# Patterns of climber distribution in temperate forests of the Americas

Annik Schnitzler, Javier Amigo, Brack Hale, Christophe Schnitzler

► To cite this version:

Annik Schnitzler, Javier Amigo, Brack Hale, Christophe Schnitzler. Patterns of climber distribution in temperate forests of the Americas. Journal of Plant Ecology, 2016, 9 (6), pp.724-733. 10.1093/jpe/rtw012. hal-01780349

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# Patterns of climber distribution in temperate forests of the Americas

Annik Schnitzler<fnref n="1" />,*, Javier Amigo<fnref n="2" />, Brack Hale<fnref n="3" /> and Christophe Schnitzler<fnref n="4" />

## Abstract

### Aims and Methods

We propose a standard protocol at the landscape to continental scale for examining to what extent the range of ecological conditions found in temperate latitudes explains the variations in climber species richness and traits. The protocol was tested in forests of the two Americas. The data set included 151 climber species. We selected four categorical traits and grouped these species into six clusters with regard to these traits. Floristic records of American forests were first gathered into alliances, second combined with bioclimatic indices (rainfall, temperature, continentality). We obtained a total of 59 vegetational units in which we calculated values of climber species richness and proportion of clusters. Vegetational units were ultimately gathered into five forest formations (characterized by leaf longevity). Wetlands and uplands were considered separately.

### Important Findings

Our results emphasize clear trends in large-scale patterns of climber distribution, independently of taxonomy. Climber species richness (in particular woody climbers) peaks in moist and warm upland forests with oceanic climates, and where conifers are rare. In flooded areas, climber richness is also very high and peaks in seasonally flooded large floodplains. In ecological conditions of frost, dryness or lack of nutrients, climber species richness, abundance and trait diversity decline, resulting in the dominance of small, twining and deciduous life traits.

**Keywords:** American forest, bioclimatic indices, climber, life traits, standard protocol, species richness

Received: 25 July 2015, Revised: 6 January 2016, Accepted: 7 February 2016

## INTRODUCTION

Climbers (both woody liana and herbaceous vines) are groups of plants characterized by flexible, narrow and fast-growing axes with a diversity of attachment types, which allow them to reach rapidly the highest forest strata in economizing support tissues without sliding or falling (Gentry 1991; Isnard and Silk 2009). Attachment types range from simple sprawling over other plants, scrambling, hooks and stem twining, to more specialized mechanisms, such as tendrils, adventitious roots and other adhesive structures. Generally climbers with adventitious roots and adhesive structures colonize broad trunks of large canopy trees, while other climber structures (tendrils) better exploit smaller diameters of secondary tree and shrub axes (Hegarty 1991). Climbing mechanisms are relatively stable at different latitudes, indicating that modes

of climbing do not respond to variations in mean annual temperature and precipitation (Gallagher and Leishmann 2012). They however vary during forest types and successful processes in both the Tropics (De Walt et al. 2000; Schnitzler et al. 2015) and the temperate area. For example, climbers of temperate alluvial deciduous forests are significantly richer in adventitious roots than upland forests; evergreen Mediterranean forests are rich in hook species (Schnitzler and Arnold 2010).

The stratum that climbers can reach in the forest is also dependent on potential height, inherited architectural model (Oldeman 1990) and growth habit. Investment in woody tissues generally helps climbers to establish in upper layers (Carter and Teramura 1988; Carrasco-Urra and Gianoli 2009; Hegarty and Caballé 1991; Munoz et al. 2003; Schnitzer and Carson 2000), while herbaceous vines live preferentially

<footnote n="1">¹ Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), UMR 7360 Université de Lorraine, Metz, France</footnote>

<footnote n="2">² Laboratorio de Botánica, Facultad de Farmacia, Universidad de Santiago de Compostela, A Coruña, Spain</footnote>

<footnote n="3">³ Franklin University Switzerland, Sorengo, Switzerland</footnote>

<footnote n="4">⁴ Faculté des Sciences du Sport, Unistra, Université de Strasbourg, Strasbourg, France</footnote>

<footnote>*Correspondence address. LIEC - UMR 7360 CNRS Université de Lorraine Campus Bridoux Rue du Gal Delestraint, F-57070 Metz, France. Tel: +33-(0)387-37-84-27; Fax: +33-(0)387-37-85-12; E-mail: annik.schnitzler@univ-lorraine.fr</footnote>
in understoreys or gaps. Woodiness is also known to be negatively correlated with extremes of minimum temperature, which increase the risk of embolism under freezing conditions. Embolism can lead to the rupturing of vessel elements, which renders the vascular system inoperable and ultimately kills the plant (Davis et al. 1999; Ewers 1985).

Embolism risks thus limit climber distribution patterns and species richness compared to the tropical and subtropical regions (i.e. >30° latitude) as well as at altitudes where frost occurs (Balfour and Bond 1993; Hu et al. 2010; Jimenez-Castillo et al. 2007; Jimenez-Castillo and Lusk 2013; Schnitzer and Bongers 2002; Schnitzer 2005). But there is a significant spectrum of variation between the relative proportions of herbaceous and woody climbers along latitudes (Gallagher et al. 2011; Gallagher and Leishman 2012).

Adaptations to embolism are however many: development of anomalous secondary growth that protects their vascular system (Hegarty 1991), increase in root pressures, flushing leaves relatively late in the spring and/or dropping leaves early in the autumn (Rundel and Franklin 1991; Scholander et al. 1955). Evergreen lianas are thus to use such strategies, which explain their vulnerability to disruptions of the vascular system, and their limited distribution to climates with mild winter (Jimenez-Castillo et al. 2007; Rundel and Franklin 1991).

The leaf characteristics of the dominant trees in temperate forests also influence climber distribution patterns through nutrient cycles. Deciduous forests offer nitrogen peak during the spring litter decomposition. The litter of evergreen broad-leaf forests has lower available nitrogen contents, and conifer litter often decomposes slowly, particularly in cold regions and acidic soils (Schnitzler and Arnold 2010). Length of the growing season, rainfall and temperatures (Teramura et al. 1991); disturbance regime (Allen et al. 1997, 2005), water constraints in floodplains (Schnitzler and Heuzé 2006; Schnitzler et al. 2007; Trémolières et al. 1998) or forest architecture linked to light, hosts and age (Carrasco-Urra and Gianoli 2009; Hegarty and Caballé 1991; Schnitzler 1995). Globally these studies give evidence that climbing plants of temperate latitudes are distinctive representatives of taxonomic and functional diversities compared to lower latitudes.

In this study, responses of climbers to temperate climates and forest habitats were considered at the landscape to continental scale of the Americas. Compared to Eurasia, Africa and Australia, American forests spread much longer in latitude (from 30 to 55° latitude north and south). They also grow in a high variety of climatic conditions and forest types. Floristic data are taxonomically distinct between North and South America (Hofstede et al. 2001).

In this protocol, we also investigated the variations in climber functional traits and/or groups of them. Traits are well-defined, measurable morphological, physiological and phenological properties of organisms which improve organismal performance in constraint environments. They are usually measured at the individual level and used comparatively across species

(McGill et al. 2006; Westoby and Wright 2006). On the basis of available literature, we chose three traits relating to height gain (climbing modes; potential height and growth habit) and one relating to metabolic rhythms (foliation phenology).

To characterize the conditions under which climbers are likely to occur in the temperate forests, the following questions are posed (i) How does variation in bioclimatic variables influence climber species richness and functional traits? (ii) Do it exists relationships between climber traits and species richness, and forest types?

# METHODS

## Data sources

Floristic lists from South American forests were extracted from phytosociological studies of the temperate regions of Chile and Argentina (i.e. the mid Chilean-Patagonian and Valdivian-Magellanic regions). The Argentina/Uruguay territory, precisely delimited in Rivas-Martinez et al. (2011), has not been included because of its too high degree of deforestation and anthropization (Cabrera and Willink 1973). About 755 plot floristic records were extracted from the literature (Amigo et al. 2000, 2004, 2011; Dollenz 1980, 1982a, 1982b; Eskuche 1999; Hildebrand-Vogel et al. 1990; Oberdorfer 1960; Pollmann 2001; Roig et al. 1985a, 1985b; Ramirez et al. 1983, 1989, 2004; San Martin et al. 1984; San Martin et al. 1991).

North American data come from temperate regions of the USA. They were extracted from 703 plot floristic records published in the online VegBank database (www.vegbank.org/vegbank/index.jsp) and from data from the literature (Collins and Wein 1993; Rivas-Martinez 1997; Rivas-Martinez et al. 1999a, 1999b).

The mean surface area of all plots was evaluated of about 100 m².

The list of climbers was extracted from these floristic records.

## Bioclimatic classification of forest types

The system developed by Rivas-Martinez (2004) is a global bioclimatic classification system that quantifies key bioclimatic indices reflective of vegetation distributions are: (i) thermotypes (i.e. hot-cold gradients), (ii) ombrotypes (i.e. wet-dry gradients, expressed with an ombrothermic Index $I_o$) and (iii) a assemblage between dry-wet and oceanic-continental gradients which gives the continentality Index $I_c$. More precisely this index expresses the range between the average temperatures of the warmest and coldest months of the year in degrees Celsius (online supplementary Appendix S1).

We only used data which gave monthly data of rainfall and temperature for fitting with the bioclimatic classification of Rivas-Martínez (2004). Climatic data were extracted from the Worldwide Bioclimatic Classification System:

http://www.globalbioclimatics.org/book/namerica2/namerica.htm for North America;
http://www.globalbioclimatics.org/book/namerica2/
namerica.htm for South America.

They were completed by geobotanical sources when avail-
able (mostly in South America: Amigo and Ramirez 1998;
Luebert and Pliscoff 2006).

Assemblage of floristic data and bioclimates: the
concept of vegetational unit

Floristic records were grouped into alliances, which are more
compositionally and structurally variable, and also more
geographically widespread (Jennings et al. 2009; Oberdorfer
1960). The name of a given alliance includes one or several
dominant tree species followed with FA for Forest Alliance.
The 755 plots from South America belong to 13 forest alliances,
already defined in Amigo and Rodríguez-Guitián (2011),
Amigo et al. (2011), Hildebrand-Vogel et al. (1990) and Roig
(1998). In North America, the 701 plots from VegBank were
gathered into 38 alliances defined by this one-line VegBank
classification.

We calculated the three bioclimatic indices within the cli-
matic space of each of the 51 alliances. We found only 33 dif-
ferent bioclimatic (thermotype, ombrotype, continentality) in
the two hemispheres considered separately, corresponding to
the following cases

1. *One alliance-one specific bioclimatic assemblage.* Alliances are restricted to one specific bioclimate assemblage. This case corresponds to 42% of the total number of alliances, generally in North America.

2. *Several alliances-one bioclimatic assemblage.* Several alliances are found in the same bioclimate assemblage. This case corresponds to 44.2% of the total number of alliances, generally in North America.

3. *One alliance-several bioclimatic assemblages.* Some alliances are geographically widespread, and found in several bioclimate assemblages. This case corresponds to 13% of the total number of alliances, mostly in South America.

Finally we provided a global set of 59 vegetational units (26 for South America and 33 for North America, see Figs 1 and 2).

Classification of vegetational units with regard to forest
formations and topographical positions

As South and North America present taxonomically distinct
floras, the vegetational units were integrated within a higher
category called ‘forest formation’. This concept is based on
leaf characteristics of dominant canopy trees (online VegBank
database). Five different forest formations were present in the
data set: evergreen rain forests (RF), needle-leaf evergreen
forests (NLE), deciduous forests (DF), mixed needle-leaf ever-
green-deciduous forests (NEDF) and mixed broadleaf ever-
green-deciduous forests (EDF). Within each forest formation,
we considered separately wetland from upland vegetational
units.

Evaluation of species richness per
vegetational unit

The mean values of total species richness (MTSR) and climber
species richness (MCSR) per vegetational unit were calculated
from the floristic lists. When several alliances were integrated
into one vegetational unit, we put together all floristic lists
whatever the alliance, and calculated the global mean values
of species richness and climber species richness. The mean
proportion of climbers per unit was deduced from these two
mean values.

The global set of 59 vegetational units, their latitudinal
range, bioclimatic indices, the number and name of the alli-
ances, their classification with regard to forest formations and
topographical positions, and their richness values are pre-
sented in supplementary Appendix S2.

Statistical investigation with regard to climber
species richness of the vegetational units

Climber species richness of vegetational units across
bioclimatic indices

In a first time, we investigated possible associations between
the mean climber species richness (MCSP) and the different
assemblages of bioclimatic indices found for each of the 59
vegetational units. For this purpose, we performed a K-means
clustering analysis. The cityblock distance dissimilarity meas-
ure and the Ward linkage method were applied to determine
profiles. Cluster analysis is a multivariate technique whose
primary purpose is to assemble objects based on the charac-
teristics that they possess. Cluster analysis classifies objects so
that each object is as similar as possible to other in the clus-
ter, and as dissimilar as possible with the objects in the other
clusters. Based on their characteristics, each climber has been
assigned by the algorithm to a particular cluster. We there-
fore used ANOVAs and Tukey post-hoc test to analyse more
precisely what the differences between the cluster were. To
determine the right number of clusters, a silhouette plot was
used (McCune et al. 2002; Rousseeux 1987). The average sil-
houette values were compared for 2, 3, 4, 5 and 6 clusters,
and were maximized with three clusters (mean of 0.35). To
avoid local minima, we replicated parameters five times and
selected the clustering solution which presented the lowest
sum of distance. For the three-cluster solution, we checked
for uniform variance and normality of the distribution of
each cluster, and carried out a series of one-way ANOVAs to
investigate the differences between categories for the vari-
ables studied. The significance level was set at *P* < 0.05. By
the present case, three clusters were found using the K-means
algorithm (Fig. 3).

Proportion of climbers in the total species richness
in vegetational units across forest formations and
topographical positions

For this purpose, we compared the variations in proportion
of climbers with regard to the total species richness of each
<figure><img src="image_2.png" /><figcaption>**Figure 1:** map situating the 26 vegetational units in South America.</figcaption></figure>

vegetational unit across formations and topographical positions using one-way ANOVAs.

**Statistical investigation with regard to trait groups (CTG)**

We sourced trait data of American climbers from floras, personal investigations and the literature. We selected four categorical traits: (i) investment in woody tissues (two categories: woody versus herbaceous perennial). (ii) potential growth height, defined with regard to forest stratification (three categories: low (<2 m), mid (2–15 m), or high (>15 m) (based on personal observations and the literature), (iii) Leaf longevity (two categories: deciduous versus evergreen) and (iv) modes of climbing (five categories: twining stems, hooks, scrambling, all varieties of tendrils within one mode and adhesive roots).

Other traits like adaptation to shade or low nutrient availability would be useful but these data were not available universally in the literature.

**Characterization of climber trait groups**

We employed these four traits as variables in a k-medians non-hierarchical cluster analysis with a Euclidean distance measure (McCune *et al.* 2002), using STATA (Version 9.2, StataCorp, College Station, TX, USA) to allow the program to randomly select initial group centers in order to create between two and seven groups out of the data. We then used the Calinski and Harabasz approach (Caliński and Harabasz 1974) to determine the optimal number of groups (NB: we henceforth refer to these groups as climber trait groups, or CTGs).

We then calculated the proportion of CTGs present in each vegetational unit.

**CTG proportions in vegetational units across bioclimatic indices**

We calculated the proportion of CTGs present in each vegetational unit. We employed one-way ANOVAs to analyze significant variation in CTGs across the bioclimatic indices. We log-transformed
<figure><img src="image_3.png" /><figcaption>**Figure 2:** map situating the 33 vegetational units in North America.</figcaption></figure>

<figure><img src="image_4.png" /><figcaption>**Figure 3:** bioclimatic characteristics of mean climber species richness (MCSR) in the three different clusters. Each bar of the stack graph represents the main characteristics of the clusters, and the lowercase letters in the post-hoc analysis shows what these differences were among clusters. Significant difference with (a) cluster 1; (b) cluster 2; (c) cluster 3 (*P* < 0.05). NS: non-significant difference across cluster.</figcaption></figure>

any data that were not normal and used a Sidak post hoc test to identify which groups differed significantly. Although we recognize that log-transformations have limitations, they are still a useful tool in data analyses (McCune et al. 2002).

### CTGs proportions in vegetational units across forest formations and topographical positions

We also examined the distribution of CTGs in the different forest formations and topographical positions using a two-way ANOVA and a Tukey post hoc test to identify differences.

## RESULTS

Overall, our data set contained 151 climber species (supplementary Appendix S3). About 96 climbers are native to North America and 46 are native to South America. The most frequent climbers found in species lists were for North America: *Toxicodendron radicans*, *Parthenocissus quinquefolia*, *Smilax rotundifolia*, *Vitis rotundifolia* and *Smilax bona-nox*, with each being found in at least half of the forest formations, and for South America: *Mitraria coccinea*, *Elytropus chilensis*, *Cissus*
striata, Boquila trifoliata, Luzuriaga radicans, L. polyphylla and Hydrangea serratifolia.

A few non-native climbers were found in our data, like *Celastrus orbiculatus* and *Lonicera japonica* (Asia), *Hedera helix* (Eurasia) and *Rubus ulmifolius* (Europe). *Mikania scandens*, originally from North and Central America, has now naturalized in South America; and *Ipomoea hederacea*, originally from South America, has now naturalized in North America.

## Climber species richness with regard to bioclimatic indices, forest formation and topographical positions

The graphical illustration of 3 clusters as a function of MCSR, continentality, ombrotype and thermotype (Fig. 3) shows that

1. Clusters 1 and 2 have close (highest) levels of climber species richness. Cluster 1 differs from cluster 2 for ombrotype (higher humidity) and thermotype (centered on mesotemperate in cluster 1; thermotemperate in cluster 2). Such bioclimatic indices are found in vegetational units of low altitudes in both North and South America (vegetational units 1, 2, 4, 45, 46).

2. Cluster 3 has lower levels of climber species richness. This cluster is found in oceanic to continental regions in the two Americas, characterized with ombrotypes varying from humid to dry; thermotypes from supra Mediterranean to supratemperate (vegetational units 8, 9 16 or 17)

The proportion of climber species among the total number of species within forest formations varied widely, from 0.000 to 0.297 (mean = 0.114; σ = 0.063). The results of the one-way ANOVA on climber species proportion showed (i) there was no significant effect of forest formation, and (ii) there was a significant effect of topographical position: wetlands exhibited higher proportion than upland sites (mean = 0.153; σ = 0.102 versus mean 0.056; σ = 0.056. P < 0.01).

## Climber trait groups: classification

Our trait-oriented cluster analysis placed the climbers into six trait groups (Table 1). This table provides the individual climber species and their CTG. CTGs 1 and 2 include short-lived species living primarily in the understory. Species tend to be deciduous and spread by tendrils and stem twining, sometimes associated with scrambling. These two groups represent 42% of the total climber species. Species in group 1

primarily occupy higher strata (>15 m), while species of group 2 preferentially establish at low strata (<15 m). These groups include two of the largest climbing families, Leguminosae and Convolvulaceae.

CTG 3 is composed mainly of twining climbers (sometimes associated with hooks). The climbers of this group are generally herbaceous perennials characterized by rapidly growing life forms. They are evergreen, with some of them leafless (in fact, very small leaves). The diameter of these climbers is generally small (around 1–3 cm dbh; the authors’ personal observations).

CTGs 4 and 5 are composed of large-sized (3–15 cm dbh), deep-rooted, woody climbers and include deciduous and evergreen species. CTG 4 climbers are twining or have tendrils, sometimes with adhesive disks or hooks. Species in this group are numerous (49). They include the largest climbing families such as Vitaceae, Smilacaceae and Caprifoliaceae and are able to colonize gaps and canopy by climbing to several supports. In North America, these climbers include *Parthenocissus quinquefolia*, *Smilax rotundifolia*, *Vitis rotundifolia*, *S. bona-nox*, *Bignonia capreolata* and *Ampelopsis arborea*, as well as the invasive exotic *Lonicera japonica*. CTG 5 climbers are also woody and have large diameters, but their preferential mode of climbing is adhesive roots or hooks, which limits them to one support. Most of these climbers are shade tolerant.

CTG 6 generally includes woody climbers that usually colonize the mid and low strata. This group is poor in species but includes *Toxicodendron radicans*, one of the most frequent lianas of North American forests according to VegBank data.

The distribution of climber species in the six CTG is indicated in supplementary Appendix S3.

## Climber trait group relationship to bioclimatic indices, forest formations and topographical positions

Analyses of variance across the bioclimatic indices revealed significant differences in CTG representation for the continentality index and thermotypes, but not for the ombrotypes.

A similar analysis with regard to forest formations found significant differences: CTG 1 (log-transformed, *F* = 7.99, *P* < 0.001) and CTG 5 (log-transformed, *F* = 3.33, *P* = 0.025). The mean percentage of climbers in CTG 1 was significantly lower in subpolar/temperate evergreen rainforests than in the other formations (Sidak post hoc test *P* < 0.01). The mean

<table><caption>**Table 1:** climber trait groups (CTG) resulting from cluster analysis</caption><thead><tr><th>CTG</th><th>N species</th><th>N families</th><th>Major climbing modes</th><th>Leaf</th><th>Stem</th><th>Height</th></tr></thead><tbody><tr><td>1</td><td>50</td><td>15</td><td>Tendril or twining</td><td>Deciduous</td><td>Herbaceous</td><td>High</td></tr><tr><td>2</td><td>14</td><td>3</td><td>Twining</td><td>Deciduous</td><td>Herbaceous</td><td>Low</td></tr><tr><td>3</td><td>12</td><td>5</td><td>Twining</td><td>Evergreen or leafless</td><td>Herbaceous</td><td>High</td></tr><tr><td>4</td><td>49</td><td>17</td><td>Tendril or twining</td><td>Deciduous or evergreen</td><td>Woody</td><td>Mid or high level</td></tr><tr><td>5</td><td>21</td><td>11</td><td>Adventitious roots</td><td>Deciduous or evergreen</td><td>Woody</td><td>Mid or high level</td></tr><tr><td>6</td><td>5</td><td>4</td><td>Tendril or twining</td><td>Deciduous or evergreen</td><td>Woody</td><td>Low</td></tr></tbody></table>
percentage of climbers in CTG 5 was significantly greater in temperate and subpolar evergreen rainforests than in the temperate and subpolar needle-leaf evergreen forests (Sidak post hoc test *P* = 0.02). Lastly, the mean percentage of climbers in CTG 4 was significantly greater in wetland forests (*t* = -2.33, *P* = 0.024). The other CTGs did not show significant differences between upland and wetland forests.

DISCUSSION

Climbing plants of the two Americas are significantly less species rich at temperate latitudes compared to extratropical and tropical biomes (Durigon et al. 2014; Gentry 1991; Schnitzer and Bongers 2002). Above 30° latitude, the structurally diverse warm temperate moist forests appeared to home the highest number of climbers, mainly from CGT4 and CGT5. The importance of woody climbers in warm temperate forests has already reported by other authors (among many: Collins and Wein 1993; Carrasco-Urra and Gianoli 2009; Munoz et al. 2003). Indeed mild climates prevent climbers from embolism risk; soils are generally nutrient rich, which promotes fast growth and limit nutrient competition; the complex structure displays fine niche partitioning with a large variety of trunk diameters and ages, substrate qualities in texture or allelopathic elements and a heterogeneous spatio-temporal light regime. The importance of climbers with adventitious roots (CTG5) in rainforests can be explained by the strategies developed in this climbing mode: availability to climb to the biggest trunks (Putz and Holbrook 1991; Silk and Holbrook 2005), to cope with shady understreys during the ascending phase (Rowe et al. 2004; Valladares et al. 2011), vulnerability to dessiccation which occur during the winter season in deciduous forests (Durigon et al. 2013; Hegarty 1989; Teramura et al. 1991).

In contrast with CTG4, 5, 6, CTG 1 and 2 dominated by herbaceous climbers, are rare, perhaps because of the competition with woody climbers for supports, but probably more because of the gloomy conditions of dense understories. These species develop mainly in gaps where they can entangle underwoods. A good example is *Chusquea valdiviana* in rainforests of South America, or a variety of small climbers in hurricane forests of North America (Allen et al. 2005).

In marked contrast with CTG4, 5 and 6, the herbaceous perennial deciduous life forms (CTG1, CTG2, CTG3) dominated by the Fabaceae family (mostly *Vicia*, *Lathyrus*) are represented in high proportions (between 66% and 100%) at altitude, whatever the bioclimate, suggesting a better adaptation to altitude-related constraints. In some forest types, the herbaceous form is present as scattered individuals (Nothofagus antarctica FA, South America; Pinus ponderosa FA, North America), possibly due to the conjunction of cold temperatures (in altitude), organic soils (in conifer forests) and high leaching (ultrahyperhumid) ombrotypes. Interestingly, southern temperate forests exhibit a greater latitudinal extent in distribution than temperate forests of North America, a fact already published in Arroyo et al. (1996); and

Gianoli *et al.* (2010). The land in temperate South America is rarely far from maritime influence, which has likely favored the presence of climbers at higher latitudes, such as *Mitraria coccinea* and *Luzuriaga marginata* living at latitudes 52–55°S, and *Philesia magellanica* at the latitude 55°44′ at Cape Horn (Dollenz 1982a, 1982b).

Wetlands

In flooded areas of large river plains, climbers benefit abundant resources in water, nutrients and light. There are however big differences between bioclimatic zones and the hydrological characteristics. The best conditions for climbers are found in seasonally flooded large floodplains found in thermo- and mesotemperate thermotypes. The rarity of frost combined with an abundant supply of water and sediments during the growing season promotes a profusion of nutrients and light (Li *et al.* 2013; Schnitzler 1995).

The complex forest architecture characterized by dense understory and open canopy provides suitable supports for all modes of climbing, from small twining herbaceous species to tall woody climbers. In these forests, CTGs 4 and 5 are dominant, a result consistent with the literature on the Mississippi Valley (Robertson and Weaver 1978). These climbers may form dense veils of clonal individuals from above the canopy to the soil, similar to many tropical climbers: e.g. *Vitis rotundifolia* is reported to cover 17–38% of the total plant cover, *Smilax tamnoides* 17%, *Campsis radicans* 17–38%, *Vitis aestivalis* up to 38% and *Bignonia capreolata* 17%, according to VegBank data. In Mediterranean climates, climbers are also abundant in riparian forests, in spite of the length of the dry season. One reason may be that fire is rare there conversely to dry upland forests. A second reason may be morphological: because of the deep roots and efficient vascular systems that allow them to reach groundwater (Schnitzler and Arnold 2010). This probably explains why the riparian *Platanus* Mediterranean forests of California contain high densities of two lianas (*Vitis californica* and *Toxicodendron diversilobum*) (Campbell 1980).

In permanently flooded areas, climbers must cope with the anaerobic soil conditions. Some species of CTGs 4, 5 and 6 have developed rather good tolerance to such conditions, although to varying degrees. *Campsis radicans* and *Brunnichia ovata* can live from six to nine weeks in anaerobic conditions, whereas *Vitis rotundifolia* and *Toxicodendron radicans* can survive only one to two weeks (Gentry 1991). The capacity to survive the conditions of marshes explains the restricted distribution of CTGs, in particular within the same genus. For example, in North Florida, *Smilax walteri* is the dominant climber along the banks and in the shallower parts of sloughs, while *Smilax rotundifolia* is the dominant climber on the low lying plain (Li *et al.* 2013). Similar segregation occurs among species of Vitaceae (personal observations along Buffalo River, Arkansas). In extreme anaerobic conditions, woody species are rare and scarce. In the Great Lakes Central Lowlands Provinces of North America, swamps have virtually no climbers, except the deciduous *Clematis virginiana* (CTG 6) (Rivas-Martínez *et al.* 2011). The *Nyssa-Taxodium*
forests of the southern swamps of the Mississippi are richer in climbers, also represented by CTG 6 species.

## The heritages of a remote past

It is surprising that the proportion of climbers did not vary significantly across the five forest formations, as the species richness differences are substantial. This may be explained by the fact that as the number of climber species decreases, so does the total number of species, likely due to the same limiting factors (e.g. drought, frost, shade). The high species richness in some forest formations among rainforests or mixed deciduous/ evergreen forests can also be explained by the paleoecological heritage. Indeed, some of these zones were ice-free during the Last Glacial Maximum (e.g. near the Appalachians or the Gulf Coast in North America) (Braun 1950; Duncan 1975) or the southern Andes in South America (Arroyo et al. 1996; Marcheli and Gallo 2006; Turchetto-Zolet et al. 2012). In these refugia, climbers have probably persisted during the ice period.

## The human heritage

A few exotic climbers, which probably escaped from fallows or rural areas, or gardens, were found in the data set. Some of them are known with native species, like the native *Celastrus scandens* with the exotic *C. orbiculatus* (Leicht-Young et al. 2007; Leicht-Young et al. 2011), which make them able to live in old-growth stands. The number and abundance of exotic climbers is however relatively limited compared to open areas, except in highly anthropized forests or wetlands. In wetland environment, *Lonicera japonica* is particularly abundant in alluvial forests (19–38% in alluvial forests of Pennsylvania according to VegBank).

## CONCLUSIONS

In this study, we have developed a protocol for analyzing the links between climber patterns to climates and forest habitats at a continental scale. The study has provided evidence of complex environmental filters in the establishment of climbers depending on the variety of constraints specific to temperate latitudes. We hope that this protocol will facilitate large-scale meta-analyses across continents in Eurasia, Africa and Australia although some research questions may require different methods.

## SUPPLEMENTARY MATERIAL

Supplementary material is available at *Journal of Plant Ecology* online.
*Conflict of interest statement.* None declared.

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