Impacts of Contrasting Xylem Structure. Austral. J. Bot. 53: 749–755.

Burns, B. R., and J. R. Leathwick. 1996. Vegetation-Environment Relationships at Waipoua Forest, Northland, New Zealand. New Zealand J. Bot. 34: 79–92.

Carleton, T. J., P. F. Maycock, R. Arnup, and A. M. Gordon. 1996. In 

situ Regeneration of Pinus strobus and P. resinosa in the Great 

Lakes Forest Communities of Canada. J. Veg. Sci. 7: 431–444.

Chabot, B. F., and D. J. Hicks. 1982. The Ecology of Leaf Life Spans. 

Annual Rev. Ecol. Syst. 13: 229–259.

Chesson, P. L., and R. R. Warner. 1981. Environmental Variability Promotes Coexistence in Lottery Competitive Environments. Amer. 

Naturalist 117: 923–943.

Cornelissen, J. H. C., P. C. Diez, and R. Hunt. 1996. Seedling Growth, 

Allocation and Leaf Attributes in a Wide Range of Woody Plant 

Species and Types. J. Ecol. 84: 755–765.

Davis, S. D., J. S. Sperry, and U. G. Hacke. 1999. The Relationship between Xylem Conduit Diameter and Cavitation Caused by Freezing. Amer. J. Bot. 86: 1367–1372.

Enright, N. J., and R. S. Hill, eds. 1995. Ecology of the Southern Conifers. Melbourne University Press, Carlton, Australia.

Enright, N. J., and J. Ogden. 1995. The Southern Conifers—A Synthesis. 

In Ecology of the Southern Conifers, N. J. Enright and R. S. Hill, 

eds., pp. 271–287. Melbourne University Press, Carlton, Australia.

Escudero, A., J. M. Delarco, I. C. Sanz, and J. Ayala. 1992. Effects of 

Leaf Longevity and Retranslocation Efficiency on the Retention 

Time of Nutrients in the Leaf Biomass of Different Woody Species. 

Oecologia 90: 80–87.

Ewers, F. W., J. B. Fisher, and S. T. Chiu. 1990. A Survey of Vessel Dimensions in Stems of Tropical Lianas and Other Growth Forms. 

Oecologia 84: 544–552.

Falster, D. S., D. I. Warton, and I. J. Wright. 2006. SMATR: Standardised 

Major Axis Tests and Routines. Version 2.0. Macquarie University, 

Sydney, Australia.

Feild, T. S., and T. Brodribb. 2001. Stem Water Transport and FreezeThaw Xylem Embolism in Conifers and Angiosperms in a Tasmanian Treeline Heath. Oecologia 127: 314–320.

Florin, R. 1963. The Distribution of Conifer and Taxad Genera in Time 

and Space. Acta Hort. Bergiani 20: 121–312.

Hammel, H. T. 1967. Freezing of Xylem Sap without Cavitation. Pl. 

Physiol. 42: 55–66.

Hattenschwiler, S., and C. Korner. 2000. Tree Seedling Responses to in 

situ CO2

-Enrichment Differ among Species and Depend on Understorey Light Availability. Global Change Biol. 6: 213–226.

Lambers, H., F. S. Chapin, and T. L. Pons. 1998. Plant Physiological 

Ecology. Springer-Verlag, New York.

Loehle, C. 1988. Tree Life-History Strategies—The Role of Defenses. Canad. J. Forest Res. 18: 209–222.

Lusk, C. H. 2001. Leaf Life Spans of Some Conifers of the Temperate 

Forests of South America. Revista Chilena Hist. Nat. 74: 711–718.

Lusk, C. H. 2008. Constraints on the Evolution and Geographical Range 

of Pinus. New Phytol. 178: 1–3.

Lusk, C. H., R. P. Duncan, and P. J. Bellingham. 2009. Light Environments 

Occupied by Conifer and Angiosperm Seedlings in a New Zealand 

Podocarp–Broadleaved Forest. New Zealand J. Ecol. 33: 83–89.

Lusk, C. H., M. Jiménez-Castillo, and N. Salazar-Ortega. 2007. Evidence 

That Branches of Evergreen Conifer and Angiosperm Trees Differ 

in Hydraulic Conductance but Not in Huber Values. Canad. J. Bot.

85: 141–147.

Lusk, C. H., and F. Matus. 2000. Juvenile Tree Growth Rates and Species 

Sorting on Fine-Scale Soil Fertility Gradients in a Chilean Temperate Rain Forest. J. Biogeogr. 27: 1011–1020.

Lusk, C. H., and J. Ogden. 1992. Age Structure and Dynamics of a 

Podocarp-Broadleaf Forest in Tongariro National Park, New Zealand. J. Ecol. 80: 379–393.

Lusk, C. H., and B. Smith. 1998. Life History Differences and Tree Species Coexistence in an Old-Growth New Zealand Rain Forest. 

Ecology 79: 795–806.

Lusk, C. H., I. Wright, and P. B. Reich. 2003. Photosynthetic Differences 

Contribute to Competitive Advantage of Evergreen Angiosperm 

Trees over Evergreen Conifers in Productive Habitats. New Phytol.

160: 329–336.

Midgley, J. J. 1989. Pollen Dispersal Distances for a Conifer Canopy Species in the Knysna Forest. S. African J. Bot. 55: 662–663.

Midgley, J. J., and W. J. Bond. 1991. Ecological Aspects of the Rise of 

Angiosperms: A Challenge to the Reproductive Superiority Hypotheses. Biol. J. Linn. Soc. 44: 81–92.

Miller, C. N. 1977. Mesozoic Conifers. Bot. Rev. 43: 217–280.

Ogden, J. 1981. Dendrochronological Studies and the Determination of 

Tree Ages in the Australian Tropics. J. Biogeogr. 8: 405–420.

Raven, P. H. 1977. A Suggestion Concerning the Cretaceous Rise to 

Dominance of the Angiosperms. Evolution 31: 451–452.

Read, J. 1995. The Importance of Comparative Growth Rates in Determining the Canopy Composition of Tasmanian Rainforest. Austral. 

J. Bot. 43: 243–271.

Read, J., and R. S. Hill. 1988. The Dynamics of Some Rainforest Associations in Tasmania. J. Ecol. 76: 558–584.

Regal, P. J. 1977. Ecology and Evolution of Flowering Plant Dominance. 

Science 196: 622–629.

Reich, P. B., D. S. Ellsworth, M. B. Walters, J. M. Vose, C. Gresham, J. C. 

Volin, and W. D. Bowman. 1999. Generality of Leaf Trait Relationships: A Test across Six Biomes. Ecology 80: 1955–1969.

Reich, P. B., M. G. Tjoelker, M. B. Walters, D. W. Vanderklein, and 

C. Bushena. 1998. Close Association of RGR, Leaf and Root Morphology, Seed Mass and Shade Tolerance in Seedlings of Nine Boreal Tree Species Grown in High and Low Light. Funct. Ecol. 12: 

327–338.

Shipley, B. 2002. Trade-offs Between Net Assimilation Rate and Specific 

Leaf Area in Determining Relative Growth Rate: Relationship with 

Daily Irradiance. Funct. Ecol. 16: 682–689.

Sperry, J. S., U. G. Hacke, and J. Pittermann. 2006. Size and Function 

of Conifer Tracheids and Angiosperm Vessels. Amer. J. Bot. 93: 

1490–1500.

Wright, I. J., P. B. Reich, J. H. C. Cornelissen, D. S. Falster, P. K. Groom, 

K. Hikosaka, W. Lee, C. H. Lusk, U. Niinemets, J. Oleksyn, 

N. Osada, H. Poorter, D. I. Warton, and M. Westoby. 2005. Modulation of Leaf Economic Traits and Trait Relationships by Climate. 

Global Ecol. Biogeogr. 14: 411–421.

Wright, I. J., P. B. Reich, M. Westoby, D. D. Ackerly, Z. Baruch, 

F. Bongers, J. Cavender-Bares, T. Chapin, J. H. C. Cornelissen, 

M. Diemer, J. Flexas, E. Garnier, P. K. Groom, J. Gulias, K. Hikosaka, B. B. Lamont, T. Lee, W. Lee, C. Lusk, J. J. Midgley, M. L. 

Navas, U. Niinemets, J. Oleksyn, N. Osada, H. Poorter, P. Poot, 

L. Prior, V. I. Pyankov, C. Roumet, S. C. Thomas, M. G. Tjoelker, 

E. J. Veneklaas, and R. Villar. 2004. The Worldwide Leaf Economics Spectrum. Nature 428: 821–827.

Zimmerman, M. H., and C. L. Brown. 1971. Trees, Structure and Function. Springer-Verlag, New York.
10 A Functional Analysis 

of Podocarp Ecology

Timothy J. Brodribb

ABSTRACT. Viewed in terms of species diversity, the Southern Hemisphere conifer family Podocarpaceae is equivalent to its northern sister the Pinaceae. However, despite their 

similar age and common heritage these two families diverge strongly in morphology, 

physiology, and ecology. Both Pinaceae and Podocarpaceae are successful families of vascular plants, and in both cases this success has been built upon contrasting and rather 

canalized adaptive differentiation. Pinaceae thrive in virtually all Northern Hemisphere 

forest environments where freezing limits the success of evergreen angiosperm competitors. In contrast, the Podocarpaceae are most successful in the tropics, where they compete directly with broad-leaved angiosperms, usually in montane rainforest. This chapter 

discusses some of the key adaptations that have enabled tropical Podocarpaceae to remain competitive during the rise of angiosperms. I also examine the hydraulic “Achilles 

heel” that limits all members of the Podocarpaceae to a mesic rainfall envelope.

Adaptation to life in tropical forests

Large, bilaterally flattened leaves are more efficient at harvesting light than 

spirally arranged needle or scale leaves (Leverenz, 1995; Pickup et al., 2005). 

This general rule is highly significant when considering the outcome of conifer–

angiosperm competition in the period since angiosperm diversification in the 

Late Cretaceous. With the exception of Gnetum, gymnosperms appear to be 

incapable of producing large laminate leaves, and as such, they cannot benefit 

from the economic advantages of efficient light harvesting and minimal selfshading that broad leaves offer (Falster and Westoby, 2003). The overwhelming dominance of broad-leaved taxa in most productive regions of the tropics 

indicates that the benefits of large leaf size reach their peak in this region (Webb, 

1968). Warm temperatures and an absence of stresses that could potentially 

limit leaf size, including cold, soil water deficiency, and abiotic mechanical damage in tropical rainforests, contribute to the predominance of large, flattened 

leaves. Given the adaptive bias toward large leaves in the tropics and the limited 

Timothy J. Brodribb, School of Plant Science, 

Private Bag 55, University of Tasmania, Hobart, 

Tasmania 7001, Australia. Correspondence:

timothyb@utas.edu.au.

Manuscript received 13 April 2010; accepted 

9 July 2010.
166 • smithsonian contributions to botany

capacity in conifers to produce large leaves (Bond, 1989), 

the modern tropics appear hostile to most conifer families. 

Remarkably, the Podocarpaceae have evolved multiple 

anatomies that allow many species to elaborate flattened 

shoots or broad leaves which appear to be instrumental to 

the unusual success of the family in the tropics.

Morphological Flattening in Short Shoots

The most obvious adaptation in podocarps to affect 

large, flattened photosynthetic surfaces is the compression 

of short shoots to form two-dimensional photosynthetic 

structures. Some 135 species of extant podocarps from 

11 genera exhibit flattened or composite photosynthetic 

structures (Figure 10.1). Flattening of short shoots is 

achieved by twisting leaves at the base such that they are 

oriented parallel to the shoot axis and arranged in a manner typical of the leaflets on angiosperm compound leaves. 

Flattened shoots are displayed perpendicular to the stem 

axis, thereby maximizing light collection. Many independent origins of shoot flattening are known (Biffin et al., 

this volume), leading to an impressive diversity of shoot 

morphologies in the family. Multiveined “broad leaves” 

are also found in two genera of Podocarpaceae (Nageia

FIGURE 10.1. Some examples of the diversity of shoot flattening in nine genera of Podocarpaceae: (a) Retrophyllum, (b) Dacrycarpus, (c) Falcatifolium, (d) Acmopyle, (e) Podocarpus, (f) Nageia, (g) Prumnopitys, (h) Phyllocladus, and (i) Sundacarpus. Along with obvious planation of 

short shoots (a, b, c, d, g), podocarps have evolved multiveined leaves (f) and phylloclades (h) and internal conducting sclereids (see text). Scale 

bar is 10 cm.
number 95 • 167

and Phyllocladus), the only genera outside the Araucariaceae with this capability. In Phyllocladus whole shoots are 

flattened into one multiveined lamina, and in the tropical 

species P. hypophyllus, flattened phylloclades are arranged 

into large structures that resemble the compound leaves of 

some palms.

The arrangement of leaves in two ranks flattened into 

a plane is not unique to podocarps, with some Northern 

Hemisphere conifer taxa such as Sequoia, Metasequoia, 

and Taxodium also exhibiting bilaterally compressed 

shoots. However, the Northern Hemisphere is overwhelmingly dominated by needle- and imbricate-leaved conifers, 

which constitute 96% of its total number of extant conifer 

species (Welch and Haddow, 1993). Shoots with strong 

bilateral compression are found only in six species in the 

Northern Hemisphere, all from the former Taxodiaceae. 

In marked contrast, about 60% of podocarp species produce distinct bilaterally flattened foliage (Hill and Brodribb, 1999).

Anatomical Adaptation in Leaves

Most conifer species possess scale or needle leaves, 

and the absence of large-leaved conifer species can be 

traced to an apparent inability among extant conifers to 

form a reticulate plumbing network in the leaf lamina 

(Bond, 1989). The hydraulic efficiency conferred by vein 

reticulation is a prerequisite for elaborating large leaves 

because without an efficient means of distributing water 

evenly across the lamina, water deficits created by evaporation from the leaf during photosynthesis would lead 

to cell damage. The evolution of the hydraulic vascular 

system in plants saw nonliving pipes (xylem) create a “superhighway” for water flow through roots, stems, and 

leaves, avoiding cell-to-cell transport limitation. However, 

these pipes terminate within the leaves, at which point 

water must flow into the living mesophyll tissue, where 

it encounters a very high resistance to flow as it moves 

into and between cells. Maximum hydraulic conductance 

would be achieved if veins of xylem branched such that 

they contacted all living cells in the leaf, but no plant 

makes this enormously complex architectural investment. 

Instead, theory suggests that productive leaves must be internally structured such that evaporating cells are in close 

proximity to the vein terminals (Brodribb et al., 2007). 

Through the 400 million years of leaf evolution there have 

been many experiments with the vascular anatomy and 

architecture of leaves (Kenrick and Crane, 1991; Boyce 

and Knoll, 2002), but only two highly convergent patterns emerge as being linked with high productivity: dense 

reticulate venation or needle leaves (Brodribb et al., 2007). 

In conifers, which typically possess a single vein in the leaf, 

narrowing of the distance from the vein to the leaf margin 

enables high hydraulic efficiency and photosynthetic rates 

in needle leaves.

Many members of the Podocarpaceae exhibit a different solution to transporting water through single-veined 

leaves, allowing them to partially overcome the narrowleaf-width limitation that applies to most other conifers. 

In eight genera of Podocarpaceae, hollow sclereids extend 

radially from the midvein out toward the leaf margins 

(Figure 10.2). Cumbersomely labeled accessory transfusion tissue (ATT) (Griffith, 1957), these sclereids have 

been shown to be nonliving water-filled cells analogous 

to xylem cells, even in their pitted end wall connections 

(Figure 10.2). In genera such as Podocarpus and Sundacarpus, accessory transfusion tissue reaches its maximum 

development, forming a layer of water-conducting cells 

between the palisade and spongy mesophyll that connect 

to the midvein through the transfusion tissue. Podocarpus 

species with well-developed ATT are able to attain widths 

in excess of 30 mm (e.g., P. dispermis). In Podocarpaceae 

genera such as Acmopyle, Falcatifolium, and Sundacarpus

the combination of accessory transfusion tissue and shoot 

flattening enables species to produce strongly planated 

shoots that attain a size and shape that falls within the 

range of associated rainforest angiosperm leaves. 

Shoot Flattening and Shade

In consideration of the economic advantages of broad 

leaves it appears likely that shoot flattening in Podocarpaceae is an adaptation that allows species to grow efficiently at low light (Brodribb and Hill, 1997), which may 

give podocarps the ability to compete with broad-leaved 

angiosperms in tropical forests. Strong support for this hypothesis was provided by a study of diverse conifer shoot 

morphologies in the Southern Hemisphere, which revealed 

that shoot flattening was associated with the light saturation characteristics of leaves (Brodribb and Hill, 1997). 

Photosynthesis in species with highly flattened leaves 

became light saturated at low light intensities relative to 

nonflattened shoots, resulting in an inverse correlation between shoot width and saturating light intensity. The low 

light requirement of rainforest podocarp leaves combined 

with the efficient light foraging that comes from shoot 

planation (Leverenz et al., 2000) makes podocarp foliage 

highly competitive in rainforest understory.

The unrivalled (among conifers) success of Podocarpaceae in competition with angiosperms in the tropics 
168 • smithsonian contributions to botany

FIGURE 10.2. Anatomical features of the accessory transfusion tissue (ATT) that conducts water radially from the vein (a) toward the 

margin. Shown in paradermal section (b), these sclereids/tracheids form tubes conducting water away from the midvein (MX). Highly 

connected ATT cells (c) form a layer between the palisade and spongy mesophyll tissue (d). Scale bars are 200 mm (b, d) and 20 mm (c), 

and stomata are indicated by “s.”
number 95 • 169

appears to be strongly linked to anatomical and morphological adaptations in the leaf that confer efficient growth 

in the shade. However, it should be noted that podocarp 

foliar architecture appears to be bound by functional limits that do not apply to the reticulate-veined broad leaves 

of angiosperms. It seems probable that ATT is a less efficient means of conducting water than reticulate venation, 

which may explain why maximum leaf size in podocarps 

never reaches the extremes seen in angiosperms. This is 

perhaps also why podocarps do not tend to be abundant 

in highly productive lowland tropical forests, in which angiosperm leaf size is at its maximum (van Royen, 1979). 

However, in montane forests, the flattened shoots of tropical Podocarpaceae are well inside the range of leaf sizes 

found in coexisting angiosperms (de Laubenfels, 1969). 

Considering the similar vegetative performance of podocarp and angiosperm leaves, it is not surprising that the 

diversity and success of podocarp species in tropical forests falls within the range of a number of moderately successful angiosperm families.

Podocarpaceae with flattened leaves or shoots first 

became successful in the early Cenozoic, demonstrating 

that these species were growing in forests with relatively 

dark understories (Hill and Brodribb, 1999; Brodribb and 

Hill, 2003). One possible explanation for the evolution 

of flattened shoots in podocarp foliage is that angiosperm 

evolution changed light quality in the conifer regeneration 

niche. The effect of this would have been either to force 

conifers into marginal habitats where canopy closure is 

delayed or incomplete or to favor the convergent evolution of broad leaves, as observed in podocarps.

Leaf Adaptation, Shade Tolerance, 

and Transequatorial Migration

Podocarps have been successful in crossing the equator from their Southern Hemisphere origin to colonize 

the low latitudes of the Northern Hemisphere (see Morley, this volume). In contrast, only one species of Pinaceae 

has colonized south of the equator (Pinus merkusii at 2oS, 

Sumatra). Furthermore, Pinaceae have no fossil record in 

the Southern Hemisphere (Millar, 1998). An interesting 

alternative to vicariance as an explanation for the contrasting fortunes of Pinus in the Northern and Southern 

hemispheres is that evergreen tropical forests pose an impenetrable ecological barrier to the southward movement 

of Pinus. In contrast to podocarps, Pinus (and Pinaceae 

in general) have been relatively unadventurous in exploring flattened leaf morphologies, with the probable consequence that virtually all species are shade intolerant and 

unable to regenerate beneath a forest canopy (for a review, see Richardson and Rundel, 1998). This conservative leaf morphology may underlie the inability of Pinus

to penetrate the equatorial zone and into what appears 

suitable habitat (Grotkopp et al., 2002) in the Southern 

Hemisphere.

Pinus krempfii is an exception to the rule of Pinaceae 

exclusion from tropical rainforest. This extraordinary species comes to within a few degrees of the equator and uses 

specialized flattened leaves that confer the ability to regenerate in the shady forest understory. The leaves of Pinus 

krempfii show striking convergence with the flattened 

leaves of rainforest Podocarpaceae. Arrays of elongated 

sclereids in the mesophyll tissue of Pinus krempfii are 

highly reminiscent of those found in most broad-leaved 

podocarp species (Figure 10.3). According to leaf hydraulic measurements, these sclereids appear to be critical for 

facilitating radial water transport from the vein toward 

the leaf margin in broad, single-veined leaves in the same 

way as Podocarpaceae (Brodribb et al., 2007). 

Podocarps and Drought

Considering their impressive ability to compete with 

angiosperms in the tropics, it is surprising the Podocarpaceae have only enjoyed limited success in temperate 

latitudes compared with the Pinaceae and Cupressaceae. I 

argue that the most significant agent preventing podocarp 

success at the higher latitudes of the Southern Hemisphere 

today is drought. A major drying trend in the temperate regions of the Southern Hemisphere through the late 

Tertiary coincides with a period of significant podocarp 

contraction and extinction in Australia and other southern landmasses (Kershaw et al., 1994). Diminishing rainfall, particularly during glacial periods, has resulted in a 

situation today whereby the podocarps from midlatitudes 

are confined to rainforest or wet montane forest and are 

absent from the dry woodlands that compose a large proportion of the forest cover in temperate Australia, Africa, 

and South America. The historical explanation for podocarp drought sensitivity most probably lies in the fact that 

the origins and diversification of the family are associated 

with cool and wet conditions on the continental margins 

of Gondwana (Hill and Brodribb, 1999). However the 

functional explanation seems to be linked to a disproportionately large trade-off in podocarp wood between construction cost and the ability to resist water stress.

Water tension increases in the xylem during soil drying and under extreme stress can become large enough 
170 • smithsonian contributions to botany

that air is drawn into the xylem conduits, cavitating the 

water in the lumen and causing them to cease functioning 

for water transport (Sperry and Tyree, 1990). The vulnerability of the xylem water column to water-stress-induced 

cavitation is an important measure of a plant’s ability to 

survive drought (Tyree et al., 2002; Brodribb and Cochard, 2009). In Southern Hemisphere conifers, xylem 

vulnerability is closely linked to distribution according 

to the rainfall in the driest quarter (Brodribb and Hill, 

1999). Podocarps sampled in this study occupied the wet 

end of the distribution-vulnerability scale (Figure 10.4).

Consequently, drought sensitivity in podocarps has been 

associated with large extinction and range contractions in 

Australia since the establishment of the circumpolar current and the onset of glacial drying cycles (Brodribb and 

Hill, 2003). 

Podocarp wood is not especially sensitive to dysfunction under water stress. Surprisingly, the range of hydraulic tensions associated with a 50% loss of xylem function 

is similar to that of Pinaceae, which appear to be far more 

tolerant of water stress. The unusual thing about podocarp 

wood is its very high density relative to vulnerability. As 

with most plant groups, there is a clear trade-off in members of the Podocarpaceae between wood density and 

xylem vulnerability, with cavitation-resistant wood being 

considerably denser than drought-sensitive wood (Hacke 

et al., 2001). Strangely, the cost of producing cavitationresistant wood is much greater in the Podocarpaceae than 

in either the Pinaceae or Cupressaceae; wood density of 

podocarp species is about 30% higher than Pinaceae and 

Cupressaceae species of equivalent cavitation resistance, 

whereas hydraulic efficiency is substantially lower in the 

podocarps (Pitterman et al., 2006). Therefore, it is probable that the high cost of drought resistance in podocarp 

wood is one of the reasons behind the weak competitiveness of podocarps in dry forest. 

A second factor likely to limit podocarp success in 

drier forest is the very same tissue that makes the family 

so successful in the tropics. The leaf sclereids that allow 

podocarps to produce broad leaves (see above) are highly 

susceptible to collapse under water tension because of 

their unsupported arrangement in the mesophyll (Figure 

FIGURE 10.3. (a–d) Pinus krempfii and (e–h) Podocarpus neriifolius growing in the same tropical understory in Vietnam. Along with producing a similar flattened morphology, the Pinus leaves exhibit convergent anatomy that sees 

sclereids (blue) pass radially from the vein to the margin. Light microscope fluorescence images are paradermal (b, f), 

cross section (c, g), and tangential (d, h).
number 95 • 171

10.5). Despite their thick walls, leaf sclereids were found 

to collapse at moderate water tensions, causing a loss of 

hydraulic and photosynthetic function in the leaf (Brodribb and Holbrook, 2005). One of the most droughtresistant podocarps, Podocarpus drouynianus, has very 

short foliar sclereids and leaves that are almost needles in 

width, supporting the idea that broad leaves and sclereids 

tend to limit the drought performance of the family. Shade 

and drought tolerance are often considered as antagonistic directions for adaptation, and Podocarpaceae appear 

to follow such a pattern (Brodribb and Hill, 2000). Such 

strong physiological canalization seems to be a characteristic of conifers. 

In contrast to podocarps, many Pinaceae are extremely 

drought resistant, producing tough needle leaves with 

high photosynthetic rates (Lusk et al., 2003; Brodribb and 

Feild, 2008). Once again, however, evolutionary canalization has proved highly limiting because the needle leaves 

of most Pinaceae are extremely inefficient in the shade, 

making them uncompetitive in tropical evergreen forests 

(Richardson and Rundel, 1998).

Pinaceae versus Podocarpaceae

Pinaceae-dominated forest covers a significant proportion of the Northern Hemisphere, whereas podocarps 

constitute a tiny proportion of the Southern Hemisphere 

forest cover. The high degree of success of Pinaceae relative to Podocarpaceae in temperate latitudes can be largely 

attributed to the harsh continental climates prevalent in 

major northern landmasses, which produce strong seasonality and regular freezing that benefit Pinaceae. Freezing 

is the “great leveler” between conifers and angiosperms 

because it greatly narrows the hydraulic advantage of 

angiosperm wood (Feild et al., 2002). When ice forms in 

the xylem of trees, the probability that air bubbles will 

form and occlude the xylem upon thawing is related to the 

size of xylem conduits (Sperry and Sullivan, 1992). The 

tiny conduits that make up conifer wood are relatively 

impervious to freeze-thaw embolism, whereas the larger 

vessels of angiosperms are prone to embolism. In much 

of the Northern Hemisphere where Pinaceae dominate, 

major freezing events are common during winter months, 

resulting in the freeze-induced shutdown of angiosperms 

at temperate latitudes for much of the year. Northern 

FIGURE 10.4. The relationship between xylem vulnerability to 

water-stress-induced cavitation and the driest natural range of 

Southern Hemisphere podocarps (open circles) and Cupressaceae 

(solid circles). Podocarps are the most vulnerable of the group, and 

genera at the wet end of the spectrum (within dashed circle) became 

extinct in Australia during Cenozoic drying. Another species appears 

to be at its rainfall limit in Australia, growing only on river edges in 

the wettest parts of Tasmania (Lagarostrobos franklinii, indicated 

by an arrow). Error bars represent standard deviations.

FIGURE 10.5. Tangential sections (cut parallel with the 

midrib) of a Podocarpus grayei leaf, showing accessory 

transfusion tissue cells (blue due to lignin fluorescence) in 

hydrated (-5 bars) and mildly water-stressed (-25 bars) 

leaves. Collapse of the accessory transfusion tissue under 

moderate water tension may limit podocarp success in 

drier climates.
172 • smithsonian contributions to botany

Hemisphere conifers benefit greatly from the sensitivity 

of angiosperms to freezing, and this benefit can be clearly 

seen in terms of an increasing dominance of conifers moving poleward from the Tropic of Cancer. In contrast, the 

moderate seasonality experienced in most parts of the 

Southern Hemisphere means that podocarps do not benefit from the freeze-thaw advantage of its Pinaceae sister 

except at high latitudes and altitudes. As such, podocarps 

have a greatly diminished opportunity for the type of biome domination achieved by Pinaceae at higher latitudes 

in the Northern Hemisphere. 

One question that remains is why Podocarpaceae 

are absent from most of the Northern Hemisphere. Biogeography probably plays a role in driving this pattern, 

given the relatively recent north–south contacts through 

Southeast Asia and Central America (Morley, this volume; Dalling et al., this volume). However, considering 

the demonstrated potential of podocarps for long-distance 

dispersal (fleshy cones and conspicuous presence on many 

recent disjunct islands such as Samoa, Fiji, and Cuba), 

biogeography alone is insufficient to explain the apparent 

inability of podocarps to colonize seasonal northern habitats. Plant functional limitations also provide a possible 

insight into the exclusion of podocarps from the Northern 

Hemisphere. Because of a comparatively warm evolutionary history podocarps appear to have relinquished some of 

the characteristics that confer freeze tolerance. The water 

transport characteristics of both wood and leaves of podocarps appear to be poorly adapted to regular sap freezing. Ice formation has a tendency to desiccate the vascular 

tissue in a similar fashion to drought. Ice has a very low 

water potential and is able to draw water out of xylem tissue, mimicking the effect of dry soil. As discussed above, 

podocarps are ill adapted to respond to desiccation stress, 

and this may contribute to an inefficient response to the 

types of freezing stresses that regularly occur in the Northern Hemisphere. The other freezing handicap for podocarps is the presence of leaf sclereids, which are likely to 

form a nucleation center for ice formation in the leaf. In 

contrast, the Pinaceae appear to have been largely canalized in the opposite direction by diversification in freezing 

climates, which has culminated in the pines that produce 

some of the most freeze-tolerant foliage found in any plant 

group. As such, podocarps are unlikely to be successful 

in competition with Pinaceae in freezing environments in 

the Northern Hemisphere. Further work is required to 

formally quantify the impact of these freezing liabilities 

for podocarps, but the fact that the podocarps are poorly 

represented in all but the wettest Southern Hemisphere 

tree lines suggests that they may not be well suited to the 

extended seasonal freezing that characterizes much of the 

Northern Hemisphere.

Conclusions

The podocarp capacity to successfully compete with 

angiosperms in tropical forests is unusual among conifers. The success of the Podocarpaceae can be traced to 

anatomical and morphological modification of leaves and 

shoots to produce large foliar units that function similarly 

to broad leaves in angiosperms. Large foliar units in podocarps probably originated in the Late Cretaceous and may 

have been a response to angiosperm radiation (Biffin et 

al., this volume). The economic advantages conferred by 

the broad leaves and shoots of podocarps are significant 

in productive tropical forests, but associated limitations 

appear to prevent podocarps from achieving the degree of 

success in either the northern or southern temperate latitudes enjoyed by Pinaceae in the Northern Hemisphere.

REFERENCES

Biffin, E., J. Conran, and A. Lowe. 2011 (this volume). Podocarp Evolution: A Molecular Phylogenetic Perspective. In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 1–20. Smithsonian Contributions to Botany, No. 95. 

Smithsonian Institution Scholarly Press, Washington, D.C.

Bond, W. J. 1989. The Tortoise and the Hare: Ecology of Angiosperm Dominance and Gymnosperm Persistence. Biol. J. Linn. Soc. 36: 227–249.

Boyce, C. K., and A. H. Knoll. 2002. Evolution of Developmental Potential and the Multiple Independent Origins of Leaves in Paleozoic 

Vascular Plants. Paleobiology 28: 70–100.

Brodribb, T. J., and H. Cochard. 2009. Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers. Pl. Physiol.

149: 575–584.

Brodribb, T. J., and T. S. Feild. 2008. Evolutionary Significance of a FlatLeaved Pinus in Vietnamese Rainforest. New Phytol. 178: 201–209.

Brodribb, T. J, T. S. Feild, and G. J. Jordan. 2007. Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics. Pl. Physiol.

144: 1890–1898.

Brodribb, T. J., and R. S. Hill. 1997. The Light Response Characteristics 

of Morphologically Diverse Group of Southern Hemisphere Conifers. Oecologia 110: 10–17.

Brodribb, T. J., and R. S. Hill. 1999. The Importance of Xylem Constraints in the Distribution of Conifer Species. New Phytol. 143: 

365–372.

Brodribb, T. J., and R. S. Hill. 2000. Increases in Water Potential Gradient Reduce Xylem Conductivity in Whole Plants. Evidence from 

a Low-Pressure Conductivity Method. Pl. Physiol. 123: 1021–

1028.

Brodribb, T. J., and R. S. Hill. 2003. The Rise and Fall of the Podocarpaceae in Australia—A Physiological Explanation. In Evolution 

of Plant Physiology, A. Hemsley and I. Poole, eds., pp. 381–399. 

Elsevier Academic Press, London.

Brodribb, T. J., and N. M. Holbrook. 2005. Water Stress Deforms Tracheids Peripheral to the Leaf Vein of a Tropical Conifer. Pl. Physiol.

137: 1139–1146.
number 95 • 173

Dalling, J. W., P. Barkan, P. J. Bellingham, J. R. Healey, and E. V. J. Tanner. 

2011 (this volume). Ecology and Distribution of Neotropical Podocarpaceae. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 43–56. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

de Laubenfels, D. J. 1969. A Revision of the Malesian and Pacific Rainforest Conifers: I. Podocarpaceae. J. Arnold Arbor. 50: 274–360.

Falster, D. S., and M. Westoby. 2003. Leaf Size and Angle Vary Widely 

Across Species: What Consequences for Light Interception? New 

Phytol. 158: 509–525.

Feild, T. S., T. Brodribb, and N. M. Holbrook. 2002. Hardly a Relict: 

Freezing and the Evolution of Vesselless Wood in Winteraceae. Evolution 56: 464–478.

Griffith, M. M. 1957. Foliar Ontogeny of Podocarpus macrophyllus with 

Special Reference to Transfusion Tissue. Amer. J. Bot. 44: 705–715.

Grotkopp, E., M. Rejmánek, and T. Rost. 2002. Toward a Causal Explanation of Plant Invasiveness: Seedling Growth and Life-History 

Strategies of 29 Pine (Pinus) Species. Amer. Naturalist 159: 396–419.

Hacke, U. G., J. S. Sperry, W. T. Pockman, S. D. Davis, and K. A. McCulloch. 2001. Trends in Wood Density and Structure Are Linked 

to the Prevention of Xylem Implosion by Negative Pressure. Oecologia 126: 457–461.

Hill, R. S., and T. J. Brodribb. 1999. Southern Conifers in Time and 

Space. Austral. J. Bot. 47: 639–696.

Kenrick, P., and P. R. Crane. 1991. Water-Conducting Cells in Early Fossil Land Plants: Implications for the Early Evolution of Tracheophytes. Bot. Gaz. 152: 335–356.

Kershaw, A. P., H. A. Martin, and J. R. C. McEwan Mason. 1994. The 

Neogene: A Period of Transition. In History of the Australian Vegetation, R. S. Hill, ed., pp. 299–327. Cambridge University Press, 

Cambridge, UK.

Leverenz, J. W. 1995. Shade Shoot Structure of Conifers and the Photosynthetic Response to Light at Two CO2

 Partial Pressures. Funct. 

Ecol. 9: 413–421.

Leverenz, J. W., D. Whitehead, and G. H. Stewart. 2000. Quantitative 

Analysis of Shade-Shoot Architecture of Conifers Native to New 

Zealand. Trees 15: 42–49.

Lusk, C. H., I. Wright, and P. B. Reich. 2003. Photosynthetic Differences 

Contribute to Competitive Advantage of Evergreen Angiosperm 

Trees over Evergreen Conifers in Productive Habitats. New Phytol. 

160: 329–336.

Millar, C. L. 1998. Early Evolution of Pines. In Ecology and Biogeography of Pinus. D. M. Richardson, ed., pp. 69–91. Cambridge University Press, Cambridge, UK.

Morley, R. J. 2011 (this volume). Dispersal and Paleoecology of Tropical Podocarps. In Ecology of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 21–41. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Pickup, M., M. Westoby, and A. Basden. 2005. Dry Mass Costs of Deploying Leaf Area in Relation to Leaf Size. Funct. Ecol. 19: 88–97.

Pitterman, J., J. S. Sperry, J. K. Wheeler, U. G. Hacke, and E. H. Sikkema. 2006. Mechanical Reinforcement of Tracheids Compromises 

the Hydraulic Efficiency of Conifer Xylem. Pl. Cell Environm. 29: 

1618–1628.

Richardson, D. M., and P. W. Rundel. 1998. Ecology and Biogeography 

of Pinus: An Introduction. In Ecology and Biogeography of Pinus, 

D. M. Richardson, ed., pp. 3–46. Cambridge University Press, 

Cambridge, UK.

Sperry, J. S., and J. E. M. Sullivan. 1992. Xylem Embolism in Response 

to Freeze-Thaw Cycles and Water-Stress in Ring-Porous, DiffusePorous, and Conifer Species. Pl. Physiol. 100: 605–613.

Sperry, J. S., and M. T. Tyree. 1990. Water-Stress-Induced Xylem Embolism in Three Species of Conifers. Pl. Cell Environm. 13: 427–436.

Tyree, M. T., G. Vargas, B. M. J. Engelbrecht, and T. A. Kursar. 2002. 

Drought until Death Do Us Part: A Case Study of the DesiccationTolerance of a Tropical Moist Forest Seedling-Tree, Licania platypus (Hemsl.) Fritsch. J. Exp. Bot. 53: 2239–2247.

van Royen, P. 1979. The Alpine Flora of New Guinea. Cramer-Verlag, 

Lehre, Germany.

Webb, L. J. 1968. Environmental Relationships of the Structural Types of 

Australian Rain Forest Vegetation. Ecology 49: 296–311.

Welch, H., and G. Haddow. 1993. The World Checklist of Conifers. 

Landsman’s Bookshop, Herefordshire, UK.

11 Podocarp Roots, 

Mycorrhizas, and Nodules

Ian A. Dickie and Robert J. Holdaway

ABSTRACT. Podocarps are often found on low-nutrient soils and further exacerbate 

nutrient limitation through the production of recalcitrant litter. Understanding podocarp ecology therefore depends on understanding the root adaptations of podocarps to 

obtain nutrients. The roots of podocarps are heterorhizic (having two root forms) with 

abundant spherical determinate short roots, a unique form of largely unknown function, 

as well as indeterminate fine roots. There is no strong evidence for nitrogen fixation in 

the nodules. Although nodules are frequently and abundantly colonized by arbuscular 

mycorrhizal fungi, they are neither required for mycorrhizal infection nor dependent on 

mycorrhizal infection for their development. The fungal symbiont community associated 

with podocarps does not appear to be distinctive from that of other plants at a global 

scale, although it may differ from co-occurring plants within a site. Perhaps the most 

obvious, yet largely overlooked, hypothesis is that the form of the nodules is the function. The presence of nodules permits a doubling of root cortex volume, while simple 

geometry indicates that a spherical form involves the lowest possible cost in producing 

cell wall and membrane material per unit of root volume. Increased root volume permits 

greater arbuscular mycorrhizal interaction, and hence, nodules may be analogous to the 

determinate ectomycorrhizal roots of the Pinaceae as a structure to maximize fungal 

interactions at minimal root construction cost.

Introduction

Podocarps (gymnosperms in the Podocarpaceae) grow on a range of soils 

from relatively fertile (e.g., C:N and C:P ratios of 12.6 and 394; Solomon et al., 

2002) to infertile soils with most mineral nutrients locked into organic forms 

(e.g., C:N ratios = ~40, C:P ratios > 1,000; Armesto et al., 1995; Coomes et al., 

2005). Nonetheless, it is the ability of podocarps to grow and compete on infertile 

sites that explains their occurrence in lowland tropical habitats (e.g., Kitayama 

et al., this volume) and their dominance on older, relatively phosphorus-limited 

temperate sites (Richardson et al., 2004; Coomes et al., 2005; Coomes and Bellingham, this volume). On higher-phosphorus soils, podocarps are more likely 

Ian A. Dickie, Landcare Research, Box 40, Lincoln 7640, New Zealand. Robert J. Holdaway,

Forest Ecology and Conservation Group, Department of Plant Sciences, University of Cambridge, 

Downing Street, Cambridge CB3 2EA, UK; presently at Landcare Research, Box 40, Lincoln 

7640, New Zealand. Correspondence: I. Dickie, 

dickiei@landcareresearch.co.nz.

Manuscript received 13 April 2010; accepted 

9 July 2010.
176 • smithsonian contributions to botany

to be outcompeted by ferns and angiosperms (Coomes et 

al., 2005; Carswell et al., 2007) and may show negative 

growth and survival responses to phosphorus or mixedfertilizer addition (Carswell et al., 2003; Pareliussen et al., 

2006). Where present, podocarps can exacerbate mineral 

nutrient limitation through the production of relatively 

low quality, high-carbon leaf litter, which can lock mineral nutrients into unavailable forms (Wardle et al., 2008). 

This litter decomposes so slowly that it can remain obvious more than 40 years after the death of a podocarp tree 

(Wardle et al., 2008). Understanding podocarp ecology 

therefore requires an understanding of the mineral nutrient uptake strategies that allow the persistence of podocarps on low nutrient soils.

In this chapter we examine the root adaptations of 

podocarps that permit efficient mineral nutrient acquisition from low-nutrient soils, both in terms of maximizing 

nutrient uptake and minimizing costs. We focus on two 

key questions: (1) Are there unique aspects of the mycorrhizal associations of podocarps that permit them greater 

mineral nutrient access on low-nutrient soils? (2) What, if 

any, is the functional role of nodules in podocarp mineral 

nutrient uptake?

Mycorrhizal associations 

of podocarps

Podocarps are arbuscular mycorrhizal, forming symbiotic associations between plant roots and fungi in the 

Glomeromycota. In these symbioses the plant provides 

carbon to the fungus, and the fungus greatly increases 

plant acquisition of phosphorus (Smith and Read, 2008). 

The presence of arbuscular mycorrhizas is typical of more 

than 50% of gymnosperm species, with the remainder, 

comprising the Pinaceae and Gnetaceae, primarily forming ectomycorrhizas (Brundrett, 2009). This potentially 

reflects a close phylogenetic relationship between these 

two families (Hajibabaei et al., 2006; Wu et al., 2007), 

although Brundrett (2009) argues for separate evolution 

of ectomycorrhizas in these groups. Although there are 

sporadic reports of ectomycorrhiza in other gymnosperms 

(e.g., Cupressaceae, Wollemia), these appear to reflect misdiagnosis or atypical definitions of ectomycorrhizas (Brundrett, 2009). Arbuscular mycorrhizas are also typical of 

74% of angiosperms, including many of the plant species 

frequently associated with podocarps (Brundrett, 2009).

Arbuscular mycorrhizal infection of podocarp roots 

is generally extremely dense. In New Zealand temperate podocarps, there are reported infection levels of 

88%–96% of root length (Hurst et al., 2002); our own 

observations indicate that nearly 100% of available root 

length (fine roots capable of forming arbuscular mycorrhizas) is infected across a number of temperate podocarp 

species (I. A. Dickie, unpublished data). These levels of arbuscular mycorrhizal infection are higher than many other 

plants and significantly higher than some, but not all, cooccurring angiosperms.

Arbuscular mycorrhizas benefit plants by increasing 

the effectiveness (extent of soil exploration) and efficiency 

(benefit:cost ratio) of phosphorus uptake (Koide et al., 

1999). Phosphorus is relatively immobile in soil, so the 

extensive hyphae of arbuscular mycorrhizal fungi provide 

a greatly increased ability to explore the soil volume. The 

relative dependence of plants on mycorrhizal infection is 

generally strongly correlated with plant root traits (Baylis, 1975; St John, 1980). Species with high specific root 

length (length/mass) and abundant and long root hairs are 

expected to have relatively lower dependence on mycorrhizal fungi than species with thick, higher-cost roots and 

fewer root hairs. 

There have been few studies of podocarp root morphology, but our own observations suggest a moderately 

coarse root system (mean diameters ~0.60 mm; specific 

root length 711 ± 85 cm g-1

, mean ± standard error), 

with abundant root hairs in some species (Figure 11.1). 

Observed root diameters are consistent with the concept 

of podocarps having a high mycorrhizal dependency (St 

John, 1980); however, the production of abundant root 

hairs in some podocarps is not. The presence of abundant 

and long root hairs and mycorrhizas may indicate they 

have different functions in mineral nutrient uptake or that 

they have complementary functions under conditions of 

poor mineral availability.

Identity of the Fungal Symbionts of Podocarps

Like all arbuscular-mycorrhizal symbiosis, the fungi 

that form arbuscular mycorrhizas with podocarps are in 

the Glomeromycota (Schüßler et al., 2001). The fungi 

appear typical of arbuscular mycorrhizal communities 

in general, with a dominance of Glomus species and less 

common Archaeospora and Diversisporaceae (Russell et 

al., 2002; Wubet et al., 2006). Two studies might be taken 

to suggest a degree of host specificity to podocarps. Wubet et al. (2006) found distinct fungal species associated 

with co-occurring Juniperus procera (Cupressaceae) and 

Afrocarpus falcatus (Podocarpaceae). Further, in a study 

of four species of podocarps, Russell et al. (2002) found 

little similarity between sequences of Glomeromycota 
number 95 • 177

from podocarp roots and existing sequences in GenBank 

(http://www.ncbi.nlm.nih.gov). Nonetheless, at least the 

results from Russell et al. (2002) may reflect the paucity 

of Southern Hemisphere Glomeromycota sequences (particularly in 2002), rather than true host specificity. Using 

the ribosomal (18s, internal transcribed spacer [ITS]) sequence data from Russell and colleagues (GenBank Accession numbers AF452624–AF452636), we reexamined 

these sequences against GenBank to assess affinities with 

more recent collections (Table 11.1). Twelve of the 13 sequences matched at 95% or greater maximum identity to 

other sequences in GenBank, of which three matched only 

sequences from New Zealand, five had nearest matches 

to sequences from elsewhere in the Southern Hemisphere, 

and four had nearest matches to sequences from the 

Northern Hemisphere. There was no evidence of any specificity of these fungi to podocarps—the nearest matches 

included liverworts, grasses, and a range of angiosperms, 

with no matches to other podocarps. Therefore, the arbuscular mycorrhizal fungi colonizing podocarps may 

be distinct from other host plants within a site (Wubet et 

al., 2006), but on a broader scale the fungi associating 

with podocarps do not appear to be particularly distinctive. Apparent host specificity within sites may reflect the 

strong effects of individual podocarp trees on soil chemical and biotic properties (Wardle et al., 2008) influencing 

local fungal community composition.

Root nodules of podocarps

The roots of the podocarps are characterized by abundant spherical protuberances, often referred to as “nodules” (Figure 11.2). Thus, podocarps are heterorhizic, 

having two distinct root forms: long indeterminate roots 

and determinate nodules. Initial nodule formation typically 

occurs as regularly spaced spheres developing in multiple 

rows along the length of fine roots, with substantial variation among plants in the regularity of nodule formation. 

Nodules arise from the root pericycle, similar to lateral 

root development (Russell et al., 2002), and are characterized by the absence of any apparent meristematic tissue or 

root cap (Khan and Valder, 1972). As nodules age, epidermal cell walls become thicker, and the color of the nodules 

becomes increasingly dark (Russell et al., 2002). Russell 

et al. (2002) noted that starch reserves were high in nodule cortical cells prior to arbuscular mycorrhizal colonization and were depleted in heavily colonized cells. In some 

cases, older nodules are shed and can become abundant 

in soil. After shedding old nodules, nodule formation may 

be reinitiated at the same location. In an interesting variation, it is also possible for apical growth to resume, potentially contributing to the formation of chains of nodules 

(discussed below). The unique form of podocarp nodules 

has led to a number of hypotheses about their functional 

FIGURE 11.1. Abundant root hairs on podocarps occur both (A) on 

long roots, as seen on Prumnopitys ferruginea, and (B) sometimes 

on nodules, as seen on Phyllocladus alpinus. Images by the authors.
178 • smithsonian contributions to botany

significance. Despite nearly 100 years of research on this 

subject, a clear explanation has yet to emerge.

Plant Phylogeny and Occurrence of Nodules

Within the gymnosperms, nodulated roots are present 

in the Podocarpaceae, Phyllocladaceae, and Araucariaceae, 

which form a single phylogenetic group, and Sciadopitys 

(Khan and Valder, 1972), which Stevens (2001–2009) suggested is a distinct but closely related clade (Figure 11.3). 

Nodules in the Araucariaceae and Sciadopitys were reported as less regular and more elongated and variable in 

size than nodules in podocarps (Khan and Valder, 1972), 

but we have observed regular, spherical nodules in Agathis 

australis (Araucariaceae; personal observation). Nodules 

are absent from the Cupressaceae and Taxaceae. 

Outside of the gymnosperms, mycorrhizal nodules 

have been reported in a number of angiosperms, including Gymnostoma (Casuarinaceae; Duhoux et al., 2001), 

Aesculus (Sapindaceae; Khan, 1972), and several Caesalpinaceae (Béreau and Garbaye, 1994). It is not clear that 

these other nodules are physiologically or genetically related to podocarp nodules. Khan and Valder (1972) outlined two traits as defining true podocarp-type nodules: 

(1) development as a normal feature of roots, not being 

dependent on any microorganism for their development 

(Baylis, 1969), and (2) being fully differentiated structures 

with no root cap or apical meristem and with an endodermis surrounding and overarching the vascular strand.

The second of these defining traits must be taken as 

temporally dynamic, as both the initial growth and, particularly, the reinitiation of apical growth in some nodules implies an apical meristem. Nonetheless, none of the 

nonpodocarp nodulated roots have been shown to fit these 

criteria. In Gymnostoma, nodules do not form as a normal 

feature of the root, as the presence of soil microorganisms 

is required to induce nodule formation. Additionally, nodules in Gymnostoma have an apical meristem, and no evidence of an endodermis overarching the vascular strand 

was reported (Duhoux et al., 2001). The nature of nodule 

formation in Aesculus remains unclear, because the one 

attempt to synthesize nodules in the absence of soil microbes failed to maintain soil sterility over the course of 

the experiment (Khan, 1972). 

There are occasional reports of nodules in other 

groups; however, these appear to be based on confusion 

between beaded roots and true podocarp-type nodules 

(Khan and Valder, 1972). Beaded roots are a commonly 

TABLE 11.1. Re-BLAST (basic local alignment search tool) searching of sequences from Russell et al. (2002) against GenBank, showing 

best match (if greater than 95% similarity) to arbuscular mycorrhizal associates of known host plants or plant communities. There is 

no evidence of host specificity to podocarps; N/A indicates not applicable.

Sequence Host plant

from Russell Sequence Best match taxonomic Collection

et al. (2002) name (>95%) Identities Host plant group location

AF452624 PODO17.1 EU417643.1 509/519 (98%) Sciaphila ledermannii Triuridaceae Cameroon

AF452625 PODO17.2 AF452625.1 305/305 (100%) Juglans neotropica Juglandaceae Ecuador

AF452626 PODO17.3 AJ716326.1 878/886 (99%) Marchantia foliacea Marchantiales New Zealand

AF452627 PODO16.1 AJ699064.1 552/557 (99%) Marchantia foliacea Marchantiales New Zealand

AF452628 PODO16.2 AJ699068.1 1,010/1,046 (96%) Marchantia foliacea Marchantiales New Zealand

AF452629 PODO1.1 DQ336488 173/181 (95%) Guarea pterorhachis Meliaceae Ecuador

AF452630 PODO1.2 EU152178 508/510 (99%) Tabebuia chrysantha Bignoniaceae Ecuador

AF452631 PODO1.3 AM384971 373/384 (97%) Thymus pulegioides Lamiaceae Switzerland

AF452632 PODO7.1 AM268195 549/564 (97%) Grassland Various Finland

AF452633 PODO7.2 FJ483156 520/529 (98%) Freshwater marsh Various United States

AF452634 PODO7.3 AM420382 566/580 (97%) Aquatic macrophyte Unclear Norway

AF452635 PODO18.1 EU159171 499/499 (100%) Neotropical rainforest Various Ecuador

AF452636 PODO18.2 None Best match only 94% N/A N/A N/A
number 95 • 179

observed root form in many tree species, where roots 

are regularly segmented by narrow constricted regions. 

Although beaded roots have occasionally been reported 

as being either ectomycorrhizal (Mineo and Majumdar, 

1996) or arbuscular mycorrhizal structures (Grand, 1969), 

it appears that beaded roots are not directly related to mycorrhizas or other soil organisms (Kessler, 1966; Beslow 

et al., 1970; Thomson et al., 1990). The development of 

beaded roots may reflect episodic growth linked to fluctuating soil moisture (Kessler, 1966), although this result 

FIGURE 11.2. Examples of variation in form among nodules and roots: (A) very small nodules on Lepidothamnus intermedius, (B) formation 

of nodules (three stages of development) of regularly spaced uniform nodules in Dacrydium cupressinum, (C) beaded roots (not nodule) in Dacrydium cupressinum (note the stele passing through beads and to the end of root with no overarching cortical cells), and (D) chained or beaded 

nodules in Manoao colensoi. A range of species are shown, but significant variation can also be found within species. Images by the authors.
180 • smithsonian contributions to botany

is not consistent across studies (e.g., Beslow et al., 1970). 

Nonetheless, beaded roots retain meristematic tissue and 

have no overarching cortex and are, therefore, distinct 

from true podocarp-type nodules. Some podocarps form 

beaded roots in addition to nodules (Figure 11.2c), and 

some podocarp nodules develop apically on previously 

formed nodules, creating a beaded-nodule chain (Figure 

11.2d). Perhaps it is not surprising that this has led to considerable confusion.

Nitrogen Fixation and Podocarp Nodules

There have been a number of studies that claim to 

show low levels of nitrogen fixation in podocarp nodules 

(e.g., Morrison and English, 1967; Grobbelaar et al., 

1971) and others that fail to find any nitrogen fixation 

(Baylis, 1969). Morrison and English (1967) reported the 

presence of an endophyte resembling an actinomycete but 

give no further details. There was also a recent report of 

the isolation of Rhizobium (along with detection of weak 

nitrogenase activity) from Podocarpus macrophyllus roots 

with nodules (Huang et al., 2007). Nonetheless, on the 

whole, the evidence for nitrogen fixation in nodules is 

weak. The levels of nitrogen fixation reported in podocarp nodules are typically described as very low. Where 

low levels of nitrogen fixation have been reported, they 

may reflect nitrogen fixation by free-living rhizobium in 

soils or associated with roots, rather than a true symbiosis. 

FIGURE 11.3. Phylogeny of the Pinales with mycorrhizal status and notes on root nodule morphology. Phylogeny follows Stevens (2008), who 

attempted to reflect current consensus. The podocarps share arbuscular mycorrhizas with the Cupressaceae and Taxaceae, but the presence of 

heterorhizic roots (i.e., short determinate roots distinct from long roots) shows similarity to the Pinaceae. Note that arbuscular mycorrhizas are 

also present in the Pinaceae, but ectomycorrhizas dominate (Horton et al., 1998).

Abies 

Pinus, etc.

Araucariaceae 

Phyllocladaceae

Podocarpaceae 

Sciadopityaceae

Cupressaceae 

Taxaceae 

Pinaceae 

Mycorrhiza 

Ectomycorrhiza 

Arbuscular mycorrhiza

Heterorhizic: nodulated roots

Root morphology 

Heterorhizic: ectomycorrhizal roots 

typically short, dichotomously or 

otherwise branched 

Non-heterorhizic roots 
number 95 • 181

This was effectively demonstrated by Silvester and Bennett 

(1973), who showed that acetylene reduction (a proxy for 

nitrogen fixation) was uniformly associated with the soil 

or surface of roots and nodules of five species of nodulated gymnosperm, with no evidence of acetylene reduction in root nodules following a relatively mild surface 

sterilization. 

The interest in nitrogen fixation in podocarp nodules 

appears to largely be driven by a superficial resemblance 

to rhizobial nodules, leading Khan and Valder (1972:40) 

to state “It is unfortunate that the word ‘nodule’ should 

have been applied at all...Had they been given a different name to begin with, it is doubtful whether confusion 

would ever have arisen in the literature concerning their 

function and mode of origin.” Confusion between mycorrhizas and nitrogen fixation is by no means restricted to 

podocarps; some of the history and causes of this confusion are reviewed by Mikola (1986).

Although there is no good evidence of symbiotic nitrogen fixation in podocarp nodules, the potential importance of asymbiotic free-living or root-associated nitrogen 

fixation should be an area for further investigation. Asymbiotic nitrogen fixation can supply significant amounts of 

nitrogen in Agathis australis forests (Silvester, 2000) and 

in other forest systems (Reed et al., 2008) and may play 

a similar role in podocarp forests (Silvester and Bennett, 

1973). Alternatively, a lack of available phosphorus under 

podocarps, partially driven by low litter quality, may limit 

the extent of asymbiotic fixation (Reed et al., 2008).

Arbuscular Mycorrhizal Infection of Nodules

The roots and nodules of podocarps are abundantly 

colonized by arbuscular mycorrhizal fungal hyphae (Figure 11.4). Nonetheless, Breuninger et al. (2000) note that 

the extensive arbuscular mycorrhizal structures in normal 

fine roots of Araucaria suggest that nodules may not play 

a major role in mycorrhizal associations. Our own observations support this, with extensive infection of long root 

cortical cells common in podocarps. Further, nodules do 

not require mycorrhizal fungi for their formation (Baylis, 1969). The presence of arbuscular mycorrhizal fungi 

is therefore neither a prerequisite for, nor dependent on, 

nodule formation. 

There is some confusion around the question of 

whether extraradical mycorrhizal hyphae are associated 

with nodules. The extraradical hyphae are the portion of 

the arbuscular mycorrhizal fungal mycelium where active 

nutrient uptake from the soil solution occurs; hence, a lack 

of extraradical hyphae would imply an atypical, perhaps 

parasitic, mycorrhizal association. The outermost layers 

of podocarp nodules were reported as “mainly free of hyphae” by Russell et al. (2002), but McGee et al. (1999) 

showed sparse hyphae in epidermal cells. Epidermal cells 

in podocarp nodules have notable thickening of cell walls 

on mature nodules, which may lend support to the idea of 

limited fungal penetration through the epidermis. Nonetheless, the occurrence of dense fungal colonization in 

the cortex with only sparse colonization of outer layers 

is actually quite typical for all plant species: arbuscular 

mycorrhizal fungi penetrate a small number of epidermal 

cells, pass through the “exodermis” layer just below the 

epidermis (if present), and then proliferate in the cortex. 

Extensive arbuscular mycorrhizal hyphae on the surface 

of nodules of Araucaria were shown by Breuninger et al. 

(2000). In our own observations of Podocarpus, Dacrydium, and Prumnopytis we have observed frequent hyphae on the surface of nodules, what appear to be typical 

appresoria (cell penetration arises from appresoria), and 

hyphae that penetrate the surface of nodules. We therefore conclude that there is an extraradical mycelium with 

apparently typical attachment to the internal infection of 

root nodules by arbuscular mycorrhizal fungi and that 

prior reports of the absence of extraradical hyphae are 

incorrect.

Whether the arbuscular mycorrhizal fungi infecting 

nodules are distinct species from those infecting other 

roots on the same plant remains unknown. As observed 

by Russell et al. (2002), the determinate growth form of 

nodules places a constraint on fungal colony growth compared to long roots, as hyphal spread along a growing root 

is not possible. Russell et al. (2002) did observe, however, 

that fungal hyphae from the disintegrating cortex of old 

nodules were able to infect newly forming nodules.

Replacement of Nodules

Root nodules, similar to fine roots in other species, 

have a limited life span (Eissenstat and Yanai, 1997). 

Nodules may be shed by the plant, with regrowth of new 

nodules at the same location. In other cases, nodules are 

formed in strings of connected nodules, which may reflect 

apical regrowth. The replacement of nodules is unlikely to 

be driven by declines in local soil fertility as there is little 

to be gained by replacement in the same location. Instead, 

there may be physiological changes in the nodules that 

render them increasingly inefficient with age. At least three 

hypothetical mechanisms may be involved. First, arbuscules, the site of nutrient transfer, are short-lived structures 

in most plants. In podocarps, collapsed fungal arbuscules 
182 • smithsonian contributions to botany
number 95 • 183

FIGURE 11.4. Internal structure of nodules from (A, facing page) Podocarpus totara and (B, above) Dacrydium cupressinum showing arbuscular mycorrhizal fungal tissue inside plant root cortical cells, with abundant arbusculate fungal coils (darker blue, fine structures within plant 

cells) and probable vesicles (ovoid structure in B) and spore (round structure in A). Microscopy was courtesy of Larry Peterson and Lewis 

Melville from material collected by the authors. Roots were stored in 2.5% glutaraldehyde in PO4

 buffer, pH 6.8, dehydrated in a graded series 

of ethanol to 100%, embedded in LR White resin (London Resin Company), sectioned (approximately 1–1.5 μm thickness) with glass knives, 

heat fixed to glass slides, stained with 0.05% toluidine blue O in 1.0% sodium borate, rinsed with water, air dried, and mounted in immersion 

oil under a cover glass.
184 • smithsonian contributions to botany

have been described as abundant in some nodule root cells 

(Russell et al., 2002). Although fungi may, in other plants, 

reinfect a previously infected cell with collapsed arbuscules, this is generally rare (Smith and Read, 2008). By 

either shedding or apically expanding nodules, podocarps 

may reestablish the symbiosis, without requiring growth 

of extensive roots. Second, nodule starch reserves rapidly 

decline during arbuscular mycorrhizal fungal infection 

(Russell et al., 2002). The reformation of nodules may be 

necessary to replenish these reserves. Finally, the thickening of epidermal cell walls in mature nodules is likely to 

prevent infection by new fungal hyphae (combined with a 

decline in established infection). If there were any nonsymbiotic mineral nutrient uptake by nodules, this would also 

be restricted by epidermal wall thickening. Further work is 

needed to better understand the role of nodule senescence 

in podocarp mineral nutrient uptake efficiency.

Functional Significance of Nodules

The extensive mycorrhizal structures found in podocarp nodules suggest a link between these nodules and 

arbuscular mycorrhiza, but given that the formation of 

nodules is neither necessary for mycorrhizal infection 

nor dependent on mycorrhizal infection to occur, this 

link must be indirect. Perhaps the simplest hypothesis is 

that nodules simply permit a plant to increase its extent 

of arbuscular mycorrhizal infection while minimizing the 

cost that would be associated with developing an extensive root system (McGee et al., 1999). This hypothesis is 

supported by the very high levels of mycorrhizal infection 

often observed in podocarp roots and the frequent occurrence of podocarps on infertile soils, where extensive mycorrhizal development is likely to be beneficial. 

Using Prumnopitys ferruginea as a model root system, 

we calculated the root surface area and volume associated 

with long roots, root hairs, and root nodules. On the basis 

of 30 segments of root examined, root diameters averaged 

0.72 mm (±0.03 standard error); there were 88 (±16) root 

hairs per mm of root, with an average length of 0.78 mm 

(±0.02) and a root hair diameter of 0.02 mm. Average volume per nodule was 0.60 mm3

 (±0.03), and there was an 

average of 0.77 (±0.06) nodules per mm of root. On the 

basis of these measurements, the presence of root nodules 

permits the plant to increase total root volume by around 

126% (±15%). Similar results were found for Dacrydium 

cupressinum (except that root hairs were absent), where 

the presence of root nodules permits the plant to increase 

total root volume by around 96% (±10%).

Thus, by forming nodules podocarps effectively double their root volume, permitting a much greater extent of 

arbuscular mycorrhizal infection than would be possible 

without nodules. The form of nodules is ideally suited for 

this purpose—a sphere creates the greatest possible increase in cortex volume at the lowest possible investment 

in vascular or epidermal tissue.

The economic analogy may be furthered by the observation that some podocarps shed their nodules while 

retaining long roots. If shedding nodules is physiologically 

necessary to maintaining mycorrhizal symbioses, then 

plants may minimize costs by forming very short roots 

with maximal volume. Where root hairs form on the nodule epidermis, the reformation of nodules with young epidermal cells may also permit plants to reestablish root hair 

growth (Figure 11.1b).

Further understanding of the mineral nutrient economy of podocarp nodules might benefit from comparison 

with the determinate, branching roots typical of ectomycorrhizal plants. The majority of ectomycorrhizal plants 

have heterorhizic roots, responding to fungal infection 

by branching or bifurcation of short, generally determinate roots. Although the function of this branching has 

not been widely evaluated, it seems logical to assume that 

localized root branching permits a greater volume of interaction between the plant and fungal symbionts and 

may be analogous to the development of nodules infected 

by arbuscular mycorrhizal fungi in podocarps. It would 

be particularly interesting to examine the formation of 

Y-shaped bifurcated ectomycorrhizal short roots in the 

Pinaceae (Preston, 1943) to determine whether this process is under the same genetic and physiological controls 

in the Pinaceae as nodule formation in podocarps. A part 

of this analysis should question why nodules and bifurcated roots are well developed in gymnosperms but not in 

angiosperms and whether this reflects other constraints on 

root morphology, including physiological limits on minimum root diameters in gymnosperms.

Other nutrient acquisition

strategies in podocarps

The most unusual nutrient acquisition strategy within 

the podocarps occurs in Parasitaxus usta (Feild and Brodribb, 2005). Endemic to New Caledonia, Parasitaxus is 

parasitic on Falcatifolium taxoides (also Podocarpaceae) 

and is apparently the only parasitic gymnosperm. Water 

relations of Parasitaxus are similar to parasitic woody 

plants (e.g., mistletoe), but significantly enriched carbon13 relative to plant host and the presence of abundant 

fungal hyphae suggest that photosynthate parasitism involves a fungal partner (Feild and Brodribb, 2005). Thus, 
number 95 • 185

Parasitaxus may be simultaneously a direct and an indirect parasite for different resources.

Synthesis and conclusions

The importance of leaf form in the success of podocarps on infertile soils has long been recognized, yet the 

importance of root form (particularly nodules) has remained enigmatic. On the basis of the best available evidence we suggest that podocarps do not differ in root 

function from other plants, at least not in any fundamental 

way. Evidence for nitrogen fixation or novel fungal associations is weak at best. Instead of invoking some unique 

function of podocarp roots, we suggest that the unique 

form of podocarp roots is itself key to understanding their 

mineral nutrient uptake strategies. Nodules on podocarp 

roots greatly increase root volume available for symbiotic 

interaction with mycorrhizal fungi at minimal cost and 

therefore maximize mineral nutrient acquisition efficiency. 

This may be further augmented by the ability of some 

podocarps to shed and re-form nodules, reestablishing the 

mycorrhizal symbiosis at minimal root construction cost. 

Nonetheless, this view must be taken as a hypothesis to 

be tested.

Despite their root and leaf adaptations, podocarps 

may not be the best adapted species for the environments in 

which they occur. Low-nutrient soils, especially those with 

an accumulation of organic matter, often favor ectomycorrhizal trees (Lambers et al., 2008). Although the arbuscular mycorrhizal associations of podocarps are efficient in 

the uptake of inorganic phosphate, ectomycorrhizal fungi 

have much greater capabilities for organic nutrient capture 

(Lambers et al., 2008). Where present, ectomycorrhizal 

trees may therefore gradually displace podocarps and other 

arbuscular mycorrhizal vegetation (Taylor et al., 2009). 

This process may be contributing to the gradual displacement of podocarp forests by ectomycorrhizal Nothofagus

in New Zealand (McGlone et al., 1996) and ectomycorrhizal Quercus in alpine South America (Van’t Veer and 

Hooghiemstra, 2000). Podocarps have a significant advantage over ectomycorrhizal vegetation, however, as they 

share arbuscular mycorrhizal fungi with many other plant 

species, whereas the spread of ectomycorrhizal trees may 

be slowed by a lack of compatible mycorrhizal symbionts 

(Baylis, 1980; Dickie and Reich, 2005).

Progress on understanding the mineral nutrient acquisition of podocarps has been slow, partially because of 

an apparent fixation (pun intended) on nodules and the 

possibility of nitrogen fixation. We suggest that further research would be aided by (1) an economic perspective on 

carbon costs and mineral nutrient efficiency of root and 

nodule formation in the podocarps, including any physiological constraints limiting alternative strategies such as 

increased specific root length, (2) an investigation into the 

genetic basis for nodule formation, testing whether this 

trait is homologous with ectomycorrhizal short roots in 

the Pinaceae, and (3) understanding the co-occurrence and 

replacement of podocarps by ectomycorrhizal trees and 

the implications of this for ecosystem processes.

Acknowledgments

We thank D. Forsyth (Arthur Rylah Institute for Environmental Research, Australia), R. Allen and V. Meyers 

(Landcare Research, New Zealand), and L. Peterson and 

L. Melville (University of Guelph, Canada) for assistance 

with surveying podocarp roots and imaging and P. Bellingham and S. Richardson (Landcare Research, New Zealand) 

for helpful discussion. Funds were provided to IAD by the 

Foundation for Research Science and Technology under 

the Ecosystem Resilience Outcome Based Investment. 

REFERENCES

Armesto, J. J., C. Villagrán, J. C. Aravena, C. Pérez, C. Smith-Ramirez, 

M. Cortés, and L. Hedin. 1995. Conifer Forests of the Chilean 

Coastal Range. In Ecology of the Southern Conifers, N. J. Enright 

and R. S. Hill, eds., pp. 156–170. Melbourne University Press, Carlton, Australia. 

Baylis, G. T. S. 1969. Mycorrhizal Nodules and Growth of Podocarpus

in Nitrogen-Poor Soil. Nature 223: 1385–1386.

Baylis, G. T. S. 1975. The Magnolioid Mycorrhiza and Mycotrophy in 

Root Systems Derived from It. In Endomycorrhizas, F. E. Sanders, 

B. Mosse, and P. B. Tinker, eds., pp. 373–389. Academic Press, New 

York.

Baylis, G. T. S. 1980. Mycorrhizas and the Spread of Beech. New Zealand J. Ecol. 3: 151–153.

Béreau, M., and J. Garbaye. 1994. First Observations on the Root Morphology and Symbioses of 21 Major Tree Species in the Primary 

Tropical Rain Forest of French Guyana. Ann. Forest Sci. 51: 407–416.

Beslow, D. T., E. Hacskaylo, and J. H. Melhuish. 1970. Effects of Environment on Beaded Root Development in Red Maple. Bull. Torrey 

Bot. Club 97: 248–252.

Breuninger, M., W. Einig, E. Magel, E. Cardoso, and R. Hampp. 2000. 

Mycorrhiza of Brazil Pine (Araucaria angustifolia [Bert. O. Ktze.]). 

Pl. Biol. 2: 4–10.

Brundrett, M. C. 2009. Mycorrhizal Associations and Other Means of 

Nutrition of Vascular Plants: Understanding the Global Diversity of 

Host Plants by Resolving Conflicting Information and Developing 

Reliable Means of Diagnosis. Pl. Soil 320: 37–77.

Carswell, F. E., P. Millard, G. N. D. Rogers, and D. Whitehead. 2003. Influence of Nitrogen and Phosphorus Supply on Foliage Growth and 

Internal Recycling of Nitrogen in Conifer Seedlings (Prumnopitys 

ferruginea). Funct. Pl. Biol. 30: 49–55.

Carswell, F. E., S. J. Richardson, J. E. Doherty, R. B. Allen, and S. K. 

Wiser. 2007. Where Do Conifers Regenerate after Selective Harvest? A Case Study from a New Zealand Conifer-Angiosperm Forest. Forest Ecol. Managem. 253: 138–147.
186 • smithsonian contributions to botany

Coomes, D. A., R. B. Allen, W. A. Bentley, L. E. Burrows, C. D. Canham, L. Fagan, D. M. Forsyth, A. Gaxiola-Alcantar, R. L. Parfitt, 

W. A. Ruscoe, D. A. Wardle, D. J. Wilson, and E. F. Wright. 2005. 

The Hare, the Tortoise and the Crocodile: The Ecology of Angiosperm Dominance, Conifer Persistence and Fern Filtering. J. Ecol. 

93: 918–935.

Coomes, D. A., and P. J. Bellingham. 2011 (this volume). Temperate and 

Tropical Podocarps: How Ecologically Alike Are They? In Ecology 

of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. 

Cernusak, eds., pp. 119–140. Smithsonian Contributions to Botany, 

No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Dickie, I. A., and P. B. Reich. 2005. Ectomycorrhizal Fungal Communities at Forest Edges. J. Ecol. 93: 244–255.

Duhoux, E., G. Rinaudo, H. G. Diem, F. Auguy, D. Fernandez, D. Bogusz, C. Franche, Y. Dommergues, and B. Huguenin. 2001. Angiosperm Gymnostoma Trees Produce Root Nodules Colonized by 

Arbuscular Mycorrhizal Fungi Related to Glomus. New Phytol.

149: 115–125.

Eissenstat, D. M., and R. D. Yanai. 1997. The Ecology of Root Lifespan. 

Advances Ecol. Res. 27: 1–59.

Feild, T. S., and T. J. Brodribb. 2005. A Unique Mode of Parasitism in 

the Conifer Coral Tree Parasitaxus ustus (Podocarpaceae). Pl. Cell 

Environm. 28: 1316–1325.

Grand, L. F. 1969. A Beaded Endotrophic Mycorrhiza of Northern and 

Southern Red Oak. Mycologia 61: 408–409.

Grobbelaar, N., J. M. Strauss, and E. G. Groenewald. 1971. Nonleguminous Seed Plants in Southern Africa Which Fix Nitrogen 

Symbiotically. Pl. Soil 35: 325–334.

Hajibabaei, M., J. Xia, and G. Drouin. 2006. Seed Plant Phylogeny: 

Gnetophytes Are Derived Conifers and a Sister Group to Pinaceae. 

Molec. Phylogen. Evol. 40: 208–217.

Horton, T. R., E. Cázares, and T. D. Bruns. 1998. Ectomycorrhizal, 

Vesicular-Arbuscular and Dark Septate Fungal Colonization of 

Bishop Pine (Pinus muricata) Seedlings in the First 5 Months of 

Growth after Wildfire. Mycorrhiza 8: 11–18.

Huang, B., C. Lü, B. Wu, and L. Fan. 2007. A Rhizobia Strain Isolated 

from Root Nodule of Gymnosperm Podocarpus macrophyllus. Sci. 

China, Ser. C 50: 228–233.

Hurst, S. E., M. H. Turnbull, and D. A. Norton. 2002. The Effect of 

Plant Light Environment on Mycorrhizal Colonisation in FieldGrown Seedlings of Podocarp-Angiosperm Forest Tree Species. 

New Zealand J. Bot. 40: 65–72.

Kessler, K. J. 1966. Growth and Development of Mycorrhizae of Sugar 

Maple (Acer saccharum Marsh.). Canad. J. Bot. 44: 1413–1425.

Khan, A. G. 1972. Podocarp-Type Mycorrhizal Nodules in Aesculus indica. Ann. Bot. 36: 229–238.

Khan, A. G., and P. G. Valder. 1972. The Occurrence of Root Nodules 

in the Ginkgoales, Taxales, and Coniferales. Proc. Linn. Soc. New 

South Wales 97: 35–41.

Kitayama, K., S. Aiba, M. Ushio, T. Seino, and Y. Fujiki. 2011 (this 

volume). The Ecology of Podocarps in Tropical Montane Forests 

of Borneo: Distribution, Population Dynamics, and Soil Nutrient 

Acquisition. In Ecology of the Podocarpaceae in Tropical Forests, 

B. L. Turner and L. A. Cernusak, eds., pp. 101–117. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Koide, R. T., I. A. Dickie, and M. D. Goff. 1999. Phosphorus Deficiency, 

Plant Growth and the Phosphorus Efficiency Index. Funct. Ecol.

13: 733–736.

Lambers, H., J. A. Raven, G. R. Shaver, and S. E. Smith. 2008. Plant 

Nutrient-Acquisition Strategies Change with Soil Age. Trends Ecol. 

Evol. 23: 95–103.

McGee, P. A., S. Bullock, and B. A. Summerell. 1999. Structure of Mycorrhizae of the Wollemi Pine (Wollemia nobilis) and Related Araucariaceae. Austral. J. Bot. 47: 85–95.

McGlone, M. S., D. C. Mildenhall, and M. S. Pole. 1996. History and 

Paleoecology of New Zealand Nothofagus Forests. In History and 

Paleoecology of New Zealand Nothofagus Forests, T. T. Veblen, 

R. S. Hill, and J. Read, eds., pp. 83–130. Yale University Press, New 

Haven, Conn.

Mikola, P. U. 1986. Relationship between Nitrogen Fixation and Mycorrhiza. World J. Microbiol. Biotechnol. 2: 275–282.

Mineo, L., and S. K. Majumdar. 1996. Ectomycorrhiza in Oaks (Quercus alba, Q. rubra) in Northeastern Pennsylvania Woodlands: Morphology, Frequency and Implied Physiology and Ecology. In Concepts in Mycorrhizal Research, K. G. Mukerji, ed., pp. 315–331. 

Kluwer Academic Press, Dordrecht, Netherlands.

Morrison, T. M., and D. A. English. 1967. The Significance of Mycorrhizal Nodules of Agathis australis. New Phytol. 66: 245–250.

Pareliussen, I., E. G. A. Olsson, and W. S. Armbruster. 2006. Factors 

Limiting the Survival of Native Tree Seedlings Used in Conservation 

Efforts at the Edges of Forest Fragments in Upland Madagascar. 

Restoration Ecol. 14: 196–203.

Preston, R. J. 1943. Studies of the Roots of Juvenile Lodgepole Pine. Bot. 

Gaz. 104: 443–448.

Reed, S. C., C. C. Cleveland, and A. R. Townsend. 2008. Tree Species 

Control Rates of Free-Living Nitrogen Fixation in a Tropical Rain 

Forest. Ecology 89: 2924–2934.

Richardson, S. J., D. A. Peltzer, R. B. Allen, M. S. McGlone, and R. L. 

Parfitt. 2004. Rapid Development of Phosphorus Limitation in 

Temperate Rainforest along the Franz Josef Soil Chronosequence. 

Oecologia 139: 267–276.

Russell, A. J., M. I. Bidartondo, and B. G. Butterfield. 2002. The Root 

Nodules of the Podocarpaceae Harbour Arbuscular Mycorrhizal 

Fungi. New Phytol. 156: 283–295.

Schüßler, A., D. Schwarzott, and C. Walker. 2001. A New Fungal Phylum, the Glomeromycota: Phylogeny an Evolution. Mycol. Res.

105: 1413–1421.

Silvester, W. B. 2000. The Biology of Kauri (Agathis australis) in New 

Zealand II. Nitrogen Cycling in Four Kauri Forest Remnants. New 

Zealand J. Bot. 38: 205–220.

Silvester, W. B., and K. J. Bennett. 1973. Acetylene Reduction by Roots 

and Associated Soil of New Zealand Conifers. Soil Biol. Biochem. 

5: 171–179.

Smith, S. E., and D. J. Read. 2008. Mycorrhizal Symbiosis. 3rd ed. Academic Press, New York.

Solomon, D., F. Fritzsche, M. Tekalign, J. Lehmann, and W. Zech. 2002. 

Soil Organic Matter Composition in the Subhumid Ethiopian Highlands as Influenced by Deforestation and Agricultural Management. 

Soil Sci. Soc. Amer. J. 66: 68–82.

Stevens, P. F. 2001–2009. Angiosperm Phylogeny Website. Version 9. 

http://www.mobot.org/MOBOT/research/APweb/ (accessed August 

2009).

St John, T. V. 1980. Root Size, Root Hairs, and Mycorrhizal Infection: 

A Re-Examination of Baylis’s Hypotheses with Tropical Trees. New 

Phytol. 84: 483–487.

Taylor, L. L., J. R. Leake, J. Quirk, K. Hardy, S. A. Banwart, and D. J. 

Beerling. 2009. Biological Weathering and the Long-Term Carbon 

Cycle: Integrating Mycorrhizal Evolution and Function into the 

Current Paradigm. Geobiology 7: 171–191.

Thomson, J., U. Matthes-Sears, and R. L. Peterson. 1990. Effect of Seed 

Provenance and Fungal Species on Bead Formation in Roots of 

Picea mariana Seedlings. Canad. J. Forest Res. 20: 1746–1752.

Van’t Veer, R., and H. Hooghiemstra. 2000. Montane Forest Evolution 

during the Last 650,000 yr in Colombia: A Multivariate Approach 

Based on Pollen Record. J. Quatern. Sci. 15: 329–346.

Wardle, D. A., S. K. Wiser, R. B. Allen, J. E. Doherty, K. I. Bonner, and 

W. M. Williamson. 2008. Aboveground and Belowground Effects 

of Single Tree Removals after Forty Years in a New Zealand Temperate Rainforest. Ecology 89: 1232–1245.
number 95 • 187

Wu, C. S., Y. N. Wang, S. M. Liu, and S. M. Chaw. 2007. Chloroplast 

Genome (cpDNA) of Cycas taitungensis and 56 cp Protein-Coding 

Genes of Gnetum parvifolium: Insights into cpDNA Evolution and 

Phylogeny of Extant Seed Plants. Molec. Biol. Evol. 24: 1366–1379.

Wubet, T., M. Weiß, I. Kottke, and F. Oberwinkler. 2006. Two Threatened Coexisting Indigenous Conifer Species in the Dry Afromontane Forests of Ethiopia Are Associated with Distinct Arbuscular 

Mycorrhizal Fungal Communities. Canad. J. Bot. 84: 1617–1627. 

Lucas A. Cernusak, The Australian National University, Canberra, Australia. Hylton Adie, University of KwaZulu–Natal, Scottsville, South Africa. 

Peter J. Bellingham and Ian A. Dickie, Landcare 

Research, Lincoln, New Zealand. Edward Biffin,

The University of Adelaide, Adelaide, South Australia, Australia. Timothy J. Brodribb, University 

of Tasmania, Hobart, Tasmania, Australia. David 

A. Coomes, University of Cambridge, Cambridge, 

UK. James W. Dalling, University of Illinois at 

Urbana-Champaign, Urbana, Illinois, USA. Neal 

J. Enright and Philip G. Ladd, Murdoch University, Murdoch, Western Australia, Australia. 

Kanehiro Kitayama, Kyoto University, Kyoto, 

Japan. Hans Lambers, The University of Western 

Australia, Crawley, Western Australia, Australia. Michael J. Lawes, School for Environmental 

Research, Charles Darwin University, Darwin, 

Northern Territory, Australia. Christopher H. 

Lusk, Macquarie University, Sydney, New South 

Wales, Australia. Robert J. Morley, Palynova Limited, Littleport, UK, and University of London, 

Egham, UK. Benjamin L. Turner, Smithsonian 

Tropical Research Institute, Balboa, Ancón, Republic of Panama. Correspondence: L. Cernusak, 

Lucas.Cernusak@anu.edu.au.

Expanded author information precedes the References section. Manuscript received 13 April 2010; 

accepted 9 July 2010.

12 Podocarpaceae in Tropical 

Forests: A Synthesis

Lucas A. Cernusak, Hylton Adie, Peter 

J. Bellingham, Edward Biffin, Timothy 

J. Brodribb, David A. Coomes, James 

W. Dalling, Ian A. Dickie, Neal J. 

Enright, Kanehiro Kitayama, Philip G. 

Ladd, Hans Lambers, Michael J. Lawes, 

Christopher H. Lusk, Robert J. Morley, 

and Benjamin L. Turner

The Podocarpaceae comprises 18 genera and about 173 species of evergreen, coniferous trees and shrubs. It is the most successful gymnosperm family 

in angiosperm-dominated tropical forests (Brodribb, this volume). Podocarps 

are distributed mainly in the Southern Hemisphere, with populations also extending as far north as China and Japan and to Mexico and the Caribbean in 

the neotropics (Dalling et al., this volume; Enright and Jaffré, this volume; Adie 

and Lawes, this volume). 

Molecular and fossil evidence suggests that the Podocarpaceae originated 

during the Triassic–Jurassic in Gondwana (Biffin et al., this volume; Morley, 

this volume). Currently, the greatest generic diversity of the Podocarpaceae is in 

Malesia (Enright and Jaffré, this volume). Podocarps did not migrate into tropical latitudes until later in their evolutionary history, appearing for the first time 

in Southeast Asia during the late Eocene, probably dispersing via the Indian 

Plate (Morley, this volume). Thus, the present latitudinal distributions have 

emerged in Asia and Africa over the last 40 million years. Although extinction 

rates in general appear to have been high within the family, a major shift in diversification rate is estimated to have taken place in the mid- to Late Cretaceous 

and Paleocene, with most extant genera becoming established in Gondwana 
190 • smithsonian contributions to botany

during this period. This shift could reflect reduced extinction and/or increased speciation in response to the expansion of angiosperm-dominated tropical forests (Biffin et 

al., this volume). An alternative explanation for the Late 

Cretaceous and Paleocene diversification could be the onset of wetter and warmer climatic conditions associated 

with the opening of the Southern Ocean (Morley, this 

volume). 

Some podocarp taxa show widespread and/or disjunct 

distributions. In the absence of molecular data, it is difficult to infer migration patterns or the potential for gene 

flow among these disjunct populations. Patterns of relatedness among populations in tropical forests could help 

reveal whether current populations are relicts of cooler 

tropical climates associated with the Last Glacial Maximum or the consequence of postglacial occupancy of suitable habitat. 

Tropical podocarps are most abundant in mid- to 

high-elevation forests, suggesting that the habitat requirements of temperate ancestors have been retained as 

podocarps radiated into the tropics. Podocarps also occur occasionally in lowland tropical rainforest, but this 

is the exception, rather than the rule (Dalling et al., this 

volume; Enright and Jaffré, this volume; Adie and Lawes, 

this volume; Coomes and Bellingham, this volume). One 

such exception is their prominence in lowland heath 

forests (kerangas) on Borneo (Enright and Jaffré, this 

volume). Thus, in Asia, podocarp taxa have apparently 

dispersed through both lowland and montane habitats. 

For example, the dispersal pathway for Dacrydium appears to have been via India through kerangas, i.e., heath 

forests growing on acidic, sandy soils that are low in nutrients, during the Paleogene. On the other hand, Dacrycarpus and Phyllocladus appear to have jumped between 

islands of montane/alpine habitat via New Guinea at the 

time of Plio–Pleistocene global cooling (Morley, this volume; Enright and Jaffré, this volume). A similar pattern of 

distributions can also be found in the neotropics, where 

podocarps are mainly montane, but with notable lowland 

exceptions (Dalling et al., this volume). There, podocarps 

are absent from most of the Amazon lowlands, except for 

the white sands around Iquitos, Peru, and nutrient-poor 

soils of the Guyana Shield. However, podocarps do occur 

at sea level on islands off both the Pacific and Atlantic 

coasts of Central America. It should also be noted that 

podocarp pollen was relatively common in lake sediments 

from the Amazon lowlands during the Last Glacial Maximum approximately 18,000 years ago but decreased to 

trace amounts during the Holocene, presumably as a result of climate warming (Colinvaux et al., 1996). 

Given that podocarps in lowland tropical forests appear to achieve their highest abundance on low-fertility 

soils (Dalling et al., this volume; Enright and Jaffré, this 

volume; Coomes and Bellingham, this volume), do they 

have high nutrient use efficiency and/or unique mechanisms for acquiring nutrients? Nutrient use efficiency can 

be defined as the product of nutrient productivity and 

mean nutrient residence time (Berendse and Aerts, 1987; 

Aerts and Chapin, 2000). Nutrient productivity is a rate 

variable, expressed as carbon uptake per unit of nutrient 

per unit time. Mean nutrient residence time is the average amount of time that a unit of nutrient spends in the 

plant between acquisition from the environment and loss 

through above- and below-ground litter production. Leaflevel measurements suggest that podocarps do not have 

nutrient productivities that can match those of tropical 

angiosperms. In a comparison of conifer and angiosperm 

seedlings grown in Panama, Podocarpus guatemalensis

had photosynthetic nitrogen productivity of 38 μmol CO2

mol-1 N s-1, whereas mean values were 64 and 162 μmol 

CO2 mol-1 N s-1 for three other conifer species and 11 

angiosperm species, respectively (Cernusak et al., 2008). 

Mean values for photosynthetic phosphorus productivity were 0.5, 0.7, and 2.5 mmol CO2

 mol-1 P s-1 for P. 

guatemalensis, three other conifer species, and 11 angiosperm species, respectively. In general, podocarps have 

low photosynthetic rates per unit leaf mass compared to 

angiosperms, in common with other conifer taxa (Lusk, 

this volume). Low mass-based photosynthetic rates contribute to low leaf-level nutrient productivities (Aerts and 

Chapin, 2000). 

It seems likely, therefore, that any advantage that 

tropical podocarps have in terms of nutrient use efficiency 

should derive from mean nutrient residence time, rather 

than from nutrient productivity. Mean nutrient residence 

time can vary as a function of leaf and root life spans, tissue nutrient concentrations, and the efficiency of nutrient 

resorption from senescing tissues. In common with other 

conifers, podocarps do tend to have long leaf life spans 

compared to angiosperms (Lusk, this volume). Podocarps 

can also have lower leaf nutrient concentrations than angiosperms: P. guatemalensis had leaf nitrogen and phosphorus concentrations of 1.5% and 2.5‰, respectively, 

compared with values of 1.2% and 2.9‰ for three other 

conifer species and 1.7% and 3.1‰ for 11 angiosperm species grown under similar soil conditions in Panama (Cernusak et al., 2008). Similarly, Podocarpus urbanii also had 

lower leaf nitrogen and phosphorus concentrations than 

co-occurring angiosperms in Jamaica (Dalling et al., this 

volume), but on Mount Kinabalu in Borneo nitrogen and 
number 95 • 191

phosphorus concentrations in the phyllodes of Phyllocladus hypophyllus were not different from those in leaves of 

co-occurring angiosperms (Kitayama et al., 2004). More 

data are therefore needed to determine whether leaf nutrient concentrations in tropical podocarps tend, in general, 

to be lower than in co-occurring angiosperm trees. There 

are no data that we are aware of for nutrient resorption 

efficiency from senescent leaves of tropical podocarps. 

Nor are we aware of data for root life spans, root nutrient concentrations, or resorption efficiency from senescing 

roots. Thus, although it is likely that tropical podocarps 

will have longer mean nutrient residence times than tropical angiosperms, the evidence currently available is insufficient to demonstrate this conclusively. 

In response to the second part of the question posed 

above, podocarps do not appear to possess any unique 

mechanism for acquiring nutrients. They do have conspicuous nodules on their roots that grow in the absence of 

fungi or bacteria; their function remains unclear, although 

they appear to play no significant role in atmospheric nitrogen fixation. Podocarp roots show very high rates of 

infection by arbuscular mycorrhizal fungi in both long 

and short nodular roots (Dickie and Holdaway, this volume). Thus, the nodules may simply serve to increase root 

volume for interaction with symbiotic mycorrhizal fungi. 

Dickie and Holdaway (this volume) argue that the nodules could minimize root construction and turnover costs 

while maximizing the root volume available to support 

mycorrhizal associations. On the basis of measurements 

on Mount Kinabalu, Borneo, Kitayama et al. (this volume) 

further suggest that podocarps may form loose symbiotic 

associations with soil microbial communities. 

In summary, there does not appear to be a single, outstanding feature that can explain why podocarps are relatively most successful on infertile soils in lowland tropical 

forests. The explanation may rather lie in a suite of traits 

that combine to enable podocarps to compete successfully 

when the productivity advantage of angiosperms is diminished by nutrient poverty (Brodribb and Feild, 2010). 

Some possible examples of such traits are long mean nutrient residence times associated with long leaf and root 

life spans and low tissue nutrient concentrations, efficient 

manipulation of mycorrhizal symbioses, and some degree 

of control over the composition of soil microbial communities by root exudates and the quality and quantity of leaf 

litter (Kitayama et al., this volume). 

Despite the frequent association of tropical podocarps 

with low-nutrient soils, it would be incorrect to assume 

that they are strictly confined to those soils. Broadleaved podocarps, in particular, can also occur on more 

productive sites. This may be because broad leaves are important for light interception efficiency and competitiveness with co-occurring angiosperms at nutrient-rich sites, 

where dense canopies cast a pronounced shadow over regenerating seedlings (Adie and Lawes, this volume). Broadleaved podocarps tend to be faster growing and shorter 

lived and have shorter leaf longevity and higher leaf litter 

quality than imbricate-leaved genera (Enright and Jaffré, 

this volume). These traits in broad-leaved podocarps may 

approach those of co-occurring angiosperms. Under African forest conditions, superior shade tolerance by broadleaved podocarps allows them to dominate competing 

angiosperms over a range of soil nutrient conditions (Adie 

and Lawes, 2009). Phylogenetic analyses suggest that the 

broad-leaved podocarps may have a higher diversification 

rate than genera with imbricate leaves (Biffin et al., this 

volume), possibly linked to differences between the two 

groups in metabolic rates. 

The ability to produce flattened, plagiotrophic leaves 

and shoots is fundamental to the success of podocarps in 

competition for light with angiosperms. Leaf flattening is 

a prominent feature within the Podocarpaceae and distinguishes the broad-leaved podocarps from most other conifer taxa. Flattened leaves are likely to be a key factor 

enabling shade tolerance of podocarps (Brodribb, this volume). The flattened leaves contain sclereids, which increase 

water transport from the leaf midvein to the sites of evaporation in the leaf lamina. Freed from the temperate-zone 

constraint of freezing, tropical broad-leaved podocarps can 

increase leaf size and thus have converged upon a strategy of leaf architecture that resembles that of co-occurring 

angiosperms. Whereas temperate podocarps tend to have 

lower leaf area ratios than co-occurring angiosperms, tropical podocarps may be more able to emulate shade-tolerant 

tropical angiosperms and intercept sunlight with a similar 

efficiency. 

In general, podocarps do not tolerate drought. This 

may be because they possess wood that is vulnerable to 

embolism by water stress and are unable to refill embolized tracheids (Brodribb, this volume). Additionally, the 

vascular system associated with homoxylous conifer wood 

may be insufficient to supply water to the relatively large 

leaf area carried by broad-leaved podocarps under conditions of high evaporative demand and/or low soil water 

potential. This may lead to excessively low leaf water 

potentials and sharply curtailed photosynthetic rates under such conditions. An extreme exception to the general 

intolerance to drought among podocarps occurs in the 

Mediterranean-type climate of southwest Australia. There, 

Podocarpus drouynianus forms a lignotuber that allows it 
192 • smithsonian contributions to botany

to resprout following shoot dieback caused by fire and/or 

drought (Ladd and Enright, this volume). Kerangas forests 

are also subject to occasional drought, and species growing in them, including podocarps, show an array of leaf 

traits, in combination with reduced plant size, that reduce 

water loss (Enright and Jaffré, this volume). 

Podocarps are long-lived in the temperate zone, and 

there is evidence that they also have a longevity advantage 

over competing angiosperms in the tropics (Kitayama et al., 

this volume). They are often subcanopy components and 

not emergent in tropical forests, unlike many New Zealand podocarps (Coomes and Bellingham, this volume). 

Landscape-scale disturbance is probably not necessary for 

regeneration of tropical podocarps, even though many species occur in areas where disturbances such as cyclones and 

landslides are common. Tropical podocarps are fire intolerant. In general, podocarp seedlings show low abundance. 

Thus, in many cases, slow growth and high persistence 

likely facilitate their ultimate recruitment to the canopy. 

Little is known about herbivory in tropical podocarps or 

their defenses against herbivores. Similarly, pollination and 

seed dispersal in tropical podocarps have been little studied. 

CONSERVATION, MANAGEMENT, 

AND GLOBAL CHANGE

In common with most tropical trees, the immediate 

threat to tropical podocarps is deforestation associated 

with timber extraction, mining, and other modern anthropogenic activities, including drainage of peat swamps and 

expansion of agricultural activities onto poor soils. Several 

podocarps are local montane endemics, and these may be 

further threatened by shifting climatic zones associated 

with global climate change and deforestation (Walther, 

2004; Jump et al., 2009). These species could become increasingly rare within narrowing altitudinal bands, particularly on islands and mountains. Tropical podocarps 

are fire and drought intolerant, so they will be particularly 

adversely affected wherever climate change leads to hotter, 

drier conditions with more frequent fires. 

Although podocarp timber has many uses for human 

activities, their slow growth rates make their exploitation 

ecologically unsustainable. Therefore, continued harvesting of existing individuals from natural stands threatens 

populations (Lawes et al., 2007). 

Habitat specialization restricts the potential area of 

suitable sites for podocarps, which requires broad-scale 

habitat conservation to capture potential conservation 

sites. The association with unusually infertile soils is also 

significant with regard to podocarp conservation. International Union for Conservation of Nature (IUCN) assessments of species conservation status are effectively 

determined by range sizes, in the absence of data on population number or population change. Many podocarps 

have large ranges (i.e., thousands of square kilometers) 

but probably only occupy a fraction of that area. Thus, 

if podocarps really are restricted to unusual habitats, then 

they may be more endangered than current assessments 

suggest. Additionally, if conservation priorities are defined 

by phylogenetic diversity, podocarps have a high conservation value because their nearest living sister taxa are 

separated by about 250 million years (Biffin et al., this 

volume). 

A summary of tropical podocarp species that are 

threatened based on assessments in the 2009 IUCN Red 

List of Threatened Species (IUCN, 2009) is provided in 

Table 12.1. In addition to these species, a number of taxa 

are also considered “near threatened” or “data deficient.” 

Thus, Table 12.1 likely represents a conservative estimate 

of the true number of tropical podocarp species currently 

under threat of extinction. Taking this conservative estimate, roughly one-fourth of tropical podocarp species are 

threatened, with five species considered critically endangered, 18 species endangered, and 16 species vulnerable 

(Table 12.1). Many of the species in Table 12.1 are island 

endemics, including four species from Madagascar, six 

species from New Caledonia, and seven species from Borneo. In addition, there are a number of species endemic to 

islands in the Western Pacific and the Caribbean. 

Because podocarp-dominated forests are often associated with ecosystems that have poor drainage and large 

accumulations of organic material on the forest floor, they 

play an important role in carbon storage. Leaf and litter 

characteristics of podocarps generally result in slow decomposition rates, leading to an accumulation of carbon 

in the litter layer and in the soil. This carbon can be rapidly lost when podocarp-dominated forests are cleared for 

other land uses (Freier et al., 2010). Thus, the UN global 

initiative to reduce emissions from tropical deforestation 

and degradation should place a high value on podocarpdominated forests. 

RECOMMENDATIONS FOR 

FUTURE RESEARCH

Podocarps are potentially good indicators of environmental change over their 250 million year history. Important aspects of the phylogeny of Podocarpaceae remain to 
number 95 • 193

be resolved, and more and better information would aid 

their use as environmental indicators. A phylogeographic 

perspective could help in understanding population connectivity under changing climate in the Holocene. 

Dispersal and recruitment dynamics of infrequent 

lowland tropical podocarps are largely unknown. As 

podocarps are mostly dispersed by large-bodied animals, 

local extinction of dispersers may particularly impact 

upon podocarp regeneration and recruitment and genetic 

diversity, especially on islands. Population genetic data 

could effectively address issues of pollen and seed dispersal, genetic diversity, and relatedness. 

TABLE 12.1. Conservation status of threatened tropical species of the Podocarpaceae (IUCN, 2009). 

Abbreviations: CR, critically endangered; EN, endangered; VU, vulnerable.

Species Status Location Habitat

Acmopyle sahniana CR Fiji Montane forest

Afrocarpus mannii VU São Tomé, Gulf of Guinea Montane forest

A. usambarensis VU East African highlands Montane forest

Dacrydium comosum EN Malay Peninsula Montane Forest

D. ericoides VU Sarawak, Borneo Hill forest, ultrabasic

D. gracile VU Sabah, Borneo Montane forest

D. guillauminii CR New Caledonia Riparian

D. leptophyllum VU Irian Jaya Montane heath forest

D. nausoriense EN Fiji Montane rainforest

Falcatifolium angustum VU Sarawak, Borneo Lowland rainforest

Nageia maxima VU Sarawak, Borneo Peat swamp forest

Parasitaxus usta VU New Caledonia Montane rainforest understory

Podocarpus affinis VU Fiji Montane rainforest

P. angustifolius EN Cuba Montane rainforest

P. aristulatus VU Cuba, Hispaniola Montane forest

P. beecherae EN New Caledonia Wet maquis

P. brevifolius VU Sabah, Mount Kinabalu Montane forest

P. capuronii EN Madagascar Montane forest

P. costalis EN Philippines, Taiwan Montane forest

P. costaricensis VU Costa Rica Lowland to montane forest

P. decumbens CR New Caledonia Montane stunted forest

P. deflexus EN Malay Peninsula, Sumatra Montane forest

P. gibbsii VU Sabah, Mount Kinabalu Montane forest

P. globulus EN Sabah, Borneo Lowland to montane forest

P. hispaniolensis EN Dominican Republic Montane forest

P. humbertii EN Madagascar Montane forest, heath

P. laubenfelsii EN Sarawak, Borneo Kerangas, montane heath

P. longifoliolatus EN New Caledonia Montane rainforest understory

P. lophatus VU Philippines Montane forest

P. nakaii EN Taiwan Subtropical forest 

P. palawanensis CR Philippines Lowland rainforest

P. pallidus VU Tonga Montane forest

P. pendulifolius EN Venezuela Montane rainforest

P. perrieri CR Madagascar Montane forest

P. polyspermus EN New Caledonia Montane forest

P. purdieanus EN Jamaica Montane forest

P. rostratus EN Madagascar Montane forest

Retrophyllum minus EN New Caledonia Riparian

R. rospigliosi VU Venezuela, Colombia, Peru Montane forest
194 • smithsonian contributions to botany

Podocarps colonize second-growth forests in some 

temperate regions. The potential for podocarps to colonize second-growth tropical forests, which are increasing 

in area in some tropical regions, is unknown. Physiological and growth responses of podocarps to variation in 

atmospheric CO2 concentration are unknown but could 

have important implications for their use as indicators of 

environmental change. 

Understanding why tropical podocarps are mostly restricted to wet, infertile environments requires information about their ecophysiology. For example, seedling leaf 

area ratios of temperate podocarps are generally low relative to co-occurring angiosperms, but virtually nothing is 

known of leaf area ratios of large-leaved lowland tropical 

podocarps. More information about physiological mechanisms of drought sensitivity, including stomatal function 

and susceptibility to cavitation, is key to understanding 

current podocarp distributions. The physiological adaptations allowing podocarp success on infertile soils, potentially including conspicuous root nodules, mycorrhizal 

symbioses, and nutrient retention strategies, are key areas 

for further research. A better understanding of podocarp 

ecophysiology is likely to be achieved through integrated, 

whole-plant studies, rather than by addressing nutrient, 

carbon, and water relations independently of each other. 

Finally, podocarps are poorly represented in permanent census plots in tropical forests, which limits knowledge of demography and habitat associations. Important 

demographic factors and environmental drivers are likely 

to be longevity, relative shade tolerance, and edaphic 

properties. Permanent plot data could provide an opportunity to collate such information. Results could provide 

a framework to inform decisions about silviculture and 

forest management of podocarps.

Expanded Author Information

Lucas A. Cernusak, Research School of Biology, The 

Australian National University, Canberra, ACT 0200, 

Australia; Lucas.Cernusak@anu.edu.au. Hylton Adie,

School of Biological and Conservation Sciences, Forest Biodiversity Research Unit, University of KwaZulu–

Natal, Private Bag X01, Scottsville 3209, South Africa. 

Peter J. Bellingham and Ian A. Dickie, Landcare Research, 

PO Box 40, Lincoln 7640, New Zealand. Edward Biffin, Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Science, 

The University of Adelaide, Adelaide, South Australia 

5005, Australia. Timothy J. Brodribb, School of Plant 

Science, University of Tasmania, Hobart, Tasmania 7001, 

Australia. David A. Coomes, Forest Conservation and 

Ecology Group, Department of Plant Sciences, University 

of Cambridge, Cambridge CB2 3EA, UK. James W. Dalling, Department of Plant Biology, University of Illinois 

at Urbana-Champaign, 265 Morrill Hall, 505 S. Goodwin Avenue, Urbana, Illinois 61081, USA. Neal J. Enright 

and Philip G. Ladd, School of Environmental Science, 

Murdoch University, Murdoch, Western Australia 6150, 

Australia. Kanehiro Kitayama, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan. Hans 

Lambers, School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, Western 

Australia 6009, Australia. Michael J. Lawes, School for 

Environmental Research, Charles Darwin University, Darwin, Northern Territory 0909, Australia. Christopher H. 

Lusk, Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia. Robert 

J. Morley, Palynova Limited, 1 Mow Fen Road, Littleport 

CB6 1PY, UK, and Department of Earth Sciences, Royal 

Holloway, University of London, Egham TW20 0EX, UK. 

Benjamin L. Turner, Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Republic of 

Panama.

REFERENCES

Adie, H. and M. J. Lawes. 2009. Explaining Conifer Dominance in Afrotemperate Forests: Shade Tolerance Favours Podocarpus latifolius

over Angiosperm Species. Forest Ecol. Managem. 259: 176–186.

Adie, H., and M. J. Lawes. 2011 (this volume). Podocarps in Africa: 

Temperate Zone Relicts or Rainforest Survivors? In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 79–100. Smithsonian Contributions to Botany, No. 

95. Smithsonian Institution Scholarly Press, Washington, D.C.

Aerts, R., and F. S. Chapin. 2000. The Mineral Nutrition of Wild Plants 

Revisited: A Re-evaluation of Processes and Patterns. Advances 

Ecol. Res. 30: 1–67.

Berendse, F., and R. Aerts. 1987. Nitrogen-Use Efficiency: A Biologically 

Meaningful Definition? Funct. Ecol. 1: 293–296.

Biffin, E., J. Conran, and A. Lowe. 2011 (this volume). Podocarp Evolution: A Molecular Phylogenetic Perspective. In Ecology of the 

Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 1–20. Smithsonian Contributions to Botany, No. 95. 

Smithsonian Institution Scholarly Press, Washington, D.C.

Brodribb, T. J. 2011 (this volume). A Functional Analysis of Podocarp 

Ecology. In Ecology of the Podocarpaceae in Tropical Forests, B. L. 

Turner and L. A. Cernusak, eds., pp. 165–173. Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, 

Washington, D.C.

Brodribb, T. J., and T. S. Field. 2010. Leaf Hydraulic Evolution Led a 

Surge in Leaf Photosynthetic Capacity during Early Angiosperm 

Diversification. Ecol. Letters 13: 175–183.

Cernusak, L. A., K. Winter, J. Aranda, and B. L. Turner. 2008. Conifers, 

Angiosperm Trees, and Lianas: Growth, Whole-Plant Water and 

Nitrogen Use Efficiency, and Stable Isotope Composition (d13C and 
number 95 • 195

d18O) of Seedlings Grown in a Tropical Environment. Pl. Physiol.

148: 642–659.

Colinvaux, P. A., P. E. De Oliveira, J. E. Moreno, M. C. Miller and M. B. 

Bush. 1996. A Long Pollen Record from Lowland Amazonia: Forest and Cooling in Glacial Times. Science 274: 85–88.

Coomes, D. A., and P. J. Bellingham. 2011 (this volume). Temperate and 

Tropical Podocarps: How Ecologically Alike Are They? In Ecology 

of the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. 

Cernusak, eds., pp. 119–140. Smithsonian Contributions to Botany, 

No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Dalling, J. W., P. Barkan, P. J. Bellingham, J. R. Healey, E. V. J. Tanner, J. T. Murillo. 2011 (this volume). Ecology and Distribution of 

Neotropical Podocarpaceae. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 43–56. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Dickie, I. A., and R. J. Holdaway. 2011 (this volume). Podocarp Roots, 

Mycorrhizas, and Nodules. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 175–

187. Smithsonian Contributions to Botany, No. 95. Smithsonian 

Institution Scholarly Press, Washington, D.C.

Enright, N. J., and T. Jaffré. 2011 (this volume). Ecology and Distribution of the Malesian Podocarps. In Ecology of the Podocarpaceae in 

Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 57–77. 

Smithsonian Contributions to Botany, No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Freier, K. P., B. Glaser, and W. Zech. 2010. Mathematical Modeling of 

Soil Carbon Turnover in Natural Podocarpus Forest and Eucalyptus Plantation in Ethiopia Using Compound Specific d13C Analysis. 

Global Change Biol. 16: 1487-1502.

International Union for Conservation of Nature (IUCN). 2009. IUCN 

Red List of Threatened Species. Version 2009.2. http://www.iucnred

list.org (accessed 22 December 2009).

Jump, A. S., C. Mátyás, and J. Peñuelas. 2009. The Altitude-forLatititude Disparity in the Range Retractions of Woody Species. 

Trends Ecol. Evol. 24: 694–701.

Kitayama, K., S. I. Aiba, M. Takyu, N. Majalap, and R. Wagai. 2004. 

Soil Phosphorus Fractionation and Phosphorus-Use Efficiency of 

a Bornean Tropical Montane Rain Forest during Soil Aging with 

Podozolization. Ecosystems 7: 259–274.

Kitayama, K., S. Aiba, M. Ushio, T. Seino, and Y. Fujiki. 2011 (this 

volume). The Ecology of Podocarps in Tropical Montane Forests 

of Borneo: Distribution, Population Dynamics, and Soil Nutrient 

Acquisition. In Ecology of the Podocarpaceae in Tropical Forests, 

B. L. Turner and L. A. Cernusak, eds., pp. 101–117. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Ladd, P. G., and N. J. Enright. 2011 (this volume). Ecology of FireTolerant Podocarps in Temperate Australian Forests. In Ecology of 

the Podocarpaceae in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 141–155. Smithsonian Contributions to Botany, 

No. 95. Smithsonian Institution Scholarly Press, Washington, D.C.

Lawes, M. J., M. E. Griffiths, and S. Boudreau. 2007. Colonial Logging 

and Recent Subsistence Harvesting Affect the Composition and 

Physiognomy of a Podocarp Dominated Afrotemperate Forest. Forest Ecol. Managem. 247: 48–60.

Lusk, C. H. 2011 (this volume). Conifer-Angiosperm Interactions: Physiological Ecology and Life History. In Ecology of the Podocarpaceae 

in Tropical Forests, B. L. Turner and L. A. Cernusak, eds., pp. 157–

164. Smithsonian Contributions to Botany, No. 95. Smithsonian 

Institution Scholarly Press, Washington, D.C.

Morley, R. J. 2011 (this volume). Dispersal and Paleoecology of Tropical 

Podocarps. In Ecology of the Podocarpaceae in Tropical Forests, 

B. L. Turner and L. A. Cernusak, eds., pp. 21–41. Smithsonian 

Contributions to Botany, No. 95. Smithsonian Institution Scholarly 

Press, Washington, D.C.

Walther, G. R. 2004. Plants in a Warmer World. Perspect. Pl. Ecol. Evol. 

Syst. 6: 169–185.

Subject Index

Page numbers followed by “t” refer to a table; page numbers followed by “f” refer to a 

figure.

accessory transfusion tissue, 167, 168f, 169, 171f

acid phosphatase activity, 111–115

Africa, 21, 79–80, 94–95, 190

and coastal forests, 92–94

and drought resistance, 129

ecology of, 86–88

endangered species in, 193t

fossil record from, 24–26, 27f, 35, 36

and podocarp ecophysiology, 85–86

and regeneration, 89–90, 94, 127

role of disturbance in, 88–89

and seed dispersal, 152, 158

and soil nutrients, 90–92

and species dispersal, 30, 35–36, 38

species distribution in, 81–85, 189

species diversity in, 22, 80–81

altitudinal range, 61–63, 66, 102–106

Amazonia

and species dispersal, 129

species distribution in, 44, 47f, 48

species of, 136

Andes

fossil record from, 44

and species dispersal, 38, 129

species distribution in, 45, 48, 54, 131

species of, 136, 137

angiosperms, 60, 63, 94, 131

and acid phosphatase activity, 112

advantages of, 70, 158

and arbuscular mycorrhizal fungi, 122

and cold temperatures, 121–122

and competitive advantages of podocarps in Malesia, 68

constraints on, 80

and gap-phase dynamics, 88

growth of, 68
198 • smithsonian contributions to botany

angiosperms (continued)

impact of climatic fluctuation on, 

94–95

impact on dispersal, 36

leaf to stem ratio of, 68

longevity of, 70

in Podocarpus-dominated forests, 

87–89

pollen record of, 27f

regeneration of, 80, 90

and seedling growth, 46

and shade, 87, 108–109

vessels of, 85–86, 159

animal dispersal

of seeds, 69, 146, 151, 152, 158, 193

Antarctica, 22, 36

antiherbivore defenses, 63

arbuscular mycorrhizal fungi, 63, 

91–92, 178t, 185

and angiosperms, 122

and lipid abundance, 114t

and root nodule, 181, 183f, 184

and roots, 176–177, 179, 180f, 191

Argentina, 136

Asia

endangered species in, 61

fossil record from, 22, 23t, 24, 26, 28, 

31, 32

and species dispersal, 26, 28–31, 36, 

38f, 172, 189–190

species distribution in, 33, 60, 102, 

129, 142

Assam, 72–75t

Australasia, 21

fossil record from, 28, 36

and species dispersal, 30

species distribution in, 131

species diversity in, 129

Australia, 70, 71t

extinction in, 131, 169, 170, 171f

fire-tolerant podocarps in, 141, 142, 

143t, 146–148, 150f, 151–154

fossil record from, 22, 30, 33–36, 

129, 151

impact of drought intolerance in, 17

and poor soil, 122

range contraction in, 2, 169, 170

and resprouting after fire, 128

seed dispersal by animals in, 69

and species dispersal, 31f, 33, 36, 38

species distribution in, 60–62, 151

species diversity in, 59–60, 72–75t

species of, 134–136

Banka Island, 133

Bayesian method, 2, 4, 7

biogeography, 81–85

birth-death model, 10, 12, 14f

Bolivia, 45, 54, 136

Borneo, 71t

altitudinal range in, 102–106

endangered species in, 192, 193t

and podocarp adaptations, 109–114, 

190–191

and population ecology, 108–109

soil types in, 106–108

and species dispersal, 33–36, 38

species distribution in, 58f, 60–63, 

130–131, 190

species diversity in, 59, 60, 72–75t

species of, 132–136

Brazil

fossil record from, 44

species distribution in, 49t, 68–69, 71

species of, 136

bryophytes, 62

Burma, 59t, 72–75t, 133, 135, 136

calcium, 67

Cambodia, 59t, 72–75t, 133

canopy, 128

architecture of, 124–125, 130, 131

and gap-phase dynamics, 88–89

Celebes, 132–136

census plot, 62

China, 2

fossil record from, 22, 28, 31

and species dispersal, 31, 36

species distribution in, 61, 189

species of, 59t, 72–75t, 132, 133, 135, 

136

chloroplast

divergence estimated using, 9, 11f, 

12f

generic schemes confirmed by, 4

climate

fluctuations in, 66, 94–95

impact of on dispersal, 31, 33, 36, 

37f, 38

impact of on diversity, 59–60

climate change, 68, 190, 192

cloud forest, 61, 68, 69, 102, 105–106

coastal forest, 92–95

as habitat, 22, 28, 45, 81, 86, 151

Colombia

conservation issues in, 54

species distribution in, 44, 45, 48, 49t, 

50, 54

species of, 136

vulnerable species in, 193t

conduit diameter, 158–160

conifers, 26, 28, 159

advantages of, 158

and angiosperm competition, 2, 60

conservation, 54, 61, 192, 193t

construction

as threat, 68

Costa Rica, 45, 49t, 136, 193t

Cuba

endangered species in, 193t

and species dispersal, 172

species distribution in, 45, 46, 50, 54

“Dacrydioid” clade, 7

diameter, stem, 50, 51, 52f

and conduit diameter, 160f

and growth rate, 63, 70, 71t

diameter, tree

growth rate of, 52, 54, 120

diameter at breast height (dbh), 106f, 

108–110f

in canopy gaps, 88

and median crown position index, 112f

in mountain forests, 61

and soil type, 104t

and tree height, 111, 112f

diversification

patterns of, 10, 12–13

rates of, 3, 14–15, 16f, 17, 189–190

Dominican Republic, 131, 193t

drought, 68, 89

adaptations to, 63

intolerance to, 17, 122, 169–170, 

191, 192

resistance to, 170–171

ecophysiology, 2, 17, 70, 85–86, 194

and seedlings, 68, 72

ectomycorrhizal fungi, 111, 122, 179, 

184–185

Ecuador, 44, 45, 49–50, 54

embolism, 63, 122

in cold climates, 86, 171–172

and conduit diameter, 159–160

and drought, 191

endangered species, 61

environmental indicators

Podocarpaceae as, 192–194

erosion, 61

evolution, 72

and drought resistance, 63

of leaves, 63, 68, 166–167, 169, 

191–192

and poor soil, 67, 129

rates of, 2

and shade tolerance, 128–129

extinction rate, 12–14, 15f, 189–190

Fiji

endangered species in, 193t

species of, 59t, 61, 72–75t, 132–133, 

135

fire, 153

impact on distribution, 67, 68, 84, 86, 

89

impact on diversity, 60

intolerance to, 17, 45–46, 128, 131, 192
number 95 • 199

and resprouting, 128, 147

and seed production, 143, 145–146

fossil record, 2, 9–10, 13

pollen in, 22–28, 30–31, 33–36, 44, 

80, 83–84, 190

fragmentation

as threat, 68, 69

general time reversible model, 4

Gondwana

Podocarpaceae originating in, 21–22, 

35, 44, 102, 169, 189–190

species distribution from, 81

species diversification in, 36

growth rate, 71t, 120

as insufficient to survive, 127

and light, 90–91, 108–109, 124f

and median crown position, 111f

and nutrients, 50, 90–91, 124f

of seedlings, 68, 120

Guatemala, 137

Guyana, 137

habitat, 60, 121, 190

cloud forest as, 61, 69, 102, 105–106

coastal forest as, 22, 28, 45, 81, 86, 

151

heath forest as, 60, 61, 190

lowland forest as, 45, 61, 190

montane forest as, 60, 61, 190

in neotropics, 46–50

peat forest as, 60, 61

tropical rainforest as, 132–137, 159, 

165–166, 190

Haita, 49t

heath forest, 60–63, 190

height, 112t, 130t

Hispaniola, 45–46, 49t, 54, 193t

humans

as threat, 67–69

hydraulic function

in cold climates, 159, 171–172

and drought, 170–171

and leaf structure, 68, 167, 169

and light conditions, 60

and tracheids, 86, 120, 122

India, 21–22

fossil record from, 25, 26, 36

and species dispersal, 28, 30, 35–36, 

189–190

species distribution in, 57, 58f, 59t, 

61, 72–75t

species diversity in, 60, 72–75t

species of, 132–133

Indochina, 24–25, 33, 133

Indonesia

fossil record from, 35

and species dispersal, 31f

species distribution in, 58f, 60

species of, 132–133, 136

International Union for Conservation of 

Nature, 192, 193t

Irian Jaya, 35, 193t

Jamaica

endangered species in, 193t

Podocarpus urbanii in, 50–54, 130, 190

species distribution in, 45, 49t, 50

species of, 134–135

Japan, 2, 69, 189

podocarp leaf structure in, 125

podocarp longevity in, 123

and regeneration after disturbance, 

128, 130

and species dispersal, 31, 36

species distribution in, 58f, 122

species of, 133, 136

Java

fossil record from, 23f, 26, 28, 30–33

and species dispersal, 36, 38

species of, 133, 135, 136

Laos, 59t, 72–75t, 133, 135

leaf mass per area, 161

leaves, 86, 126f, 130t, 131–132

adaptations to, 63, 68, 124–125, 128, 

165–167, 191–192

comparison of between conifers and 

angiosperms, 159–162

flattening of, 2, 17, 191

longevity of, 70, 123, 161–162

nutrients in, 190–191

phylogenetic studies on, 3–4

size of, 60, 142, 149, 151, 171

structure of, 60, 63, 68

light

and competition with angiosperms, 

60, 68, 124

and growth, 90–91, 108–109, 124f

and hydraulic function, 60

and leaf structure, 124–125, 128, 167

and photosynthesis, 68

and regeneration, 86–88, 92, 94, 

126–127

lignotubers, 146–147, 152–153

logging, 54, 61, 68, 69, 93–95, 192

longevity

of leaves, 70, 123, 161–162

of podocarps, 17, 70, 71t, 94, 192

of podocarps in Asia, 111, 114, 123

of podocarps in New Zealand, 94, 

127–129, 131

and wood density, 123

lowland forest, 45, 60–62, 190

Madagascar, 21

endangered species in, 192, 193t

species diversity in, 80–81

species of, 137

magnesium, 67

Malaya, 59t, 62–63, 72–75t, 132–135

Malay Peninsula

endangered species of, 193t

and species dispersal, 33f, 36, 38

species of, 133

Malaysia, 59, 62, 132–133, 135

Malesia, 21, 57, 70–75t

altitudinal range of podocarps in, 

61–63

ecophysiology of podocarps in, 68

obstacles to studying podocarps in, 

71–72

population ecology in, 68–69

and species dispersal, 28, 30

species distribution in, 58f, 59t, 

60–61, 72–75t

species diversity in, 43–44, 57, 58f, 

59–60

species of, 22, 132, 135

manganese, 67

masting, 69

Mexico, 2, 189

species distribution in, 45, 49t, 69

species of, 137

mining, 67, 68, 192

molecular clock hypothesis, 2

molecular data, 2–7t, 44

Moluccas, 59t, 72–75t, 132–135

montane forest, 45, 60–62, 190

morphology, 3–4

mycorrhizal fungi. See arbuscular 

mycorrhizal fungi; ectomycorrhizal 

fungi

neotropics

altitudinal range of podocarps in, 

45–46, 48f

conservation concerns in, 54

fossil record from, 44

habitats in, 46–50

species distribution in, 44–45, 49t, 

190

species diversity in, 43–44

Nepal, 57

species of, 59t, 61, 72–75t, 132–133

New Britain, 132–133

New Caledonia, 63, 64–65f, 66–68, 71t

and catastrophic regeneration, 131

endangered species in, 193t

species diversity in, 43, 58f, 59–60, 

72–75t

species of, 132–135

New Guinea, 71t

and fire, 89

fossil record from, 23t, 25, 26, 36, 38

seed dispersal in, 69
200 • smithsonian contributions to botany

New Guinea (continued)

and species dispersal, 31f, 33, 34, 36, 

38, 190

species distribution in, 58f, 60–63, 66, 

102, 129–131

species diversity in, 59, 72–75t

species of, 132–136

New Hebrides, 132, 135

New Zealand, 71t

fossil record from, 33

and mycorrhizal infections, 176–177, 

185

podocarp foliage in, 126f

podocarp longevity in, 94, 127–129, 

131

and regeneration, 89–90, 92, 127–

129, 131

and role of disturbance, 88–89

and seed dispersal, 152

and soil quality, 91, 112, 120, 

122–124

species distribution in, 46, 58f, 

121–122, 125, 127

species of, 132

nickel, 67

nitrogen, 67

and acid phosphatase activity, 115

concentration of, 51

efficient use of by conifers, 70

fixation of, 112–113, 180–181

and growth, 50, 90–91

leaf concentration of, 190–191

and leaf longevity, 123

relationship of to podocarp abundance, 107–108, 110

reserves of, 95

nutrient residence time, 190–191

paleoclimates

to clarify relationships, 24

pollen used in reconstruction of, 45, 

129

palynological data, 44

Panama, 190

and regeneration, 131

species distribution in, 45, 48–50

Patagonia, 21–22

fossil record from, 28, 30, 33, 35–36

and species dispersal, 38

peat forest, 31–32, 60–63

Peru

species distribution in, 45, 49, 54, 

190

species of, 136

vulnerable species in, 193t

Philippines

endangered species in, 193t

and species dispersal, 33

species distribution in, 58f, 61

species diversity in, 59, 72–75t

species of, 132–136

phosphorous, 67

and acid phosphatase activity, 

111–112, 114

concentration of, 51

efficient use of by conifers, 70

and growth, 50

leaf concentration of, 190–191

and leaf longevity, 123

relationship of to podocarp abundance, 107–108, 110

photosynthesis, 70

and adaptation of flattened leaves, 

166–167

and canopy architecture, 124–125, 

130, 131

and drought, 191

and leaf life span, 161–162

low capacity for, 68, 86, 120

and nutrient use, 114, 190

photosynthetically active radiation, 87, 

91f, 92, 124, 125

phylloclades, 17, 167

phylogenetic relationships, 2–4, 7, 8f

“Podocarpoid” clade, 7

pollen, 34f, 35, 38, 44, 69

dispersal of, 70–71

fossil record of, 22–28, 30–31, 33–36, 

44, 80, 83–84, 190

and paleoclimate reconstruction, 45, 

129

types of, 22–24

wind dispersal of, 68, 119

population ecology, 68–69

potassium, 67

“Prumnopityoid” clade, 7

rainforest, tropical, 132–137, 159, 

165–166, 190

recreational tracks

as threat, 68

recruitment, 53, 69

regeneration, 114, 128–129

after disturbance, 125, 127–131

and gap-phase dynamics, 88–89

and light, 86–88, 92, 94, 126–127

patterns of, 80, 89–90

and shade tolerance, 88, 89–90, 125

relaxed-clock method, 2, 7

relaxed molecular clock, 2–3

resprouting, 63, 152–154, 191–192

after fire, 128, 147

root hairs, 176, 177f

root nodule, 177–178, 191

and mycorrhizal fungi, 180f, 181, 

183f, 184

and nitrogen fixation, 180–181

replacement of, 181, 184

roots

and acid phosphatase activity, 

111–115

and arbuscular mycorrhizal fungi, 

176–177, 179, 180f, 191

as beaded, 178–180

São Tomé, 81, 84, 193t

saprophytic fungi, 113–114

sclereids, 166f, 167, 168f, 169, 191

and cold temperatures, 172

and drought, 122, 170–171

seedlings

ecophysiology of, 68, 72

growth of, 68, 90–91, 120

seeds

animal dispersal of, 69, 146, 151, 

152, 193

dispersal of, 69–71, 84–85, 158

germination of, 69, 84, 142, 143, 

145f

production of, 69, 143, 145–146

shade tolerance, 71t, 88, 120

evolution of, 128–129

and flattened leaves, 191

and photosynthesis, 86

and regeneration, 88–90, 125

shoot flattening, 166–167, 169, 191

soil lipid biomarkers, 113–114, 115f

soil microbial communities, 113–114

soil quality, 92f, 102

and acid phosphatase activity, 111

and adaptation to drought, 63

and competition with angiosperms, 

60, 68, 70, 80, 120, 124

and growth, 108, 110f, 112f, 112t, 

124f, 130t

and leaf life span, 123

and light, 90–91, 124, 124f

and nutrient capture, 122–125, 

175–176

as poor and podocarp tolerance 

to, 67, 103–104, 106–109, 129, 

190–191

Solomon Islands, 59t, 61, 72–75t, 

132–135

South America, 21, 71t

fossil record from, 28, 30, 33, 35, 36, 

44

and impact of disturbance, 88–89

and regeneration, 89, 126–127

species distribution in, 44, 45, 47f, 

48–50, 54, 68–69, 71, 102, 121, 

131

species diversity in, 43

species dispersal, 26, 28, 30, 33–36, 

129, 172, 190

climatic impact on, 31, 33, 36, 37f, 

38
number 95 • 201

species distribution, 21–22, 58f, 59t, 

72–75t, 89, 189–190

in Africa, 81–85

in Amazonia, 44, 47f, 48

in Asia, 33, 57, 60–63, 102, 129–131, 

142

in Australasia, 131

in Australia, 60–62, 151

in Central America, 44–46, 48–50, 54

in neotropics, 44–45, 190

in New Caledonia, 66–67

in New Zealand, 46, 58f, 121–122, 

125, 127

in South America, 44, 45, 47f, 48–50, 

54, 68–69, 71, 102, 121, 131

species divergence

chloroplast used to estimate, 9, 11f, 

12f

time estimation of, 2, 7, 9

species diversity, 1–3, 72–75t

in Africa, 22, 80–81

in Asia, 59, 60

in Australasia, 129

in Australia, 59–60, 72–75t

influences on, 59–60

in Malesia, 43–44, 57, 58f, 59–60

in neotropics, 43–44

sporophylls

production of after fire, 143, 145–146

stem diameter, see “diameter, stem”

Sulawesi, 35, 59t, 72–75t

Sumatra

endangered species of, 193t

and species dispersal, 33, 36, 38

species distribution in, 62–63

species of, 59t, 61, 72–75t, 132–136, 

169

Sunda Islands, 59t, 72–75t, 132–136

Taiwan

endangered species in, 61, 193t

fossil record from, 28

species distribution in, 57

species of, 59t, 72–75t, 133, 134, 136

temperature

and embolism in cold climates, 86, 

171–172

and frost resistance, 121–122

and hydraulic function in cold 

climates, 159, 171–172

temporal stand replacement model, 

89–90

Thailand, 59t, 68, 72–75t, 132–133

Tonga, 72–75t, 193t

torus-margo pit, 86

tracheids, 85–86

Vanuatu, 59t, 60, 72–75t

Venezuela

endangered species of, 193t

species distribution in, 45, 48, 54

species of, 49t, 136, 137

Vietnam

fossil record from, 28, 31

and species dispersal, 36

species of, 59t, 62, 69, 72–75t, 

132–133, 135, 136, 170f

wood density, 120, 123, 169–170

Index of Scientific Names

Page numbers followed by “t” refer to a table; page numbers followed by “f” refer to a 

figure.

Acmopyle, 2

distribution of, 59t, 63

diversification shift point of, 16f

phylogeny of, 8f, 11f

shoot flattening of, 17, 166f, 167

Acmopyle pancheri, 5t, 65f

distribution of, 66–68, 72t

Acmopyle sahniana, 72t

conservation status of, 193t

as endangered, 61

phylogenetic analysis of, 5t

Actinostrobus acuminatus, 152

Aesculus, 178

Afrocarpus, 95

distribution of, 22, 81–82, 84, 85

and divergence time estimation, 9t

diversification shift point of, 16f

phylogeny of, 7, 8f, 11f, 80

shoot flattening of, 17

Afrocarpus dawei, 81t

Afrocarpus falcatus

arbuscular mycorrhizal fungi in, 92, 176

dispersal of, 84

distribution of, 81t, 85, 86, 91, 95

in dry conditions, 122, 129

life history properties of, 71t

phylogenetic analysis of, 5t

phylogeny of, 80

regeneration of, 69, 92–94

Afrocarpus gaussenii, 5t, 81t

Afrocarpus gracilior, 5t, 80, 81

Afrocarpus mannii, 5t, 81, 84, 193t

Afrocarpus usambarensis, 81t, 193t

Agathis, 104, 115, 162

Agathis australis, 6t, 178, 181
204 • smithsonian contributions to botany

Agathis borneensis, 63, 104

Agathis kinabaluensis, 104, 108, 110f, 

111–113

Alisporites, 24, 25f

Alisporites similis, 26

Alnus, 34f

Alseis blackiana, 131

Angophora hispida, 151

Apterocladus, 22

Araucaria, 24, 44, 62, 67, 69, 181

Araucaria angustifolia, 71

Araucaria biramulata, 6t

Araucariacites, 24, 26

Araucaria heterophylla, 6t

Araucaria nemorosa, 68

Archaeospora, 176

Aristotelia serrata, 128

Beilschmiedia tawa, 121

Betula, 124

Callialasporites, 22

Callitris, 70

Calophyllum, 61

Castanopsis, 62

Casuarina, 31, 32, 124

Cathaysia, 22

Cecropia, 159

Ceiba pentandra, 131

Classopollis, 24–26

Clethra occidentalis, 50, 51

Cryptomeria japonica, 123

Cunonia, 66

Cyrilla racemiflora, 50

Dacrycarpidites antarcticus, 23f, 23t

Dacrycarpus

altitudinal range of, 22, 61, 105, 106, 

129

dispersal of, 33, 36, 38, 190

distribution of, 59t, 60, 62, 63, 104

and divergence time estimation, 9t

diversification shift point of, 16f

phylogeny of, 7, 8f, 11f

pollen of, 23

shoot flattening of, 17, 166f

and soil lipids, 114t, 115f

Dacrycarpus cinctus, 5t, 61, 72t, 134

Dacrycarpus compactus, 134

distribution of, 61, 62, 72t

as fire tolerant, 131

phylogenetic analysis of, 5t

Dacrycarpus cumingii, 72t, 136

Dacrycarpus dacrydioides, 71t, 126f

and catastrophic disturbance, 

127–128, 131

phylogenetic analysis of, 5t

Dacrycarpus expansus, 72t, 131, 136

Dacrycarpus imbricatus, 70, 101, 105f, 

106f, 135

and acid phosphatase activity, 112

altitudinal range of, 61, 62, 102, 

104–105

diameter of, 110f

dispersal of, 33f, 37f

distribution of, 72t, 131

life history properties of, 71t

and nitrogen fixation, 112–113

phylogenetic analysis of, 5t

pollen of, 28

and seed dispersal, 69

and soil quality, 113, 114, 115f

Dacrycarpus kinabaluensis, 136

altitudinal range of, 61, 62, 105

distribution of, 72t, 108

size of, 110f, 111, 112f

Dacrycarpus linifolius, 9t

Dacrycarpus mucronatus, 9t

Dacrycarpus steupii, 72t, 136

Dacrycarpus vieillardii, 132

altitudinal range of, 66

distribution of, 67, 72t

and disturbance, 131

phylogenetic analysis of, 5t

Dacrydium

and acid phosphatase activity, 

113–114

altitudinal range of, 22, 61, 105, 106, 

129

animal dispersal of seeds of, 158

and arbuscular mycorrhizal fungi, 181

dispersal of, 36, 37f, 38, 190

distribution of, 59t, 63

and divergence time estimation, 9t

diversification shift point of, 16f

fire intolerance of, 131

fossil record of, 30–33

habitats of, 31–32, 60

juveniles of, 62

leaves and stems of, 124

phylogeny of, 7, 8f, 11f

pollen of, 23f, 23t, 24, 30

and soil lipids, 114t, 115f

and soil quality, 104, 130

Dacrydium araucarioides, 5t, 66, 71t, 

72t, 133

Dacrydium balansae, 5t, 66, 67, 72t, 

132

Dacrydium beccarii, 31, 61, 73t, 134

Dacrydium comosum, 73t, 135

conservation status of, 61, 69, 193t

Dacrydium cornwallianum, 61, 63, 73t, 

136

Dacrydium cupressinum

carbon uptake by, 123, 130

foliage of, 126f

growth of seedlings of, 127

life history properties of, 71t

light use by, 125

phylogenetic analysis of, 5t

and regeneration, 128

roots of, 179f, 183f

Dacrydium elatum, 73t, 133

Dacrydium ericoides, 73t, 135, 193t

Dacrydium franklinii, 24

Dacrydium gibbsiae, 73t, 134

diameter of, 110f

and soil quality, 62, 111–112

Dacrydium gracile, 73t, 102, 134

conservation status of, 193t

diameter of, 110f, 111f

and nitrogen fixation, 112–113

and soil quality, 114, 115f

Dacrydium guillauminii, 65f, 73t, 132

conservation status of, 193t

habitats of, 66–67

phylogenetic analysis of, 5t

pollen of, 23t, 24

Dacrydium laxifolium, 24

Dacrydium leptophyllum, 61, 73t, 136, 

193t

Dacrydium lycopodioides, 5t, 66, 73t, 

135

Dacrydium magnum, 73t, 132

Dacrydium medium, 61, 73t, 135

Dacrydium nausoriense, 5t, 61, 73t, 

133, 193t

Dacrydium nidulum, 5t, 63, 71t, 73t, 132

Dacrydium novo-guineense, 73t, 131, 

135

Dacrydium pectinatum, 61–63, 73t, 

104, 130, 132

Dacrydium spathoides, 61, 73t, 135

Dacrydium xanthandrum, 61, 73t, 134

Dasyphyllum diacanthoides, 127

Doryanthes excelsa, 151

Eidothea hardeniana, 70

Ephedripites, 26

Eucalyptus, 124, 152

Eucalyptus marginata, 150f

Eucryphia milliganii, 120

Exesipollenites tumulus, 24

Falcatifolium, 22, 63, 130

distribution of, 59t, 60

and divergence time estimation, 9t

diversification shift point of, 16f

phylogeny of, 7, 8f, 11f

shoot flattening of, 17, 166f, 167

Falcatifolium angustum, 61, 73t, 133, 

193t

Falcatifolium falciforme, 73t, 108, 133

altitudinal range of, 62
number 95 • 205

diameter of, 110f, 111f

life history properties of, 71t

and nitrogen fixation, 112–113

phylogenetic analysis of, 5t

as shade tolerant, 131

size of, 51, 69–70

Falcatifolium gruezoi, 5t, 73t, 135

Falcatifolium papuanum, 73t, 136

Falcatifolium taxoides, 5t, 66, 73t, 134

Parasitaxus usta as parasitic to, 67, 

130, 184–185

Ficus, 109, 114

Fitzroya cupressoides, 123

Foliolatus, 8f, 142, 149, 151

Garcinia, 61

Ginkgo biloba, 152

Gleichenia bolanica, 62

Glomus, 176

Gnetum, 131, 165

Gymnostoma, 31, 178

Gymnostoma deplancheanum, 66

Gymnostoma nobilis, 31

Halocarpus, 9t, 16f, 124

phylogeny of, 7, 8f, 11f

Halocarpus bidwillii, 5t, 122, 128

Halocarpus biformis, 5t, 123, 125, 126f

Halocarpus kirkii, 5t

Harrisiocarpus, 22

Hedyosmum arborescens, 51

Isoglossa woodii, 86, 93

Juniperus procera, 176

Lagarostrobos, 2, 9t, 16f

phylogeny of, 7, 8f, 11f

Lagarostrobos franklinii, 120, 123, 171f

phylogenetic analysis of, 5t

and regeneration, 127, 128

Laureliopsis philippiana, 127

Lepidothamnus, 16f, 43, 124

phylogeny of, 7, 8f, 11f

Lepidothamnus fonkii, 5t, 122

Lepidothamnus intermedius, 123, 128, 

179f

Lepidothamnus laxifolius, 5t, 24

Lithocarpus, 62, 103, 114t, 115f

Lithocarpus clementianus, 113, 115f

Lygistepollenites florinii, 23f, 23t, 24

Lyonia octandra, 51

Macaranga, 109, 114, 159

Manoao, 9t, 16f, 124

phylogeny of, 7, 8f, 11f

Manoao colensoi, 5t, 123, 179f

Masculostrobus warrenii, 22

Mataia podocarpoides, 9t

Melicytus ramiflorus, 128

Metapodocarpoxylon, 24

Metasequoia, 167

Metrosideros, 66

Microcachrydites antarcticus, 26

Microcachrys, 2, 23t, 124

diversification shift point of, 16f

fossil record of, 35, 36

phylogeny of, 8f, 11f

Microcachrys antarcticus, 23t, 35

Microcachrys tetragona, 5t

Microstrobos, 2, 124

Microstrobos fitzgeraldii, 5t

Microstrobos niphophilus, 5t

Nageia

dispersal of, 28, 30

distribution of, 59t

and divergence time estimation, 9t

diversification shift point of, 16f

habitats of, 22, 60, 129

phylogeny of, 7, 8f, 11f, 80

pollen of, 23f

shoot flattening of, 17, 68, 132, 

166–167

Nageia fleuryi, 68–69, 131, 133

distribution of, 73t

as endangered, 61

habitat of, 62

phylogenetic analysis of, 5t

Nageia formosensis, 5t, 73t

Nageia maxima, 63, 73t, 132, 193t

Nageia motleyi, 62, 132

distribution of, 73t

Nageia nagi, 133

distribution of, 73t

flattened leaves of, 125

phylogenetic analysis of, 5t

and regeneration, 128

sex ratio of, 69

size of, 51

and soil quality, 122

Nageia wallichiana, 68, 70, 133

distribution of, 73t

habitats of, 61–63, 131

life history properties of, 71t

phylogenetic analysis of, 5t

Nemuaron, 66

Nothodacrium, 22

Nothodacrium warrenii, 9t, 22

Nothofagus, 61, 121

Nothofagus grandis, 63

Nothofagus nitida, 126–127

Oncosperma, 32

Palaquium, 114t, 115f

Palaquium rioense, 113, 115f

Pancheria, 66

Pandanus, 63

Papuacedrus, 61

Papuacedrus papuana, 61

Paracryphia, 66

Parasitaxus, 9t, 16f, 59t, 63

phylogeny of, 7, 8f, 11f

Parasitaxus usta, 5t, 66, 73t, 133

conservation status of, 68, 193t

as parasitic to Falcatifolium taxoides,

67, 129–130, 184–185

Pherosphaera, 8f, 11f, 16f

Phyllocladites palaeogenicus, 23f, 23t

Phyllocladus, 3, 102

dispersal of, 36, 38, 190

distribution of, 22, 59t, 103

diversification shift point of, 16f

phylogeny of, 7, 8f, 11f

pollen of, 23, 23t, 34–35

shoot flattening of, 17, 166f, 167

Phyllocladus alpinus, 5t, 122, 128, 177f

Phyllocladus aspleniifolius, 5t

Phyllocladus hypophyllus, 134

altitudinal range of, 105, 130

diameter of, 110f

distribution of, 61, 73t

leaf nutrients of, 190–191

phylogenetic analysis of, 5t

pollen of, 23f

shoot flattening of, 167

and soil quality, 111–113

Phyllocladus toatoa, 5t

Phyllocladus trichomanoides, 5t

Picea balfouriana, 123

Pinus, 34f, 124, 158, 169

Pinus cubensis, 46

Pinus krempfii, 169, 170f

Pinus merkusii, 169

Pinus occidentalis, 131

Pinus radiata, 120

Podocarpidites, 23f, 23t, 24, 26

Podocarpoxylon, 26

Podocarpus, 95

accessory transfusion tissue of, 167

in Africa, 79–80

altitudinal range of, 45–46, 48, 61, 

129

animal dispersal of seeds of, 158

antimicrobial chemicals in bark of, 

123

and arbuscular mycorrhizal fungi, 181

conservation of, 54

as dioecious, 68

dispersal of, 28, 29f, 30, 35–36, 38

distribution of, 25f, 47f, 49t, 57, 59t, 

82, 84

and divergence time estimation, 9t
206 • smithsonian contributions to botany

Podocarpus (continued)

diversification shift point of, 16f

diversity of, 2, 43–44, 60, 63

as dominant, 87–89, 94

and fire intolerance, 128

fossil record of, 22, 26, 30

habitats of, 22, 60, 129

phylogeny of, 7, 8f, 11f

pollen of, 23f, 23t, 24, 28, 158

shade tolerance of, 132

shoot flattening of, 17, 166f

and soil quality, 130

Podocarpus acuminatus, 48f, 136

Podocarpus affinis, 5t, 61, 73t, 193t

Podocarpus alpinus, 5t

Podocarpus angustifolius, 45, 46, 54, 

193t

Podocarpus annamiensis, 5t, 73t

Podocarpus archboldii, 73t, 135

Podocarpus aristulatus, 5t, 193t

distribution of, 45–46, 48f, 49t, 50, 

131

Podocarpus atjehensis, 73t, 136

Podocarpus beecherae, 67, 73t, 133, 

193t

Podocarpus borneensis, 74t, 136

Podocarpus bracteatus, 74t, 136

Podocarpus brasiliensis, 44, 136

Podocarpus brassii, 6t, 74t, 135

Podocarpus brevifolius, 74t, 136, 193t

Podocarpus buchholzii, 44, 47f, 48f, 

136

Podocarpus capuronii, 81, 193t

Podocarpus celatus, 45–48f

Podocarpus chinensis, 6t, 74t

Podocarpus chingianus, 74t

Podocarpus colliculatus, 67, 74t

Podocarpus confertus, 61, 74t, 132

Podocarpus coriaceus, 45, 46, 48f, 54

Podocarpus costalis, 6t, 61, 74t, 133, 

193t

Podocarpus costaricensis, 45, 47f, 48f, 

193t

Podocarpus crassigemmis, 74t, 135

Podocarpus cunninghamii, 6t

Podocarpus decumbens, 64f, 66, 67, 

74t, 193t

Podocarpus deflexus, 74t, 135, 193t

Podocarpus degeneri, 74t

Podocarpus dispermus, 6t, 62, 74t, 136, 

167

Podocarpus drouynianus, 69, 141–142

distribution of, 143, 144f, 144t

as drought resistant, 122, 171

as fire resistant, 128

growth of, 146

leaves of, 142, 149

lignotubers of, 146–147, 152–153

morphological adaptations of, 151, 

153

phylogenetic analysis of, 6t

population structure of, 149

pyrogenic reproduction of, 151, 153

and resprouting, 153, 154, 191–192

seeds of, 142, 143, 145f, 146, 

151–152

size of, 150f

and soil quality, 152

Podocarpus elatus, 6t, 74t

Podocarpus elongatus, 6t, 80, 81, 152

Podocarpus ensiculus, 80

Podocarpus fasciculus, 74t

Podocarpus gibbsiae, 61, 74t, 112–113, 

135, 193t

Podocarpus glaucus, 74t, 135

Podocarpus globulus, 61, 74t, 133, 193t

Podocarpus glomeratus, 47f, 48f, 136

Podocarpus gnidioides, 6t, 66, 74t, 135

Podocarpus grayae, 68, 74t, 131, 151, 

171f

Podocarpus guatemalensis, 6t, 54, 190

distribution of, 45, 47–48f, 49t, 50

Podocarpus hallii, 71t, 122, 127

Podocarpus henkelii, 6t, 80, 81t, 86

Podocarpus hispaniolensis, 45, 48f, 49t, 

54, 193t

Podocarpus humbertii, 47f, 81t, 193t

Podocarpus ingensis, 46–48f, 136

Podocarpus insularis, 74t, 132

Podocarpus lambertii, 6t, 44, 48f, 

68–69, 136

Podocarpus latifolius, 6t, 68, 80–81, 

85f, 95

distribution of, 81t, 82f, 86, 94

and gap-phase dynamics, 88

habitats of, 87, 92

life history properties of, 71t

regeneration of, 80, 90, 127

seeds of, 84, 91f

Podocarpus laubenfelsii, 63, 74t, 134, 

193t

Podocarpus lawrencei, 6t, 71t, 122

Podocarpus ledermannii, 74t, 133–134

Podocarpus levis, 74t, 134

Podocarpus longifoliolatus, 6t, 66, 67, 

74t, 193t

Podocarpus lophatus, 61, 74t, 136, 193t

Podocarpus lucienii, 66, 74t

Podocarpus macrocarpus, 74t, 136

Podocarpus macrophyllus, 6t, 74t, 136, 

180

Podocarpus madagascariensis, 81t

Podocarpus magnifolius, 45, 47f, 48f, 

136

Podocarpus matudae, 6t, 69, 137

distribution of, 45, 48f, 49t

Podocarpus micropedunculatus, 74t, 

133

Podocarpus milanjianus, 37f, 80–81

Podocarpus monteverdeensis, 45

Podocarpus nakaii, 61, 74t, 134, 193t

Podocarpus neriifolius, 131–133, 136, 

170f

distribution of, 61, 74t

habitats of, 62, 63, 71

phylogenetic analysis of, 6t

pollen of, 28

seeds of, 69

Podocarpus nivalis, 6t

Podocarpus novae-caledoniae, 65f, 66, 

67, 74t

Podocarpus nubigenus, 6t, 71t, 123, 

126–127

Podocarpus occidentalis, 45

Podocarpus oleifolius, 45–49, 54

Podocarpus palawanensis, 74t, 193t

Podocarpus pallidus, 61, 74t, 193t

Podocarpus parlatorei, 45, 47f, 48f

Podocarpus pendulifolius, 48f, 193t

Podocarpus perrieri, 81, 193t

Podocarpus pilgeri, 61, 74t

Podocarpus polyspermus, 66, 74t, 131, 

193t

Podocarpus polystachyus, 6t, 28, 74t, 

133

Podocarpus pseudobracteatus, 74t, 134

Podocarpus purdieanus, 45, 50, 54, 193t

Podocarpus ridleyi, 74t, 135

Podocarpus roraimae, 47f, 48f, 137

Podocarpus rostratus, 81, 193t

Podocarpus rotundus, 75t, 134

Podocarpus rubens, 75t, 134

Podocarpus rumphii, 6t, 75t, 136

Podocarpus rusbyi, 47f, 48f

Podocarpus salignus, 6t, 123

Podocarpus salomoniensis, 75t

Podocarpus sellowii, 44, 47f, 48f, 49t, 

136

Podocarpus smithii, 6t, 75t, 134

Podocarpus spathoides, 61, 75t, 134

Podocarpus spinulosus, 129, 134, 

141–142

chichi structure of, 152, 153

distribution of, 143, 144f, 144t

as fire resistant, 128

growth of, 146

leaves of, 142, 149

lignotubers of, 146–147, 153

morphological adaptations of, 151, 

153

phylogenetic analysis of, 6t

population structure of, 149, 151

reproduction of, 151

and resprouting, 152–154
number 95 • 207

seeds of, 142, 143, 145f

and soil quality, 152

stems of, 142, 147–149

Podocarpus sprucei, 44, 47f, 48f, 49t, 

137

Podocarpus steyermarkii, 47f, 48f, 137

Podocarpus strzeleckianus, 9t

Podocarpus subtropicalis, 75t

Podocarpus sylvestris, 6t, 66, 67, 75t

Podocarpus tepuiensis, 44, 45, 47f, 

49–50, 137

Podocarpus teysmannii, 75t, 133

Podocarpus totara, 6t, 71t, 120–122, 

182f

and catastrophic regeneration, 

127–128, 131

Podocarpus trinitensis, 45, 54

Podocarpus urbanii, 134–135

distribution of, 45, 48f, 49t, 50

growth of, 130

leaf nutrients of, 190

mortality rates of, 52–54

and soil quality, 50–52

Podocarpus woltzii, 81, 137

Protophyllocladoxylon, 24

Prumnopitys, 4, 181

dispersal of, 28, 30

distribution of, 22, 43, 45, 59t, 63

and divergence time estimation, 9t

diversification shift point of, 16f

habitats of, 60

phylogeny of, 7, 8f, 11f

pollen of, 23f

shoot flattening of, 17, 166f

Prumnopitys andina, 6t

Prumnopitys exigua, 45

Prumnopitys ferruginea, 6t, 126f

life history properties of, 71t

regeneration of, 125, 127

root system of, 177f, 184

Prumnopitys ferruginoides, 6t, 66, 67, 

75t

Prumnopitys harmsiana, 45, 54

Prumnopitys ladei, 6t, 71t, 75t, 136

Prumnopitys limaniae, 9t

Prumnopitys montana, 45, 137

Prumnopitys opihiensis, 9t

Prumnopitys standleyi, 45, 136

Prumnopitys taxifolia, 6t, 71t, 126f, 

127–128

Quercus, 44

Quintinia, 66

Rapanea vaccinioides, 62

Retrophyllum, 80

distribution of, 28, 43, 45, 59t, 63, 

66

and divergence time estimation, 9t

diversification shift point of, 16f

phylogeny of, 7, 8f, 11f

shoot flattening of, 17, 166f

Retrophyllum comptonii, 6t, 63, 135

distribution of, 66, 67, 75t

Retrophyllum minus, 64f, 66–67, 75t, 

133, 193t

Retrophyllum rospigliosii, 45, 54, 136, 

193t

Retrophyllum vitiense, 6t, 75t

Rhizobium, 180

Rhizophora, 32

Rhus tomentosa, 87

Rissikia, 9t, 22

Rugubivesiculites reductus, 26

Saxegothaea, 17

distribution of, 2, 43

diversification shift point of, 16f

phylogeny of, 8f, 11f

pollen of, 22, 24, 36

Saxegothaea conspicua, 6t, 71t, 123, 

126–128

Scarburgia, 22

Sciadopitys, 178

Sequoia, 167

Shorea ovata, 63

Shorea revoluta, 63

Sphenostemon, 66

Stalagma samara, 22

Stirlingia latifolia, 151

Sundacarpus

distribution of, 59t, 60

phylogeny of, 4, 7, 8f, 11f

shoot flattening of, 166f, 167

Sundacarpus amarus, 6t, 69, 135

distribution of, 61–63, 75t

Synoum, 151

Syzygium, 103

Tasmannia lanceolata, 159

Taxodium, 167

Taxus, 158

Telopea speciossima, 151

Toona australis, 131

Trimenia, 66

Trisaccites, 23

Tristaniopsis, 103, 113, 114t, 115f

Tsuga, 24

Tsuga sieboldii, 123

Vaccinium meridionale, 50

Weinmannia, 44

Weinmannia racemosa, 128

Weinmannia trichosperma, 126–127

Widdringtonia nodiflora, 152

Wollemia, 176

Zygogynum, 66
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Figure captions should be provided in a separate MS 

Word file.

Figures (e.g., photographs, line art, maps) should be numbered sequentially (1, 2, 3, etc.) in the order called out; be 

placed throughout text, not at end of manuscript; have all 

components of composites lettered with lowercase letters and 

described in the caption; include a scale bar or scale description, if appropriate; include any legends in or on the figure 

rather than in a caption. 

Art must not be embedded in the main text.

Figures must be original and submitted as individual TIFF 

or EPS files. Resolution for art files must be at least 300 dpi 

for grayscale and color images and at least 1200 dpi for line 

art. Electronic images should measure no more than 100% 

and no less than 75% of final size when published. JPG files 

will not be accepted. Color images significantly increase 

costs so should be included only if required. Funding for 

color art is subject to approval by SISP and the Publications 

Oversight Board.

In-text references should be used rather than bibliographic notes and should follow the author-date system in the 

following format: “(author last name, year)” or “. . . author 

(year)”; “(author, year:page used within the text)” or “. . . 

author (year:page).” A full citation should be included in a 

“References” section.

Endnotes are to be used in lieu of footnotes and should 

be keyed manually into a separate MS Word file, in a section titled “Notes”. Notes should not contain bibliographic 

information. Manually type superscript numerals in text and 

use full-sized numerals at the beginning of each note in the 

“Notes” section. SISP will determine the best placement of the 

notes section, either at the end of each chapter or at the end 

of the main text.

References should be in alphabetical order, and in chronological order for same-author entries. Each reference should 

be cited at least once in main text. Complete bibliographic 

information must be included in all citations (e.g., author/editor, title, subtitle, edition, volume, issue, pages, figures). For 

books, place of publication and publisher are required. For 

journals, use the parentheses system for volume(number):pagination [e.g., “10(2):5–9”]. Do not use “et al.”; all authors/

editors should be included in reference citations. In titles, 

capitalize first word, last word, first word after colon, and all 

other words except articles, conjunctions, and prepositions. 

Examples of the most common types of citations are provided 

in the SISP Manuscript Preparation and Author Style Guide. 

For questions regarding the guidelines, please email SISP at 

schol.press@si.edu. 

requirements for smithsonian series publication