the mg-calcite composition of antarctic echinoderms: important implications for predicting the...

The Mg-Calcite Composition of Antarctic Echinoderms: Important Implications for Predictingthe Impacts of Ocean AcidificationAuthor(s): James B. McClintock, Margaret O. Amsler, Robert A. Angus, Roberta C. Challener,Julie B. Schram, Charles D. Amsler, Christopher L. Mah, Jason Cuce, and Bill J. BakerSource: The Journal of Geology, Vol. 119, No. 5 (September 2011), pp. 457-466Published by: The University of Chicago PressStable URL: http://www.jstor.org/stable/10.1086/660890 .

Accessed: 26/08/2014 01:53

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to TheJournal of Geology.

http://www.jstor.org

This content downloaded from 81.208.26.61 on Tue, 26 Aug 2014 01:53:26 AMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=ucpress

http://www.jstor.org/stable/10.1086/660890?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


[The Journal of Geology, 2011, volume 119, p. 457–466] � 2011 by The University of Chicago.All rights reserved. 0022-1376/2011/11905-0002$15.00. DOI: 10.1086/660890

457

The Mg-Calcite Composition of Antarctic Echinoderms: ImportantImplications for Predicting the Impacts of Ocean Acidification

James B. McClintock,1,* Margaret O. Amsler,1 Robert A. Angus,1

Roberta C. Challener,1 Julie B. Schram,1 Charles D. Amsler,1

Christopher L. Mah,2 Jason Cuce,3 and Bill J. Baker3

1. Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170, U.S.A.;2. Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington DC, 20013-7012, U.S.A.;

3. Department of Chemistry, University of South Florida, Tampa, Florida 33620-5250, U.S.A.

A B S T R A C T

The Southern Ocean is considered to be the canary in the coal mine with respect to the first effects of oceanacidification (OA). This vulnerability is due to naturally low carbonate ion concentrations that result from the effectof low temperature on acid-base dissociation coefficients, from the high solubility of CO2 at low temperature, andfrom ocean mixing. Consequently, the two calcium carbonate polymorphs, aragonite and calcite, are expected tobecome undersaturated in the Southern Ocean within 50 and 100 years, respectively. Marine invertebrates such asechinoderms, whose skeletons are classified as high-magnesium carbonate (14% mol MgCO3), are even more vul-nerable to OA than organisms whose skeletons consist primarily of aragonite or calcite, with respect to both increasedsusceptibility to skeletal dissolution and further challenge to their production of skeletal elements. Currently, despitetheir critical importance to predicting the effects of OA, there is almost no information on the Mg-calcite compositionof Antarctic echinoderms, a group known to be a major contributor to the global marine carbon cycle. Here we reportthe Mg-calcite compositions of 26 species of Antarctic echinoderms, representing four classes. As seen in tropicaland temperate echinoderms, Mg-calcite levels varied with taxonomic class, with sea stars generally having the highestlevels. When combined with published data for echinoderms from primarily temperate and tropical latitudes, ourfindings support the hypothesis that Mg-calcite level varies inversely with latitude. Sea stars and brittle stars, keyplayers in Antarctic benthic communities, are likely to be the first echinoderms to be challenged by near-term OA.

Introduction

Anthropogenic emissions of atmospheric CO2 areresulting in a significant elevation of sequesteredCO2 in the world’s oceans. This uptake of CO2 is,in turn, reducing both surface seawater pH and thesaturation state of calcium carbonate, a collectiveprocess that has come to be known as ocean acid-ification (OA; Caldeira and Wickett 2003; Feely etal. 2004; Orr et al. 2005). While it is estimated thatthe pH of the world’s oceans has decreased, on av-erage, by a tenth of a unit since the Industrial Rev-olution (Sabine et al. 2005), the oceans are not equalin terms of the time line of the anticipated effectsof OA. Even the two poles are not equivalent inthis regard. The Southern Ocean offers a consid-

Manuscript received January 14, 2011; accepted April 26,2011.

* Author for correspondence; e-mail: [email protected].

erably greater surface area than the Arctic Oceanfor CO2 uptake, with 40% of the total globalinventory of CO2 uptake occurring south of 40�S(Fabry et al. 2009). According to the Intergovern-mental Panel on Climate Change (IPCC 2007) busi-ness-as-usual emissions projections, the saturationhorizon in the Southern Ocean for aragonite is ex-pected to shoal to the surface by as soon as mid-century (2050); with calcite being less soluble inseawater, it is expected to follow suit by the endof the century (Feely et al. 2004; Orr et al. 2005).

Representatives of all five classes of the Echi-nodermata constitute an exceptionally importantcarbonate-producing phylum (Lebrato et al. 2010).The CaCO3 standing stock of echinoderms de-creases with ocean depth, with 80% of the globalCaCO3 at relatively shallow to moderate depths (0–


mailto:[email protected]


458 J . B . M C C L I N T O C K E T A L .

800 m). This bathymetric pattern holds true for theSubantarctic and the Antarctic (Arntz et al. 1994)and may be caused by decreases in organic matterwith increases in depth (Lampitt et al. 2001; Le-brato et al. 2010). Moreover, Antarctic echinodermCaCO3 standing stocks are 15 times those mea-sured in the Arctic ( vs. 2.65 g C/m2;mean p 32.21reviewed by Lebrato et al. 2010).

The susceptibility of echinoderms’ inorganic car-bon to dissolution via OA is exacerbated becauseof relatively high concentration of Mg-calcite (14%mol Mg-calcite; Bøggild 1930; Weber 1969; Dickson2002) in their skeletal elements. Mg-calcite is evenmore soluble than aragonite, and aragonite is moresoluble than calcite (Bischoff et al. 1987). Moreover,unique characteristics of the Southern Ocean arepredicted to cause shoaling of saturation horizonsand rapid dissolution of aragonite and calcite poly-morphs under conditions of OA. These character-istics include the inverse correlations between CO2

solubility and temperature, the sensitivity of acid-base dissociation coefficients at low temperature,and ocean mixing patterns (Fabry et al. 2009). Whenshallowing QCa (global calcite saturation) horizonslead to undersaturated Antarctic waters, echino-derms are likely to face increasing difficulty in bothproducing and maintaining their skeletal elements,and even if some species can compensate by in-creasing rates of calcification, there could be trade-offs with other life-sustaining processes (Wood etal. 2008; Fabry et al. 2009).

In addition to the high abundance of this phylumin Antarctica, many echinoderms play keystoneroles in the community dynamics of the benthos(Dayton et al. 1974; Arntz et al. 1994; McClintock1994). Nonetheless, despite the abundance and im-portance of echinoderms and their high level of sus-ceptibility to OA, the skeletal Mg-calcite compo-sition has been measured for only one Antarcticechinoid (Weber 1969; Grzeta et al. 2004) and threeAntarctic crinoids (Chave 1954). Such informationis critical in making predictions about pending ef-fects of OA on this important Antarctic phylum.For example, Sewell and Hofmann (2011) indicatethat while there has been considerable study of theMg content of echinoid skeletons, there is almostno information on Antarctic species. Indeed, theywere obliged to use the single Antarctic species ex-amined to date (the test and spines of the regularurchin Sterechinus neumayeri) as a proxy for Mg-calcite composition so as to predict the effects ofchanging saturation horizons on deep-water Ant-arctic echinoids as a whole. The purpose of ourstudy is to begin to remedy this lack of informationby presenting the first comprehensive analysis of

the Mg-calcite composition of a suite of Antarcticechinoderms. In addition to interpreting our datato make predictions about how OA will affect var-ious Antarctic echinoderm groups, we combine ourfindings with those for temperate, tropical, and po-lar species to evaluate the hypothesis that there isan inverse correlation between skeletal Mg-calcitelevel and latitude in calcifying marine inverte-brates (Chave 1954; Andersson et al. 2008).

Samples and Methods

Collections, Preservation, and Shipment. Represen-tatives of adult sea stars, sea urchins, sea cucum-bers, and brittle stars (crinoids were too rare in ourcollections to analyze) were collected by hand (viascuba diving) or by ship-based trawl in the australfall of 2010 (February–June 2010) from the westernAntarctic Peninsula, in a range from Elephant Is-land (61�S) on the north to the Banana Trench (66�Son the south; collection sites, longitude, latitude,collection depths, and bathymetric ranges are pre-sented in table 1). As at least one individual of everyspecies we collected was included in the analysis,the suite of echinoderms examined in our studyrepresents an unbiased survey of the phylum. In-dividuals collected by hand were immediately re-turned to Palmer Station, photographed, placed innumbered ziplock baggies, and frozen at �80�C. In-dividuals collected by ship-based trawl were pho-tographed, placed in numbered ziplock bags, andfrozen at �80�C aboard ship and then transferredto a �80�C freezer at Palmer Station. For speciesthat we could not immediately identify, a voucherwas preserved in 70% ethanol for later identifica-tion by one of us (C.L.M.) at the SmithsonianInstitution, Washington, DC. Echinoderms for Mg-calcite analysis were shipped frozen to the Uni-versity of Alabama at Birmingham (UAB) for fur-ther processing.

Dissection Protocols. Echinoderms were thawedbefore dissection. For all asteroids, with the excep-tion of two very small species (Kampylaster incur-vatus and Granaster nutrix) that were digested in-tact, an arm was excised at its base with scissorsand the pyloric ceca and gonad removed with fineforceps from the arm body-wall tissue. The calcar-eous ring that encircles the pharynx of the sea cu-cumbers was removed with scissors. The oral diskand at least one arm of each brittle star were re-moved with scissors and combined for analysis.Regular echinoids were divided into three discreteskeletal body components: spines, test, and Aris-totle’s lantern. The spines were scraped from thetest with a single-edge razor blade, and then the



Journal of Geology A N T A R C T I C E C H I N O D E R M M G - C A L C I T E 459

Table 1. Collection Location and Bathymetric Range of 27 Species of Antarctic Echinoderms Analyzed forSkeletal Mg-Calcite

Species Collection location Latitude (S) Longitude (W) Depth (m)

Reportedbathymetric

range (m)

Echinoidea:Amphipneustes

similis Hugo Island 64�45.53′ 65�28.26′ 670–700 70–690Ctenocidaris

perrieri Hugo Island 64�45.53′ 65�28.26′ 670–700 62–690Sterechinus

neumayeri Hugo Island 64�45.53′ 65�28.26′ 670–700 6–805S. neumayeri Norsel Point 64�45.62′ 64�05.90′ 5–40 6–805S. neumayeri Lemaire Channel 65�04.66′ 63�58.21′ 5–40 6–805

Holothuroidea:Molpadia musculus Hugo Island 64�45.53′ 65�28.26′ 670–700 40–5395Pseudostichopus

spiculiferus Banana Trench 66�17.63′ 66�36.18′ 850–950 326–2100Ophiuroidea:

Ophionotusvictoriae Arthur Harbor 64�46.47′ 64�03.29′ 5–40 13–1684

Ophiosparte gigas Arthur Harbor 64�46.47′ 64�03.29′ 5–40 25–746Asteroidea:

Acodontaster ∗cf.hodgsoni Dallmann Bay 64�09.45′ 62�44.73′ 150–170 4–540

Acodontasterconspicuus Lemaire Channel 65�04.66′ 63�58.21′ 5–40 24–460

Diplasterias brandti Arthur Harbor 64�46.47′ 64�03.29′ 5–40 0–450Granaster nutrix Arthur Harbor 64�46.47′ 64�03.29′ 5–40 0–250Henricia sp. Renaud Island 65�40.48′ 67�24.49′ 145–175 NAKampylaster

incurvatus Dallmann Bay 64�09.45′ 62�44.73′ 150–170 93–750Macroptychaster

accrescens Low Island 63�31.84′ 62�45.07′ 140–215 97–655Neosmilaster

georgianus Arthur Harbor 64�46.47′ 64�03.29′ 5–40 0–335Odontaster

meridionalis SE Bonaparte Pt. 64�46.76′ 64�02.53′ 5–40 0–646Odontaster

penicillatus Dallmann Bay 64�09.45′ 62�44.73′ 150–170 0–646Paralophaster

godfroyi Low Island 63�31.84′ 62�45.07′ 140–215 180–2450Paralophaster sp. Low Island 63�31.84′ 62�45.07′ 140–215 NAPerknaster aurorae Stepping Stones Is. 64�47.18′ 63�59.85′ 5–40 45–310Perknaster densus Low Island 63�31.84′ 62�45.07′ 140–215 101–232Perknaster fuscus Lemaire Channel 65�04.66′ 63�58.21′ 5–40 45–137Perknaster sp. Low Island 63�31.84′ 62�45.07′ 140–215 NAPorania antarctica Dallmann Bay 64�09.45′ 62�44.73′ 150–170 4–2930Diplopteraster

verrucosus Banana Trench 66�17.63′ 66�36.18′ 850–950 NALabidiaster

annulatus Elephant Island 61�12.81′ 56�01.11′ 160–170 35–550L. annulatus Lemaire Channel 65�04.66′ 63�58.21′ 5–40 35–550L. annulatus Renaud Island 65�40.48′ 67�24.49′ 145–175 35–550

Note. The sea urchin S. neumayeri and the sea star L. annulatus were collected from three discrete sites. Bathymetricranges for species are from Lemaitre et al. (2009). NA p not available.

test was cut open with scissors and the gonads andintestine removed with fine forceps. Finally, thelantern was removed with forceps. The one speciesof irregular echinoid, Amphipneustes similis, wasdivided into test and spines. During the dissections,

we discovered that three female individuals of thisspecies were brooding young (bearing spines andresembling newly released juveniles) in their mar-supial chambers. We used fine forceps to removeapproximately 50 juvenile individuals from these




Table 2. Mean Percentages of MgCO3 by Weight andMoles in Skeletons of Echinoderm Species Collectedfrom the Western Antarctic Peninsula

wt% mol%

Class, species Mean SE Mean SE n

Asteroidea:Perknaster densus 7.47 ... 11.74 ... 1Diplopteraster

verrucosus 8.12 .01 12.73 .02 2Granaster nutrix 8.29 .38 12.97 .57 5Perknaster aurorae 8.86 .55 13.81 .82 3Perknaster sp. 8.99 .96 14.01 1.42 2Kampylaster

incurvatus 9.28 .63 14.43 .93 4Paralophaster sp. 9.28 .06 14.44 .08 3Neosmilaster

georgianus 9.37 .05 14.56 .08 3Acodontaster

conspicuus 9.39 ... 14.60 ... 1Odontaster

meridionalis 9.50 .04 14.76 .05 3Diplasterias brandti 9.52 .15 14.78 .22 3Paralophaster

godfroyi 9.59 ... 14.89 ... 1Labidiaster

annulatus 9.79 .04 15.18 .06 9Henricia sp. 9.83 .09 15.23 .12 2Macroptychaster

accrescens 9.83 .16 15.24 .23 3Acodontaster

hodgsoni 9.85 .02 15.27 .03 3Odontaster

penicillatus 9.91 ... 15.35 ... 1Perknaster fuscus 9.92 ... 15.38 ... 1Porania antarctica 10.20 .07 15.78 .10 3

Echinoidea:Sterechinus

neumayeri 6.04 .10 9.58 .15 6Amphipneustes

similis 7.51 .74 10.48 .56 4Ctenocidaris

perrieri 7.61 .24 11.96 .36 3Holothuroidea:

Pseudostichopusspiculiferus 7.49 ... 11.78 ... 1

Molpadia musculus 8.26 .17 12.92 .26 3Ophiuroidea:

Ophiosparte gigas 9.13 ... 14.21 ... 1Ophionotus

victoriae 9.20 .10 14.31 .14 3

three females and combined them into a singlesample for skeletal analysis.

Tissue Digestion and Skeletal Preparation. Por-tions of body components, discrete body compo-nents, or intact echinoderms were soaked in 10%sodium hypochlorite (Fisher) for a period of severaldays to remove all organic material. The solutionwas exchanged daily as needed to promote diges-tion. Cleaned skeletal material was Buchner-vac-uumed onto qualitative filter paper, generouslyrinsed with deionized H2O and allowed to vacuum–air dry for several minutes. The filter was foldedand dried at 50�C for 2 d to a constant mass. Driedskeletal material was removed from the filter paperand ground into a fine powder with a mortar andpestle.

Elemental Analyses. Powdered echinoderm skel-etal material was commercially analyzed byActlabs in Ancaster, Ontario (http://www.actlabs.com). There, 90–500 mg of each samplewas digested with aqua regia (nitro-hydrochloricacid, which is formed by freshly mixing concen-trated nitric acid and concentrated hydrochloricacid, usually in a molar ratio of 1 : 3) for 2 h at95�C. Samples were cooled and diluted with deion-ized water. Samples were subsequently analyzed ona PerkinElmer ICP (inductively coupled plasma)atomic emission spectroscope for Mg�� and Ca��.USGS geochemical standards served as controlsand, along with a blank, were analyzed every 13samples. The analytical accuracy of ICP for bothMg�� and Ca�� was consistently within 0.01% ofthe known value for the standards.

Results of the analyses were reported as per-centage of the digested material that was (byweight) Mg�� and Ca��. Since the weights of thedigested material were known, the percentages ofMg�� and Ca�� were converted to weight (in g) ormoles. The Mg percentage was calculated as thepercentage of the total in the sample�� Mg � Ca(as either g or moles).

Other Studies. To broaden the scope of this study,we have included data on the Mg content of echi-noderms from various latitudes reported in Clarkand Wheeler (1922), Chave (1954), Pilkey andHower (1960), and Weber (1969, 1973).

Results

The mol% MgCO3 and wt% MgCO3 of the 26 spe-cies of echinoderms are presented by class in table2. Overall, MgCO3 values for echinoderms (usingthe skeletal test to represent echinoids) ranged from9.58 to 15.78 mol% and from 6.04 to 10.20 wt%.By class, the means and ranges of the mol% MgCO3

values for echinoids (test only), holothuroids (cal-careous ring), ophiuroids (arm and disk), and aster-oids (arm or intact) were 10.67 (range p

; species), 12.35 (9.58–11.96 n p 3 range p; species), 14.26 (11.78–12.92 n p 2 range p; species), and 14.56 (14.21–14.31 n p 2 range p; species), respectively. In terms11.74–15.78 n p 19

of wt% MgCO3, the class-specific means and rangesfor echinoids, holothuroids, ophiuroids, and aster-oids were 7.05 ( ; species),range p 6.04–7.61 n p 3


http://www.actlabs.com

http://www.actlabs.com



Table 3. Mean Percentages of MgCO3 by Weight andMoles in the Skeletal Elements of the MultiarmedAntarctic Asteroid Labidiaster annulatus Collectedfrom Three Sites

wt% mol%

Site Mean SE Mean SE n

Elephant Island 9.87 .03 15.30 .04 3Lamaire Channel 9.65 .02 14.97 .03 3Renaud Island 9.86 .04 15.28 .06 3

Note. The Lamaire Channel mean differs significantlyfrom those of the other two sites.

7.88 ( ; species), 9.17range p 7.49–8.26 n p 2( ; species), and 9.37range p 9.13–9.20 n p 2( ; species), respectively.range p 7.47–10.20 n p 19

The mean � SE mol% MgCO3 for the primaryspines of the regular sea urchins Sterechinus neu-mayeri and Ctenocidaris perrieri and the irregularsea urchin Amphipneustes similis were 5.34 �

( ), ( ), and0.18 n p 3 6.14 � 0.87 n p 3 5.97 � 0.16( ), respectively. The mean � SE mol%n p 2MgCO3 for the Aristotle’s lantern of the regular seaurchins S. neumayeri, and C. perrieri were

( ) and ( ), re-10.69 � 0.71 n p 6 11.63 � 0.88 n p 3spectively. The mol% MgCO3 for the brooded ju-veniles of the irregular sea urchin A. similis was6.75 ( ; pooled collection of approximately 50N p 1brooded juveniles from three adult females).

A statistical comparison of the mean MgCO3 val-ues for individuals of the sea star Labidiaster an-nulatus collected from three distinct geographicsites indicated site-specific differences (table 3). AnANOVA using arcsine-transformed wt% of MgCO3

showed a significant difference in means betweensites ( [ ], ). The meanF p 16.238 df p 2, 6 P p .004percentage of Mg�� among the individuals col-lected in the Lemaire Channel differed significantlyfrom the means of those collected at Renaud Islandor Elephant Island ( for both comparisons;P ! .01Tukey HSD test). Mean MgCO3 levels did not differsignificantly between the latter two sites (P p

; Tukey HSD test). Similar results were ob-.964tained from an ANOVA using arcsine-transformedwt% of MgCO3.

The relationship between latitude and wt%MgCO3 for skeletal components of four classes ofechinoderms (asteroids, ophiuroids, echinoids, andcrinoids) from temperate, tropical, and polar lati-tudes is shown in figure 1. Linear regression anal-ysis indicated that there was a significant negativeassociation between latitude and MgCO3 levels( [95% confidence intervalslope p �0.0140

to �0.122], ). When we(CI) p �0.159 P K .001added mol% MgCO3 data for 26 species of Antarcticechinoderms in our study to this analysis (fig. 1),the slope of the regression between latitude andMgCO3 levels became slightly less negative butstill remained highly significant (slope p �0.123[ to �0.109], ). The 95%95% CI p �0.138 P K .001CIs for the slope estimates with and without theUAB data overlap. Linear regression analysis ofwt% Mg versus latitude are presented for asteroids,regular echinoids, an irregular echinoid, crinoids,and ophiuroids in figure 2. All groups showed asignificant negative slope, except for ophiuroids.

Discussion

This study begins to fill the void in our currentknowledge of the potential effects of OA on Ant-arctic echinoderms, a group of marine invertebrateswhose skeletons contain a significant proportion ofmagnesium ions. This is important because marineorganisms whose skeletons contain high levels ofMgCO3 have significantly higher levels of mineralsolubility than those with skeletons of aragonite orcalcite (Andersson et al. 2008). In terms of carbon-ate minerals, seawater saturation state is lower inpolar than in temperate or tropical seas (Orr et al.2005; Andersson et al. 2008; Fabry et al. 2009). Aspoignantly noted in Andersson et al. (2008), calci-fying species that are high in Mg-calcite from high-latitude, low-saturation-state cold waters will bethe first responders to OA. However, it is importantto consider that the relationship between seawatersaturation state and Mg content is not strictly achemical phenomenon. In echinoderms, this is alsoa biological phenomenon, because calcifying cellsestablish high local concentrations of Mg. The de-gree to which Mg in the interstitial body fluid isinfluenced by calcifying cells requires furtherstudy.

All 26 of the Antarctic echinoderm species ex-amined in this study had skeletal components thatmet the defined standards for “high-Mg-calcite”species (14% mol MgCO3; Bøggild 1930). Whileother groups of marine organisms, including redcoralline algae, bryozoans, and benthic and pelagicforaminiferans, contain Mg-calcite, echinoderms,because of their generally high biomass, are keyplayers in global carbonate cycles (Lebrato et al.2010). Antarctic echinoderms are no exception tothis rule, often dominating benthic biomass in shal-low nearshore waters as well as shelf, slope, anddeep-sea environments of the Southern Ocean(McClintock et al. 1988; Brey 1991; Arntz et al.1994; Dahm 1999; Lebrato et al. 2010).

While the small numbers of species analyzed inthis study for three of the four classes of Antarctic




Figure 1. Association between latitude (either north or south) and wt% Mg content of echinoderm skeletons. Thesolid symbols represent data from Clark and Wheeler (1922), Chave (1954), Pilkey and Hower (1960), or Weber (1969,1973); open symbols represent data from the current University of Alabama at Birmingham (UAB) study. Regressionlines are shown for all studies except the current study (solid line) and for all studies (dashed line).

echinoderms precluded class-level statistical com-parisons of MgCO3, the trends appeared to be sim-ilar to those reported for extant temperate and trop-ical species (Chave 1954), as well as for thoserecorded from fossil echinoderm skeletons(Dickson 2002). In our study, levels of Mg-calcite(9.58–15.78 mol% MgCO3) were, on average,ranked from highest to lowest as follows: sea stars1 brittle stars 1 sea cucumbers 1 echinoids. This issimilar to the pattern seen by Chave (1954), whoused x-ray spectrometry to measure MgCO3 andreported levels that were generally highest in seastars, followed by brittle stars, crinoids, and finallyechinoids. No sea cucumbers were examined byChave (1954), perhaps because they are poorly cal-cified, having only minute spicules imbedded inthick body wall tissue and a small calciferous ringaround the esophagus. As members of the Aster-oidea and Ophiuroidea generally had the highest

ratio of magnesium to calcite, they are likely to bethe most vulnerable to dissolution under condi-tions of increasing OA in the Southern Ocean. Inthis regard, it is important to note that despite hav-ing an endoskeleton, echinoderms remain vulner-able to skeletal dissolution because their skeletalelements are covered only by a thin epithelial layer(Lawrence 1987), which is permeable (Binyon 1976,1980; Sewell and Hofmann 2011). For example, sev-eral studies have demonstrated that OA reducestest thickness and test growth in echinoids despitethe presence of an endoskeleton (Shirayama andThornton 2005; Miles et al. 2007).

Sewell and Hofmann (2011) indicate that levelsof MgCO3 in echinoids may vary at the level of theindividual, species, or population. In our study, wefound that levels of MgCO3 were similar betweenindividuals (as evidenced by small standard errors;table 2). However, a comparison of three discrete



Figure 2. Association between latitude (either north or south) and wt% Mg content of groups of echinoderms. Thedata for the irregular echinoid represent a single species (solid symbols; Pilkey and Hower 1960) and two speciesfrom the current study (species overlay each other). In all plots, open symbols represent data from this study.




body components (test, primary spines, and lan-tern) in the two regular Antarctic echinoid speciesexamined indicated differences in MgCO3 levels.For example, echinoid primary spines consistentlyhad lower levels of MgCO3 than did either the lan-tern or the test. This is consistent with the obser-vations of Chave (1954), who also reported valuesthat were generally, but not exclusively, lower inspines than in the tests of temperate and tropicalsea urchins. Our measurement of a mean value of3.5 wt% MgCO3 (5.4 mol% MgCO3) for the primaryspines of the common regular Antarctic sea urchinSterechinus neumayeri is similar to that reportedby Grzeta et al. (2004) for the same species (4.1 wt%MgCO3).

In order to evaluate variability in skeletal MgCO3

at the population level, we targeted collections ofindividuals of the large multiarmed sea star Labi-diaster annulatus from three distinct geographicsites. We found evidence both for and against pop-ulation-level differences in skeletal Mg-calcite, assea stars in two of the populations (Renaud Islandand Elephant Island) had similar levels of skeletalMgCO3 (15.28 and 15.30 mol% MgCO3, respec-tively), while the mean in individuals collectedfrom the Lemaire Channel was slightly, but statis-tically significantly, lower (14.97 mol% MgCO3).There was no correlation between the proximity ofthe sites to one another and the level of skeletalMg-calcite measured, nor, at this restricted geo-graphical scale, was there a pattern of decreasingMg content with increasing latitude.

While there are a growing number of studies thathave evaluated the effects of OA on fertilization,early embryogenesis, larval development, and mor-phometrics in echinoderms (e.g., Kurihara and Shi-rayama 2004; Clark et al. 2009; Byrne et al. 2009,2010; O’Donnell et al. 2010), there are no data onthe susceptibility of early juvenile phases. Sewelland Hofmann (2011) make the case that the pro-portion of skeletal to organic tissue in brooded ju-veniles of Antarctic echinoids is high, as are thenumbers of juveniles produced. They therefore sug-gest that as OA in the Southern Ocean challengescalcification in brooded juveniles, it could result inweaker tests that render juveniles more susceptibleto predation (see McDonald et al. 2009) and perhapseven the production of smaller brood numbers. Inour study, we measured a level of 6.75 mol%MgCO3 in the skeletal components (tests combinedwith spines) of brooded juveniles in the irregularbrooding Antarctic sea urchin Amphipneustes si-milis. This level of skeletal Mg-calcite is towardthe lower end of the spectrum that we detected inAntarctic echinoderms and thus places juveniles of

A. similis at the lower end of vulnerability to OA.However, because spines and tests of juveniles werenecessarily combined and in this study the spinesof adults have about half the Mg content of adulttests, this Mg content may be an underestimate forjuveniles; if so, their vulnerability would beheightened.

Mg-calcite levels in calcifying marine organismshave been postulated to decline with increasing lat-itude (Chave 1954; Mackenzie et al. 1983; Anders-son et al. 2008). This pattern has been hypothesizedto be related to seawater temperature, light avail-ability, and seawater saturation state, which all de-crease with increasing latitude. The Mg-calcitecontent of calcified marine organisms has also beenhypothesized to decline with increasing depth(Schlager and James 1978). While the low range incollection depths for our suite of Antarctic echi-noderms precluded a test of the depth hypothesis,we were able to assess the latitudinal hypothesis(Andersson et al. 2008) for the Echinodermata. Wedid this by first plotting and analyzing wt% MgCO3

data for skeletal components of temperate, tropical,and the few polar species available as a function oflatitude (data from Clark and Wheeler 1922; Chave1954; Pilkey and Hower 1960; Weber 1969, 1973).It is noteworthy that the Chave (1954) databasecontained Mg-calcite data for only two Antarcticcrinoids. We then included in this regression anal-ysis our data for the 26 Antarctic echinoderm spe-cies examined in our study. In both instances, wefound a significant negative correlation betweenlatitude and Mg-calcite content. The slope of theregression was reduced slightly with the inclusionof our Antarctic data but remained highly signifi-cant. The slopes were similar, and their 95% CIsoverlapped. To the best of our knowledge, ours isthe first test of this latitudinal hypothesis that plotsexclusively data for the Echinodermata. Anderssonet al. (2008) examined latitude versus Mg contentfor all the Chave (1954) data, which included a suiteof echinoderms among data for a broad spectrumof calcareous marine organisms. When we evalu-ated the data shown in figure 1 by taxonomic group(fig. 2), we found a significant negative associationbetween Mg content and latitude for all groups ex-cept ophiuroids. Ophiuroids also exhibited a neg-ative trend, and it is possible that with additionaldata the trend may become significant. Furtherstudies are needed to evaluate whether this inverserelationship is being driven by physical factors suchas temperature, light, salinity, and seawater satu-ration state and/or by biological factors, includinglife span, growth rate, and energy availability (Mac-kenzie et al. 1983; Andersson et al. 2008; Borre-




mans et al. 2009). Certainly, the variability in Mgcontent at a given latitude indicates that it cannotbe solely attributable to temperature (Weber 1973;this study).

In summary, because the Southern Ocean will bethe ocean first and foremost affected by OA andsince the skeletons of echinoderms are comprisedof high-Mg calcite, they, along with other dominantAntarctic marine organisms with Mg-calcite skel-etons, such as coralline algae (whose levels ofMgCO3 have yet to be determined), are likely tobecome canaries in the coal mine under near-termOA. Our findings suggest that asteroids and ophiu-roids will be particularly vulnerable because theirskeletal elements have, on average, the highest lev-els of Mg-calcite. This may have important rami-fications, as Antarctic sea stars and brittle stars playkey roles in Antarctic benthic community struc-ture (Dayton et al. 1974; Dearborn 1977).

A C K N O W L E D G M E N T S

We wish to acknowledge the outstanding assis-tance provided by Raytheon Polar Service supportstaff at Palmer Station, Antarctica. We also thankH. W. Dietrich for so generously facilitating accessto his ship-based trawling operations along thewestern Antarctic Peninsula. C. Mooi and M.O’Laughlin generously provided assistance withtaxonomy. E. Hofmann of Actlabs kindly providedvaluable input on assay protocols. This work wassupported by National Science Foundation awardsANT-0838773 to C. D. Amsler and J. B. McClintockand ANT-0838776 to B. J. Baker. J. B. McClintockacknowledges the support of an Endowed Profes-sorship in Polar and Marine Biology provided bythe University of Alabama at Birmingham. We ap-preciate the helpful editorial comments and in-sights of two anonymous reviewers.

R E F E R E N C E S C I T E D

Andersson, A.; Mackenzie, F.; and Bates, N. 2008. Lifeon the margin: implications of ocean acidification onMg-calcite, high latitude and cold-water marine cal-cifiers. Mar. Ecol. Prog. Ser. 373:265–273.

Arntz, W.; Brey, T.; and Gallardo, V. 1994. Antarctic zoo-benthos. Oceanogr. Mar. Biol. Ann. Rev. 32:241–304.

Binyon, J. 1976. The permeability of the asteroid bodywall to water and potassium ions. J. Mar. Biol. Assoc.UK. 56:639–647.

———. 1980. Osmotic and hydrostatic permeability ofthe integument of the starfish Asterias rubens L. J.Mar. Biol. Assoc. UK. 60:627–630.

Bischoff, W.; Mackenzie, F.; and Bishop, F. 1987. Stabil-ities of synthetic magnesium calcites in aqueous so-lution: comparison with biogenic materials. Geochim.Cosmochim. Acta 51:1413–1423.

Bøggild, O. 1930. The shell structure of the mollusk. K.Dan. Vidensk. Selsk. 9:235–326.

Borremans, C.; Hermans J.; Baillon, S.; Andre, L.; andDubois, P. 2009. Salinity effects on the Mg/Ca and Sr/Ca in starfish skeletons and the echinoderm relevancefor paleoenvironmental reconstructions. Geology 37:351–354.

Brey, T. 1991. Population dynamics of Sterechinus an-tarcticus (Echinodermata: Echinoidea) on the WeddellSea shelf and slope, Antarctica. Antarct. Sci. 3:251–256.

Byrne, M.; Ho, M.; Selvakumaraswamy, P.; Nguyen, H.D.; Dworjanyn, S.; and Davis, A. R. 2009. Tempera-ture, but not pH, compromises sea urchin fertilizationand early development under near-future climatechange scenarios. Proc. R. Soc. B 276:1883–1888.

Byrne, M.; Soars, N.; Selvakumaraswamy, P.; Dworjanyn,S.; and Davis, A. 2010. Sea urchin fertilization in a

warm, acidified and high pCO2 ocean across a rangeof sperm densities. Mar. Environ. Res. 69:234–239.

Caldeira, K., and Wickett, M. 2003. Anthropogenic car-bon and ocean pH. Nature 425:365.

Chave, K. 1954. Aspects of the biogeochemistry of mag-nesium. 1. Calcareous marine organisms. J. Geol. 62:266–283.

Clark, D.; Lamare, M.; and Barker, M. 2009. Response ofsea urchin pluteus larvae (Echinodermata: Echinoidea)to reduced seawater pH: a comparison of tropical, tem-perate, and a polar species. Mar. Biol. 156:1125–1137.

Clark, F. W., and Wheeler, W. C. 1922. The inorganicconstituents of marine invertebrates. U.S. Geol. Surv.Prof. Pap. 124, 56 p.

Dahm, C. 1999. Ophiuroids (Echinodermata) of southernChile and the Antarctic: taxonomy, biomass, diet andgrowth of dominant species. Sci. Mar. 63:427–432.

Dayton, P. K.; Robilliard, G.; Paine, R.; and Dayton, L.1974. Biological accommodation in the benthic com-munity at McMurdo Sound, Antarctica. Ecol. Monogr.44:105–128.

Dearborn, J. H. 1977. Food and feeding characteristics ofAntarctic asteroids and ophiuroids. In Llano, G. A.,ed. Adaptations within Antarctic ecosystems. Hous-ton, Gulf, p. 293–326.

Dickson, J. 2002. Fossil echinoderms as monitor of theMg/Ca ratio of Phanerozoic oceans. Science 98:1222–1224.

Fabry, V. J.; McClintock, J. B.; Mathis, J.; and Grebmeier,J. 2009. Ocean acidification at high latitudes: the bell-wether. Oceanography 22:160–171.

Feely, R.; Sabine, C.; Lee, K.; Berelson, W.; Kleypas, J.;Fabry, V.; and Millero, F. 2004. Impact of anthropo-genic CO2 on the CaCO3 system in the oceans. Science305:362–366.




Grzeta, B.; Medakovic, D.; and Popovic, S. 2004. Newmethod for estimation of the magnesium fraction inmagnesian calcite. Mater. Sci. Forum 443–444:55–58.

IPCC (Intergovernmental Panel on Climate Change).2007. Climate change 2007: the physical science basis.Contribution of Working Group 1 to the Fourth As-sessment of the Intergovermental Panel on ClimateChange. Intergovermental Panel on Climate Change,Geneva, 1099 pp.

Kurihara, H., and Shirayama, Y. 2004. Effects of increasedatmospheric CO2 on sea urchin early development.Mar. Ecol. Prog. Ser. 274:161–196.

Lampitt, R. S.; Bett, B. J.; Kiriakonlaki, K.; Popova, E. E.;Ragueneau, O.; Vangriesheim, A.; and Wolff, G. A.2001. Material supply to the abyssal seafloor in thenortheast Atlantic. Prog. Oceanogr. 50:27–63.

Lawrence, J. M. 1987. A functional biology of echino-derms. Baltimore, Johns Hopkins University Press.

Lebrato, M.; Iglesias-Rodrıguez, D.; Feely, R. A.; Greeley,D.; Jones, D. O. B.; Suarez-Bosche, N.; Lampitt, R. S.;Cartes, J. E.; Green, D. R. H.; and Alker, B. 2010.Global contribution of echinoderms to the marine car-bon cycle: CaCO3 budget and benthic compartments.Ecol. Monogr. 80:441–467.

Lemaitre, R.; Harasewych, M.; and Hammock, J., eds.2009. ANTIZ v 1.07: a database of Antarctic and Sub-antarctic marine invertebrates. Washington, DC, Na-tional Museum of Natural History, Smithsonian In-stitution, http://invertebrates.si.edu/ANTIZ/about.cfm.

Mackenzie, F.; Bischoff, W.; Bishop, F.; Loijens, M.;Schoonmaker, J.; and Wollast, R. 1983. Magnesiumcalcite: low temperature occurrence, solubility andsolid-solution behavior. In Reeder, R. J., ed. Carbon-ates: mineralogy and chemistry. Reviews in Miner-alogy 11. Washington DC, Mineralogy Society ofAmerica, p. 97–143.

McClintock, J. B. 1994. The trophic biology of Antarcticechinoderms. Mar. Ecol. Prog. Ser. 111:191–202.

McClintock, J. B.; Pearse, J. S.; and Bosch, I. 1988. Pop-ulation structure and energetics of the common Ant-arctic sea star Odontaster validus. Mar. Biol. 99:235–246.

McDonald, M.; McClintock, J. B.; Amsler, C. D.; Ritt-schof, D.; Angus, R.; Orihuela, B.; and Lutostanski, K.2009. Effects of ocean acidification over the life his-

tory of the barnacle Amphibalanus amphitrite. Mar.Ecol. Prog. Ser. 385:179–187.

Miles, H.; Widdicombe, S.; Spicer, J.; and Hall-Spencer,J. 2007. Effects of anthropogenic seawater acidificationon acid-base balance in the sea urchin Psammechinusmiliaris. Mar. Poll. Bull. 54:89–96.

O’Donnell, M. J.; Todgham, A. E.; Sewell, M. A.; Ham-mond, L. M.; Ruggiero, K.; Fangue, N. A.; Zippay, M.L.; and Hofmann, G. E. 2010. Ocean acidification al-ters skeletogenesis and gene expression in larval seaurchins. Mar. Ecol. Prog. Ser. 398:157–171.

Orr, J.; Fabry, V. J.; Aumont, O.; Bopp, L.; Doney, S. C.;Feely, R. A.; Gnanadesikanet, A.; et al. 2005. Anthro-pogenic ocean acidification over the twenty-first cen-tury and its impact on calcifying organisms. Nature437:681–686.

Pilkey, O. H., and Hower, J. 1960. The effect of environ-ment on the concentration of skeletal magnesium andstrontium in Dendraster. J. Geol. 68:203–216.

Sabine, C. L.; Key, R. M.; Kozyr, A.; Feely, R. A.; Wan-ninkhof, R.; Millero, F. J.; Peng, T.-H.; Bullister, J. L.;and Lee, K. 2005. Global Ocean Data Analysis Project(GLODAP): results and data. Carbon Dioxide Infor-mation Analysis Center, Oak Ridge National Labo-ratory, U.S. Department of Energy, ORNL/CDIAC-145, NDP-083.

Schlager, W., and James, N. P. 1978. Low-magnesium cal-cite limestones forming at the deep-sea floor, Tongueof the Ocean, Bahamas. Sedimentology 25:675–702.

Sewell, M. A., and Hofmann, G. E. 2011. Antarctic echi-noids and climate change: a major impact on broodingforms. Global Change Biol. 17:734–744.

Shirayama, Y., and Thornton, H. 2005. Effect of increasedatmospheric CO2 on shallow water marine benthos.J. Geophys. Res. 110, C09S08, doi:10.1029/2004JC002618.

Weber, J. 1969. The incorporation of magnesium into theskeletal calcites of echinoderms. Am. J. Sci. 267:537–566.

———. 1973. Temperature dependence of magnesium inechinoid and asteroid skeletal calcite: a reinterpreta-tion of its significance. J. Geol. 81:543–556.

Wood, H.; Spicer, J.; and Widdicombe, S. 2008. Oceanacidification may increase calcification rates, but at acost. Proc. R. Soc. B 275:1767–1773.


http://invertebrates.si.edu/ANTIZ/about.cfm

http://invertebrates.si.edu/ANTIZ/about.cfm


the mg-calcite composition of antarctic echinoderms: important implications for predicting the...

Documents