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52872_cover.indd 2 
smithsonian contributions to the marine sciences • number 40

The Coralline Genus 

Clathromorphum Foslie emend. Adey

Biological, Physiological, and Ecological 

Factors Controlling Carbonate Production 

in an Arctic-Subarctic Climate Archive

Walter H. Adey, 

Jochen Halfar, and Branwen Williams

WASHINGTON D.C.

2013
ABSTRACT

Adey, Walter H., Jochen Halfar, and Branwen Williams. The Coralline Genus Clathromorphum Foslie emend. Adey: Biological, Physiological, and Ecological Factors Controlling Carbonate Production in an Arctic-Subarctic Climate Archive. Smithsonian Contributions 

to the Marine Sciences, number 40, iv + 42 pages, 29 figures, 1 table, 2013.— The coralline algal genus Clathromorphum is a dominant 

calcifier in the rocky Subarctic biogeographic region, stretching through the lower Arctic from the Labrador Sea to the Bering Sea. 

Although commonly 2–10 cm in thickness, Clathromorphum can reach a thickness of up to 50 cm while forming an annually layered 

structure that can reach currently documented ages of up to 850 years. Geochemical and growth information archived in annual growth 

bands of Clathromorphum sp. has been used to provide long time series of past environmental conditions in regions that are poorly understood major drivers of Northern Hemisphere climate. However, information on Clathromorphum calcification, growth, and ecology 

that would allow interpretation of these records has previously been quite limited. Here we relate extensive field and laboratory data on 

the biology, physiology, and ecology of species of this genus and their controlling environmental parameters. We show that Clathromorphum has evolved a unique mode of double calcification, with high-magnesium calcite crystals, that enhances long life and leads to a 

multielement climate archive. Growth rates are controlled by temperature, and carbonate density is controlled by light, determined by 

both latitude and sea ice cover, whereas carbonate buildup and ultimate thickness are determined by local geomorphology and faunal 

interactions. Reproduction is complexly linked to vegetative anatomy. Precise paleoenvironmental information can be retrieved from 

Clathromorphum because of its unique cytological and anatomical structures, described and modeled for the first time in this volume.

Cover images: (left) One thousand year-old Clathromorphum compactum mound buried in a rhodolith bed (Lithothamnion 

tophiforme) in northern Labrador. Photo by Michael D. Fox; (center) Boulders at 25m depth heavily encrusted with C. compactum

on the shore of low rocky island in northern Labrador. © Nick Caloyianis. Reprinted with permission; (right) Boulder with 200–300 

year-old crust of C. compactum from southern Labrador. Coralline crusts on boulder sides are mostly Lithothanmnion spp. © Nick 

Caloyianis. Reprinted with permission.

Published by SMITHSONIAN INSTITUTION SCHOLARLY PRESS

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Copyright © 2013 Smithsonian Institution

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Library of Congress Cataloging-in-Publication Data

Adey, Walter H.

The coralline genus Clathromorphum foslie emend. adey : biological, physiological, and ecological factors 

controlling carbonate production in an arctic-subarctic climate archive / Walter H. Adey, Jochen Halfar, and Branwen Williams.

 pages cm — (Smithsonian contributions to the marine sciences ; number 40)

Includes bibliographical references and index.

1. Coralline algae. 2. Algae—Effect of temperature on. 3. Ecology—Cold regions. I. Halfar, Jochen, 1969-

II. Williams, Branwen, 1980- III. Title. 

QK569.C8A325 2013

581.7--dc23

2013026877

ISSN: 0196-0768 (print); 1943-667X (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

INTRODUCTION 1

The Subarctic Shallow Benthos and Cold-Water Carbonates 1

The Distribution of Clathromorphum Species 2

Biology and Ecology of Clathromorphum 4

Calcification 6

The Need for an Arctic-Subarctic Archive 6

Corallines as Climate Proxies 8

 Mg/Ca Ratios and Seawater Temperature 8

 Ba/Ca Ratios and Salinity 8

 Growth as a Climate Archive 8

 Isotopic Composition 8

MATERIALS AND METHODS 8

Clathromorphum compactum (North Atlantic, Labrador Sea, and Arctic) 10

Clathromorphum nereostratum (Aleutian Islands) 11

Specimen Preparation 11

Terminology 11

RESULTS 11

Reproduction 11

 Reproduction in Clathromorphum compactum 14

 Reproduction in Clathromorphum nereostratum 16

Cellular and Anatomical Structure 17

Biologically Induced Etching as a Source of Information 21

Growth Rate 22

Wall Structure and Calcification 24

Ecology and Geomorphology 28

Tissue Irregularity 31

 Chiton Grazing 31

 Sea Urchin Grazing 32

 Conceptacle Breakout 33

 Death Due to Disease 33

DISCUSSION 33

Climate Archives 33

Mechanisms of Calcification 34
i v • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Primary Production and Growth Rates 34

Interfilament Calcification 35

Conceptacle-Based Growth Analyses 37

Changing Ocean pH 37

CONCLUSIONS 38

ACKNOWLEDGMENTS 39

REFERENCES 39
INTRODUCTION

Millennial understanding of past climate variability in the Subarctic and Arctic regions is crucial to prediction of the impacts of anthropogenic climate change both in the 

Northern Hemisphere and globally. In warmer latitudes, abundant tree ring and pollen 

data in the terrestrial environment and coral and bivalve data in the marine environment 

can provide data on past climates. However, considering the crucial role that sea ice, 

with its albedo effect, plays in controlling incoming solar energy, midlatitude data are 

inadequate to provide an understanding of global climate processes. Although recent 

studies have shown that encrusting coralline algae, abundant in shallow high-latitude 

seas, can record paleoclimatic information, considerable variation of unknown origin 

has provided conflicted analyses. In this volume we endeavor to show how an extensive 

field and laboratory effort directed at species of the coralline genus Clathromorphum

can provide a detailed understanding of the complex biology, physiology, ecology, and 

habitat geomorphology of these species, which, in turn, can direct laboratory analysis 

and data interpretation. 

The Subarctic Shallow Benthos and Cold-Water Carbonates

The Northern Hemisphere Subarctic region, as defined by the Thermogeographic 

Model, quantitatively demonstrated with crustose corallines (Adey and Steneck, 2001), 

and further supported by quantitative analyses of benthic seaweeds (Adey and Hayek, 

2011), stretches from the northwestern North Pacific to the northwestern North Atlantic. 

Many benthic species that characterize the Subarctic occur in both Pacific and Atlantic 

segments of the region (Olsen et al., 2004; Adey et al., 2008), although the separated 

populations tend to be genetically distinct (Addison and Hart, 2005; Coyer et al., 2006). 

Relatively few species are endemic to the North Atlantic Subarctic, whereas many species are endemic to the considerably larger North Pacific Subarctic (Briggs, 2003). The 

Arctic has very few endemic genera and only a small number of species; it is dominated 

by Subarctic species (Adey et al., 2008).

The Coralline Genus Clathromorphum

Foslie emend. Adey

Biological, Physiological, and Ecological Factors Controlling 

Carbonate Production in an Arctic-Subarctic Climate Archive

Walter H. Adey, Department of Botany, National 

Museum of Natural History, Smithsonian Institution, Washington, D.C., 20013-7012, USA; 

Jochen Halfar, Department of Chemical and 

Physical Sciences, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada; 

Branwen Williams, Keck Science Department, 

Claremont McKenna-Pitzer-Scripps Colleges, 

Claremont, California 91711, USA. Correspondence: W. H. Adey, adeyw@si.edu. Manuscript 

received 17 October 2012; accepted 5 June 2013.
2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

scientific dispute, a basal calcified coralline crust with centuries 

of growth, is the least studied element.

Several species each of the genera Clathromorphum, Lithothamnion, and Leptophytum are the dominant producers of the 

Subarctic-Arctic cor-strome. In the fully Subarctic northwestern 

North Atlantic, Clathromorphum compactum is an abundant 

species encrusting rocky bottoms in the mid-photic zone (10–20 

m; Adey, 1966b), being largely replaced by Clathromorphum 

circumscriptum in shallower waters and Lithothamnion glaciale

in deeper waters. Lithothamnion glaciale also tends to replace 

C. compactum as the dominant cor-strome producer in inner bays 

and fjords, where siltier and fresher waters usually dominate. 

In many localities, depressions within the rocky cor-strome bottoms are filled with mobile nodules (rhodoliths) largely derived 

from fragments fractured from the Lithothamnion cor-strome by 

waves and bioturbation. Extending below the rocky cor-strome 

and continuing to significant depths (20–60 m), beds of rhodoliths, usually as part of a shelly gravel substrate, are widespread. 

However, the full extent of these beds is poorly known. Two 

species of Lithothamnion (L. glaciale and L. tophiforme) are the 

dominant producers of rhodoliths, the former species being more 

Subarctic and the latter more Arctic (Adey et al., 2005).

As previous studies have demonstrated (Halfar et al., 2007, 

2008, 2011a; Frantz et al., 2005; Hetzinger et al., 2011; Williams 

et al., 2011), these centuries-old carbonate formations, through 

analysis of their temperature- and light-dependent growth layers 

and the trace chemical structure of their carbonate cell walls, 

can provide significant climate archives. The coralline provides 

a surface for algal epiphytes, and both the corallines and the 

epiphytes are grazed by many invertebrates. They are also very 

important producers of secondary biomass, mostly by providing 

a porous, reef-like habitat to innumerable invertebrates that utilize mostly planktonic sources of primary production (Chenelot 

et al., 2011). Additionally, they provide significant ecosystem 

support for Subarctic-Arctic fisheries that are now expanding in 

importance. These key Arctic and Subarctic ecosystems have a 

detailed history written into their basal biogenic carbonate; to 

read this history, we need only to extract the Rosetta stone of 

anatomical and geochemical information. 

The Distribution of Clathromorphum Species

Although a few species of the genus Clathromorphum

have been described for the colder Southern Hemisphere 

(http://www.algaebase.org), their relationship to the abundant Northern Hemisphere species is currently uncertain. In 

the Northern Hemisphere, the four epilithic species are largely 

restricted to the Subarctic and Arctic or its fringes, including 

the Aleutian Islands (Lebednik, 1976). Two additional species, 

C. parcum and C. reclinatum, are obligate epiphytes with limited 

archival value, and we will not discuss them further; phylogenetic studies currently underway (Adey et al., unpublished) show 

that these two species belong to a different clade. They are Boreal and fringe Subarctic in distribution only in the North Pacific.

Wherever rocky bottom occurs in the sublittoral Subarctic 

(typically to 40 m, depending upon exposure and salinity), it is irregularly coated by an extensive but patchily discontinuous crust 

of biogenic calcium. This carbonate crust (typically 0.5–10 cm 

thick, but to over 0.5 m in thickness; Lebednik, 1976) is present 

on all but the most mobile or friable rock surfaces (Frantz et al., 

2005; Adey and Hayek, 2011). Because it is a high-magnesium 

carbonate, laid down mostly by coralline red algae, this crust 

can be called a cor-strome. It also occurs in the Arctic, where 

it is built largely by Subarctic coralline species (specimens and 

images in the U.S. National Herbarium); however, its continuity 

is unknown. The depth zone immediately below the cor-strome, 

where broken fragments accumulate and some species of Lithothamnion continue to grow in the mobile state as rhodoliths, has 

received some attention (Freiwald and Heinrich, 1994), but the 

cor-strome itself remains largely unstudied.

In both the Atlantic and the Pacific, these carbonateencrusted bottoms have been widely referred to as “coralline, 

sea urchin barrens” (Mathieson et al., 1991; Estes and Duggins, 

1995; Steneck et al., 2002); however, this description is certainly 

a misnomer, as they may well be among the richer shallow marine bottoms of the marine Holarctic (Himmelman, 1991; Chenelot et al., 2011). The Chenelot et al. (2011) study focused on 

abundant invertebrates resident in Clathromorphum nereostratum in the Aleutian Islands, but it is likely that a similar relationship exists for cor-stromes in the northwestern North Atlantic. 

Drying fragments of cor-strome on research vessel laboratory 

benches generally release large quantities of invertebrates, especially grazing chitons and filter-feeding brittle stars. A Labrador 

fjord Lithothamnion glaciale cor-strome produced 740 macroinvertebrates from 637 cm2

 of crust (Adey, unpublished field 

notes). Thus, there is little question of the coral reef–like richness 

of these bottoms; what is lacking is geographically widespread 

quantitative research on invertebrate diversity and biomass.

Considerable debate exists concerning the primary ecological drivers of ecological structure on Subarctic-Boreal rocky 

bottoms (e.g., Steneck et al., 2002; Springer and Estes, 2003; 

Estes et al., 2005; Trites et al., 2007); is it climate, top predators, overfishing, or some complex of the three that drives the 

major fluctuations of the associated kelp beds observed over the 

last half century? These issues carry special weight because of 

the collapse of numerous major cold-water fisheries over the last 

several decades, the currently expanding Arctic fisheries, and the 

ongoing debate over climate change and its causes. Much of this 

debate has focused on the Bering Sea and Aleutian Islands and 

the Gulf of Maine and Nova Scotia. However, the carbonate 

bottom, with the rich diversity it harbors, has been considered 

at best a backdrop in the debate over large seaweeds, grazing 

invertebrates, and sea mammals and at worst a “barren” created 

by imbalances among the major, large players. As we will discuss at depth, the age of the cor-strome frequently reaches one to 

three centuries, and the maximum age of specimens now under 

study exceeds 800 years in the Aleutian Islands and 600 years 

in the Labrador Sea. The biological constant in these regions of 
NUMBER 40 • 3

an Arctic species, although it is more likely Subarctic in origin 

and distribution. Although collection sites in the Arctic are only 

scattered, Clathromorphum compactum is generally an abundant 

species wherever it is found, and rock substrate, coastal salinity, 

and a high sediment load are not limiting.

Clathromorphum nereostratum (Figure 1) and Clathromorphum loculosum are cor-strome formers and appear to be largely 

restricted to the Aleutian Islands; both species are reported for 

the Asian mainland coasts, but insufficient definitive work has 

been carried out in the Okhotsk and western Bering Seas to determine whether they are significant components of the algal flora. 

Clathromorphum loculosum has a leafier growth morphology 

(Lebednik, 1976), and its archival potential is unknown. Clathromorphum nereostratum is the most massive of the Clathromorphum species, largely because of its Subarctic-Boreal fringe 

environment in the Aleutian Islands. Clathromorphum nereostratum and C. compactum are conspicuously layered, often 

with buried conceptacles, and provide the greatest opportunities 

for climate archiving. Both the Arctic and the northeastern Asian 

mainland and its off-lying islands provide a largely unknown and 

potentially rich region for cor-strome climate archiving. Here we 

Clathromorphum circumscriptum is the most widely distributed member of the genus, ranging from Hokkaido, Japan, 

and British Columbia (Adey et al., 1976; Lebednik, 1976) in the 

North Pacific through the Arctic to the southern Gulf of Maine in 

the western Atlantic and Iceland and the Norwegian fjords south 

to Trondheimsfjord (Adey, 1965, 1971) in the eastern Atlantic. 

Restricted largely to intertidal pools and the shallow sublittoral, C. circumscriptum can (rarely) achieve 5–10 cm in thickness. However, both the conceptacles and the intraconceptacle 

vegetative crust in this species always break out at reproductive 

maturity, considerably disrupting thallus layering. Together with 

a tendency to experience greater environmental disturbance, it is 

a possible, but generally poor, subject for climate archiving.

Clathromorphum compactum, a cold-water carbonate 

builder and a primary subject of this volume, extends from northeastern Hokkaido, Japan, through the Arctic to the central Gulf 

of Maine in the western Atlantic (Adey et al., 2008) (Figure 1). 

Clathromorphum compactum is not reliably known from Iceland 

or Norway, occurs in deeper water, and is conspicuously more 

limited to colder water than C. circumscriptum (Adey, 1965; 

Adey et al., 1976). Adey et al. (2008) treated C. compactum as 

FIGURE 1. Known geographic distribution of principal Clathromorphum clathrostrome formers. 

Clathromorphum nereostratum has been reported from the mainland coast of easternmost Asia, 

but records need to be verified.
4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 2A. Clathromorphum compactum buildup (clathrostrome) crowning large cobble in cor-strome, including branching Lithothamnion

spp. at 20 m depth in southern Labrador. Crusts are 2–4 cm thick and 100–250 years old. Green sea urchins (Strongylocentrotus droebachiensis) are 30–50 mm in diameter. © Nick Caloyianis. Reprinted with permission. 

introduce the term clathrostrome to refer to extensive carbonate 

crustal buildups dominated by the two Clathromorphum species, C. compactum and C. nereostratum.

Biology and Ecology of Clathromorphum

As with most red algae, crustose corallines have a basic 

filamentous structure; in this group, the filaments are fused into 

a calcified crust (Figures 2A–2C). As described by Adey (1964, 

1965, 1966a, 1966b) and Adey et al. (1982; 2005), crustose 

corallines combine these filaments into complex tissues with 

the filaments linked by fusions and/or secondary pits. Also, several different patterns of growth, within the carbonate framework, characterize different genera (Adey et al., 2005). In many 

cases the development of reproductive structures occurs within 

perithallial tissue and is integrated with the growth of that tissue. 

Given damage to the overlying meristem or in the formation of 

conceptacle fertile discs, meristematic activity can be reinitiated 

within the uppermost years of perithallial tissue (forming characteristic wound repair tissue).

Like many higher plants and unlike all other red algae, corallines have an intercalary meristem (Adey, 1964; Adey et al., 

2005; Figure 2C); along with other elements of their anatomy 

and reproduction, this characteristic has led to their separation 

as an order of red algae (Corallinales; Silva and Johansen, 2007). 

Recent phylogenetic work suggests the group may be separable 

at the level of subclass on the basis of the structure of cell pit 

connections (Bittner et al., 2011). In a multigene analysis of genera with multipored conceptacles, currently under development 

with colleagues (Adey et al., unpublished), we are able to show 

that Clathromorphum forms a distinct clade most closely related 

to Leptophytum and distant from the Lithothamnion and Phymatolithon clades. 

Corallines occurring on hard bottoms in shallow seas can 

be reef formers in the tropics (Adey, 1998) and rock-blanketing 

carbonate formers (cor-stromes) in colder waters. They are often 
NUMBER 40 • 5

FIGURE 2B. Polished section of 4-cm-thick, 220-year old 

mound of C. compactum (same locality as Figure 2A). Note 

distinctive yearly banding, variably abundant conceptacles 

(ovoid holes), and large unconformity near the base of the 

specimen (up arrow). Partial unconformities are scattered 

throughout crust (down arrow). 

FIGURE 2C. SEM image of fractured C. compactum mound. The 

lower right face (right arrow) shows calcified perithallium filaments. 

The upper thin slab breaking off is epithallium. The exposed surface 

to the left (left arrow) is meristem, separated through the middle of 

the layer at the plane of growth and calcification. 

fossilized and have been used as paleoecological indicators from 

the early Tertiary (Adey, 1979). Coralline growth is slow; yearly 

bands in Clathromorphum in the warmer fringes of the Subarctic 

and the Aleutian Islands are 300–400 μm in thickness. In the 

colder Subarctic, the principal habitat of C. compactum, they are 

considerably thinner and drop below 100 μm yr–1 in the Arctic. 

Although the potential for climate archiving with corallines has 

been known since the 1960s (Adey, 1965; Chave and Wheeler, 

1965), its application has been frustrated until recently by a lack 

of understanding of their anatomical complexity and its irregularities, as well as by the lack of appropriate instrumental tools.

Species of Clathromorphum have a unique anatomy that is 

particularly useful in the development of climate archives in Subarctic marine environments (Adey, 1965; Halfar et al., 2011a). 

Unlike the progressive cell growth in other Subarctic corallines, 

where maximum cell length is achieved several to a dozen cells 

below the meristem, creating a diffuse, time-delayed band of calcifying cells, Clathromorphum produces all of its growth and 

calcification in the meristem cell layer (a cambium analog; Adey 

et al., 2005; Figure 2C). As shown here, in Clathromorphum the 

band of calcification and growth is even narrower than meristem 

cell length, occurring on a plane a few microns thick passing laterally through the meristem; this ensures the tight temporal linking of ambient water climate and chemistry to a narrow plane 

of calcite crystals. These species have an intricate anatomy that 

includes calcite crystals that preserve, in their trace element and 

isotopic structure, an array of environmental proxies.

In addition to their carbonate skeleton, species of Clathromorphum have evolved partial protection against grazing by 

invertebrates in both their anatomy (the sunken meristem) and 

their primary asexual reproduction (conceptacles are sunken in 

the crust and produced in winter). Working with Clathromorphum circumscriptum, Steneck (1982) demonstrated a “coevolved interdependency” with the limpet Acmaea testudinalis. 

Removal of epithallial surface cells by limpets during grazing 

equaled the production rate of epithallial cells in the meristem 

while freeing the surface of epiphytes. The same relationship 

likely exists for C. compactum and C. nereostratum, as fine grazing marks are abundant on the surface of most collected specimens (in most of the Subarctic, the chiton genera Tonicella and 

Ischnochiton dominate). Since routine grazing by chitons and 

limpets is concentrated on the upper surface of the epithallium, 

the perithallium, which builds cell-by-cell below the meristem, 
6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

can provide an archive of water climate that is often undisturbed 

for centuries by grazers or other organisms.

Most corallines form reproductive structures in peripherally uncalcified packets, called conceptacles, which can be scattered or densely arrayed across the crust surface; conceptacles 

are integral with perithallial tissue but can either be buried below 

the surface or protuberant above the crust surface. Patterns of 

origin and development, relative to the perithallial tissue, vary 

widely between genera. In some genera, conceptacles originate 

deep within the perithallium, sloughing off caps of overlying 

perithallial carbonate at maturity (e.g., Phymatolithon and 

Leptophytum; Adey, 1964, 1966a). In Clathromorphum conceptacles originate in the meristem, develop upward, as allowed 

by the growth of the surrounding vegetative tissue, and remain 

buried in that carbonate-encasing tissue at least until maturity 

(Adey, 1965). Some species of Clathromorphum, including 

C. compactum and C. nereostratum, bury their conceptacles 

with continued growth; successive years leave layers of conceptacle “holes” in the crust that document seasonality (Figures 2B, 2D, 2E). The principal Clathromorphum species with 

archival value initiate conceptacle development in the early 

autumn, apparently regardless of latitude. In the later stages 

of conceptacle maturation, to make room for the enlarging 

sporangia, the calcite in the immediately surrounding tissue 

is first dissolved, and then the remaining organic tissues are 

crushed by the enlarging sporangia; roughly 30%–50% of a 

conceptacle cavity’s height and 50% of its width result from 

this crushing. 

FIGURE 2D. Vertical fracture of C. compactum from southern 

Labrador with late mature asexual (multipored) conceptacles. The 

conceptacle to the right shows a roof and sporangial pore, exposed 

by the breakout of the conceptacle cap (epithallial plug overlying 

developing conceptacles). The roof of the postmature conceptacle to 

the left is growing in with new meristem. 

Calcification

The skeletal carbonate in corallines forms as prismatic highmagnesium calcite crystals, perpendicular to the filament axis, 

within the organic wall of each cell (Adey, 1998). In most coralline genera, a thin layer of tabular crystals forms between the 

individual filaments and serves as a “glide plane,” allowing differential cellular extension (growth; Adey et al., 2005). Clathromorphum species lack differential cellular growth and have 

a very different mode of calcification, which we will describe in 

detail below. In the Subarctic and its fringes, some Clathromorphum species can be very long-lived (at least many centuries). 

Given favorable environmental and geomorphological circumstances, C. compactum and C. nereostratum can build crusts 

with a substantial thickness of biogenic, high-magnesium carbonate (Figures 2B, 2F). With the convergence of an enhanced 

understanding of species ecology and preservational geomorphology, multiple complementary analytical techniques, and a 

full understanding of cellular anatomy, limitations to the climate 

archive potential of these species are finally being overcome.

The Need for an Arctic-Subarctic Archive

Much of the climate variability in the North Atlantic is dictated by the North Atlantic Oscillation (NAO), which is a hemispheric meridional oscillation in atmospheric mass with centers 

near Iceland (low) and over the subtropical Atlantic (high; Hurrell, 1995). However, the Labrador Sea and its coastal currents 

(the West Greenland Current and the Labrador Current) function somewhat independently of the NAO. Variability in North 

Atlantic Deep Water formation in the Labrador Sea impacts both 

the global Thermohaline Circulation and the cold and relatively 

fresh Labrador Current (Drinkwater and Mountain, 1997; Colbourne, 2004). Future climate predictions depend on a clear understanding, reaching back many centuries, of the relationships 

among the dominant climate parameters: the NAO, water temperature and salinity, the North Atlantic Deep Water formation, 

and Labrador Current mass transport.

The main branch of the Labrador Current flows along 

the edge of the Labrador and Newfoundland shelf (Lazier and 

Wright, 1993), whereas an inshore branch follows the various 

cross-shelf saddles and inshore troughs (Colbourne, 2004). 

Rapid climate changes beginning in the late 1980s produced an 

enhanced outflow of low-salinity waters from the Arctic and a 

general freshening of the Labrador Current (Greene and Pershing, 2007). Recent and substantial evidence for rapid changes 

in North Atlantic climate include increased Arctic air temperatures (Thompson and Wallace, 1998), decreased sea ice extent 

(Comiso, 2006), record minimum sea ice (Gersonde and Vernal, 

2013), increased melting of the Greenland ice sheet, and freshening of the North Atlantic (Curry and Mauritzen, 2005). Understanding the mechanisms responsible for the recently observed 

changes in the strength of the Labrador Current and climate 

variability in the subarctic Atlantic requires analysis of long climate time series (Sutton and Hodson, 2003).
NUMBER 40 • 7

FIGURE 2E. Polished slab of C. nereostratum from the Aleutian Islands, showing 244 years of growth. 

FIGURE 2F. Clathromorphum nereostratum from the Aleutian Islands. At 20 cm thick, the crust is over 400 years old. 
8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

using laser ablation–inductively coupled plasma–mass spectrometry and electron microprobe analyses. Research currently underway is producing data covering multicentury time scales.

Ba/Ca Ratios and Salinity

The barium content of the calcium carbonate skeletons of 

several marine calcifiers has served as a proxy for identifying 

changes in the mixing of cold, nutrient-rich deep waters at the 

surface (Lea et al., 1989; Fallon et al., 1999) or as a tracer for 

riverine inputs. Chan et al. (2011) have shown that changes in 

the Ba/Ca ratio in Clathromorphum indicate freshwater-induced 

changes in ocean stratification. Analyses of this ratio provide a 

proxy for assessment of salinity changes resulting from meltwater introduced into the Gulf of Alaska and the Alaskan Coastal 

Current, as well as being an important source of information on 

freshwater delivery into the Arctic Ocean.

Growth as a Climate Archive

A 115-year growth record from specimens of C. compactum

from Newfoundland and Quebec (Figure 5) produced a centurylong proxy archive for temperature in the northwest Atlantic 

(Halfar et al., 2011b). This chronology was successfully compared 

to climate patterns of the Atlantic Multidecadal Oscillation. Halfar 

et al. (2011a) linked information from yearly band widths with 

cloud cover related to the Aleutian low-pressure system. Combined 

with Mg as a proxy for temperature, a 640-year record of annual 

growth for C. compactum in the Labrador Sea has been correlated 

with sea ice cover (Halfar et al., unpublished manuscript).

Isotopic Composition

The oxygen isotope composition in the skeletons of Clathromorphum species records ambient seawater temperature. 

Similarly, the high-magnesium carbonate content of these species 

records δ13C values from the dissolved inorganic carbon in the 

surrounding seawater. Williams et al. (2011) measured δ13C in 

the coralline alga C. nereostratum to reconstruct the entry of 

anthropogenic CO2

 into the northern North Pacific Ocean and 

Bering Sea (Figure 6). From 1887 to 2003, the average decadal 

rate of decline in δ13C values increased from 0.03% yr–1 in the 

1960s to 0.095% yr–1 in the 1990s; this result is higher than expected from the δ13C Suess effect. The authors concluded that an 

increasing intensity of the Aleutian atmospheric low was responsible for the upwelling of carbon-rich deep water. 

MATERIALS AND METHODS

The collections utilized in this study were taken on scuba 

dives based from small research vessels, which allowed bottom 

surveys and assessments of the ecology and geomorphological 

characteristics of cor-stromes. The research vessels were equipped 

with laboratory facilities that allowed microscopic examination 

Likewise, a millennial understanding of past ocean climate 

variability in the North Pacific–Bering Sea region is crucial to 

the prediction of the impacts of anthropogenic climate change 

on this rich ecosystem and on the role played by this region in 

Northern Hemisphere climate at large. Links between the North 

Pacific and North Atlantic climates clearly exist, but they are 

poorly understood (Hetzinger et al., 2012). The Bering Sea, a 

region transitional between Arctic, Subarctic, and Boreal regions 

in the North Pacific (Adey and Hayek, 2011), is particularly sensitive to warming because of its seasonal ice cover (Sigler, 2010); 

continuation of the warming trend of the past decade (Overland 

and Stabeno, 2004) will have a major impact on its fisheries 

and seabird and marine mammal populations (Grebmeier et al., 

2006). As in the Labrador Sea, limited instrumental climate data 

for the North Pacific and Bering Sea are available, only from 

1900; significant sea surface temperature (SST) information is 

available only from the mid-1950s (Hetzinger et al., 2012). 

At present, schlerochronological analyses of the bivalve mollusk Arctica islandica provide the bulk of annual- to subannualresolution paleoclimate data for near-surface waters in the northwestern North Atlantic (Wanamaker et al., 2008, 2011). However, the northernmost confirmed occurrences of A. islandica are 

found along the southern shore of Newfoundland (Dahlgren et 

al., 2000), which is the southern boundary of the core Subarctic. 

Limited paleoproxy archives exist for the North Pacific, but most 

high-resolution climate reconstructions are inferred from tree 

ring chronologies and do not provide oceanic SST patterns (Hetzinger et al., 2011). Recent studies have shown that encrusting 

coralline algae are high-quality recorders of extratropical paleoclimatic signals because of their (1) abundance in mid- to highlatitude oceans, (2) multicentury life span (Halfar et al., 2011a), 

and (3) annual incremental growth patterns in a high-Mg calcite 

framework that can be targeted for high-resolution geochemical 

sampling (Halfar et al., 2007; Williams et al., 2011).

Clathromorphum has an intricate anatomy and reproduction; the climate history of the late Holocene is written in its 

yearly banding and calcite crystals. This study demonstrates 

how an understanding of the biology, physiology, ecology, and 

habitat geomorphology of two principal species of this genus is 

essential to the further development of a high-resolution climate 

archive for the Arctic and Subarctic. Reading this climate archive 

requires not only an intimate knowledge of the interactions between climate and the complex linkages among the reproduction, growth, anatomy, and ecology of these two species but also 

high-resolution analytical techniques that reveal the underlying 

structural details that are the outcome of these interactions.

Corallines as Climate Proxies

Mg/Ca Ratios and Seawater Temperature

The magnesium content of coralline algal skeletons records temperature changes (Figures 3, 4; Adey, 1965; Chave and 

Wheeler, 1965). Such records have been greatly expanded (Hetzinger et al., 2009, 2011; Gamboa et al., 2010; Kamenos, 2011) 
NUMBER 40 • 9

FIGURE 3. (top) Annual Mg/Ca cycles (moles) measured by laser ablation–inductively coupled plasma–

mass spectrometry. (bottom) Mg/Ca cycles superimposed on a cross-section view of C. compactum. The 

white line laser transect is along the growth axis (Halfar et al., 2011a).

FIGURE 4. Mg/Ca time series from C. compactum near St. Johns, Newfoundland (average of two samples), and 

instrumental temperatures at a nearby oceanographic station (station 27.0 m depth; 1950–2004); rannual = 0.51, 

p < 0.001 (Gamboa et al., 2010).
1 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the Gulf of St. Lawrence, the island of Newfoundland, and 

the Labrador coast northward to Cape Chidley, were sampled by Walter Adey and his students. The Gulf of Maine 

(GOM) specimens were collected primarily from 1960 to 

1963. Some of the Labrador (LAB), northeast Newfoundland 

(NENF) and northern Gulf of St. Lawrence (NGSL) specimens were collected during a 1964 cruise, and a limited number of photographic bottom images are available from that 

cruise. However, the majority of the C. compactum specimens 

were collected during expeditions of the R/V Alca i during 

the summers of 2010 and 2011. The research base comprises 

and specimen labeling, drying, and initial measurement. Extractions from rocky bottoms were mostly made manually, with a 

hammer and chisel; although 10%–20% of specimens were removed with the rock substrate still attached to the base, the majority separated cleanly from the substrate.

Clathromorphum compactum (North Atlantic, 

Labrador Sea, and Arctic)

More than 200 stations, at depths ranging from approximately 0 to 35 m, including the Gulf of Maine, Nova Scotia, 

FIGURE 6. Annually resolved δ13C values for three C. nereostratum specimens collected off two Aleutian Islands with the 3-year running mean in bold. 

(Williams et al., 2011).

FIGURE 5. Ten-year moving average of 115-year growth increments; master chronology of Newfoundland C. compactum compared to the Atlantic Multidecadal Oscillation (AMO; r = 0.74; Halfar et al., 2011a).
NUMBER 40 • 1 1

aligning a fixed grid to the specimen growth lines on the mosaic then measuring yearly thickness wherever conceptacles were 

present. These rates are supported by seasonal cycling of Mg as 

measured by laser-mass spectrograph and electron microprobe. 

Some direct measurements of yearly growth were made on solution ridges in Hiatella cavities. Conceptacle dimensions were 

obtained by measuring all conceptacles in a mosaic for which 

the pore plate could be clearly discerned. Seasonal stages of reproduction were estimated by examining multiple, haphazardly 

selected specimens with a dissecting microscope.

Terminology

In this volume we use modified classical terms for coralline anatomy. Hypothallium applies to the basal cell filaments, 

where the long axis of the cell is parallel to the substratum (in 

Clathromorphum, multiple layers of cells grow parallel to the 

substratum). The bulk of the thallus, built with filaments whose 

cells have their long axis perpendicular to the substratum, is 

termed the perithallium. When the intercalary meristem was 

first described (Adey, 1964), two new cell types, the meristem 

itself and the photosynthetic epithallium (previously called cover 

cells) distal to the meristem, were added to the lexicon. In Clathromorphum, the cells of both perithallial and hypothallial filaments become linked horizontally by fusion tubes that serve to 

transport metabolites. Epithallium, perithallium, and hypothallium are primary tissues; additional secondary tissues are formed 

in reproduction and wound healing as we shall describe in this 

volume.

RESULTS

Reproduction

Like most corallines, Clathromorphum species have a basic 

red algal triphasic life cycle in which isomorphic 2n (diploid) 

plants (asexual in much of the literature) bear either n (haploid through meiosis) or 2n spores in sporangia, which are in 

turn borne in reproductive structures called conceptacles. The 

2n spores produce new (asexual) spore-bearing plants. The n

spores, on the other hand, produce separate isomorphic male 

and female plants. Both male and female plants produce either 

spermatangia or carpogonia (egg cells) in similar conceptacles 

that are typically considerably smaller than the asexual conceptacles. When the carpogonia are fertilized by the amoeboid spermatia released from the spermatangia, they produce fusion cells 

that in turn develop filaments bearing 2n carpospores. This set of 

2n filaments, borne on the n female plants, is sometimes referred 

to as a carposporophyte generation. The carpospores give rise 

to the 2n (asexual) generation (Adey, 1965; Lebednik, 1976). 

The maturing sporangia and/or their spores of both asexual 

and carposporophyte concptacles dissolve the calcified perithallium surrounding the conceptacle, considerably enlarging the 

approximately 4,000 specimens of coralline algae, including 

C. compactum, now housed at the Smithsonian’s National 

Museum of Natural History in Washington, DC. These collections have not been formally accessioned to the U.S. National 

Herbarium, but are available by contacting the first author. 

During the 2010–2011 cruises, the bottoms from which the 

collections were taken were extensively documented with 

digital still images and video. This digital image archive will 

be available with the collections. A single large sample of 

several fused plants, partially reported here, was collected by 

M. Goobie and E. Edinger at Arctic Bay in northern Baffin 

Island at 72°N. Digital images of the cor-strome bottom in 

Arctic Bay are available with the collection.

Clathromorphum nereostratum (Aleutian Islands)

Three important C. nereostratum specimens utilized in this 

study were collected by Lebednik (1976) at Amchitka; two others were collected by R. Steneck in 2004. The remainder of the 

material (21 specimens) was collected in the summer of 2008 by 

Jochen Halfar (JH, with S. Hetzinger and R. Steneck) on a cruise 

from Akun Island (165°W) in the east to Attu Island (175°E) in 

the western Aleutian chain.

Specimen Preparation

Many of the specimens collected from 1960 to 1964 were 

diamond sawed into smaller blocks and then fixed, decalcified, 

and microtome sectioned in paraffin before being studied with a 

compound light microscope. A large microscope slide collection 

remains part of this material. Recently collected large specimens 

were usually first cut with a diamond saw and then fractured (essentially randomly) with wire cutters. Fragments with the desired 

orientation were then selected for mounting and then carbon 

coated for examination with a Leica Stereoscan 440 scanning 

electron microscope (SEM).

Hiatella arctica is an abundant mollusk clathrostrome borer, 

especially in the Labrador Sea but also in the Aleutian Islands 

(Chenelot et al., 2011). Shells of this bivalve are relatively soft and 

ill suited to scraping; burrows are clearly constantly enlarged by 

dissolution of the Clathromorphum skeleton, perhaps by release 

of an acid. The net effect this enlargement is a natural etching of 

the coralline skeleton. Burrow walls were extracted by diamond 

sawing followed by wire cutter trimming. The appropriate surfaces, carbon coated for SEM examination, have been invaluable 

for understanding biological and mineralogical patterns.

The SEM images were typically taken at 50×, 500×, and 

3,000× (occasionally at 10,000×) as appropriate to the data 

sought. Although many single images were utilized, especially 

of cellular and calcification features, often multiple images were 

compiled into mosaics of vertical fractures. These mosaics allow 

large-scale examination of conceptacle and anatomical layering as well as the determination of the vertical growth pattern 

over time. Conceptacle-based growth rates were determined by 
1 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

mature conceptacles, with roof dimensions and burial depth at 

maturity, are provided in Adey (1965) and Lebednik (1976). 

Since gametangial conceptacles develop in spring rather than 

autumn (when sporangial conceptacles develop), distinguishing 

between them may be necessary in temporal analyses of tissue 

chemical composition. 

Adey (1965; for C. compactum) and Lebednik (1976; for 

C. nereostratum) provided photographic images of several stages 

of development of sporangial conceptacles. However, neither author showed the details of development, particularly relative to 

the simultaneous and essential growth in vegetative tissue, that 

are required for understanding the relationship between anatomy and seasonality. This information is potentially important 

in climate archiving for determining the seasonality of carbonate 

deposition in each vegetative cell. Figure 8 shows the stages of 

development of sporangial conceptacles in C. compactum relative to the surrounding vegetative tissue. Developmental stages 

conceptacle. Whereas sexual and cystocarpic gametangial conceptacles have a single large pore at their apex, asexual sporangial conceptacles are multipored.

Sporangial (apparently diploid) plants (with abundant bior tetrasporangium-bearing conceptacles) are seasonally common among the principal Clathromorphum species, whereas 

gametangial plants (apparently haploid male and female) and 

conceptacles are more or less rare. Adey (1965) examined reproduction in C. compactum, and Lebednik (1976) extensively 

studied reproduction in C. nereostratum. Herein we provide additional information for both species. The earlier work by Adey 

and Lebednik was accomplished with decalcified material studied with light microscopes. Here we emphasize SEM sections, 

observing the conceptacles as they occur buried in the fully calcified skeleton. The diameter and height of sporangial conceptacles 

for both species and for sexual conceptacles of C. nereostratum

are given in Figure 7. Complete dimensional analyses of surficial, 

FIGURE 7. Dimensions of mature conceptacles of C. compactum (105 conceptacles, 13 plants, and 9 stations) 

and C. nereostratum (84 conceptacles, 11 plants, and 7 stations). Colored squares are means of individual 

plants. Female conceptacle data are for C. nereostratum Lebednik, 1976. Male and cystocarpic data are derived 

from a combination of this study and Lebednik (1976). The long arrow describes the path of development of 

C. nereostratum female conceptacles, from unfertilized carpogonia through postfertilization to mature 

carposporangia.
NUMBER 40 • 1 3

FIGURE 8. Development of asexual, bispore-producing C. compactum conceptacles described from specimens collected in the northeastern Gulf of Maine. (A) Early sporangial mother cells and distinctive supporting cells (September–October). Fertile disk (nemathecium) 100–120 μm in diameter; it expands vertically, without primary calcification 

(sporangia or intersporangial filaments), to form a fertile uncalcified cylinder. Initiated as meristem cells at 10–20 μm 

of length, sporangia expand vertically, accommodated by growth in the surrounding calcified vegetative tissue. (B) 

Later stage: sporangia over 100 μm in length with a thick, organic, apical wall or cuticle (to form spore release pore). 

Here a decalcification “front” below and to the sides of the fertile cylinder is seen; cell crushing has yet to occur. Eight 

to 12 vegetative cells have developed in the surrounding vegetative crust to allow sporangial growth. (C) SEM image 

of an aborted conceptacle just prior to the stage shown in B (northern Labrador). (D) Later stage with further decalcification; sporangial enlargement laterally and some crushing of surrounding vegetative cells. The overlying epithallial 

cells have broken off to expose the conceptacle roof (white disks seen from surface). A later surface view of this stage 

is shown in Figure 9C, D. (E) Light microscopic image of mature conceptacle at full, mature dimensions (December–

January), with decalcification and crushing of lateral and underlying vegetative cells, and spores forming inside the 

sporangia. A, B, and D were drawn from microtome sections of winter plants. C is a SEM image of a calcified, fractured section. E is a decalcified and stained microtome section. All images are at the same scale, indicated by the bar.
1 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 9. SEM images of typical C. compactum surfaces from different regions showing reproductive state during midsummer (see 

Table 1). (A) Northeastern Newfoundland, conceptacles mostly grown in, but remain clearly visible. (B) Southern Labrador, conceptacles 

ranging from immediately postmature to grown in. (C) Northern Labrador, conceptacles mostly fully mature; the low mound in the 

lower center is a submature conceptacle with a conceptacle cap not fully broken out. (D) Conceptacle roof at larger scale; pores for exit of 

the spores are mostly free of sporangial cap walls; a few dried pore plugs remain. During summer in the Gulf of Maine, conceptacle roofs 

with visible pores are not found, and only faint conceptacle “ghosts” appear in 60%–70% of the population. Note the strong chiton 

grazing marks in A and C and also in B, although somewhat grown out.

of C. nereostratum are not shown in similar detail since full seasonal, decalcified, and sectioned material is not available. However, it is clear from preliminary analyses that the patterns are 

very much the same.

Reproduction in Clathromorphum compactum

Adey (1965) demonstrated the seasonally determined development of sporangial conceptacles in C. compactum in the 

Gulf of Maine, where conceptacles are initiated in early autumn 

(September and October), reach maturity in midwinter, and are 

fully overgrown by late spring. The farther north C. compactum

plants grow, the later their reproductive maturity is; in northern 

Labrador, most plants are at the peak of the reproductive cycle in 

midsummer, the surficial conceptacles being full of ripe sporangia (Figure 9; Table 1). Conceptacle initiation is likely controlled 

by the photoperiod, with light rapidly diminishing in September and October; temperature is likely not a significant factor 

as there is a considerable difference in temperature from south 

(approximately 10°C ) to north (approximately 5°C) at this time.

The developmental morphology of a typical sporangial conceptacle of C. compactum from southern Labrador is shown in 
NUMBER 40 • 1 5

analysis of conceptacle bands in a C. compactum plant from Labrador (Figure 12A,B), where every fifth to seventh year a growth 

ring is devoid of a conceptacle band. Specimens have been found 

in which extensive conceptacle production has occurred for several consecutive years, followed by years with few or no conceptacles (Figure 2B). In one very old specimen from northern 

Labrador, several hundred years’ worth of missing conceptacle 

bands were seen. This phenomenon implies that anatomy must 

be consulted, in addition to measuring the number of conceptacle bands or the thickness between bands, in order to obtain 

an accurate yearly archive. If it is suspected that several years are 

missing, this suspicion is relatively easy to confirm with anatomy. 

If conceptacles were apparently missing for many years, it would 

be necessary to confirm by counting each year’s Mg cycle. As 

shown in Figure 12B, broken-out conceptacles can “grow in” 

by regrowth of vegetative cells from the base and sides, nearly 

obliterating evidence of the presence of the conceptacle in a superficial analysis. The perithallial tissue that has grown back into 

the conceptacle cavity will have formed several months later than 

the surrounding tissue, depending on geographic latitude.

In the specimen shown in Figure 12B, the years 2005 and 

2006 lack buried conceptacles. For the year 2007, a brokenout conceptacle appears on the right (note the presence of a full 

conceptacle farther to the left). During the summer following 

breakout, new tissue formed at the base of the conceptacle and 

refilled the cavity during the following summer. This new tissue 

was formed months later than the surrounding vegetative tissue. 

A laser scan passing through the broken-out and grown-in conceptacle would show carbonate chemistry totally out of phase 

with that of the larger specimen on the same plane, unless the 

presence of this grown-out conceptacle were taken into consideration. Conceptacle cavities are oblate spheroids; because sporangial formation begins in autumn (see Figure 10), a horizontal 

plane through the principal diameter of the spheroid approximately marks the beginning of October.

Figure 10A. The sporangial caps (plugs), which are embedded in 

the calcified conceptacle roof tissue, and the uncalcified sporangial mother cells are together about 150 μm long at maturity (before spore formation). The sporangia and surrounding vegetative 

filaments form a developmentally uncalcified fertile cylinder that 

is approximately 100 μm in diameter and 100 μm long before 

final expansion to sporangial maturity. As we shall show, fertile 

cylinder development requires the accompanying production of 

about 10–12 cells in each filament of the surrounding vegetative 

tissue. Near sporangial maturity, the carbonate component of an 

80-μm-thick underlying vegetative tissue is dissolved beneath the 

enlarging sporangia, with an additional 70–80 μm of carbonate 

also dissolved laterally, to make room for the large sporangia to 

fully mature. The sporangia produce bispores, each of which is 

approximately 1,000 times greater in volume than the individual 

surrounding vegetative cells. The total noncalcified, organic volume of crushed vegetative cells is approximately equal to the 

final spore volume. In the southwestern Labrador Sea, this final 

expansion phase occurs in late spring and early summer, just 

after ice breakup, when available light should be at a maximum. 

Figure 10B, reduced to show primarily sporangial development, 

provides a mean pattern for northern Labrador, where conceptacle maturation is delayed even longer into the next summer.

Sporangial conceptacle development is initiated in early autumn, and at maturity carbonate solution and crushing of previously formed summer vegetative tissue occurs to about 80 μm 

below the plane of sporangial initiation. In southern Labrador 

and northernmost Newfoundland, there is a greater level of vegetative cell fusion for a limited period at the time of sporangial 

initiation. This cell fusion creates a weak zone in the carbonate, 

and horizontal fractures are easily induced on this plane, as can 

be seen in Figure 11.

As shown by Adey (1965) for the Gulf of Maine and here 

for the core Subarctic (Table 1), 20%–30% of the plant surface 

in each year does not become reproductive. This is seen in an 

TABLE 1. Summer reproductive state as a percentage of specimen surface.

Subregion

Not reproductivea

(%)

Initial stateb

(%)

Mature 

conceptacles 

(%)

Conceptacles 

growing out 

(%)

Faint conceptacle 

remains 

(%)

Northern Labrador 19 0.3 40 36 3.5

Southern Labrador 32 0 32 31 4.5

NE Newfoundland 62 0 3 15 20

Northern Gulf of St. Lawrence 52 0 Trace 3.1 45

Gulf of Mainec 30 0 0 10 60

a

Midsummer (July–August) reproductive (asexual) state in Clathromorphum compactum from northern Labrador to the Gulf of Maine. The values 

for each of the Subarctic subregions are estimated from 40 haphazardly selected sets of undamaged specimens with a 20–50 cm2 surface, estimated 

using a dissecting microscope. 

b

Conceptacle caps. 

c

From Adey (1965).
1 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 10. Clathromorphum compactum conceptacle and sporangial formation. (A) Dimensional and cellular development of average bisporic conceptacle in southern Labrador 

relative to season and vegetative tissue. Numbers to the right are averages and can vary with 

region of development. (B) Sporangial development with time in northern Labrador. In the 

Gulf of Maine, because of higher vegetative growth rates, this process occurs from October 

to January.

Reproduction in Clathromorphum nereostratum

A detailed developmental analysis of reproduction in 

C. nereostratum is not available and would require a set of 

specimens taken in the Aleutian Islands throughout the autumn. 

Nevertheless, the photographic images published by Lebednik 

(1976) are adequate to show that the pattern is similar enough 

to that of C. compactum to allow the use of Figure 8 (developed 

for Gulf of Maine populations) but not Figure 10 (developed 

for Labrador). However, there are a number of additional differences that are critical to interpretation for climate archiving. 

Of the 26 specimens of C. nereostratum examined from the 

Aleutian Islands, 24 were collected in summer (June–August) 

and 2 in December. Of the 24 specimens collected during the 

summer, 2 had single-pored gametangial conceptacles at their 

surface. One of these two plants had mature fertilized female 

conceptacles (carposporangial conceptacles), whereas the other 

had postprime male conceptacles with open pores remaining. 
NUMBER 40 • 1 7

are somewhat larger in diameter than sporangial conceptacles 

(Figures 7, 13). However, they are not as tall, suggesting that 

carposporangial tissue dissolution is not as extensive beneath the 

conceptacle. Since carposporangia are produced only laterally 

from fertilized carpogonia (egg cells), centrally there is no dissolution, resulting in the formation of a central columnella, leading 

to dumbbell-shaped conceptacles. For a detailed description of 

the development of sexual conceptacles in C. nereostratum, see 

Lebednik (1976). Carposporangial conceptacle development has 

not been described in C. compactum, but it is likely quite similar. The presence of a central columnella and dumbbell-shaped 

conceptacles shows that it is the developing sporangia (bisporic, 

tetrasporic, or carposporic), not the vegetative cells, that provide 

the acid for surrounding carbonate dissolution.

Female conceptacles are located midway through the yearly 

cycle (Figure 13B,C), with a sharp perithallial boundary in late 

autumn (see below). On the other hand, sporangial conceptacles 

are located near the upper (later) boundary of the cycle (Figure 13A). In medial sections, sporangial conceptacles are oval in 

shape, whereas female conceptacles are dumbbell shaped, with 

a central columnella. In sporangial conceptacles, the recalcified 

sporangial walls are vertical, whereas the female conceptacle carposporangia and supporting structures appear as packed spheres 

of many sizes (Figure 13B). 

Cellular and Anatomical Structure

Aside from a basic pattern of upright filaments of cells 

combining to form a calcified mat showing vague “rings,” the 

perithallial vegetative anatomy of Clathromorphum, as seen in 

Although degenerate (broken-out) or faint ghosts of growing-in 

sporangial conceptacles were sometimes present in the remaining 

22 specimens and buried sporangial conceptacles were present 

in section, no mature, multipored sporangial conceptacles were 

seen at their surfaces. In section, the most recent band of buried 

conceptacles occurred about 100 μm below the meristem, indicating maturity the previous winter.

Both specimens collected in December presented premature 

to mature sporangial conceptacles (Figure 13A). It is not usually 

possible in SEM images to distinguish between bisporangia and 

tetrasporangia in buried conceptacles (the latter likely indicating meiosis and reduction to the haploid state in the spores). 

However, both December specimens presented tetrasporangia, 

and Lebednik (1973) found only tetrasporangial conceptacles in 

this species. Although the data are minimal, this finding suggests 

that C. nereostratum generally has the triphasic and isomorphic 

alternation of generations described earlier. In this case, sporangial (2n) plants reproduce in autumn, maturing in winter (as in 

C. compactum in the Gulf of Maine and Nova Scotia) and gametangial (1n) plants reproduce in spring, maturing in summer.

On the basis of available collections, gametangial plants are 

probably infrequent in C. nereostratum (very extensive collections demonstrate rarity in C. compactum). Thus, especially in 

C. nereostratum, it is essential to identify the type of conceptacle 

(sporangial or gametangial) in order to determine the developmental timing of the conceptacle compared to the vegetative tissue. Male and female conceptacles are quite small compared to 

sporangial conceptacles; although both become buried, they are 

not likely to be confused for sporangial conceptacles (Figures 7, 

13). Fertilized female conceptacles (producing carposporangia) 

FIGURE 11. Horizontal fracture in a specimen of C. compactum collected in summer of 2010 (Great Northern Peninsula of Newfoundland). (A) The narrow bench to the left is the meristem fracture zone. (B) The main fracture bench (center in A) occurred on a plane with 

a high level of cell fusion in the autumn of 2009 (when sporangial development initiated). Also visible is the transition from summer to 

winter in perithallial tissues.
1 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 12. (A) Thickness of yearly bands in C. compactum from southern Labrador (specimen 10-7S (1a)). The 

number of asexual conceptacles in each band, in the limits of the SEM mosaic, is indicated. (B) SEM of C. compactum from the Great Northern Peninsula of Newfoundland, showing yearly bands of conceptacles. This is a faceted 

specimen, with the facet boundary represented by the abrupt change in the slope of the conceptacle planes and ragged 

vertical lines on the left (see Figure 18). A broken-out conceptacle (2006/2007) is shown by the arrow on the right, 

with tissue formed from the base of the conceptacle refilling cavity; this tissue formed months later than the surrounding vegetative tissue. 
NUMBER 40 • 1 9

in the summer and early fall (Figures 14A, 14B, 15). This pattern 

is strongly apparent in most C. nereostratum specimens from the 

Aleutian Islands but less so in C. compactum specimens from the 

northwestern North Atlantic. 

Since total filament diameter, including the calcified cell 

walls, is fixed at roughly 10–11 μm in C. nereostratum and 

9–10 μm in C. compactum (except when filament branching 

and tissue expansion is occurring), it is the total calcified cell 

wall thickness that changes seasonally (Figure 16A,B). As can be 

seen clearly in Figures 16 and 17, there is a well-defined inner 

wall, with small, prismatic, radially oriented calcite crystals that 

maintain about the same length (1 μm) and character throughout their distribution and annual cycle. This wall type has 

been described for most corallines for the last several decades 

a dissecting microscope view of a vertical fracture or polished 

slice, may superficially appear to be without structure. However, 

at higher magnification, it is seen to be a rich mosaic, deriving 

from the genetic control of cellular and tissue development as 

influenced by the physical and biological environment. Measurements of cell dimensions in SEM images demonstrate this 

genetic-physical interaction. As shown in Figures 14A, 14B, and 

15, cell dimensions change seasonally. Cells within each filament 

are linked by pore plates (pit connections and pit plugs in most 

red algae), and the length, pore plate to pore plate, varies more 

or less consistently from about 8 to 15 μm for both species; the 

cell lumen diameter likewise ranges from 2 to 6 μm. There is a 

strong tendency for cells to be shorter and wider in the winter 

and early spring, with a lengthening and narrowing of the lumen 

FIGURE 13. Clathromorphum nereostratum conceptacles in SEM images. Note that recalcified sporangium cell walls tend to be vertical 

in asexual conceptacles (A; reflecting vertical orientation of sporangia), whereas cystocarpic conceptacles (B) appear as small angular 

circles of various sizes (left arrow in B; cells of gonimoblast filaments [upper arrow] produce cystocarpic sporangia laterally). (A) Yearly 

layers of buried bi- or tetrasporangial conceptacles (sporangial walls recalcified after burial; arrows). (B) Mature female (cystocarpic) 

conceptacles. Midsections show a dumbbell shape (bottom right arrow) because of dissolution of the surrounding carbonate by peripherally developed spores. (C) Small, ovoid, male conceptacles with recalcified spermatangial mother cell walls (arrow). 
2 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

individual plants are common, especially in the warmer part of 

the C. compactum range, domes featuring more or less flat facets 

separated by slightly grooved ridges are more typical (Figure 18). 

Facets arise when the scattered filament branching required to 

form the domed morphology of C. compactum occurs in localized vertical planes. Facets can shift with time or split in two 

for several years. Conceptacles generally do not form near facet 

boundaries; when a facet does develop, previous nearby conceptacle areas can become nonreproductive. Also, different facets 

on the same plant can grow at different rates. For that reason, 

growth rates in mound-forming C. compactum are taken in the 

middle of the dome.

Clathromorphum nereostratum can develop into a much 

thicker crust (up to 50 cm) than C. compactum (up to 12 cm). 

This is partly due to the much slower growth of C. compactum

in the colder water of the core Subarctic and Arctic (see below). 

The crust thickness achieved by C. compactum in warmer Labrador waters, for example, is comparable to that of C. nereostratum, taking into account the difference in the yearly growth 

(reviewed by Adey, 1998; see also Adey et al., 2005). However, 

in Clathromorphum species, especially during summer and autumn, the space between the filaments becomes filled with much 

larger, often spear-shaped, vertically or diagonally oriented calcite crystals (interfilament crystals). As shown in Figure 17C, the 

inner-wall crystals are formed within the organic membranes of 

the cell, whereas the deltoid interfilament crystals are formed 

in the cavity between the filaments (Figures 16A, 17B,C). This 

phenomenon is coincident with the narrowing of cell lumens. 

Interfilament crystals tend to be present year-round. However, 

in winter they are far less abundant, the cell lumens being larger 

in diameter. Thus, summer and fall tissue is considerably denser 

than winter tissue.

Unlike the closely related, sheet-forming species Clathromorphum circumscriptum (which occurs in shallower water and tide 

pools), mature C. compactum tends to be dome shaped. Large 

sheetlike (clathrostrome) formations often develop, especially in 

the northern Subarctic, but they form from the coalescing of adjacent C. compactum plants. Although smooth, dome-shaped, 

FIGURE 14A. Clathromorphum compactum variation in cell dimensions with depth in perithallium: mean perithallial cell dimensions, 

as measured in two crusts, from meristem, with depth (summer collected in southern Labrador; mean of two consecutive years, three 

cell rows). L/W = length/width. 

FIGURE 14B. Clathromorphum compactum variation in cell dimensions with depth in perithallium: mean dimensions from five 

continuous years, matched peak to peak (summer collected from 

northern Labrador). L/W = length/width; Tk = thickness
NUMBER 40 • 2 1

damage to crusts, and likely because of less successful recruitment, 

C. compactum plants are more scattered and rarely exceed several centimeters in thickness and 100 years of age. As noted 

above, C. nereostratum likely evolved from a C. compactum–

like ancestor (Adey, unpublished data); the primary innovation 

was the development of a thicker hypothallium allowing a freestanding cantilevered morphology.

Biologically Induced Etching as a Source of Information

Hiatella arctica is a common Subarctic bivalve that establishes burrows within the calcified perithallium tissue of Clathromorphum crusts. Apparently, H. arctica larvae settle at the 

margin or on a damaged surface of a young plant and are buried 

by plant growth. The bivalve then grows along with the perithallium, enlarging its burrow by gradually decalcifying the coralline walls surrounding it. If a coralline sample is collected with 

the animal still alive, the burrow wall can be seen to be etched 

into ridges and valleys corresponding to the yearly layers of C. 

compactum growth (Figures 19, 20). The etching is probably accomplished with an acid secretion, although localized CO2

 production by the bivalve, accompanied by pH reduction within the 

confined space of the burrow, could also be a factor. The cell wall 

carbonate formed in summer, being about two times denser than 

that in winter, forms the ridges, and the less dense winter cell 

walls form the valleys. Also, particularly as seen in longitudinal 

rates. However, even in the Gulf of Maine, the southern limit 

of C. compactum, where the yearly mean temperature and 

growth rates are similar to those of C. nereostratum, C. compactum plants remain much thinner. This is partly due to the 

“leafy” growth morphology of the hypothallium (the basal tissue that grows parallel to the substrate) of C. nereostratum. In 

C. compactum, the hypothallium has a mean thickness of 3.5 

cells (maximum 6 cells) and 22 μm (maximum 43 μm), and 

the cells are tightly adherent to the substrate (Adey, 1965). In 

C. nereostratum, on the other hand, the hypothallium has a mean 

thickness of 16.8 cells (maximum 24) and 135 μm (maximum 

206 μm; Lebednik, 1976); the growing margin is thick enough to 

be structurally freestanding and often becomes cantilevered off 

the substrate for a considerable distance.

Clathromorphum nereostratum is thus capable of growing over obstacles, and if the growing margin is damaged, a 

secondary hypothallium, formed from perithallium, grows out 

over the damaged area (primary hypothallium develops initially 

from a settled spore on the rock or shell substrate). Individual 

C. nereostratum plants can thus be much broader than those 

of C. compactum (Figure 2F) and have the capability to 

achieve greater thickness in a single plant. Clathromorphum 

compactum produces a clathrostrome largely by the fusion of 

many individual small plants. These can be any size, depending upon the recruitment density. At the warmer margin of its 

temperature limits in the Gulf of Maine, perhaps because of the 

warmer summer temperatures, which allow greater invertebrate 

FIGURE 15. Clathromorphum nereostratum cellular anatomy. Cell dimensions with depth in 

perithallial tissue. (left) Amchitka plant taken in the 1970s. Mean cell dimensions, two successive 

years. (right) Plant from Amchitka, taken in 2008. Mean, three parallel filaments, single year.
2 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Growth Rate

On the basis of combined analyses of conceptacle bands 

and cellular anatomy, the thickness of yearly bands in Clathromorphum compactum and C. nereostratum can be defined using 

mosaics of SEM images. Further combined with measurements 

of the bivalve-etched ridges, as described earlier, regional growth 

rates for Clathromorphum compactum are shown in Figure 21. 

There is a highly significant and consistent drop in overall crustal 

growth rate from south (Gulf of Maine) to north (northern Labrador and Arctic Bay, Baffin Island). The plants for which these 

intervals were measured were selected haphazardly from available SEM sections having clearly defined conceptacle bands. No 

effort has been made to compare the same years in each region, as 

this would require a more defined ecological depth range for each.

fractures (Figures 16B, 17C,D), interfilament crystals are much 

larger (to 5–6 μm long) than inner-wall crystals and tend to be 

arrowhead shaped (Figure 17B). 

A closer look at the etched valleys shows that the smaller, 

radial, inner-wall crystals are more resistant to solution than the 

larger, vertically oriented, interlamellar crystals. This is a difference in crystal morphology that results in winter cells that tend 

to break out of the carbonate matrix as silt-sized, hollow grains 

(Figures 19D, 20A). The inner-wall crystals are embedded in an 

organic matrix that likely controls their development (Giraud 

and Cabioch, 1979). Thus, they are somewhat protected from 

dissolution (Ries, 2011). As discussed below, the interfilament 

(interlamellar) crystals may be precipitated because of CO2

 removal in the inorganic interfilament space and therefore lack 

protection from dissolution from an organic matrix.

FIGURE 16. Clathromorphum compactum calcified wall structure. (A) Transverse fracture showing summer cells with large interfilament calcite crystals between rings of small, radial, inner-wall crystals (crystals 1 μm long). (B) Longitudinal fracture of summer cells 

showing large, angular interfilament calcite crystals and thin inner walls of fine, radially oriented crystals. (C) Winter cells of fine, radial, 

inner-wall calcite crystals. Interfilament crystals are only at cell “corners.”
NUMBER 40 • 2 3

information (Figure 22), converted to monthly rates and plotted 

against the regional temperature curves (Figure 23A), monthly 

regional growth curves can be derived (Figure 23B). Total yearly 

growth and the rate of conceptacle maturation (based on the 

regional height requirement for maturation) can then be summed 

from the monthly rates. The latter match the data presented in 

Table 1. Although laboratory-produced growth rates for Clathromorphum compactum are not yet available, those for C circumscriptum (Adey, 1970, 1973) suggest that at temperatures 

below 5°C–6°C, temperature (and not light) is the primary environmental factor controlling vertical growth. Monthly growth 

The regional growth rates presented in Figure 21 are plotted 

as a function of yearly mean regional temperature in Figure 22. 

The Arctic Bay temperature is an estimate based on a 9-month 

sea ice interval of –1.8°C and a 3-month ice-free interval of 

3.5°C. As we will show in a future paper (Halfar and Adey, unpublished), when sea ice is consistently present longer than about 

2 months, growth ceases, probably because of a lack of sufficient stored photosynthate. This drop in expected growth relative to temperature is producing a highly significant proxy for 

sea ice cover. Using the straight-line (GOM to southern Labrador) part of the yearly growth curve with the greatest amount of 

FIGURE 17. Clathromorphum nereostratum from the Aleutian island of Amchitka. (A) SEM of vertical fracture with overlying epithallium, underlying perithallium, and meristem with a break in calcification. Inner cell layer of radial crystals (red arrow); vertically oriented 

interfilament crystals (blue arrow). (B) SEM looking downward into meristem with epithallium removed. A smooth organic material 

coats the inner wall (red arrow); large deltoid interfilament crystals (blue arrow), apparently with no integral or overlying organic material, lie between the inner wall organic material. (C) Unfractured meristem cells showing the inner-wall inner membrane (IM) and outer 

membrane (OM), the fractured calcification zone (CZ), and the precipitation cavity (PC). (D) Clathromorphum nereostratum from Rat 

Islands, Aleutian Islands. Summer perithallial cells showing cell fusions formed after burial in the perithallium (horizontal arrows) and 

pit connections (vertical arrows) between cells of a filament.
2 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

corallines (Adey et al., 2005), the interfilament calcite crystals in 

Clathromorphum are larger and more irregular than the innerwall crystals; the latter are short, prismatic, very fine, and oriented radially. The interfilament crystals are oriented vertically 

or diagonally and tend to be deltoid in shape. The thickness of 

the radial, inner-wall crystals remains largely unchanged seasonally, whereas interfilament calcification is thick in summer and 

absent or thin and irregular in winter. This pattern also occurs 

in the naturally etched surfaces of bivalve-bored cavities, where 

the layers form ridges in the summer and grooves in the winter 

(Figures 19, 20).

In decalcified sections (Figure 8E), epithallial filaments, 

lacking cell fusions, often disaggregate. In perithallial tissues, the 

filaments are mostly cohesive because of the fusions organically 

linking adjacent filaments. Nevertheless, between the fusions and 

in the cells below the meristem where fusions are lacking, filaments can locally disaggregate since there is no common interfilament wall. In the perithallium, inner calcified cell walls are 

organically framed, whereas the space between the filaments is 

apparently devoid of organic material and may or may not be 

filled with carbonate, depending on the season. It has been widely 

accepted that calcification in corallines is “simple” precipitation 

resulting from removal of CO2

 during photosynthesis, with organic nucleation centers specifying calcite rather than aragonite 

(Ries, 2010; however, see Adey, 1998). This is highly unlikely in 

Clathromorphum species of Arctic and Subarctic seas because as 

rate as a function of temperature fully explains differences in 

both mean yearly thickness and conceptacle maturity time for 

C. compactum from the Gulf of Maine to Labrador and for C. 

nereostratum in the North Pacific. Since detailed temporal conceptacle development data are not available for C. nereostratum, 

approximate temperature-growth curves are presented, but conceptacle development is not included on the graph. On the basis 

of a comparison with Gulf of Maine data, conceptacle maturation of C. nereostratum in the North Pacific should be similar 

to, but a little slower than, that of C. compactum in the Gulf of 

Maine. Field data from the Aleutian Islands are inadequate to 

fully verify this hypothesis.

Wall Structure and Calcification

As demonstrated by Adey (1965) for C. compactum and 

by Lebednik (1976) for C. nereostratum, all perithallial growth 

and calcification in Clathromorphum occurs in the primary 

meristem. Herein growth and calcification are shown to occur 

along a narrow horizontal plane through the meristem (Figures 

17, 24). With no bridging calcification (perithallium to epithallium), a fracture plane can be easily induced. Although a secondary meristem can form within broken-out conceptacles or 

on damaged surfaces (in the uppermost perithallium), the primary meristem produces most of the calcified tissue. As shown 

in Figures 16A,B, 17B,D, and 24B and unlike other genera of 

FIGURE 18. Shallow-water habitat (3–5 m), with young (estimated 60 years old), 

mound-forming plants of C. compactum in NE Newfoundland. Some plants are 

strongly faceted (right arrow); others are more dome-shaped without facets (top arrow). 

Several plants are fusing and with time will develop clathrostromes. The branching red 

coralline is Lithothamnion glaciale (left arrow). Image by Alok Mallick.
NUMBER 40 • 2 5

FIGURE 19. Images from Hiatella-etched cavities in C. compactum from southern Labrador. (A) Ten years of growth with ridges and 

valleys for each year (summer, top arrow; winter, bottom arrow). (B, C) Surface of summer-fall ridge showing dense interfilament crystals 

(vertical arrow) maintaining structural integrity (horizontal arrow in C shows inner radial crystals). (D) Winter valley showing the breaking out of minimal interfilament crystals (horizontal arrows) and the integrity of individual cells and their organic radial-crystal-embedded 

walls (vertical arrow). (E) Oblique view of the ridge side, showing the intermediate breakdown stage and the great difference between fine 

inner-wall crystals (vertical arrows) and large, angular interfilament crystals (horizontal arrows).
2 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

on organic templates and metabolically emplaced by ion pumps 

in cell membranes. If so, rather than being diffusely distributed 

over the length of the meristem cell and into upper perithallial 

cells, these carbonate additions occur in a plane in the meristem 

(i.e., a ring around the “middle” of each cell). On the other hand, 

interfilament calcite formation in northern waters, strongly tied 

to summer tissues, could result from precipitation as a result of 

photosynthetic CO2

 removal by the epithallium. This remains to 

be determined in laboratory studies.

Clathromorphum spp., along with many coralline genera, 

not only have a considerable ability to turn calcification on and 

off (for example, in conceptacle formation) but are also broadly 

has been shown (discussed further below), they can continue to 

grow and calcify for at least part of a sunless winter. (Laboratory 

studies underway also show repairs to damage of the perithallium with growth in total darkness; Adey et al., unpublished).

Moreover, in Labrador and the high Arctic, where clathrostromes lie 10–30 m deep under several meters of sea ice and 

snow for 6–10 months of the year, winter calcification driven 

directly by photosynthetic CO2

 removal seems unlikely. The 

pattern of inner-wall calcification remains seasonally constant, 

changing only in cell length and requiring only additional radially placed integral crystals of the same form. As suggested by 

Adey (1998), inner-wall crystals in corallines are likely nucleated 

FIGURE 20. Sections of C. compactum from nearby stations in northern Labrador, 

off Nain, over a single year of growth, showing two summer bands (arrows) of 

dense interfilament calcification separated by a wide band of winter cells having 

little interfilament calcite. (A) Etched wall of a Hiatella cavity, 9–11 m depth at Jenks 

Island. (B) Vertical fracture of a plant from Baker Island, 12–14 m depth. These 

yearly bands are not of the same age; B shows a year with 20% more year growth 

than A, as arrows indicate. 
NUMBER 40 • 2 7

capable of dissolving already emplaced carbonate. In the conceptacle fertile cylinder, during the formation of sporangia from the 

meristem, carbonate is not laid down in the cell walls of intrasporangial filaments; 100 μm away in the vegetative tissue, normal calcification continues to occur. As sporangia enlarge, they 

are able to dissolve a large volume of cell wall carbonate in the 

surrounding and underlying vegetative tissue. These decalcified 

tissues are crushed by the final enlargement of sporangia prior to 

spore formation. Later, after spores are released, the thin, empty 

sporangial walls become calcified (Figures 12B, 13A). Likewise, 

the inner walls of meristem cells and the interfilament space are 

(in summer) emplaced in the meristem fracture zone with carbonate; when cut off by cell division, this carbonate joins the 

underlying perithallium. Then, two to five cells into the perithallium, passages (fusions) are excavated out of calcified cell walls, 

laterally, to join the lumina of adjacent cells. Especially in the 

autumn, when sporangia begin development, these fusions may 

extend laterally for several cells (Figure 11B). Although the number of fusions varies considerably at the autumn “break,” when 

sporangial formation is initiated, they are often so abundant 

that they develop a plane of weakness that fractures horizontally 

when breaking stresses are applied when creating fracture sections (Figure 11A).

Where bivalve boring (and carbonate etching) and deeply 

grooved sea urchin grazing occur, breaking the “seal” of living 

tissue over dead carbonate, alteration of carbonate chemistry is 

likely. These diagenetic zones have ecological signatures, often 

with the formation of epi- and endophytes on the dead crust. Also, 

in thick clathrostromes, occasional fractures develop because of 

wave or moving substrate stresses. Alteration of carbonate along 

FIGURE 21. Clathromorphum compactum. Regional yearly crustal accretion of haphazardly selected specimens and years as a function of 

latitude in the northwestern North Atlantic, Labrador Sea, and Arctic Bay, northern Baffin Island. The red squares are individual specimens. 

In Newfoundland (NF) and Labrador, each data set included one sample from Hiatella-etched burrows; otherwise, data are from analyses of 

conceptacle layers on SEM mosaics.
2 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

especially on the more protected parts of outer coast island complexes, where wave exposure is moderated, clathrostromes are 

often well developed. Particularly, where stable bedrock shores 

have a minimum overburden of glacial till (avoiding wave tools) 

yet have enough wave action to seasonally limit sea urchin grazing, an optimum environment for carbonate production in C. 

compactum is present. Low-lying, domed bedrock islets lacking 

the high cliffy shores that could shed falling boulders and cobbles 

onto the underlying shore can have particularly well-developed 

clathrostromes. Moderately steep bottoms of cobbles and large 

boulders that limit downslope movement create the optimum 

conditions for preserving clathrostromes for many centuries.

such fractures is sometimes clearly visible in SEM images. Generally, such alteration occurs only near damage sites and is easily 

detected and avoided. As older clathrostromes are discovered, it 

will be necessary to carefully examine the oldest part of the coralline carbonate for potential diagenesis.

Ecology and Geomorphology

The 2010–2011 cruises to Labrador demonstrated that outer 

coast islands can provide localized optimum conditions (Figures 

2A,B, 25A,B) for the development of clathrostromes of Clathromorphum compactum. On the leeward sides of these islands and 

FIGURE 22. Growth rate of C. compactum (red) and C. nereostratum (blue) as a function of mean yearly ambient temperature. The regional 

temperature derivation is described in the Figure 23 caption. The downturn in the curve on the right is due to the length of winter sea ice (Halfar, 

unpublished data).
NUMBER 40 • 2 9

FIGURE 23. Model demonstrating regional temperature control of monthly growth in thickness and reproductive maturation in C. compactum, using the yearly temperature curve of Figure 22 (see text for complete description). (A) Regional temperature at 12–17 m depth for coastal 

waters (the Gulf of Maine from Gulf of Maine Ocean Observing System buoys, mean of Penobscot and eastern shelf buoys, 2 and 20 m, 2011 

data, –1.0°C for samples from 1960s) and southern Labrador and NE Newfoundland summer data from 1964 and 2003–2011 cruises of the 

R/V Alca i, with winter estimated as –1.5°C when sea ice was present (from U.S. Navy Hydrographic Office Sailing Directions). (B) Expected 

regional monthly growth rates derived from the curves in A and Figure 22, summed for yearly means. The expected time of conceptacle development based on 100-μm perithallial growth to reach expansion phase and 1 month for expansion and 1 month to maturity. Dashed horizontal 

lines are conceptacle development time. Clathromorphum nereostratum curves are added for comparison, but conceptacle development is not 

shown (see text). 
3 0 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

Thus, there is an inverse relationship between the success of 

C. compactum and H. arctica; when the factors supporting strong 

clathrostrome development are optimal, boring by H. arctica is 

most limited. Burial of the base of old C. compactum mounds by 

accumulating fine sediment can also create anaerobic zones that 

prevent further Hiatella boring. Under these conditions, continuous carbonate accumulations exceeding 1000 years can develop 

(Adey, unpublished).

Lithothamnion lemoineae, a branching coralline species, 

has an ecology similar to that of Clathromorphum compactum. 

Although generally less abundant, it is an integral component of 

northwestern Atlantic clathrostromes. Lithothamnion lemoineae

is a particularly important component of clathrostromes in that 

it often “seals” the sides of C. compactum mounds, thereby 

Hiatella arctica, a boring bivalve, is the chief biotic component responsible for degrading and limiting Clathromorphum 

compactum buildup in the northwestern Atlantic. Hiatella arctica also occurs in C. nereostratum in the North Pacific (Chenelot et al., 2011), but it is overshadowed by an abundance of 

other invertebrate infauna. Hiatella arctica must gain access to 

the C. compactum crust during settlement at a growing coralline 

margin or following sea urchin grazing or other injury. The intercalary meristem, with an epithallium subject to constant chiton 

grazing (and more occasionally sea urchin and limpet grazing), 

prevents most invertebrate and seaweed recruitment. When recruitment of several coralline species has been optimal, entirely 

covering a rock surface with coralline carbonate, and when sea 

urchin grazing is limited, H. arctica recruitment is minimal. 

FIGURE 24. Meristem fracture and calcification zone in a specimen of C. compactum from southern Labrador for comparison with 

C. nereostratum (Figure 17). (A) The meristem (arrow to the right) shows fracturing in the calcification zone. The conceptacle formed the 

previous fall and winter, with expansion down into the previous summer band. A new meristem formed over roof but has not yet filled 

the depression in the epithallium (see Figure 9B). (B) Fracture zone in the meristem. (C) Fracture zone in the meristem opened up to reveal 

distinct interfilament grooves (precipitation cavities?) between meristem cells (arrows). (D) Meristem fracture zone (in summer) looking 

into the perithallium. Dense organic material covers the inner-wall crystal band, with interfilament crystals having no organic cover.
NUMBER 40 • 3 1

FIGURE 25. (A) Typical boulder slope on low islands in northern 

Labrador (at 25 m depth). Rock surfaces covered with coralline 

crust dominated by C. compactum. Large, angular, sheet-fractureproduced boulders protect glacial cobbles and small boulders from 

downslope movement. (B) Diver with 105-mm-thick clathrostrome 

extracted from the same locality. At a summer temperature of 5°C–

8°C, the growth rate of this crust was about 130 μm yr–1, with an 

age exceeding 800 years.

clathrostrome development (Figure 26). Since all collections 

(2010–2011) were taken by a single individual and dives were of 

a uniform length, the number of samples (N) taken at each station depth are an indicator of the abundance of thick material. 

As shown in Figure 26, for southern Labrador, clathrostrome 

buildup also tends to peak at optimum abundance depths and 

at mid-wave exposures. This is generally below the shallower 

Alaria kelp zone but within the Agarum savanna (Adey and 

Hayek, 2011), from 10 to 25 m. In northeastern Newfoundland and the northern Gulf of St. Lawrence, where the water 

is generally more turbid, peak clathrostrome development occurs at shallower depths (5–10 m). The thickest C. compactum

collected in the northwest North Atlantic to date were taken 

off Hopedale, Labrador, in the summer of 2011. Several crusts 

exceeding 100 mm in thickness were found.

Tissue Irregularity

Under some conditions, the perithallial tissues of Clathromorphum compactum and C. nereostratum, as produced 

by an essentially planar (faceted) or domed meristem, can be 

quite regular. However, grazing by sea urchins, death due to 

disease, and grow-out from damaged postmature conceptacles 

can change not just cellular orientation but also planar temporal variations in seasonality and therefore calcite crystal 

chemistry. When the meristem and upper perithallial tissue 

are removed by grazing or other abrasion, meristem regeneration is possible, approximately to level of the base of the most 

recent layer of conceptacles (200–500 μm deep). While wound 

tissue tends to repair these irregularities, in large part, it is this 

meristem regeneration on an irregular surface, rather than on 

a planar or domed surface, that renders archiving potentially 

problematic.

The most difficult scenarios for climate archiving are the 

removal of calcified tissue and the death of the meristem and 

upper perithallium to below the level at which cells are capable 

of meristem regeneration. In the clathrostrome environment, 

this “dead” surface is for a time occupied by other crustose or 

filamentous species of algae, boring algae, and encrusting invertebrates. Eventually, the dead surface is likely to be overgrown 

by new Clathromorphum tissue from the sides or in some cases 

by new spore settlement. However, several years may intervene, 

creating a disconformity or even an unconformity of unknown 

longevity. By matching several seasonal bands or patterns in adjacent perithallium or other plants or by dating, it may be possible to fill in such unconformities.

Chiton Grazing

In the northwestern North Atlantic Subarctic, chitons and 

limpets are prominent grazers of Clathromorphum compactum

surfaces. Chitons, particularly the species Tonicella rubrum, are 

ubiquitous on coralline surfaces, especially those of C. compactum. Collected specimens of C. compactum, left to dry, usually 

reveal many small animals that were not visible at the time of 

limiting Hiatella access. In the more protected bays and fjords of 

inner coasts, C. compactum is considerately less abundant and 

often absent. Where lower salinities and higher sedimentation 

are present, Lithothamnion glaciale becomes the dominant coralline species of northern rocky bottoms.

In the northwestern Atlantic, Clathromorphum compactum is most abundant, relative to other corallines, at midphotic depths (10–20 m; Adey 1965, 1966b). We have developed 

a clathrostrome index utilizing the number of samples from 

each station depth, the mean thickness of collected samples, 

and the maximum single-sample thickness as an indicator of 
3 2 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

FIGURE 26. Clathrostrome index for the southern Labrador coast (see text for explanation of formula) from the 2010 

cruise of the R/V Alca i. The base diagram is a community structure model for western Atlantic Subarctic rocky shore 

from Adey and Hayek (2011). Abundance and thickness of C. compactum crusts peak from 12 to 20 m on moderately 

exposed shores. LWST = low water spring tides. 

of Strongylocentrotidae join with S. droebachiensis. These species are typically grazers of brown seaweeds, including Alaria, 

Saccharina, Laminaria, and Chordaria, where they are available. Green sea urchin grazing can be strongly limited by wave 

action in exposed, shallow waters, and they are known to move 

to deeper waters in winter to avoid the more destructive wave 

action common at that time of the year. Controlled by shallowwater wave action, they will aggregate into “fronts” or lines and 

can graze into the margins of shallow kelp beds, reducing the kelps 

to stubble or “barren grounds.” However, S. droebachiensis will 

actively avoid some common algae of northern Atlantic regions 

(e.g., Agarum, Desmarestia, Ptilota) because they are protected 

by distasteful or toxic chemical compounds. At the depths where 

C. compactum is most abundant and well-developed clathrostromes are most common, it is these protected species of fleshy 

algae that form the overstory; these species create a patchy “savanna” of coralline alternating with fleshy algal forests that have 

been mistakenly referred to as coralline-urchin barrens. Strongylocentrotus droebachiensis, at moderate density but with insufficient 

collection; these mostly nocturnal invertebrates crawl out of numerous crevices and borings in the drying crusts. The shallow, 

parallel, scraped groove patterns of chiton grazing are abundant 

and easily visible in SEM images of C. compactum surfaces (Figure 9). However, chitons rarely affect the regularity of carbonate 

buildup since they graze only the surficial part of the epithallial tissue; indeed, like grazers of grasslands, chitons are probably nearly symbiotic in their relationship to Clathromorphum

plants, preventing settling by organisms, algal or invertebrate, 

that otherwise might cover the surface (Steneck, 1992).

Sea Urchin Grazing

Strongylocentrotus droebachiensis, the green sea urchin, is 

an often-abundant species on most shallow rocky shores in the 

northwestern North Atlantic. Like Clathromorphum, the echinoid S. droebachiensis is a member of a North Pacific group (the 

Strongylocentrotidae) and is circumboreal in distribution, North 

Atlantic and North Pacific. In the Bering Sea, additional species 
NUMBER 40 • 3 3

algal food, can survive by severely slowing their growth and can 

even become reproductive on overgrazed coralline bottoms (see 

Adey and Hayek, 2011, for a review of this topic).

In the northwestern Atlantic, when larger fleshy algae are 

not available, large populations of very small green sea urchins 

can subsist in crevices, without growth, on diatom and filamentous algal mats (Himmelman, 1986). Coralline-dominated bottoms, including clathrostromes, usually harbor populations of 

young urchins that can survive for many years awaiting more 

favorable feeding conditions. This is an unstable situation, and 

although very small “standby” urchins are not likely to significantly affect the growth and anatomy of Clathromorphum compactum, population explosions leading to larger urchins, with 

transitory fleshy algae for support, can do considerable damage 

to C. compactum plants. Occasionally, adult green sea urchins 

will graze surfaces of C. compactum. Although the sea urchins 

typically remove only scattered patches or grooves of coralline 

surface that will be regenerated, this grazing can create an irregular terrain of secondary tissue. When sea urchin grazing is very 

extensive, reaching below the regenerative surface band, an unconformity will develop. Usually, this surface is overgrown again 

from the side, beginning with new basal, or hypothallial, tissue. 

The result can be several years of missing carbonate. Sometimes 

this is obvious (Figure 2B) because a layer of epiphytes and endozoic green algal borers, or even other corallines, have settled; 

however, if the missing periods are not recognized from SEM observations, the resulting archive can be seriously misinterpreted.

Conceptacle Breakout

Typically, during post reproduction and after spores are released, cells at the margins of the conceptacle roofs, or the roof 

itself, will regenerate meristem cells (Figures 9, 10, 12B). This 

leaves conceptacle cavities often with secondary calcification in 

the sporangium walls; these are quite visible and easily avoided 

during geochemical analysis. However, in some cases, a conceptacle roof can break out, either autonomously or because of 

grazing. When that happens, secondary meristems form, and 

new tissue from the sides and bases of the conceptacle cavities 

develops (Figure 12B). The accompanying cellular carbonate, 

although showing a minimum pattern disruption, is formed 

many months later than the surrounding carbonate. This can 

be hard to recognize without SEM examination.

Death Due to Disease

Killing disease has been documented in corallines (Littler and 

Littler, 1994) and has long been recognized in Subarctic waters. 

Typically seen as white, expanding patches with green centers (as 

epiphytic and endophytic algae occupy the dead crust), these patches 

are usually no more than a few to 10 cm in diameter. However, they 

can expand to a meter or more. Generally, when the patches are 

small, they are regrown laterally by secondary hypothallium; in the 

case of larger patches, resettlement probably occurs. Sometimes, 

grazing by green sea urchins on the epiphytic and endophytic secondary algae in the dead patch can remove several years of Clathromorphum carbonate accretion. This can develop an unconformity, 

with new growth layers not being parallel to the pre-disruption layers; the number of missing layers would have to be documented by 

matching of cyclic patterns or cross dating.

DISCUSSION

We have described the patterns of growth, reproduction, 

and layered carbonate formation, the intricacies of calcification, and the basic ecological patterns for the most abundant 

Subarctic-Arctic Clathromorphum spp. This description provides 

a framework for increasing our understanding of a key element 

of a widespread and characteristic ecosystem and its basal biogenic carbonate component. The structure of the overlying fleshy 

seaweed community in the northwestern Atlantic, characterized 

with quantitative data and supported by many published studies 

of plant-animal interactions, has been summarized by Adey and 

Hayek (2011). Although ecological studies of the Subarctic fringe 

occurrence of this ecosystem in the Aleutian Islands have been 

published (e.g., Steneck et al., 2002; Springer and Estes, 2003; 

Estes et al., 2005; Trites et al., 2007; Chenelot et al., 2011), the 

information for the northwestern North Pacific and for C. nereostratum is more fragmentary. A better understanding of the autecology of C. nereostratum in the Aleutian Islands and the island 

and mainland coasts of the Bering and Okhotsk Seas is necessary.

Climate Archives

The information we have presented can also provide critical support for further development of already promising ArcticSubarctic climate archives from both C. compactum and 

C. nereostratum. In the skeletons of these species, there is potentially a wealth of ecological and water state (climate) information available in the complex formation of yearly layers of 

carbonate-encased cells and reproductive structures. Also, there 

is no known biological limitation, inherent in the coralline structure itself, to the preservation of the information built into the 

carbonate, although the high-magnesium calcite itself is relatively 

unstable and subject to later diagenesis. Given geographic identification of sites with the geomorphological and oceanographic 

conditions that produce long-term continuous accumulation of 

carbonate, more than a thousand years of detailed subannual 

ecological and climate information can be obtained. Data derived solely from anatomical features not degraded by chemical 

alteration (e.g., thickness of yearly bands) could extend the archive considerably further. Recovery of specimens transported to 

sedimentary environments could also produce records of longer 

duration. However, as we have described, the complexity of the 

Clathromorphum skeleton is such that considerable care needs 

to be taken to understand the details inherent in the anatomy of 

this genus if analytical variation is to be separated from environmental variation.
3 4 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

to a tropical temperature of 25°C, yearly accretion would be 1–2 

mm yr−1, approximately the rate of algal ridge accretion in the 

Caribbean by Porolithon pachydermum (Adey, 1978).

Except for a few obligate parasites, crustose corallines are 

photoautotrophs with plastids, chlorophyll a, and phycobiliprotein pigments; photosynthesis is required at least at some point 

in a plant’s life cycle. Whereas Adey (1998) had presented a 

model for crustose coralline calcification that is driven by ion 

pumps, some recent researchers (Ries, 2010) have suggested 

that all calcification in corallines is directly driven by the photosynthetic removal of CO2

 followed by a corresponding pH 

increase and chemical precipitation. The calcified tropical green 

algae Halimeda is a well-published model for CO2

 removal–

induced aragonite formation in enclosed algal tissues. However, 

as we have described, at least in Clathromorphum, where winter 

growth in Arctic darkness and additionally beneath sea ice is a 

significant part of total calcification, the formation of highmagnesium calcite crystals must be metabolically driven using 

stored photosynthate. 

Precipitation might be the dominant form of calcification in 

non melobesioid tropical genera of corallines, which have been the 

subject of most calcification research. However, a survey of highmagnification SEM scans of several tropical genera has shown 

that inner-wall calcification morphology is quite similar to that 

described here. It is likely that other Arctic-Subarctic genera (e.g., 

Lithothamnion and Leptophytum), which lack significant interfilament calcification (see Adey et al., 2005), also calcify metabolically, 

not only during the dark of Arctic winters but also year-round.

Primary Production and Growth Rates

Crustose corallines, particularly at higher latitudes, are very 

low-level primary producers (Adey, 1970, 1973) and commonly 

are the deepest abundant algae at all latitudes. In laboratory experiments, Clathromorphum circumscriptum, an intertidal and 

shallow sublittoral plant, demonstrated a compensation point 

of 35 lux at 0.3°C; at the highest temperatures usually encountered by this species (10°C–16°C), the compensation point was 

200–300 lux. In the same experiments, the deeper-water Subarctic Leptophytum leave showed compensation points at optimum 

growth temperatures (5°C–12°C) of 35 lux. Both C. compactum and C. nereostratum are mid-depth species. It is likely that 

the compensation points at the temperatures that both of these 

species encounter range from approximately 10 to 50 lux. As 

we demonstrated above, the growth rate of C. compactum in 

the northwestern Atlantic ranged from roughly 100 to 400 μm 

yr−1 latitudinally; our analysis suggests a direct relationship with 

temperature. One could argue that light could also be a factor 

over that north–south range. However, Gulf of Maine waters are 

highly turbid because of tidal mixing; also, in the years that WHA 

collected the Gulf of Maine samples from which the growth data 

were extracted, Saccharina kelp was abundant in most C. compactum habitats. In contrast, the Labrador C. compactum samples used for growth analysis were taken from very clear waters, 

with near-tropical visibilities, and from savanna-like habitats of 

Mechanisms of Calcification

The mechanisms of calcification in Clathromorphum also 

need to be fully understood with intensive laboratory research if 

sources of measurement variation are to be removed from these 

archives. In this genus multiple calcification sites and autogenic 

dissolution are general capabilities of the organism. Whether 

secondary calcification (e.g., sporangial wall calcification) is 

metabolic or, as is more likely, simply carbonate chemistry in 

the mostly enclosed conceptacle cavity environment remains 

unknown. Although the precise chemistry of carbonate dissolution by both vegetative cells (fusions) and sporangia remains 

unknown, there is little question of its routine occurrence. This 

is also true for the interfilament (outer cell wall) formation of 

calcite crystals, although a role for light in directly controlling 

chemistry seems possible in this case.

As we noted in the Introduction, all coralline genera have 

cell walls with prismatic, high-magnesium calcite crystals inserted in the cell wall perpendicular to the cell lumen. Since 

cell elongation in some genera is progressive with depth in the 

perithallium and in many genera each filament has independent 

cell division and growth, cells have a very thin outer wall of flat 

crystals parallel to the filament axis that functions as a glide 

plane (Adey et al., 2005). On the other hand, two very different, 

concurrent mechanisms for calcification in Clathromorphum are 

distinguished in this volume. Although developed specifically 

on the basis of the abundant information available for C. compactum, there is little obvious difference found in the tissues of 

C. nereostratum. Primary calcification is likely an ion pump–

driven process that forms inner cell walls that include highmagnesium calcite crystals. These crystals are embedded in an 

organic matrix that provides a mineralogical template. At winter 

temperatures (0°C to –1.8° C) on the southern Labrador Coast, 

cells of C. compactum are typically 9–10 μm long; at summer 

temperatures (3°C–4°C), they are longer (12–13 μm) and have a 

length-based increase of inner-wall carbonate volume.

The production of new inner cell walls with calcite crystals 

appears to be directly controlled by temperature; the higher the 

temperature is, the greater the vertical extension of the organic 

wall is. Vertical extension (growth) occurs with crystal emplacement in the inner-wall matrix of a meristem cell, along with organic wall material. In the Labrador winter, not only is there a 

roughly 20% reduction in cell length, there is also an approximately 30% reduction in the number of cells produced per month. 

These factors are reflected in the 60% reduction in yearly growth 

from the south northward on the North American coast and a 

further 75% reduction continuing northward to northern Baffin 

Island (Figures 21, 22). The thickness of inner cell walls, with 

their embedded prismatic calcite crystals being radially oriented 

and less than a micron in length, is constant with temperature, 

light, and time. It would appear that Clathromorphum species 

and perhaps crustose corallines in general have “boxed” themselves into a carbonate framework that is limited by temperature 

control of metabolic calcite crystal emplacement and not by potential productivity. If the growth curve of Figure 22 is extended 
NUMBER 40 • 3 5

Interfilament Calcification

The large and coarse interfilament (outer wall) crystals appear to be growing downward (perithallium) and upward (epithallium) from the fracture plane between meristem cells (Figure 

28). It seems likely that these crystals are precipitated in the 

small cavities that ring each filament in the meristem calcification zone, perhaps because of removal of CO2

 by the overlying 

photosynthetic epithallium. From decalcified paraffin sections 

and SEM imaging of the meristem fracture zone, it seems likely 

that no organic material is present in this interfilament area. This 

process could involve a secondary mechanism of ion pumps delivering calcium ions to and removing hydrogen ions from the 

interfilament spaces of the fracture zones. However, the meristem 

fracture plane is directly below the primary photosynthetic tissue of these plants (epithallium), and the overlying carbonate 

(within the epithallium) appears to be made up of large, but thin, 

vertical sheets that likely provide a quite porous connection to 

the water at the surface of the plant. Also, in the Labrador Sea, 

the perithallium interfilament crystals are only formed during 

summer in any significant quantity. Thus, the interfilament wall 

component could represent the CO2

 removal and carbonate formation suggested by Ries (2011). 

Agarum clathratum (Adey and Hayek, 2011), with mostly open 

C. compactum terrain. Laboratory experiments to confirm this 

analysis are now underway; however, it seems unlikely that light 

variation is a significant direct growth rate factor in the middepth range of C. compactum and C. nereostratum.

There is no anatomic or reproductive indication that growth 

in C. compactum ceases during low temperatures. Growth experiments currently underway have shown at least short term 

growth in total darkness at 2°C. Also, growth curves suggest 

that under the null light conditions below sea ice in northern 

winters growth continues for a short period. Figure 27 shows a 

10-year mean plot of molar Mg/Ca in four C. compactum crusts 

collected off Quirpon in northernmost Newfoundland. These 

data were derived from equally spaced points in vertical sections. Here sea ice usually arrives along the coast in late January 

and remains until sometime in early April, when temperatures 

are near or below –1°C (Figure 23). The cold and warm peaks 

are virtually symmetrical, both occurring at midlevels of solar 

radiation, making this a temperature proxy with little direct 

light component. Farther north in northern Labrador and Baffin 

Island, these curves are quite asymmetric, suggesting that with 

much longer sea ice intervals (December–June), growth stops because of a lack of sufficient stored photosynthate.

FIGURE 27. Ten-year mean molar Mg/Ca from four C. compactum specimens taken off Quirpon, northern 

Newfoundland (sample QP4-3; see text). See curves for the Mg/Ca molar ratio (proxy for temperature) in 

Figure 3.
3 6 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

the return of sunlight is greatly delayed, and the summer band of 

high density is very narrow (Figure 20). On the other hand, in 

deeper water in the same region, at the lower extent of the C. compactum range, peak summer temperature and maximum growth 

occurs in October, whereas light peaks earlier in June, at nearly the 

minimum water temperature. Thus, whereas high carbonate density corresponds approximately to high growth rates and long, narrow cells over most of the range of both Clathromorphum species, 

under some environmental conditions, the reverse occurs, with 

maximum density (due to interfilament formation) coinciding with 

short cells formed under low temperature. In the Aleutian Islands, 

C. nereostratum often has very strong seasonal banding, 

The seasonal formation of these crystals, narrows the cell lumina (since the inner-wall crystals remain the same length), and 

typically creates the summer high carbonate density and characteristic seasonal banding obvious in many Clathromorphum plants. 

However, development of this banding, which is partly dependent 

upon available sunlight, is complex. In the southernmost locality 

known for C. compactum in the Gulf of Maine, where sunlight 

is present in winter, seasonal banding tends to be weak because 

some interfilament crystals form year-round. In northern Newfoundland, with less winter sunlight, the banding tends to be more 

pronounced. However, in the western Labrador Sea, where sea ice 

forms in midwinter and remains through a large part of the spring, 

FIGURE 28. Working model of calcification in C. compactum. Inner-wall crystals (short, prismatic crystals perpendicular to the filament axis) 

form in the meristem (fracture) plane within an organic matrix and form year-round at the same dimensions; increasing numbers of calcite 

crystals and their organic matrix (longer cells) and production of a greater number of cells produce increased growth. Note the organic wall 

extending across the inner-wall crystal zone but not extending into interfilament space. Interfilament crystals (large, angular crystals parallel or 

diagonal to filament axes) formed, primarily in summer, in nonorganic space between filaments. Interfilament crystals extend upward into the 

epithallium and are thinner and flatter.
NUMBER 40 • 3 7

Arctic (Figure 29), and it is likely that this species can provide a 

pan-Arctic climate archive of considerable significance. High Arctic reconnaissance, collection, and study will need to be undertaken to fully understand the extent of clathrostrome formation.

Changing Ocean pH

In the last decade, ocean acidification, resulting from increasing CO2

 diffusion from the atmosphere, has been recognized 

as a potential problem limiting organism calcification. Aragonite 

formation and high-magnesium calcite, where the magnesium 

concentration exceeds about 12 mol %, are susceptible to reductions in rates of formation and increase in rates of dissolution 

(Morse et al., 2006; Anderson et al., 2008) at lower pH. The seasonal MgCO3 range in C. compactum in the southern Labrador 

Sea is about 6–12 mol %, and therefore, the effects of reduced 

carbonate saturation on cor-stromes may be minimal. In tropical 

waters, where magnesium content is much higher, this may be an 

issue of concern (however, see Nash et al., 2013).

Primary C. compactum calcification is metabolic, and as we 

have discussed, the organism maintains significant physiological control over both placement and dissolution of carbonate. 

Decreased pH might reduce secondary interfilament precipitation (and therefore skeletal density of summer growth). However, secondary calcification takes place internally, within highly 

photosynthetic tissues; it is light that limits skeletal density, and 

how much of a role ambient water pH plays is uncertain (Roleda 

et al., 2012). Chan et al. (unpublished) did not find a significant 

decrease in Clathromorphum calcification rates in recent decades 

in the North Pacific. 

The primary function of the calcium carbonate in corallines 

is grazing protection. There are competing, noncalcified red species that form crusts and are more or less abundant, but usually 

not dominant, in Labrador Sea clathrostromes. These species 

and the dominant macroalgae of the community (Agarum clathratum, Desmarestia viridis, and Ptilota serrata) probably possess 

protective chemicals (Adey and Hayek, 2011). Perhaps lower 

pH levels could shift the balance between competing crusts, so 

that the noncalcified crusts would become dominant, greatly 

limiting development of clathrostrome structure and secondary 

production. 

Grazers are abundant on clathrostrome bottoms. Limpets 

and chitons have a mutualistic relationship with C. compactum, 

feeding on epithallial cells and epiphytes; not only do they rarely 

impact the crusts on which they feed, but they likely enhance 

productivity by preventing abundant algal and invertebrate epiphytism. Epithallium calcification is quite “chalky,” probably as 

a result of minimal inner-wall carbonate and the more “leafy” 

interfilament calcification. Reduced calcification might increase 

grazing depth, eventually reaching the meristem and causing 

reduced growth. However, in the short term, increased grazing 

depth could remove additional decaying epithallial cells and increase photosynthesis and secondary calcification. Sea urchins 

can significantly damage coralline surfaces and primary calcification. However, adult sea urchins do not target corallines, and 

presumably related to the intense storminess and heavy cloud 

cover of late winter and spring.

One of the difficulties of potentially mapping yearly layers 

solely from changes in carbonate density (due to interfilament 

crystallization that is directly photosynthesis driven) is that interfilament crystallization is directly responsive to the light regime. 

Although light tends to parallel temperature, ecological variation in the availability of light is extensive; perhaps more critical, shading by sea ice and snow cover on the Labrador Coast 

and farther north greatly delays the return of light in the spring. 

Although the winter temperature in shore waters at 10–20 m is 

little different from northern Labrador (0°C to –1.8°C) to the 

Gulf of Maine (0°C–1°C), the winter solar radiation under the 

sea ice in northern regions is nil and is greatly reduced until at 

least May, whereas in the Gulf of Maine and the Aleutian Islands, 

solar radiation is considerable throughout the winter. In southern 

Labrador, in shallow water (8–12 m), the period of significant 

interfilament crystallization is mid-May through mid-September.

Conceptacle-Based Growth Analyses

As shown in Figures 2B and 12B, reproduction, especially 

in C. compactum, can be patchy in time and space, limiting the 

use of simple conceptacle-based analyses in archiving. Also, 

damage to and even loss of yearly perithallial tissue from urchin 

grazing and other physical factors commonly disrupts simple 

seasonal layering. However, SEM imaging and mapping, accompanied by SEM-matched microprobe analysis, not only solves 

this problem but concurrently increases ecological and climatic 

discrimination. Laser ablation–inductively coupled plasma–mass 

spectrometry (LA-ICP-MS) has been successfully employed on 

C. compactum and C. nereostratum to detect changes in Mg/

Ca (for temperature) and Ba/Ca (for salinity; Gamboa et al., 

2010; Chan et al., 2011; Hetzinger et al., 2011), although with 

considerable unidentified variability (Figure 3; Gamboa et al., 

2010; Williams et al., unpublished). Kamenos et al. (2008) have 

employed microprobe and LA-ICP-MS methods for identifying 

Mg/Ca variation with time, and herein extensive SEM imaging 

has identified structural and reproductive complexities. It seems 

likely that SEM mapping of laser tracks, with parallel microprobe sensing wherever anatomical complexities appear, could 

resolve most of the variation inherent in plant structure. This 

would require specimen manipulation (e.g., back-to-back analysis) since geochemical methods require polished surfaces that 

prevent detailed SEM analyses.

Finally, although Clathromorphum compactum is primarily 

an outer coast rather than a bay species, ecological and oceanographic variation in temperature and salinity along the complex 

rocky shores frequented by C. compactum is a widespread and 

inevitable source of variation. It is essential for accurate environmental archiving that multiple samples from known depths and 

localities be secured for analysis. The value of C. compactum as 

a millennial climate archive will also likely be enhanced by lesser 

growth rates in the lower SST of northern Labrador and the high 

Arctic. Clathromorphum compactum occurs throughout the 
3 8 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES

integrated anatomy and reproduction, modified by numerous environmental elements. Understanding this complexity is essential to 

the accurate interpretation of geochemical analyses of the skeleton 

and has already led to the development of a new archive for sea 

ice providing paleoclimatic information not previously available. 

Also, the role of corallines in general, and keystone Clathromorphum species in particular, in forming cold-water rockybottom carbonates has been widely interpreted as a degraded 

ecosystem resulting from intensive overfishing. As we show, 

Clathromorphum species grow very slowly, primarily under temperature control, and have developed anatomical and cellular 

structures that potentially allow longevities of many centuries. 

This understanding is crucial to interpreting the ecological importance of this widespread carbonate structure, with its unique 

associations of organisms as a key ecosystem of Subarctic and 

Arctic rocky shores; its age shows clearly that it is not a degraded 

system. Also, we show how understanding geomorphological 

if fleshy algae production were to be enhanced in a more acidic 

sea, sea urchin grazing on corallines might actually be reduced 

because of greater access to preferred seaweed foods. Finally, 

most significant grazers in clathrostrome environments also have 

critical carbonate hard parts that could be impacted by increased 

seawater acidity. Ocean acidification will certainly impact benthic communities, but the changes will be hard to predict without extensive ecosystem level experiments. Single-species studies 

are inadequate to the task.

CONCLUSIONS

Calcified encrusting coralline algae have a considerably more 

complex anatomical structure than a reading of current literature 

would suggest. As we document here, the genus Clathromorphum, widespread in Subarctic and Arctic seas, provides a highly 

FIGURE 29. Cor-strome, with abundant C. compactum, from 10–20 m in Arctic Bay in northernmost Baffin Island (73°N). These plants are 

growing in an inner-bay environment, not the optimum habitat for this species. Although only a single image, it suggests that extensive clathrostrome development in intermediate-exposure, island-complex environments is likely in the high Arctic. © Nick Caloyianis. Reprinted with 

permission.
NUMBER 40 • 3 9

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controls laid on ecological patterns identifies carbonate buildups, potentially of millennial ages, which are further crucial to 

acquiring lengthy paleoclimatic data.

Finally, contrary to the prevailing view of corallines as simple cushions built by filaments, we show how multiple complex 

anatomical features, which can be called tissues, and reproductive structures of combined tissues, which can be interpreted as 

organs, are the norm. These are key elements to understanding 

phylogenetic analyses and evolutionary patterns in corallines 

and other red algae.

ACKNOWLEDGMENTS

This was a multiyear project that covered thousands of 

miles of coast and was carried out with a research vessel that at 

times used the services of many boatyards and ports in the Canadian Maritimes and the Gulf of Maine. It would be impractical 

to acknowledge individually the many crew members and shore 

supporters who helped our research, and here we credit only the 

key individuals involved directly in collection and research.

Matthew Suskiewicz was our chief diver for the 2010 and 

2011 cruises and did all of the collecting during that period. 

Nick Caloyianis provided the key underwater images, and David 

Grimard and Steve Allen were the principle support divers. 

Karen Loveland Adey and Erik Adey provided considerable logistic support both at sea and during the analytical phases. The 

superb SEM facilities of the Smithsonian’s National Museum of 

Natural History and the ever-present and critical support of its 

director, Scott Whittaker, made possible the large set of critical 

SEM images. Dean Calahan and Jennifer Barker provided significant editorial services. Collections made in the Aleutian Islands 

and Baffin Island were credited in Materials and Methods.

Funding for this project was provided by Ecological Systems 

Technology, Natural Sciences and Engineering Research Council 

of Canada, through the University of Toronto and Laval University and the Botany Department of the Smithsonian’s National 

Museum of Natural History.

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