Pteropods in Southern Ocean ecosystems

Progress in Oceanography 78 (2008) 193–221

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Review

Pteropods in Southern Ocean ecosystems

B.P.V. Hunt a,*, E.A. Pakhomov a,b, G.W. Hosie c, V. Siegel d, P. Ward e, K. Bernard f

a Department of Earth and Ocean Science, University of British Columbia, 6339 Stores Road, Vancouver, BC, Canada V6T 1Z4b Zoology Department, University of Fort Hare, Private Bag X1314, Alice 5700, South Africac Australian Antarctic Division, Channel Highway, Kingston, Tasmania 7050, Australiad Sea Fisheries Institute, Palmaille 9, 22767 Hamburg, Germanye British Antarctic Survey (Natural Environment Research Council), High Cross, Madingley Road, Cambridge CB3 0ET, UKf Southern Ocean Group, Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6139, South Africa

a r t i c l e i n f o

Article history:Received 24 August 2007Received in revised form 30 May 2008Accepted 29 June 2008Available online 8 July 2008

Keywords:PteropodsLimacinaClioSouthern OceanAntarcticOcean acidification

0079-6611/$ - see front matter � 2008 Elsevier Ltd. Adoi:10.1016/j.pocean.2008.06.001

* Corresponding author.E-mail address: [email protected] (B.P.V. Hunt).

a b s t r a c t

To date, little research has been carried out on pelagic gastropod molluscs (pteropods) in Southern Oceanecosystems. However, recent predictions are that, due to acidification resulting from a business as usualapproach to CO2 emissions (IS92a), Southern Ocean surface waters may begin to become uninhabitablefor aragonite shelled thecosome pteropods by 2050. To gain insight into the potential impact that thiswould have on Southern Ocean ecosystems, we have here synthesized available data on pteropod distri-butions and densities, assessed current knowledge of pteropod ecology, and highlighted knowledge gapsand directions for future research on this zooplankton group.

Six species of pteropod are typical of the Southern Ocean south of the Sub-Tropical Convergence,including the four Thecosomes Limacina helicina antarctica, Limacina retroversa australis, Clio pyramidata,and Clio piatkowskii, and two Gymnosomes Clione limacina antarctica and Spongiobranchaea australis.Limacina retroversa australis dominated pteropod densities north of the Polar Front (PF), averaging60 ind m�3 (max = 800 ind m�3) and 11% of total zooplankton at the Prince Edward Islands. South ofthe PF L. helicina antarctica predominated, averaging 165 ind m�3 (max = 2681 ind m�3) and up to >35%of total zooplankton at South Georgia, and up to 1397 ind m�3 and 63% of total zooplankton in the RossSea. Combined pteropods contributed <5% to total zooplankton in the Lazarev Sea, but 15% (max = 93%) tomacrozooplankton in the East Antarctic. In addition to regional density distributions we have synthesizeddata on vertical distributions, seasonal cycles, and inter-annual density variation.

Trophically, gymnosome are specialist predators on thecosomes, while thecosomes are considered pre-dominantly herbivorous, capturing food with a mucous web. The ingestion rates of L. retroversa australisare in the upper range for sub-Antarctic mesozooplankton (31.2–4196.9 ng pig ind�1 d�1), while those ofL. helicina antarctica and C. pyramidata are in the upper range for all Southern Ocean zooplankton, in thelatter species reaching 27,757 ng pig ind�1 d�1 and >40% of community grazing impact. Further researchis required to quantify diet selectivity, the effect of phytoplankton composition on growth and reproduc-tive success, and the role of carnivory in thecosomes.

Life histories are a significant knowledge gap for Southern Ocean pteropods, a single study having beencompleted for L. retroversa australis, making population studies a priority for this group. Pteropods appearto be important in biogeochemical cycling, thecosome shells contributing >50% to carbonate flux in thedeep ocean south of the PF. Pteropods may also contribute significantly to organic carbon flux throughthe production of fast sinking faecal pellets and mucous flocs, and rapid sinking of dead animals ballastedby their aragonite shells. Quantification of these contributions requires data on mucous web productionrates, egestion rates, assimilation efficiencies, metabolic rates, and faecal pellet morphology for applica-tion to sediment trap studies.

Based on the available data, pteropods are regionally significant components of the Southern Oceanpelagic ecosystem. However, there is an urgent need for focused research on this group in order to quan-tify how a decline in pteropod densities may impact on Southern Ocean ecosystems.

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194 B.P.V. Hunt et al. / Progress in Oceanography 78 (2008) 193–221

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1942. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1943. Results and discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196

3.1. Species composition and biogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1963.2. Spatial and temporal density distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200

3.2.1. Regional abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2003.2.2. Relative contribution to zooplankton communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2013.2.3. Diel vertical migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2013.2.4. Seasonal variation in abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2043.2.5. Inter-annual variation in abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205

3.3. Feeding biology and grazing impact . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207
3.3.1. Thecosome feeding biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2073.3.2. Gymnosome feeding biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2093.3.3. Grazing impact . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 212
3.4. Reproduction and life cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213
3.4.1. Thecosomes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2133.4.2. Gymnosomes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215
3.5. Contribution to vertical flux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216
4. Summary and directions for future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219

1. Introduction

Southern Ocean zooplankton research has traditionally focusedon the perceived key ecosystem components, predominantly Ant-arctic krill (Euphausia superba) but including several copepod spe-cies, e.g. Calanoides acutus, Rhincalanus gigas, Metridia gerlachei (e.g.Schnack-Schiel and Hagen, 1994; Fransz and Gonzalez, 1997;Atkinson, 1998; Voronina, 1998). More recently the tunicate Salpathompsoni has been added to this list due to its seasonally highdensities, high grazing rates, contribution to vertical flux, andsouthward range expansion in response to ocean warming (Pakho-mov et al., 2002a; Atkinson et al., 2004). However, data on otherplanktonic groups remains sparse, despite being essential to ourunderstanding of the functioning of Southern Ocean ecosystemsand the ecological impacts of climate change. One such group isthe pteropods, a general term for gastropod molluscs that haveadopted an entirely pelagic life cycle. Pteropods fall into two or-ders, the Thecosomata (shelled pteropods) and Gymnosomata(naked pteropods). Although evidence from zooplankton commu-nity studies indicates that they are consistent, and sometimesdominant components of the Southern Ocean zooplankton, untilvery recently the role of pteropods in Southern Ocean ecosystemshas largely been ignored and few studies have focused exclusivelyon the ecology or biology of this group. For example, no studieshave been conducted on the life cycle of the Antarctic pteropodspecies, and only one in the sub-Antarctic (Dadon and de Cidre,1992).

It has recently been demonstrated that thecosome pteropodsmay be severely impacted by increasing atmospheric CO2 concen-trations (Orr et al., 2005). The ocean plays a pivotal role in regulat-ing atmospheric CO2. By taking up anthropogenic CO2 the oceanshelp to moderate the effects of climate change. It is estimated thatthe oceanic sink accounts for �48% of fossil-fuel and cement man-ufacturing CO2 emissions between 1800 and 1994 (Sabine et al.,2004). However, one of the consequences of increased CO2 uptakeis an increase in ocean acidity and a decrease in carbonate ion con-centrations (Orr et al., 2005). This will result in a reduction in cal-cium carbonate saturation levels, making the production ofbiogenic calcium carbonate more difficult for marine organisms,particularly those such as thecosome pteropods that produce ara-

gonite, the thermodynamically unstable form of calcium carbon-ate. Currently, the surface of the Southern Ocean is saturatedwith respect to aragonite to �700–1000 m depth, below whicharagonite dissolution begins to occur. However, models predictthat following a business as usual approach to CO2 emissions(IS92a) Southern Ocean surface waters may begin to becomeundersaturated with respect to aragonite by 2050, extendingthrough the entire Southern Ocean by 2100 (Orr et al., 2005).

An experimental study using the Arctic thecosome Clio pyrami-data found that shell dissolution in this species began to occurwithin 48 h at the undersaturation levels predicted for the South-ern Ocean in 2100, following IS92a (Orr et al., 2005). Increasingocean acidity may therefore result in a major change to the distri-bution of thecosome pteropods, and their possible disappearancefrom Southern Ocean ecosystems. This would impact directly onthe Southern Ocean gymnosome pteropod species as they aremonophagous predators of their thecosome relatives. However,what impact a northward shift, and possible disappearance, ofpteropods will have on the ecology of the Southern Ocean at theecosystem level is presently unknown. In this paper, we reviewcurrent knowledge of Antarctic pteropods in an attempt to provideinsight into this question, and assess knowledge gaps and direc-tions for future research on this group. This is done through a com-bination of reviewing and extracting data from previous studies,and collating and analyzing largely unpublished data sets fromAustralian, South Africa, German and British surveys.

2. Methods

Five major components of pteropod ecology and biology wereassessed:

� species composition and biogeography;� spatial and temporal density distribution;� feeding biology and grazing impact;� life cycle;� contribution to carbon flux.

For the purpose of this study the northern extent of the South-ern Ocean was defined as the Sub-Tropical Convergence. Raw

Table 1List of pteropod density data sources used in this review, including region sampled, month, year, ship, voyage name where available, voyage number assigned for this study,number of samples per voyage, and net used for sampling

Region Month Year Voyage Voyage # Number of samples Net

Antarctic Peninsula February 1982 1 187 RMT8Antarctic Peninsula February–April 1985 2 158 RMT8Antarctic Peninsula May–June 1986 3 92 RMT8Antarctic Peninsula November–December 1987 4 79 RMT8Antarctic Peninsula October–November 1988 5 59 RMT8Antarctic Peninsula October–November 1988 5 58 RMT8Antarctic Peninsula January–February 1994 7 22 RMT8Antarctic Peninsula January–February 1994 7 24 RMT8Antarctic Peninsula December–January 1989/1990 8 255 RMT8South Georgia December 1998 JR38 8 22 BongoEast Antarctic February–March 1985 9 59 IKTEast Antarctic December–March 1985/1986 10 78 IKTEast Antarctic January–March 1987 11 69 IKTEast Antarctic January–March 1987 11 91 BongoEast Antarctic December–April 1987/1988 12 99 IKTEast Antarctic February–April 1988 13 52 BongoEast Antarctic January–February 1988 14 57 0.2MTEast Antarctic February–April 1989 14 34 BongoEast Antarctic February–March 1988 15 60 0.2MTEast Antarctic November–March 1988/1989 16 71 0.2MTEast Antarctic January–March 1990 17 48 BongoEast Antarctic February–March 1990 18 49 BongoLazarev Sea/South Atlantic January–February 1993 V70 19 53 BongoLazarev Sea/South Atlantic December–January 1994/1995 V77 20 76 BongoLazarev Sea/South Atlantic December–January 1994/1995 V77 20 51 RMTLazarev Sea/South Atlantic December–January 1997/1998 V86, SWEDARP 21 34 BongoPrince Edward Islands April 1989 MOES II 22 17 BongoPrince Edward Islands April–May 1996 MIOS 1 23 25 BongoPrince Edward Islands April/May 1997 MIOS 2 24 27 BongoPrince Edward Islands May 1997 V84 25 16 RMT8Prince Edward Islands May 1997 V84 25 21 BongoPrince Edward Islands April 1998 MIOS 3 26 57 BongoPrince Edward Islands April 1998 MIOS III 26 41 RMT8Prince Edward Islands April 1999 MIOS 4 27 39 BongoPrince Edward Islands April 2000 MIOSV 28 144 BongoPrince Edward Islands April 2001 MOEVS I 29 25 BongoPrince Edward Islands April 2002 MOEVS II 30 13 WP2Prince Edward Islands April 2003 DEIMIC II 31 9 RMT8Prince Edward Islands April 2004 MOEVS IV 32 10 BongoPrince Edward Islands April 2005 MOEVS V 33 24 WP2South Georgia February 1994 34 8 BongoSouth Georgia January 1996 JR11 35 22 BongoSouth Georgia December 1996 JR17 36 22 BongoSouth Georgia January 1998 JR28 37 22 BongoSouth Georgia January–February 2000 JR47 39 122 RMT1

South Georgia January–February 2002 JR70 40 59 BongoScotia Sea January–February 2003 JR82 41 61 BongoSouth Georgia March 2004 JR100 42 19 BongoSouth Georgia January 2005 JR116 43 57 BongoSouth Georgia December–January 2000/2001 JR57 44 32 Bongo140�E transect November 2001 CLIVAR 45 19 NORPACSouth of Australia January–December 1997/2006 Multiple voyages 16,456 CPR

B.P.V. Hunt et al. / Progress in Oceanography 78 (2008) 193–221 195

pteropod density data from vertical or obliquely hauled nets werecollated from 45 voyages, a total of 2848 individual net hauls(Table 1). In addition we included 16,456 samples from the South-ern Ocean Continuous Plankton Recorder (CPR) Survey. The spatialdistribution of samples is illustrated in Fig. 1.

The samples were divided into mesozooplankton (200–2000 lm) and macrozooplankton size fractions (>2000 lm) basedon the mesh size used. Mesozooplankton were collected with amesh size of 200–350 lm, and nets included Bongo (0.5 m2;300 lm mesh), MT (0.2 m2; 300 lm mesh) WP2 (0.25 m2;200 lm mesh), RMT1 (1 m2; 300 lm mesh) and NORPAC(0.45 m2; 270 lm mesh). Macrozooplankton were collected with4.5 mm mesh and nets included RMT8 (8 m2, 4.5 mm mesh) andIKT (5.5 m2; 4.5 mm mesh). Although East Antarctic samples werecollected with Bongo and MT nets only organisms larger than9 mm in length or diameter were counted and so these data werealso grouped as macrozooplankton. All densities were standard-

ized as individuals m�3. Samples were not evenly distributed butconcentrated in six regions, the Antarctic Peninsula, South Georgia,Prince Edward Islands, Lazarev Sea, East Antarctic, and the CPRsamples south of Australia. Accordingly, the analysis focused onthese regions and there is a conspicuous gap in data points forthe western sector of the Southern Ocean, between 180�W and90�W.

Much of the data in the remaining sections were drawn fromthe literature, and readers are referred to the source material.However, an additional two components of the data set are previ-ously unpublished. These include the stable isotope data presentedin Fig. 15 (Section 3.3.1) and some of the gut pigment data in Figs.16 and 17 (Section 3.3.3). Samples for stable isotope analysis werecollected from the Prince Edward Island region in April 1999 andthe Lazarev Sea in April 2004. All samples were then frozen at�18 �C for storage. After return to the laboratory, organisms weredried for 24 h at 50 �C, crushed and homogenized with a mortar

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Fig. 1. Map showing the distribution of sample points used in this study. The major sampling regions are highlighted by dashed boxes: SG – South Georgia, AP – AntarcticPeninsula, LS – Lazarev Sea, PEI – Prince Edward Islands, EA – East Antarctica, CPR – Continuous Plankton Recorder Survey. The position of the Sub-Antarctic Front (SAF), PolarFront (PF) and Southern Boundary (SB) of the Antarctic Circumpolar Current are indicated.


and pestle, and then treated with 2 N HCl to remove carbonates. Inorder to minimise variation in the isotope signature due to species’differences in the concentration of isotopically lighter lipids, PrinceEdward Island samples were defatted in a solution of methanol,chloroform and water (2:1:0.8) after the method of Bligh and Dyer(1959). This was not done for the samples from the Lazarev Sea.After a final wash in distilled water, samples were once more dehy-drated, and small quantities from each sample (0.45–0.6 mg) wereweighed into tin combustion cups. d13C and d15N determinationwas carried out on a Finnigan-MAT 252 stable light isotope massspectrometer, after sample combustion in an on-line Carlo-Erbapreparation unit. Merck gelatine was used as an internal standard,calibrated against several International Atomic Energy Agency ref-erence materials. Results are expressed in the standard delta nota-tion, as dX = ([Rsample/Rstandard] � 1)1000, where X = the element inquestion and R = the ratio of the heavy over the light isotope.

The isotopic ratios of both carbon and nitrogen change as theseelements pass through a food web (Fry and Sherr, 1984; Wadaet al., 1991). Organisms use lighter isotopes preferentially in met-abolic processes and because of this they are either respired or ex-creted before the heavier forms. As a consequence heavier isotopesaccumulate in organisms during growth and, in addition, the ratioof heavy to light isotopes in an organisms organic material in-creases with its position in the food chain. Importantly, the isotopicratios of carbon and nitrogen change in a predictable fashion rela-tive to an organisms diet. In marine consumers, depending on thetissue type sampled, d13C typically becomes enriched by �1‰ (Fryand Sherr, 1984; France and Peters, 1997) and d15N by 3–4‰

(Owens, 1987; Wada et al., 1991) relative to their prey. As d13C be-

Table 2Distributions and maximum size of the eight major pteropod taxa (6 species) found in th

Order Species Maximum length M

Thecosomata Clio piatkowskii 13.5 1Clio pyramidata forma antarctica 17 –Clio pyramidata f. sulcata 20 1Limacina helicina antarctica f. antarctica – 6Limacina helicina antarctica f. rangi 2.0 3Limacina retroversa australis 2.5 1

Gymnosomata Clione limacina antarctica 40 –Spongiobranchaea australis 22

PF – Polar Front; ACC – Antarctic Circumpolar Current; STC – Sub-Tropical ConvergenceFull names, with describers in parenthesis, for the eight pteropod taxa found in the Sout1767) forma antarctica (Dale, 1908); Clio pyramidata (Linnaeaus, 1767) f. sulcata (Pfeffer(Woodward, 1854); Limacina helicina (Phipps, 1774) antarctica f. rangi (d’ Orbingy, 1836limacina (Phipps, 1774) antarctica (Smith, 1902); Spongiobranchaea australis (d’ Orbingy,

comes enriched more slowly through a food web it provides infor-mation on the primary source of food web carbon, while the morerapid change in d15N provides information on a consumer’s trophiclevel within the food web (de Niro and Epstein, 1976; Wada et al.,1991).

Gut pigment data were collected in the Lazarev Sea in 1994/1995, 1997/1998, 2003/2004 and 2006/2007 and are presentedin Figs. 16 and 17. Fig. 15a–d is previously published. Data pre-sented in Fig. 16e and f, and all of Fig. 17, with the exception ofFig. 17e, are previously unpublished. For the determination ofthese new gut pigment content data pteropod specimens weresorted immediately after capture, specimens placed in plastic cen-trifuge tubes with 8 ml of 90% acetone, and stored at �20 �C for24 h. Five to ten replicates (tubes) were generally used per species.After centrifugation at 5000 rpm, chlorophyll a and phaeopig-ments, were measured with a Turner Designs fluorometer, beforeand after acidification (Mackas and Bohrer, 1976). Gut contentswere expressed in terms of pigment equivalents per individualand calculated according to Strickland and Parsons (1968), as mod-ified by Conover et al. (1986). When the chlorophyll a: phaeopig-ment ratio of the gut content was higher than 0.25, total pigmentlevels were corrected according to Baars and Helling (1985).

3. Results and discussion

3.1. Species composition and biogeography

van der Spoel et al. (1999) recorded 74 species of pteropodfrom the South Atlantic sector of the Southern Ocean. However,

e Southern Ocean, taken from van der Spoel et al. (1999)

aximum width/diameter Distribution

6 Recorded in Weddell Sea, mesopelagicMainly north of the PF

0 Mainly south of PF to Antarctic coast.5 Antarctic coast to southern ACC.5 Predominantly STC–PF, occurring south to SB.5 Predominantly STC to PF

STC to Antarctic coast, predominantly AntarcticSTC to Antarctic coast, predominantly sub-Antarctic

; SB – Southern Boundary of the ACC.hern Ocean: Clio piatkowskii (van der Spoel et al., 1992); Clio pyramidata (Linnaeaus,, 1879); Limacina helicina (Phipps, 1774) antarctica (Woodward, 1854) f. antarctica); Limacina retroversa (Fleming, 1823) australis (Eydoux and Souleyet, 1840); Clione1836).

Fig. 2. The six major species and forms of pteropod found in the Southern Ocean (f. – forma). Pictures from van der Spoel et al. (1999).


south of the Sub-Tropical Convergence (STC) six species are typ-ical of Southern Ocean ecosystems, four Thecosomata and twoGymnosomata (Table 2; Fig. 2). Both Limacina helicina antarcticaand C. pyramidata are recognized as having two different forms.Four of the species, namely Clione limacina, L. helicina, Limacinaretroversa and C. pyramidata, occur in both southern and north-ern hemisphere temperate/polar oceans. However, the SouthernOcean sub-species of C. limacina, L. retroversa and L. helicina(both forms), and both forms of C. pyramidata are unique tothe Southern Ocean. All species and forms of thecosome canbe identified by their shell morphology (Fig. 2). A major featureseparating the two species of gymnosome is the presence of twolateral arms, each with 7 to >20 suckers in Spongiobranchaea aus-tralis, while C. limacina antarctica has six tentacle-like buccalcones. When alive S. australis is a brown/grey coloration, whileC. limacina antarctica is red. In the Southern Ocean literaturethe different sub-species and forms of L. retroversa, L. helicina,

C. pyramidata and C. limacina are typically not identified or re-ferred to. As this review gains insights into some aspects ofSouthern Ocean pteropod ecology from biological studies ofnorthern hemisphere species, we use sub-species and formswhen referring to the Southern Ocean taxa whenever these dataare available, in order to differentiate them from their northerncounterparts.

In addition to the above species a number of temperate/sub-tropical species are occasionally advected across the STC into theSub-Antarctic Zone (SAZ) (Lalli and Wells, 1978; van der Spoelet al., 1999). Expatriates in the data set compiled for this study in-cluded one record of Diacria sp. from near the Sub-Antarctic Front(SAF) in the Indian Ocean sector, two records of Cymbulia sp. fromthe South Atlantic near the SAF, and one record of Limacina inflatato the north of South Georgia. These rare species are not reviewedhere, and we focus on the eight true Southern Ocean species andforms currently recognized.


The biogeography of pteropods in the Atlantic sector of theSouthern Ocean was reviewed by van der Spoel et al. (1999) andthe distributions determined by these authors are summarized inTable 2. These were compared with distribution maps generatedfrom the combined data sets of Table 1, produced by plotting onlythose samples where a species was present (Fig. 3). Data for theWeddell and Ross seas were derived from the literature. The CPRsamples were only included in the map for Limacina spp., due toshell damage during collection by the CPR preventing species levelidentification and other species being rarely recorded possibly due

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Fig. 3. Samples within the entire sample data base, indicated by triangles, in whichdifferentiated within the CPR samples, these were only used for Limacina spp. Data pointsthe Weddell Sea were derived from Boysen-Ennen and Piatkowski (1988) and Fisher etSouthern Boundary.

to a combination of the shallow CPR sampling depth and damageto the soft bodies gymnosomes.

Prior to this study Clio piatkowskii had only been recorded fromthe mesopelagic Weddell Sea (van der Spoel et al., 1992, 1999).This species was rare in the present study, occurring in only eightsamples. Two of these were in the vicinity of the Polar Front (PF) inthe South Atlantic (upper 300 m of the water column), while theremaining six were collected in the Lazarev Sea (Fig. 3). Stratifiednet tows indicated that this species did not occur in the upper100 m of the water column although five occurrences were in the

0˚ 30˚ 60˚ 90˚ 120˚ 150˚

0˚ 30˚ 60˚ 90˚ 120˚ 150˚

0˚ 30˚ 60˚ 90˚ 120˚ 150˚

icina antarctica

versa australis

na spp.

pteropod species were present. As pteropod species could not consistently befor the Ross Sea were derived from Foster (1989) and Knox et al. (1996), and data foral. (2004). Cpk – Clio piatkowskii, SAF – Sub-Antarctic Front, PF – Polar Front, SB –

Clione limacina antarctica

-80˚

-70˚

-60˚

-50˚

-40˚-30˚

-150˚ -120˚ -90˚ -60˚ -30˚ 0˚ 30˚ 60˚ 90˚ 120˚ 150˚

-80˚

-70˚

-60˚

-50˚

-40˚-30˚

-150˚ -120˚ -90˚ -60˚ -30˚ 0˚ 30˚ 60˚ 90˚ 120˚ 150˚

-80˚

-70˚

-60˚

-50˚

-40˚-30˚

-150˚ -120˚ -90˚ -60˚ -30˚ 0˚ 30˚ 60˚ 90˚ 120˚ 150˚

Spongiobranchaea australis

Clio pyramidata

6xCpk

2xCpk

SAF

PF

SB

SAF

PF

SB

SAF

PF

SB

Fig. 3 (continued)


upper 500 m (Fig. 12). The absence of C. piatkowskii from the EastAntarctic sector samples indicates that this species may only occurin the South Atlantic. However, in view of the predominantlymesopelagic distribution of C. piatkowskii, the lack of net tows inour data set to depths >500 m in regions outside of the SouthAtlantic may have contributed to the observed regional distribu-tion, while misidentification of this species as C. pyramidata canalso not be excluded.

The genus Limacina is widespread in the Southern Ocean(Fig. 3), however, the two forms of L. helicina antarctica are to alarge extent geographically distinct (Table 2). Limacina helicinaantarctica f. rangi typically occurs north of the PF while L. helicinaantarctica f. antarctica is typical of Antarctic waters, occurring

largely south of the PF to the Antarctic coast. None of the data setsused in this study differentiated between the two forms of L. heli-cina antarctica. A search of the literature indicates that this is thenorm, and there are few instances where the two forms have beenseparated. As L. helicina antarctica occurred from the AntarcticCoast to the SAZ (Fig. 3) it probably included both forms of thissub-species. Forma antarctica attains double the shell width of for-ma rangi (6.5 mm as opposed to 3.5 mm). The absence of L. helicinaantarctica from the macrozooplankton samples north of the PFtherefore appears to confirm that in this sub-Antarctic region thesmaller forma rangi predominated.

The remaining Limacina species, L. retroversa australis, attains asmaller size than L. helicina antarctica, reaching a maximum shell


width of 1.5 mm (Table 2). It is considered to be predominantly asub-Antarctic species and in this study it was the principal ptero-pod species and had its highest densities at the Prince Edward Is-lands (Tables 2 and 3a). However, L. retroversa australis can occursouth of the PF and was recorded south of the Southern Boundaryof the Antarctic Circumpolar Current in both the South Georgia andAntarctic Peninsula regions, as well as along a 140�E transect (Voy-age #45 – Table 1) south of Australia (Fig. 3).

As with L. helicina antarctica, the two forms of C. pyramidata areconsidered geographically distinct (Table 2). Clio pyramidata f. ant-arctica occurs predominantly in the SAZ while C. pyramidata f. sul-cata is more typical of Antarctic waters, occurring south of the PF tothe Antarctic coast. van der Spoel et al. (1999) noted that the latterform appears to be absent from the Southern Ocean between�180�W and 90�W. Due to a lack of data, this cannot be assessedin the present study. The two forms of C. pyramidata were rarelyseparated in the data sets available to us. However, the distributionof C. pyramidata from the SAF to the Antarctic coast indicated thatboth forms were present (Fig. 3). The two gymnosome species,C. limacina antarctica and S. australis, were broadly distributed be-tween the STC and the Antarctic coast (Table 2, Fig. 3). However,C. limacina antarctica is considered to be a more typically Antarcticspecies, occurring predominantly south of the PF, while S. australisis more common north of the PF, in the Polar Frontal Zone (PFZ)and SAZ.

3.2. Spatial and temporal density distribution

3.2.1. Regional abundanceAverage pteropod species densities (individuals m�3), including

Limacina spp. from the CPR survey, were calculated for each of theregions highlighted in Fig. 1. As a compromise between being asinclusive as possible of samples from each region while comparinga similar seasonal time period, data used were limited to samplescollected between October and May. Stratified tows were inte-grated across the depth range sampled and the data set used forthe regional comparison was constrained to depths 6500 m. Dueto the differences in the mesh size of nets used and the large sizedifference between pteropod species, separate tables were pro-duced for samples collected as meso- and macrozooplankton (Ta-bles 3a and 3b, respectively). It should be noted, however, thatthe Limacina species may have been substantially undersampled

Table 3aAverage densities ± standard deviations (individual m�3) of pteropods collected in mesozo

Prince EdwardIslands

South Georgia Antarctic Peninsula

n 402 330 142Month April–May December–March October–November

January–MarchYear 1996–2002,

2004–20051994, 1996, 1998,2000–2005

1988, 1994, 2000,2003

Clio piatkowskii – – –

Clio pyramidata 0.058 ± 0.119(0.59)

0.003 ± 0.022(0.256)

0.003 ± 0.011(0.103)

Clione limacinaantarctica

0.015 ± 0.049(0.473)

2.980 � 10�4 ± 0.005(0.093)

0.001 ± 0.004(0.028)

Limacina spp.

Limacina helicinaantarctica

0.882 ± 2.671(29.67)

165.149 ± 387.324(2681.04)

0.556 ± 2.485(21.9)

Limacinaretroversaaustralis

60.098 ± 97.770(802.34)

1.705 � 10�4 ± 0.002(0.029)

0.002 ± 0.008(0.076)

Spongiobranchaeaaustralis

0.011 ± 0.059(0.752)

1.307 � 10�4 ± 0.001(0.012)

0.001 ± 0.003(0.028)

Sample number (n) and sampling months and year are indicated. Data were constraineda Data source: Foster (1989) and Knox et al. (1996).

by even the mesozooplankton nets. A comparison of 76 lm,202 lm and 330 lm mesh nets (50, 50, and 100 cm diameter,respectively) on Eltanin cruise #23 (April–May 1966) found densi-ties of Limacina spp. in the 76 lm mesh of 21.96 ind m�3, whilethey were absent in the 202 lm and 330 lm mesh nets (Hopkins,1971). Juvenile Limacina species may therefore be an importantfraction of the microzooplankton.

The two Limacina species were the major contributors to totalpteropod abundance in the mesozooplankton samples (Table 3a).Limacina retroversa australis was the dominant pteropod at thesub-Antarctic Prince Edward Islands, averaging 60 ind m�3 andreaching up to 800 ind m�3. South of the PF this species occurredat low densities or was completely absent. On a single transectsouth of Australia, collected along 140�E during Voyage #45 (Table1), L. retroversa australis densities averaged 1.23 ind m�3 from theSAZ to south of the SB. Overall, L. helicina antarctica was the dom-inant pteropod species south of the PF. At South Georgia densitiesaveraged 165 ind m�3 with maximum densities of 2681 ind m�3.The literature values for L. helicina antarctica in the Ross Sea re-ported in Table 3 are low. However, Pane et al. (2004) recordeddensities of up to 1397 ind m�3 for combined Limacina and Clionein Terra Nova Bay (Ross Sea) during January/February 1995, usinga 200 lm WP2 net. It is likely that L. helicina antarctica was the ma-jor contributor to these high densities. Hopkins (1987) noted thatdensities of L. helicina antarctica may reach 300 ind m�3 in the RossSea, and other studies have demonstrated this species to be a dom-inant component of the Ross Sea plankton (Hecq et al., 1992, inGoffart et al., 2000; Accornero et al., 2003). Average densities ofboth Limacina species were low in the Antarctic Peninsula and Laz-arev Sea regions (<0.6 ind m�3) (Table 3a). Densities of Limacinaspp. sampled by the CPR samples south of Australia averaged3.7 ind m�3 but reached up to 479 ind m�3. After the two Limacinaspecies, the next most abundant taxon in the mesozooplanktonwas C. pyramidata, while C. limacina antarctica and S. australis werealways present at background levels.

Due to its small size, L. retroversa australis was completely ab-sent from the large mesh macrozooplankton nets (Table 3b). Lima-cina helicina antarctica was present in the macrozooplanktonsamples south of the Polar Front, although, at substantially lowerdensities than in the mesozooplankton nets. The 4.5 mm mesh sizeof the macrozooplankton nets used to collect these data indicatedthat these were specimens of the larger L. helicina antarctica forma

oplankton samples, with maximum densities in parenthesis

CPR EastAntarctic

Lazarev Sea WeddellSea

Ross Seaa

16,456 128 108November–April

December–January October–December

1997–2006 1990, 1993, 1994/1995,1998/1997

1976, 1985,1987

– 7.626 � 10�6 ± 8.627 � 10�5

(0.001)0.009 ± 0.106(4.160)

0.003 ± 0.008(0.050)0.009 ± 0.014(0.084)

0.462a

3.739 ± 19.011(479.37)

0.014 ± 0.039(0.382)

0.404a

– –

1.317 � 10�5 ± 1.489 � 10�4

(0.002)

to depths <500 m and the months October–May.

Table 3bAverage densities ± standard deviations (individual m�3) of pteropods collected in macrozooplankton samples, with maximum densities in parenthesis

Prince EdwardIslands

SouthGeorgia

Antarctic Peninsula CPR East Antarctic Lazarev Sea Weddell Seaa RossSea

n 66 501 660 26Month April–May October–May December–March December–JanuaryYear 1997, 1999, 2003 1982, 1985–1990, 1994 1985–1990 1994/1995Clio piatkowskii – – – 9.052 � 10�6 ± 2.682 � 10�6

(0.0001)–

Clio pyramidata 2.131 � 10�4 ± 4.724� 10�4 (0.003)

9.561 � 10�5 ± 0.005(0.009)

0.008 ± 0.049(0.996)

3.341 � 10�4 ± 4.923 � 10�4

(0.002)8.724 � 10�4 a

Clione limacinaantarctica

– 1.574 � 10�4 ± 7.219 � 10�4

(0.015)0.001 ± 0.002(0.021)

6.865 � 10�4 ± 5.736 � 10�4

(0.003)9.728 � 10�4 a

Limacina spp. – –Limacina helicina

antarctica– 0.001 ± 0.005

(0.062)0.005 ± 0.012(0.153)

6.736 � 10�5 ± 1.202� 10�4

(0.0004)

0.041a

Limacinaretroversaaustralis

– – –

Spongiobranchaeaaustralis

2.455 � 10�4 ± 4.011� 10�4 (0.002)

5.809 � 10�5 ± 4.553 � 10�4

(0.009)2.305 � 10�4 ± 6.396� 10�4 (0.006)

9.039 � 10�6 ± 4.609 � 10�6

(0.0002)7.354 � 10�5 a

Sample number (n) and sampling months and year are indicated. Data were constrained to depths <500 m and the months October–May.a Data source: Boysen-Ennen and Piatkowski (1988) and Fisher et al. (2004).


antarctica, rather than forma rangi. In the macrozooplankton netsC. pyramidata rivaled the densities of L. helicina antarctica, and itwas the most abundant pteropod in the East Antarctic and LazarevSea sectors (Table 3b). As highlighted above, C. piatkowskii wasonly recorded in and north of the Lazarev Sea (Fig. 3), and the den-sities of this species were extremely low (Table 3b). Clione limacinaantarctica was not recorded in the macrozooplankton samplesfrom the Prince Edward Islands.

3.2.2. Relative contribution to zooplankton communitiesAs a measure of the contribution of pteropods to zooplankton

communities, their proportional abundance was calculated wher-ever total zooplankton densities were available for the voyageslisted in Table 1. For the Prince Edward Islands data set, the1996–1999 data included all pteropod species, while the 2000–2005 data included only L. retroversa australis densities and sothe proportional contribution of pteropods were underestimatedfor these years. Pteropods were a major community componentin this region, contributing an average of 11% to total mesozoo-plankton densities (Fig. 4). There was substantial variation bothwithin and between years, with a sample high of �85% in 1999and a year average high of 27% in 2000.

In the East Antarctic region pteropods were a major compo-nent of the IKT samples, averaging 14.5% and reaching up to93% of total macrozooplankton abundance (Fig. 4). Percentagecontribution was lowest in 1988 (5.7%) but was P14% from1985 to 1987. In the case of Bongo/0.2MT nets the percentagecontribution of pteropods was >20% in 1987, 6% in 1988, and<2.3% in 1989 and 1990. Clio pyramidata sulcata was the mostimportant pteropod in this sector, and the low percentage con-tribution from 1988 to 1990 reflected, in part, low densities ofthis species in these years (Fig. 5).

The average contribution of pteropods to CLIVAR, CPR, and V70mesozooplankton, V77 meso- and macrozooplankton, and MIOS3macrozooplankton samples was always less than 5% (Fig. 4). How-ever, pteropods did contribute up to 100% to total zooplanktondensities in CPR samples. The CLIVAR samples comprised the NOR-PAC net tows along 140�E (Table 1). The V77 and V70 samples pre-dominantly come from the Lazarev Sea where pteropods hadconsistently low densities. The MIOS3 macrozooplankton sampleswere collected at the Prince Edward Islands, where the small L. ret-roversa australis dominated densities and made a large contribu-tion to the mesozooplankton (Table 3a, Fig. 4). However, this

small species was clearly not captured with macrozooplanktonnets (Table 3b).

Additional data from the literature highlights the regionalimportance of pteropods. In the Ross Sea, February 1983, L. helicinaantarctica contributed 63.2% and 23% to density and biomass ofzooplankton, respectively (Hopkins, 1987). These data were col-lected with a combination Tucker trawl (4.8 m2) and planktonnet (0.44 m2) and so reflected both macro- and mesozooplankton.A repeat transect in the Polar Frontal Zone north of South Georgia,completed in December and January of 1996 and 1998 with a200 lm Bongo net, showed that pteropods contributed on average11% to mesozooplankton densities, the second largest contributionafter copepods (Ward et al., 2003). In January 1994, during a phy-toplankton bloom, Limacina sp. contributed on average >35% tomesozooplankton abundance at South Georgia (Atkinson et al.,1996). By February/March the average contribution had decreasedto 15%, although being 44% and 53% at two of eight South Georgiastations sampled (Pakhomov et al., 1997). In the southern shelf ofthe Weddell Sea 1–2 mm Limacina spp. contributed 16.6% to zoo-plankton biomass in February–March 1983 (Boysen-Ennen et al.,1991).

3.2.3. Diel vertical migrationFrom amongst the archived data outlined in Table 1, stratified

net data with day/night coverage were available for the EastAntarctic, Lazarev Sea and a single transect south of Australia(along 140�E). These data were all collected between Novemberand February and are presented in Figs. 5–7. Three un-stratified24 h stations from the Lazarev Sea, sampling to 300 m depth,provided additional information on diel vertical migration(Fig. 7).

Limacina helicina antarctica had a variable diel vertical migra-tion pattern in summer. In the East Antarctic macrozooplanktonsamples this species did not show a distinct diel migration pattern,but was observed in the surface 50 m during the day on 21/2/89and 23/2/89 (Fig. 5). In the Lazarev Sea samples, including thethree 24 h stations, this species appeared to have a more distinctdiel pattern of day time migration out of and night time migrationinto surface waters (Figs. 6 and 7). Vertical distribution data for L.retroversa australis were only available from a 140�E transect southof Australia (Voyage #45), and indicated that this species under-went a weak diel migration, occurring at highest densities in theupper 50 m at night (Fig. 6).

0

1020

30

4050

60

70

8090

100

1996 1997 1998 1999 2000 2001 2002 2003 2004 2005

year

pte

rop

od

/ t

ota

l zo

op

lan

kto

n (

%)

max

Prince Edward Islands (meso)

0

10

20

30

40

50

60

70

80

90

100

1985 1986 1987 1988year

pte

rop

od

/ t

ota

l zo

op

lan

kto

n (

%)

East Antarctic - IKT (macro)

0

10

20

30

40

50

60

70

80

90

100

1987 1988 1989 1990year

pte

rop

od

/ t

ota

l zo

op

lan

kto

n (

%)

East Antarctic Bongo/0.2MT (macro)

0

10

20

30

40

50

60

70

80

90

100

CLIVAR(meso)

V77(meso)

V70(meso)

CPR(meso)

V77(macro)

MIOS3(macro)

pte

rop

od

/ t

ota

l zo

op

lan

kto

n (

%)

Fig. 4. Percentage contribution of pteropods to total zooplankton abundance, for Table 1 cruises where both data were available. Error bars are standard deviations andmaximum values are indicated by a solid diamond. In the case of the East Antarctic samples, both IKT and Bongo/0.2MT net types were only analyzed for macrozooplankton.Voyage names in the bottom figure correspond with those in Table 1, while meso and macro refer to mesozooplankton and macrozooplankton, respectively.


February data for C. pyramidata sulcata from the East Antarcticshowed that this species generally underwent a pronounced dielmigration, occurring in the surface 0–25 m layer during the dayin only three out of nine samples (Fig. 5). This diel migration wasalso evident on the 140�E NORPAC transect (Voyage #45), andthe 24 h stations conducted in the Lazarev Sea where C. pyramidatasulcata generally only occurred in the upper 300 m of the watercolumn at night (Figs. 6 and 7). The mesopelagic tows from theLazarev Sea provided further evidence for diel migration, at leastduring the summer months, with this species occurring below200 m during the day and down to the 1000–500 m layer (Fig. 8).Unlike C. pyramidata, C. piatkowskii was only sampled in the 90–

1000 m layers, and our data therefore agree with the assertion ofvan der Spoel et al. (1999) that this is primarily a mesopelagic spe-cies (Fig. 8).

Clione limacina antarctica showed a variable diel migration pat-tern. In the East Antarctic samples no distinct diel cycle was appar-ent, and on 21/2/89, and 23/2/89 the vertical density distributionof C. limacina antarctica closely tracked the maximum densities ofL. helicina antarctica (Fig. 5). High day time densities of C. limacinaantarctica were observed in the Lazarev Sea in 1994/1995, while astrong diel migration was observed for this species on the 140�ENORPAC transect (Voyage #45) (Fig. 6) and the mesopelagic Laza-rev Sea samples (Fig. 8). The only data on diel variation for the

Fig. 5. Vertical distribution of pteropod densities (individuals m�3) in East Antarctic macrozooplankton samples (1985–1990). Sampling date is indicated on each figure anderror bars (standard deviations) are given where more than one sample (n) was collected. White bars indicate day-time densities and dark bars indicate night-time densities.

0 2 4 6 8

30-0

90-30

200-90

denisty (ind.m-3)

day

night


1-2 Jan 1995RMT8

0 0.01 0.02 0.03 0.04

30-0

90-30

200-90

denisty (ind.m-3)

day

night


2 Jan 1995Bongo

0 0.05 0.1 0.15

30-0

90-30

200-90

denisty (ind.m-3)

day

night

Limacina helicina antarctica

2 Jan 1995Bongo

0 0.2 0.4 0.6 0.8

30-0

90-30

200-90

denisty (ind.m-3)

day

night

Clio pyramidata sulcata

1-2 Jan 1995RMT8

Limacina retroversa

0 1 2 3 4

0-20

20-50

50-100

100-150

density (ind.m-3)

day

night

Nov 2001NORPAC

Clio pyramidata

0 0.2 0.4 0.6

0-20

20-50

50-100

100-150

density (ind.m-3)

day

night

Nov 2001NORPAC


0 0.02 0.04 0.06

0-20

20-50

50-100

100-150

density (ind.m-3)

day

night

Nov 2001NORPAC


0.00 0.01 0.02

0-20

20-50

50-100

100-150

density (ind.m-3)

day

night

Nov 2001NORPAC

Lazarev Sea

140oE NORPAC net transect south of AustraliaDep

th (

m)

Fig. 6. Vertical distribution of pteropod densities (individuals m�3) in the Lazarev Sea in 1995 (RMT8 – macrozooplankton; Bongo – mesozooplankton) and along a 140�Etransect south of Australia in 2001 (NORPAC sample – mesozooplankton). White bars indicate day-time densities and dark bars indicate night-time densities.


gymnosome S. australis were from the East Antarctic NORPAC sam-ples, and showed that this species occurred in the surface 20–150m of the water column during day and night (Fig. 6).

Both of the Southern Ocean gymnosomes have been demon-strated to produce fish anti-feedant chemicals. In the case ofC. limacina antarctica the chemical is a pteroenone linear b-hydrox-yketone (C14H2402) (Bryan et al., 1995), while in S. australis it

appears to be a polyunsaturated fatty acid (14:3) (Phlegeret al., 1999). The effectiveness of these anti-feedants is apparentin the hyperiid amphipod Hyperia dilatata abducting these gym-nosome species as a defence against fish predation (McClintockand Janssen, 1990; Phleger et al., 1999). The captured gymno-some is secured dorsally against the abdominal segments usingthe sixth and seventh pereiopods. At McMurdo Sound up to

0.0000

0.0050

0.0100

0.0150

0.0200

0.0250

0.0300

0.0350

0.0400

00:49

03:42

05:44

08:12

12:15

15:54

18:42

21:51

00:33

Cps

Cla

Lha

28-29/12/1994Bongo net

0.0000

0.0050

0.0100

0.0150

0.0200

0.0250

0.0300

0.0350

0.0400

0.0450

11:21

15:55

19:01

22:01

00:31

03:47

06:56

Cps

Cla

Lha

5-6/1/1995Bongo net

0.0000

0.0002

0.0004

0.0006

0.0008

0.0010

0.0012

0.0014

16:04

19:28

00:09

04:14

07:50

11:50

16:10

20:06

Time

Cps

Cla

Lha

29-30/12/1995Bongo net

Den

sity

(in

d.m

-3)

Fig. 7. Temporal variation in pteropod densities (individuals m�3) at three 24 hstations in the Lazarev Sea (1994/1995), collected as 300 m depth oblique Bongo nettows sampling the mesozooplankton size fraction. Dark horizontal bars indicateperiods of darkness. Cps – Clio pyramidata antarctica; Cla – Clione limacinaantarctica; Lha – Limacina helicina antarctica.


74% of H. dilatata have been observed to carry C. limacina antarc-tica (McClintock and Janssen, 1990). It is possible that due to areduction in predation pressure imparted by these anti-feedantstheir vertical distribution may be more strongly determined bytheir prey distribution rather than predator avoidance behavior.Both are specialist predators on thecosome pteropods, C. limacinaantarctica feeding on Limacina species and S. australis feeding onC. pyramidata (see Section 3.2). There is some evidence for thevertical distribution of C. limacina antarctica tracking that ofL. helicina antarctica in the East Antarctic samples (on 21/2/89,and 23/2/89), and in the Lazarev Sea macrozooplankton samples(Figs. 5 and 6).

3.2.4. Seasonal variation in abundanceSeasonal cycles of abundance (individuals m�3) were illustrated

for regions with good monthly coverage, produced by merging datacollected over a number of years. Seasonal data were constrainedto depths 6500 m and the macro- and mesozooplankton size frac-

tions were considered separately. The Antarctic Peninsula meso-zooplankton samples were collected with an RMT1 (330 lmmesh), deployed as part of an RMT8+1 dual net system. Conse-quently, the Antarctic Peninsula macro- and mesozooplanktonsamples for the months October, November, and January–Marchwere collected congruently (Figs. 10 and 11). As the RMT8 didnot sample small size fractions due to its large 4.5 mm mesh size,the combination of RMT8 and RMT1 samples gave insight into theseasonal changes in the population structure of pteropod species.Stratified net tows, sampling the upper 300–1000 m of the watercolumn, were collected seasonally in the Antarctic Peninsula re-gion during Voyages #1, 3, 5 and 8 (Table 1), covering November,January, February, April, May and June (Fig. 9). Although the latterdata had good seasonal coverage, they comprised a small numberof samples and had no day/night differentiation, and consequently,provide only qualitative insight into seasonal changes in pteropodvertical distribution. The CPR survey provided the only coverage ofall 12 months of the year although, as L. helicina antarctica andL. retroversa australis could not be separated in these samples, onlyfor Limacina spp. (Fig. 12).

Macro-size fraction L. helicina antarctica were present in Antarc-tic Peninsula samples from October to January but were virtuallyabsent from the top 500 m between February and June (Fig. 10).However, L. helicina antarctica densities were relatively high inthe mesozooplankton samples in January and February indicatinga shift to a juvenile dominated population (Fig. 11). In the East Ant-arctic macrozooplankton samples L. helicina antarctica had highestdensities in December (0.14 ind m�3), and declined consistentlythrough to April when they were almost completely absent. AtSouth Georgia L. helicina antarctica occurred at highest densitiesin the mesozooplankton in December and January (>170 ind m�3),but were present in the upper 500 m until at least March (>32 in-d m�3), the latest that samples were collected.

Like, L. helicina antarctica, L. retroversa australis only occurred inthe January and February mesozooplankton samples from the Ant-arctic Peninsula, while in the South Georgia region it was only re-corded in January (Fig. 11). As both of these regions are at thesouthern extreme of L. retroversa australis range they are likelynot representative of the species, and high densities were observedin the vicinity of the sub-Antarctic Prince Edward Islands in April/May (60 ind m�3) (Table 3a). The CPR samples showed that, withinthe mesozooplankton size fraction, the combined Limacina spp.had a strong seasonal cycle, appearing in the surface waters inNovember, reaching maximum densities in February and decliningthrough to May. From May to October, however, Limacina spp.were almost completely absent from the CPR samples. As theCPR sampled only the surface �10 m it is not possible to saywhether the seasonal cycle observed in these data were due toan autumn decline in densities or a seasonal migration to deeperin the water column. No mesozooplankton data sampling belowthe upper 10 m of the water column were collected later thanthe April Prince Edward Island samples where densities of L. retro-versa australis remained high, indicating that at least in autumnLimacina species may have occurred deeper in the water column.Limacina helicina antarctica were present in the 500–345 m layerin a single macrozooplankton sample from the Antarctic Peninsula,however, these data are two few to provide conclusive evidence forseasonal vertical migration.

Clio pyramidata had the same seasonal distribution pattern inboth the RMT8 and RMT1 samples from the Antarctic Peninsula,being abundant only in October and November (>0.002 ind m�3),when it occurred throughout the water column (surface to1000 m), but being absent from March (Figs. 9–11). At South Geor-gia C. pyramidata occurred at highest densities in December andJanuary (>0.002 ind m�3) but was completely absent from theupper 500 m of the water column in February and March. The

0 0.0002 0.0004

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density (ind.m-3)

Clio piatkowskii

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30-0

90-30

200-90

500-200

1000-500

density (ind.m-3)

Limacina helecina antarctica

Lazarev Sea - Mesopelagic (January 1995)

Fig. 8. Vertical distribution of pteropod densities (individuals m�3) in macrozooplankton samples collected from the upper 1000 m of the water column in the Lazarev Sea,January 1995. Error bars are standard deviations. Sample numbers (n): Day: 0–30 m, n = 2; 30–90 m, n = 2; 90–200 m n = 3; 200–500 m, n = 2; 500–1000 m, n = 3. Night:0–30 m, n = 4; 30–90 m, n = 4; 90–200 m n = 3; 200–500 m, n = 2; 500–1000 m, n = 5. White bars indicate day-time densities and dark bars indicate night-time densities.


absence of C. pyramidata from both Antarctic Peninsula and SouthGeorgia samples in late summer and autumn is noteworthy. Thismay have been partly due to seasonal migration to deeper layers,however, C. pyramidata has also been found in surface layers, andfeeding, in winter (Perissinotto, 1992; Figs. 16 and 17). In the EastAntarctic average C. pyramidata sulcata densities were relativelyconsistent between December and March, with highest sampledensities occurring in February and March (P0.01 ind m�3).

The Gymnosome C. limacina antarctica occurred at highest den-sities in the Antarctic Peninsula macrozooplankton samples inOctober and November, decreasing dramatically by December(Fig. 9). In the Antarctic Peninsula mesozooplankton samplesC. limacina antarctica occurred at >0.002 ind m�3 in spring (Octo-ber–November), and remained at relatively high densities in Janu-ary and February, reflecting an increased contribution of meso-sizefraction individuals to the population during these months(Fig. 11). Although C. limacina antarctica was present in the surface500 m until June, stratified net tows demonstrated that in the Ant-arctic Peninsula samples this species was found predominantly be-low 250 m after February (Fig. 9). In the East Antarcticmacrozooplankton samples C. limacina antarctica had a decliningtrend in average density from December to April which mirroredthe seasonal decline of its prey L. limacina antarctica (Fig. 10), whileat South Georgia C. limacina antarctica only occurred in the meso-zooplankton samples in January (Fig. 11).

Similar to C. limacina antarctica, S. australis was most abundantin the Antarctic Peninsula macrozooplankton samples in Octoberand November, but high standard deviations from December toFebruary indicated that this species remained relatively abundantduring these months (Fig. 10). The increasing densities of S. austral-is observed in the mesozooplankton samples in February (Fig. 11)were therefore not necessarily due to a population dominated by

juveniles. Stratified net tows showed that this species frequentlyoccurred below 500 m (Fig. 9), however, it was present above500 m until at least June (Fig. 10). At South Georgia S. australis onlyoccurred in the mesozooplankton samples in January, however,while in the East Antarctic macrozooplankton samples S. australiswas relatively abundant in all months sampled.

3.2.5. Inter-annual variation in abundanceUnbroken inter-annual time series were available for East Ant-

arctica (1985–1990), the Prince Edward Islands (1996–2005) andthe CPR Survey (1997–2005) (Figs. 13 and 14). As with seasonality,inter-annual data were expressed as individuals m�3, constrainedto depths 6500 m, and divided into meso- and macrozooplanktonsize fractions. In addition, the influence of seasonal variability wasreduced by limiting the East Antarctic samples to those collectedfrom December to March and the CPR samples to those collectedbetween November and April. The Prince Edward Island sampleswere all collected in April and May.

In the East Antarctic L. helicina antarctica, C. pyramidata sulcataand S. australis were present in all years (Fig. 13). Limacina helicinaantarctica and S. australis were scarce in 1989, C. pyramidata sulcatawas almost completely absent from 1988 to 1990, while C. limacinaantarctica was completely absent in 1989. At the Prince Edward Is-lands all species recorded were almost completely absent in 1997(Fig. 13). Limacina retroversa australis occurred at low densitiesfrom 1996 to 1999, but was very abundant in 2000 (�148 in-d m�3), and remained relatively abundant until 2004 before againbeing depleted in 2005. The CPR Survey provided inter-annual datafrom 1997 to 2005 (Fig. 14). In 1997, 1999 and 2005 Limacina spp.occurred at low abundance, but in the remaining years their den-sity was relatively consistent and standard deviations and maxi-mum values indicated that they occurred in high density patches.


Inter-annual variation in primary production has been proposedas a major determinant of inter-annual variation in thecosomepteropod population densities (Seibel and Dierssen, 2003). Unfor-tunately data on chlorophyll a biomass are not available for theEast Antarctic and CPR data sets. In the former, a late retreat ofwinter sea-ice in 1989 may have resulted in lower chlorophyll abiomass, particularly in early summer (December/January), andthis may have been a contributing factor to the low pteropod den-sities observed in this year (Hunt et al., 2007). At the Prince EdwardIslands April/May (Autumn) chlorophyll a biomass was within the

Fig. 9. Vertical distribution of pteropods (individuals m�3) collected from the upper 10001). November samples included collections with both RMT1 (grey bars) and RMT8 (blac

normal range for this region in 1997 (�0.5 mg m�3) while in 2005levels were low (60.14 mg m�3) (Hunt et al., 2001; Bernard, 2006).Although these autumn data may not be representative of summerchlorophyll a biomass levels, the 2005 data do lend support to therole of primary production in determining pteropod densities.However, the almost complete absence of pteropods from thePrince Edward Islands in 1997, despite average chlorophyll a bio-mass levels and typical oceanographic conditions, suggested thatfactors other than primary production may also play a role indetermining the occurrence of pteropods in this region.

m in the Antarctic Peninsula region between November and June, 1982–1994 (Tablek bars).


0 0.0001 0.0002

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Fig. 9 (continued)


3.3. Feeding biology and grazing impact

3.3.1. Thecosome feeding biologyEarly laboratory studies of L. retroversa led to the conclusion

that food was derived from water drawn by ciliary action throughthe mantle cavity where particles were trapped on mucous se-creted by the pallial gland (Morton, 1954). It was only when thefirst in situ observations were made, using SCUBA, that it becameapparent that all thecosomes capture food using a spherical mu-cous web several times the size of their body (Gilmer, 1972; Gilmerand Harbison, 1986). The diameter and mesh size of mucous websproduced by Southern Ocean species is unknown, however, theweb sizes of northern hemisphere specimens (North Atlantic) were40–55 mm (max volume 80 ml) for 11 mm shell diameter L. helici-na, 20 mm (max volume 10 ml) for a 6 mm shell length L. retrover-sa, and 30–40 mm (max volume 50 ml) for a 10 mm shell length C.pyramidata (Gilmer and Harbison, 1986). The mucous web, mostlikely produced by the pallial gland, is suspended above the animalduring feeding, when swimming stops, and imparts neutral buoy-ancy to the normally negatively buoyant L. helicina, L. retroversaand C. pyramidata. Field observations of Limacina spp. show thatthe mucous web can be deployed in �5 s and retracted in <20 s(Gilmer and Harbison, 1986), however, web production rates areunknown (Lalli and Gilmer, 1989). As far as we are aware naturalfeeding behavior, with a mucous web, has not yet been observedunder controlled laboratory conditions for any species of theco-some, even using containers of up to 2000 l capacity (Gilmer andHarbison, 1986; Lalli and Gilmer, 1989). This has important impli-cations for determination of thecosome grazing rates, as discussedin Section 3.3.3.

Thecosome pteropods are described as passive feeders that donot produce a feeding current (Gilmer, 1990), and food capture oc-curs through a combination of trapping motile organisms (Gilmerand Harbison, 1991) and collection of sinking particles, the latterdescribed as ‘‘flux feeding” (Jackson et al., 1993). Gut content anal-ysis of L. helicina shows that both trapping and flux feeding occur.However, comparison of water column and gut prey proportionsindicates that motile unicellular and multicellular organisms arecaptured at above their concentrations in the water column (Gil-mer and Harbison, 1991). In a number of thecosome pteropods(e.g. Creseis virgula) sorting of particles appears to take place beforeingestion, with rejected particles being expelled in mucous strings

(pseudo-faeces) (Gilmer and Harbison, 1986). Although pseudo-faeces production has not yet been observed in Clio or Limacinaspecies (Lalli and Gilmer, 1989), they may be important contribu-tors to Southern Ocean vertical flux (see Section 3.5).

Only four studies have investigated the gut contents of SouthernOcean thecosome pteropods and these are summarised in Table 4.Diatoms dominated the gut contents of L. helicina from the RossSea and South Georgia (Hopkins, 1987; Hart in Morton, 1954). Dia-toms were an important dietary component for C. pyramidata sulcatain the Weddell Sea, but larger motile organisms, including copepods,made a substantial contribution (Hopkins and Torres, 1989). Aspteropods readily shed their mucous webs when disturbed it is un-likely that this reflected cod end feeding (Gilmer and Harbison,1986). No gut content data are available for L. retroversa australis inthe Southern Ocean. However, gut content data summarized fromthe North Pacific and North Atlantic showed a dominance of diatoms,dinoflagellates and microzooplankton in the diet of L. retroversa,L. helicina and C. pyramidata (Lalli and Gilmer, 1989). Later work onL. helicina collected in the Arctic found that diatoms and dinoflagel-lates dominated gut contents by frequency of occurrence andtogether contributed 35% to total gut carbon, but that zooplankton(predominantly copepod nauplii and juvenile L. helicina) accountedfor on average 46% of total prey volume and 40% of carbon (Gilmerand Harbison, 1991). It should be noted that these were large speci-mens of L. helicina (5–13 mm). In addition, this study did not attemptto enumerate particles <10 lm, but these were considered to con-tribute little to total volume.

Two additional sources of dietary information are lipid and sta-ble isotope analyses. The fatty acid content of L. helicina antarcticaspecimens from the Weddell Sea (1–6 mm specimens) andAntarctic Peninsula (size not given), and for C. pyramidata fromthe Antarctic Peninsula (size not given), indicated that the diet ofboth species is phytoplankton dominated (Phleger et al., 1997,2001; Kattner et al., 1998). However, the fatty acid 20:1(n�9), con-sidered to be a crustacean marker, was present in all three species,pointing to some carnivory. Lipid analyses of L. helicina (size not gi-ven) in the Arctic (Kongsfjorden, Spitsbergen) yielded similar re-sults (Falk-Petersen et al., 2001; Gannefors et al., 2005). The lowlevels of 20:1(n�9) markers suggested that crustaceans made upa substantially smaller component of the diet than observed inthe gut content analyses of Gilmer and Harbison (1991). It is pos-sible that this discrepancy may be due to preferential catabolism of

Clio pyramidata

0.0000.0020.0040.0060.0080.0100.0120.0140.0160.0180.020

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0.0000.0020.0040.0060.0080.0100.0120.0140.0160.018

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Macrozooplankton samples

Antarctic Peninsula

East Antarctic

Fig. 10. Average monthly densities (individuals m�3) of pteropods collected in macrozooplankton samples from 6500 m in the Antarctic Peninsula and East Antarctic sectorsof the Southern Ocean. The number of samples for each month is indicated in parenthesis on the x-axis. Error bars are standard deviations.


these long chain monosaturates (Gannefors et al., 2005). Possibly amore important factor is size related differences in the ability ofpteropods to handle larger prey, with the incidence of crustaceanprey increasing with the size of L. helicina and C. pyramidata. Datafrom the Arctic for veligers of L. helicina indicated that particulateorganic matter was an important dietary component at this stageof the life cycle (Gannefors et al., 2005).

Stable isotope data for two species of Southern Ocean theco-some pteropod are available from the Lazarev Sea and the PrinceEdward Islands. The methods and basic principles of this techniqueare described in the methods. The d13C of particulate organic mat-ter (POM) from the Lazarev Sea had a wide range of values, indicat-ing contributions from different phytoplankton size classes as wellas sea ice algae, although possibly influenced by lipids not being

Fig. 11. Average monthly densities (individuals m�3) of pteropods collected in mesozooplankton samples from 6500 m in the Antarctic Peninsula and South Georgia regionsof the Southern Ocean. The number of samples for each month is indicated in parenthesis on the x-axis. Error bars are standard deviations.

0

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Limacina spp.

Fig. 12. Average monthly densities (individuals m�3) of Limacina spp. in Continuous Plankton Recorder samples collected south of Australia from 1997 to 2006. The numberof samples for each month is indicated in parenthesis on the x-axis. Error bars are standard deviations. Maximum densities for each month are indicated by �.


removed from these samples (Fig. 15a; Kaehler et al., 2000;Schmidt et al., 2003). The d13C of C. pyramidata sulcata was inter-mediate within the range of POM. Its average d15N of 1.54‰ wasone trophic level up from POM (d15N of ��2‰) and slightly lowerthan that of <1 mm copepods (d15N 2.76‰), which we assumed tobe predominantly herbivorous based on the gut contents of a rangeof species within this category (Hopkins and Torres, 1989). The sta-ble isotope data therefore indicated that C. pyramidata sulcata hada predominantly herbivorous diet. Limacina retroversa australis atthe Prince Edward Islands shared the lowest d15N values, andhence trophic level, with unidentified copepods. These two groupswere at least one trophic level below large calanoid copepods andthe omnivorous Euphausia vallentini (Fig. 15b). As stable isotopedata represent an integration of diet over the time scale of tissueturnover rates, herbivory would appear to be the dominant feedingmode for both C. pyramidata sulcata and L. retroversa australis, sup-porting the fatty acid data. It should be noted that L. retroversa aus-tralis is the smallest Limacina species (62.5 mm length) and thatthe C. pyramidata sulcata in the isotope analysis (16.83 mm length)were on the small side of the size range shown by Hopkins and Tor-

res (1989) to be feeding on copepods. As indicated above, largerspecimens may have a more omnivorous diet.

3.3.2. Gymnosome feeding biologyGut content data from the Ross Sea indicates that the C. limacina

antarctica is a monophagous predator on L. helicina antarctica in theSouthern Ocean (Table 4). This was reflected by the similar fattyacid profiles and sterol composition of these two species (Phlegeret al., 1997), while the d15N isotope data from the Lazarev Sea indi-cated that C. limacina antarctica was approximately one trophiclevel above primary consumers (Fig. 15a). In the northernhemisphere C. limacina feeds on L. helicina in polar waters andL. retroversa in sub-polar/temperate waters (Lalli and Gilmer,1989), and it is probable that C. limacina antarctica also feeds on L.retroversa australis in the SAZ and PFZ waters of the Southern Ocean.For the northern hemisphere C. limacina it has been demonstratedthat only the veliger stage does not feed on Limacina, consumingphytoplankton during this life stage (Conover and Lalli, 1972).However, 48–72 h after metamorphosis from the veliger stage topolytrochous larvae (at �0.3 mm length) C. limacina began feeding


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Macrozooplankton

Fig. 13. Average yearly densities (individuals m�3) of pteropods in Prince Edward Island mesozooplankton samples (collected in April/May), and East Antarcticmacrozooplankton samples (collected between December and March). The number of samples for each year are indicated in parenthesis on the x-axis. Error bars are standarddeviations.


on Limacina veligers. At sizes >0.6 mm they began to consumemetamorphosed Limacina prey and they did so exclusively oncethey exceed 1.75–2 mm in length (Conover and Lalli, 1972). Clionecaptures its Limacina prey with its six buccal cones, and the probos-

cis is used to draw the body out of the shell. A detailed descriptionof the feeding activity is provided by Lalli and Gilmer (1989).

The feeding specialization of Clione is reflected by numerousadaptations. As even the early polytrochous larvae of Clione feed

Table 4Gut contents for pteropod species from the Southern Ocean and the northern hemisphere temperate and polar oceans

Size (mm) Region Food item %N %V Reference

Southern OceanLimacina helicina antarctica 2.2–3.2* Ross Sea (McMurdo Sound) Diatoms 87.0 1

Ross Sea (McMurdo Sound) Dinoflagellates 13.0 1Limacina helicina antarctica South Georgia Diatoms 2Limacina retroversa australis No Southern Ocean DataClio pyramidata f. sulcata 16–23 Weddell Sea MIZ Diatoms 32.6 3

Sillicoflagellates 3.3 3Dinoflagellates 8.7 3Tintinnids 28.3 3Foramininferans 2.2 3Copepods 22.8 3Polychaetes 2.2 3

Clio pyramidata f. sulcata ? Antarctic Diatoms 4Clione limacina antarctica 9–16 Ross Sea Limacina helicina 100 1

Northern hemisphereLimacina helicina ? Subarctic, North Pacific Diatoms 5

Dinoflagellates 5Tintinnids 5

Limacina helicina 5–13+ North Atlantic, Arctic 10–20 lm cells 52.5 2.1 6Dinoflagellates 31.5 9.6 6Diatoms 12.0 15.9 6Tintinnids 3.8 16.8 6Limacina spp. 0.6 24.3 6copepods 0.4 23.1 6

Limacina retroversa Subarctic Diatoms 5Dinoflagellates 5Coccolithophorid 5Tintinnids 5

Limacina retroversa Bay of Fundy, Canada Dinoflagellates 7

%N – percentage of prey items by number; %V – percentage of prey items by volume. MIZ – marginal ice zone.References: 1. Hopkins (1987); 2. Hart (in Morton, 1954); 3. Hopkins and Torres (1989); 4. Richter (1977, in Lalli and Gilmer, 1989); 5. Boas (1886, in Lalli and Gilmer, 1989); 6.Gilmer and Harbison (1991); 7. White (1977).* – how size measured not indicated; + – size is shell diameter; ? – size not given.

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CPR survey - Limacina spp.

Fig. 14. Inter-annual variation in densities (individuals m�3) of Limacina spp. in Continuous Plankton Recorder samples collected south of Australia, calculated as averages forthe months November to April (1997–2006). The number of samples for each year is indicated in parenthesis on the x-axis. Error bars are standard deviations. Maximumdensities for each year are indicated by �.


on Limacina, their life cycles are necessarily closely synchronized(Lalli and Gilmer, 1989). Physiologically, the metabolic activity ofC. limacina antarctica is strongly correlated with L. helicina antarc-tica, pointing to the coevolution of these species in the SouthernOcean (Seibel et al., 2007). Clione has very high assimilation effi-ciencies, being able to assimilate carbon from its prey at >90% effi-ciency and nitrogen at nearly 100% efficiency (Conover and Lalli,1974).

No gut content data are available for S. australis, however,observations indicate that it is a specialist predator on C. pyramidata(Lalli and Gilmer, 1989). This trophic relationship was indicated

by stable isotope data from the Lazarev Sea with S. australisd15N being approximately one trophic level above C. pyramidatasulcata (Fig. 15a), and approximately one trophic level aboveprimary consumers at the Prince Edward islands (Fig. 15b).Notably, the d15N of S. australis was approximately 2‰ higherthan C. limacina antarctica at the Prince Edward Islands, indicat-ing that the formers prey may have had a more omnivorousdiet. Prey capture is probably similar to that described forC. limacina antarctica, but in S. australis is by means of two lat-eral arms, each with 7 to >20 suckers, as opposed to buccalcones.

Prince Edward Islands (April 1999)

-4

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8

-28 -26 -24 -22 -2013C(‰)

15N

(δ

δ

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unidentified copepods

Euphausia longirostris

Euphausia vallentini

Limacina retroversa

Sagitta gazellae

Spongiobranchaea australis(ave length = 11.12mm)

large calanoid copepod

Lazarev Sea (April 2004)

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Clio pyramidata sulcata(ave length = 16.83mm)

Clione limacina antarctica(ave length = 9.3mm)

copepods (< 1mm)

POM

Spongiobranchaea australis(ave length 12.67mm)

Thysanoessa macrura

a

b

Fig. 15. d13C (x-axis) and d15N (y-axis) stable isotope measurements for pteropodsin the (a) Lazarev Sea (April 2004) and (b) Prince Edward Islands (April 1999).


3.3.3. Grazing impactTo date there are seven published studies of thecosome ptero-

pod grazing impact in the Southern Ocean, and the results of sixthese are presented in Table 5. Bernard and Froneman (2005) over-estimated ingestion rates for L. retroversa australis due to overesti-mated gut pigment destruction rates, and the corrected valuespresented here come from Bernard (2006). The studies of Perissin-otto (1992) and Pakhomov and Perissinotto (1997) list the ptero-pod species examined as Limacina sp. As these studies werelocated at the sub-Antarctic Prince Edward Islands and the Sub-Tropical Convergence, respectively Limacina sp. was most likelyL. retroversa australis, although it is possible that the STC specimenswere a mixture of L. retroversa australis and L. inflata. Diel variabil-ity in thecosome gut pigment content were extracted from com-munity measurements in previously published manuscripts(Fig. 16a–d) or are new data (Fig. 16e and f). All gut pigment datapresented in Fig. 17 are previously unpublished with the exceptionof Fig. 17e. The method used for generating new gut pigment dataare presented in Section 2.

Perissinotto (1992) found strong diel variation in the feedingbehavior of Limacina sp. (retroversa) at the Prince Edward Islands,with highest gut pigment levels always being found at night, whileBernard and Froneman (2005) found no significant diel variabilityin gut pigment levels for L. retroversa in the same region. Diel var-iability was not published for the STC region study by Pakhomovand Perissinotto (1997) but is now presented in Fig. 16, and no sig-nificant diel pattern in gut pigment levels was observed. A diel pat-tern in gut fluorescence was apparent for L. helicina antarctica fromthe Lazarev Sea in December/January of 1994/1995 (Fig. 16, Pakho-mov et al., 2002b). Few day time gut pigment values were collectedin December/January of 1997/1998, however, there were indica-tions of no diel variability (Fig. 16). Clio pyramidata sulcata showeda pronounced diel variability in December/January of 1997/1998,no evidence of diel variability in April 2004, and low diel variability

in June/August 2006 (Fig. 16). Based on the high variability in dielvertical migration in the two Limacina species, and a more markeddiel vertical migration of C. pyramidata sulcata, it would be ex-pected that the latter species would show the more pronounceddiel variation in gut pigment content.

Gut evacuation rates (K) for L. helicina antarctica and L. retrover-sa australis ranged from 0.25 to 1.33 with a mean of 0.65 (Table 5).Gut pigment destruction rates (b0) were only determined experi-mentally in one study, for L. retroversa australis (Bernard, 2006),obtaining a value of 58%, similar to the default b0 of 50–60% usedby the other studies. In two instances the K values for pteropodswere the lowest for the species measured (Pakhomov and Perissin-otto, 1997; Pakhomov and Froneman, 2004). No K or b0 values haveyet been established for C. pyramidata sulcata, and the values usedfor this species were those of L. helicina antarctica. Since thecosomepteropods have not been induced into natural feeding behavior,with mucous web production, in the laboratory (Lalli and Gilmer,1989), it is likely that K was underestimated and b0 overestimatedfor all three species.

Ingestion rates for L. retroversa australis ranged from 31.2 to4196.9 ng(pig) ind�1 d�1. As highlighted above, the ingestion rates>7000 ng(pig) ind�1 d�1 reported by Bernard and Froneman (2005)for April 2004 were overestimates, and the values of�4000 ng(pig) ind�1 d�1 in Table 5 are the corrected ones (Bernard,2006). The ingestion rates reported for Limacina sp. (retroversa)were in the upper range for the mesozooplankton measured byPerissinotto (1992) and Pakhomov and Perissinotto (1997), andsecond only to E. vallentini adults in the former study. Assumingthat all Limacina sp. (retroversa) were L. retroversa australis, thisspecies contributed an average of 25% (range of 4–60%) to the totalgrazing impact of the species measured (comprising 25–90% of thetotal mesozooplankton density), and consumed up to 19% of dailyprimary production. This contribution was high relative to theiraverage 6.5% contribution to total density of measured grazers.Pakhomov et al. (1997) calculated the grazing impact of Limacinaspp. (apparently with a high contribution of L. inflata) at SouthGeorgia in summer using the average ingestion rates of Perissinot-to (1992). Accordingly, Limacina spp. contributed an average of 22%to measured community grazing impact, but up to 67% (Table 5,Pakhomov et al., 1997). This represented up to 5.5% of total chloro-phyll a standing stock and 43% of daily primary production.

Data for L. helicina antarctica are from the Lazarev Sea in earlysummer of 1994/1995 and 1997/1998 (Table 5). The ingestionrates of L. helicina Antarctica (�2000–6000 ng(pig) ind�1 d�1) in1994/1995 were equivalent to those of S. thompsoni and higherthan any other taxon, while in 1997/1998 their ingestion rates(�2000 ng(pig) ind�1 d�1) were second only to C. pyramidata sul-cata and S. thompsoni (Pakhomov et al., 2002b; Pakhomov andFroneman, 2004). Due to their low densities (<0.05 ind m�3) atthe stations where grazing experiments were conducted in both1994/1995 and 1997/1998 (comprising <0.3% of total zooplankton)the contribution of L. helicina antarctica to community grazing im-pact was low (<3%). However, outside of the 24 h stations in 1997/1998 L. helicina antarctica abundance was up to two orders of mag-nitude higher. In view of their high ingestion rates, their grazingimpact at these stations would have been substantial. Ingestionrates for C. pyramidata were determined from the Lazarev Sea inearly summer 1997/1998 (Table 5). Values were extremely high(16,627 and 27,757 ng(pig) ind�1 d�1), and comparable to thoseof 3–5 cm S. thompsoni (Pakhomov and Froneman, 2004). Clio pyra-midata sulcata contributed up to 41% to the community grazing im-pact in that study.

One of the aims of this review was to establish a usable relation-ship between gut pigment content and pteropod size. These datawere only available from the Lazarev Sea for C. pyramidata sulcataand L. helicina antarctica (Fig. 17). A linear function provided the

Table 5Published data on thecosome pteropod grazing impact

Species Region Month Year Size(mm)

Average dry mass(mg ind�1)

K(h�1)

b0 IR Reference % of measured grazerdensity

% of measuredcommunity grazing

Limacina sp.(retroversa)

PEI April–May 1985 and1989

0.2084 0.98 60% (assumed) 76.12 1 14.1 27.38



0.2084 0.98 60% (assumed) 301.87 1 7.9 26.15



0.2084 0.98 60% (assumed) 31.22 1 13.4 14.17



0.2084 0.98 60% (assumed) 134.01 1 6.1 23.37


STC June–July 1993 0.355 50% assumed 540.5 2 2 15


STC June–July 1993 0.355 50% assumed 701.6 2 0.4 21


STC June–July 1993 0.355 50% assumed 170 2 0.2 4

Limacinaretroversa

PFZ April 2002 1.33 58% 4146.51 3 8.37 52.36

Limacinaretroversa

PFZ April 2004 1.33 58%(experimental)

4128.68 3 11.81 59.48

Limacinaretroversa

PFZ April 2005 1.33 58% 4196.88 3 0.85 7.48

Limacina spp. SG February–March

1994 161c 6 15 21.74

Limacina helicina LS December–January

1994/1995

1–6b 0.327 50% assumed 2204 4 <0.01 0.40


1994/1995

1–6b 0.327 50% assumed 2429 4 <0.01 0.60


1994/1995

1–6b 0.327 50% assumed 5980 4 <0.01 2.60


1997/1998

2–5b 2.2 0.25 50% assumed 2103 5 <0.3 3

Clio pyramidatasulcata

LS December–January

1997/1998

10–20a 0.25b 50% assumed 27,757 5 <0.3 41.12


LS December–January

1997/1998

10–20a 0.25b 50% assumed 16,627 5 <0.1 5

K (h�1) – gut evacuation rate; b0 – gut pigment destruction; IR – ingestion rate (ng(pig) ind�1 d�1); PEI – Prince Edward Islands; STC – Sub-Tropical Convergence; PFZ – PolarFrontal Zone; SG – South Georgia; LS – Lazarev Sea. overleaf . . ..References: 1. Perissinotto (1992); 2. Pakhomov and Perissinotto (1997); 3. Bernard (2006); 4. Pakhomov et al. (2002b); 5. Pakhomov and Froneman (2004); 6. Pakhomovet al. (1997).

a Ingestion Rate was taken as the average from Perissinotto (1992).b K (h�1) for C. pyramidata sulcata applied from that established for Limacina helicina antarctica by Pakhomov and Froneman (2004).c IR calculated as average from Perissitnotto (1992).


best fit for L. helicina antarctica in December/January of 2006/2007and December/January of 1994/1995 (Fig. 17d and e) while apower function provided the best fit in all other plots.

3.4. Reproduction and life cycle

3.4.1. ThecosomesThe reproductive biology of thecosome and gymnosome ptero-

pods has been relatively well studied, and the reader is referred tothe detailed descriptions in the review by Lalli and Gilmer (1989).All thecosome species examined are protandrous hermaphrodites,maturing and functioning first as males and then as females withdegeneration of male reproductive organs. With the exception ofL. inflata, all Limacina species produce free floating egg masses. Inthe Arctic L. helicina veligers hatched 2–6 days after spawning (Lalliand Wells, 1978; Gannefors et al., 2005) at a size of 0.1–0.2 mm(Conover and Lalli, 1972), and the time required for metamorpho-sis of veligers appears to be longer than 30 days (Paranjape, 1968).

Unlike the reproductive biology, few studies have investigatedpteropod life cycles and there appears to be only one detailedstudy of a Southern Ocean pteropod. Dadon and de Cidre (1992)investigated the life cycle of L. retroversa australis off the east coastof South America from autumn 1978 to summer 1978/1979, usinga combination of reproductive histology and shell height as a mea-sure of population structure. They concluded that L. retroversa aus-tralis survived for a maximum of one year, producing two

generations during this time, the first in spring and the second inlate summer. The late summer generation overwintered and ma-tured at �1.2 mm shell length, spawning the following spring ata minimum shell length of �1.99 mm. The disappearance of thelargest size fraction from the population after spring spawningindicated that the spawners probably died. The spring generationmatured at a smaller size, as small as 0.6 mm shell length, andwas responsible for the production of the second late summer gen-eration, spawning beginning at a minimum size of �1.25 mm. Asimilar two generation per year life cycle was been observed forthe northern hemisphere L. retroversa off the coast of Nova Scotia,however, in the English Channel spawning has been observedthrough most of the year (Lalli and Gilmer, 1989).

The combined meso- and macrozooplankton seasonal densitydata presented in Section 3.2.4 indicated that L. helicina antarcticaalso has a one year life cycle. In the Antarctic Peninsula region thelarge macrozooplankton specimens collected in early summer rep-resented overwintering adults and these appeared to die off by latesummer. The appearance of high densities of mesozooplanktonspecimens in summer indicated that this die off occurred postspawning. This interpretation is supported by Massy (1920, in Lalliand Gilmer, 1989) who reported that the largest L. helicina antarc-tica specimens (up to 6 mm diameter) were found from Decemberto February, and that spawning was observed in January. High den-sities of Limacina spp. in 76 lm mesh nets (21.96 ind m�3) inApril–May, and absence from 202 lm to 330 lm mesh nets

0

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) Limacina helicina antarcticaLazarev SeaDec/Jan 94/95

b

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Clio pyramidata sulcataLazarev SeaApr 2004

e

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Clio pyramidata sulcataLazarev Sea Jun-Aug 2006

f

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gu

t p

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(ng

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) Limacina (retroversa)STC, Jun/Jul 1993

a

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Clio pyramidata sulcataLazarev Seasummer 1998

d

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Limacina helicina antarcticaLazarev Seasummer 1998

c

Fig. 16. Diel variation in gut pigment content (ng individual�1) for thecosome pteropod species. Species, region and sample date are indicated in each figure panel. In (a) STCis the Sub-Tropical Convergence and Limacina (retroversa) is in parenthesis as the species may have been a mix of Limacina retroversa and Limacina inflata. Data for (a) and (b)were extracted from Pakhomov and Perissinotto (1997) and Pakhomov et al. (2002b), respectively, while data for (c) and (d) are replicated from Pakhomov and Froneman(2004). Data for (e) and (f) are previously unpublished and the methods used are described in Section 2.


(Hopkins, 1971), provided additional evidence of autumn spawn-ing of this genus in the Southern Ocean. However, as these samplescame from the Antarctic Convergence Zone, they may have beeneither L. retroversa australis or L. helicina antarctica. In the RossSea an autumn die off of adult L. helicina antarctica, mostly>1 mm diameter, has been observed from sediment traps (Collieret al., 2000; Accornero et al., 2003). Although no data are availableon whether this was associated with an autumn spawning event,these studies do indicate that high autumn mortality may havecontributed significantly to the seasonal decline in Limacina spp.densities observed in the CPR data set (Fig. 12).

A one year life cycle with autumn spawning has been suggestedfor northern hemisphere L. helicina in Kongsfjorden, Spitsbergen(�79�N) (Gannefors et al., 2005). However, data collected forL. helicina from drifting ice stations in the central Arctic Ocean founda 1.5–2 year life span and spring spawning (Kobayashi, 1974). Themaximum size attained by L. helicina in the Arctic Ocean popula-tion was �3.7 mm while at Kongsfjorden L. helicina reached sexualmaturity at 5 mm diameter and had a maximum diameter of

11 mm (Gannefors et al., 2005). Assuming that the one year life cy-cle proposed by Gannefors et al. (2005) was correct, L. helicina hada substantially higher growth rate at Kongsfjorden (up to 1 mm permonth) than the 0.18 mm per month reported by Kobayashi(1974). Probably the major contributing factor to this was differ-ences in food availability, with there being a short period of en-hanced primary production at the Arctic site (June–August).Primary production has significant spatial variability in the South-ern Ocean (Comiso et al., 1993). In view of the regional differencesin Northern Hemisphere L. helicina life cycles, there may be sub-stantial circum-Antarctic and regional variability in both the sizestructure and life cycle of thecosome pteropods in the SouthernOcean. An additional facet of Southern Ocean thecosome pteropodlife cycles that remains unknown is differences between the twoforms of both L. helicina antarctica and C. pyramidata. In regardsto the latter species, the reproductive anatomy and histology aresimilar to Limacina (Lalli and Gilmer, 1989), however, the repro-ductive cycle of this species is not yet understood (van der Spoelet al., 1999). No data are available on the life cycle of C. piatkowskii.


Lazarev SeaDec/Jan 06/07

n = 277

y = 328.96x - 560.91R2 = 0.3826

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y = 230.2x1.0271

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Clio pyramidata sulcatab

Lazarev SeaJun/Jul 2006

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y = 336.65x0.5561

R2 = 0.1342

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Clio pyramidata sulcatac.


n=9

y = 645.28x - 634.7R2 = 0.7514

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Limacina helicina antarcticaeLazarev SeaJun/Jul 2006

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y = 4.0481x3.6401

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Limacina helicina antarcticaf



n = 299

y = 113.25x1.1808

R2 = 0.1943

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length (mm)

a

Fig. 17. Relationship between gut pigment (ng individuals�1) content and individual size for pteropods collected in the Lazarev Sea. Month, year, sample number (n), andequation and R2 for the best fit trendline are indicated on each figure. Figures (a)–(c) are for Clio pyramidata sulcata and (d)–(f) for Limacina helicina antarctica. Note that thesize measurements are shell length and shell diameter for C. pyramidata sulcata and L. helicina antarctica, respectively. Data used for (e) were extracted from Pakhomov andPerissinotto (1997), while the data for the remaining figures are previously unpublished and the methods used are described in Section 2.


A key component of thecosome life cycles is their overwinteringbehavior. As highlighted above overwintering may occur as eitherthe spring or autumn generation. Winter densities were low forboth L. helicina antarctica and C. pyramidata. This may have beeninfluenced by an autumn population die off, winter migration outof the surface layer to >500 m depth, or a predominance of individ-uals too small to be sampled by the nets used in this study. Gutpigment data from the Lazarev Sea indicated that both L. helicinaantarctica and C. limacina antarctica were feeding during the wintermonths (June/July) (Fig. 17). However, data from the Ross Sea dem-onstrated a 30% and 50% reduction in metabolic activity of L. heli-cina antarctica and C. limacina antarctica, respectively, in responseto reduced food availability, indicating that this may be an impor-tant strategy for both of these species to survive reduced winterphytoplankton concentrations (Seibel and Dierssen, 2003). Consid-ering the negative buoyancy of thecosome pteropods, winter dor-

mancy is unlikely, and continued winter feeding with reducedmetabolic activity may therefore be the norm.

3.4.2. GymnosomesGymnosomes have a similar reproductive anatomy to theco-

some pteropods (Lalli and Gilmer, 1989). However, gymnosomesmay function as simultaneous hermaphrodites at maturity, malereproductive organs not degenerating in females as they do inthecosomes. Similar to L. helicina and L. retroversa, eggs are laidin a free floating gelatinous mass (Lalli and Gilmer, 1989). Eggshatch into a shelled veliger stage, which subsequently metamor-phoses into a shell-less polytrochous larva (after �2 weeks at16 �C) (Lalli and Conover, 1973). The polytrochous larvae areinitially wingless and movement is by three ciliary bands. Theygradually grow wings and lose the ciliary bands as they becomeadults.


Data from studies of northern hemisphere species shows that,like the two Limacina species, C. limacina varies considerably in sizeat completion of metamorphosis into the adult form, occurring at3 mm in the English Channel and >15 mm in more northern areas(Lalli and Gilmer, 1989). In the former region neotonous develop-ment has also been observed, with specimens maturing at 2 mmwhen ciliary bands typical of polytrochous larvae are still present.It has been shown that the size attained by C. limacina has a signif-icant positive correlation with the size of the Limacina prey avail-able, rather than the Limacina density (Conover and Lalli, 1972).In view of the variation in size attained by different Limacina spe-cies in the Southern Ocean, and the biogeographic separation ofthese species, there may be significant regional variation in the sizeattained by C. limacina antarctica. In particular, C. limacina antarc-tica specimens may be smaller in the sub-Antarctic where L. retro-versa predominates. Indeed, Table 3 indicates that this is the caseas C. limacina antarctica was not collected in macrozooplanktonsamples (4.5 mm mesh) from the Prince Edward Islands despiteoccurring in mesozooplankton samples (300 lm mesh) (Hunt,2000). No study has been conducted on the life cycle of C. limacinaantarctica. However, in view of their specialized predation on Lima-cina spp., their reproductive cycle is likely to closely follow that ofthese Southern Ocean thecosomes (Section 3.3.2). Based on a com-bination of seasonal population structure and lipid content, Böeret al. (2005) deduced that the northern hemisphere C. limacina,from the Arctic, has at least a two year life cycle. The main spawn-ing of C. limacina occurs in spring, but there is evidence for spawn-ing all through the year, including autumn and winter.

The perennial life cycle of C. limacina appears to be supportedby the biosynthesis of the diacylglycerol (DAGE), a lipid that hasonly been found in trace amounts (<2%) in other plankton (Phlegeret al., 1997). Phleger et al. (2001) found that DAGE comprised 46%of the total lipids (29–36 mg g�1 wet weight) in C. limacina antarc-tica. DAGE is equivalent to wax esters, comprising fatty acids andalcohols, and appears to play an important role as a long-term en-ergy reserve (Kattner et al., 1998), while also being used for matu-ration and reproduction during the summer months (Böer et al.,2005). DAGE also generates 23% more buoyancy than triacylglyce-rols (TAG) and may have a buoyancy function (Phleger et al., 1997).As an energy store it is indicative of an animal adapted to takingadvantage of a pulsed and patchy prey biomass and surviving longperiods of starvation (Falk-Petersen et al., 2001). In recent labora-tory studies of C. limacina collected near Svalbad, specimens sur-vived in aquaria for 356 days without food (Böer et al., 2006,2007). Starvation resulted in an average shrinkage in body sizefrom 22.4 mm to 12 mm, and involved gonad re-absorption, slowlipid consumption and reduced metabolic activity.

No data on reproduction and life cycle are available for S. aus-tralis. Unlike C. limacina antarctica, DAGE has only ever been re-corded at low levels, 0.9–1.7%, in S. australis and total lipids are<10% of that recorded in C. limacina antarctica, indicating that S.australis may employ different strategies for starvation survivale.g. reduced metabolic activity (Phleger et al., 1997).

3.5. Contribution to vertical flux

The thecosomes C. pyramidata sulcata, L. retroversa australis andL. helicina antarctica have been shown to have amongst the highestingestion rates of any Southern Ocean plankton, and their grazingimpact may be substantial (consuming up to >40% of daily primaryproduction). But how much of the carbon ingested by thecosomepteropods is transferred vertically? Currently, there are no dataon assimilation efficiencies, egestion rates, or faecal pellet produc-tion rates for Clio or Limacina species. A comparison of gut and fae-cel pellet contents for L. helicina specimens from the North Atlanticfound that diatoms contributed twice as much in volume to faecal

pellets compared to guts (Gilmer and Harbison, 1991). Conversely,dinoflagellates were two to three times more abundant than dia-toms in the gut but equal to diatoms in faecal pellets. In addition,�67% of diatom cells in faecal pellets fluoresced whereas less than50% of intact dinoflagellates fluoresced. This indicated that diatomswere less easily digested than dinoflagellates. In the SouthernOcean, where diatoms are seasonally dominant, thecosomes maytherefore package a significant fraction of daily primary productioninto faecal pellets.

Yoon et al. (2001) described the faecal pellets of Clio sp. fromthe northeastern tropical Atlantic (Yoon et al., 2001). Pellets wereconical with a mean length of 1.1 mm, a length to diameter ratioof 12:4, and were sticky (probably due to mucous). Sinking veloc-ities were 120.3–646.4 m d�1 and second only to salps in thatstudy. Pteropod faecal pellets may therefore contribute signifi-cantly to vertical flux in the Southern Ocean, and is possibly en-hanced in C. pyramidata by this species’ stronger diel migrationtaking pellets below the mixed layer. Accornero et al. (2003) attri-bute their ‘‘oval B” faecal pellets in the Ross Sea to L. helicina ant-arctica. ‘‘Oval B” pellets were major components of both surfaceand near bottom sediment traps during the period of highest pelletflux observed in April 1996, during an intense diatom bloom, con-tributing 95.5% to mass and 97.2% to organic carbon in traps. Basedon the numerical dominance of L. helicina antarctica in the zoo-plankton it was assumed that this species produced the ‘‘oval B”pellets. However, there is clearly a need for the identification anddescription of pteropod faecal pellets in order to quantitativelymeasure their contribution to vertical flux measured by sedimenttraps.

In addition to possibly high diatom egestion rates, pteropodsare also expected to capture particles that would otherwise be re-tained and recycled within surface waters. As discussed in the sec-tion on feeding, the mesh size of Southern Ocean thecosomes isunknown. Gilmer and Harbison (1991) found that 10–20 lm cellsdominated the gut contents of L. retroversa while particles<10 lm contributed little to gut volume. However, laboratory stud-ies show that the mucous produced by L. retroversa can scavenge asignificant proportion of <2 lm particles from the water column(Noji et al., 1997). It is believed that particle capture occurs byadhesion and is therefore independent of mesh pore size (Silverand Bruland, 1981; Noji et al., 1997). Given the passive drift feed-ing of thecosome pteropods, sinking particles such as fecal pelletswould be expected to collect in feeding webs (‘‘flux feeding”)(Jackson et al., 1993), and gut content analysis has shown this tobe the case (Gilmer and Harbison, 1991). Accretion of fine particlesand small faecal pellets into fast sinking faecal pellets would there-fore facilitate their more rapid removal from the surface layers tothe deep ocean.

Faecal pellets are not the only means by which thecosomes cancontribute to organic carbon flux. Although not yet observed in Clioor Limacina species, a number of pteropod species produce pseudo-faeces which aggregate into in mucous strings below the feedinganimal (Gilmer and Harbison, 1986). In experiments with L. retro-versa Noji et al. (1997) demonstrated that <2 lm particles becameaccreted into large mucous aggregates (>0.4 mm) which had aver-age sinking rates of �300 m d�1, but up to 1000 m d�1. Althoughthe mucous production in these experiments occurred underunnatural conditions, high in situ mucous production appears tooccur naturally under certain conditions. When disturbed by tur-bulence L. retroversa and L. helicina were observed to swim awayfrom their webs (Gilmer and Harbison, 1986), and so mucous pro-duction may be enhanced during periods of increased surface tur-bulence associated with wind events (Tsurumi et al., 2005).Mucous production also increases during spawning and is believedto have been the source of mucous aggregates in the southern Nor-wegian Sea in August 1988 observed simultaneously in surface


sediment traps deployed at 100 m (Bathmann et al., 1991a) andbox-core samples from sediments at 1200 m (Noji et al., 1997).Thecosome mucous production may therefore be a seasonallyand regionally important source of marine snow.

Our list of literature showing predation on pteropods in theSouthern Ocean is by no means comprehensive (Table 6). However,thecosome pteropods are shown to be important components of

Table 6Occurrences in the literature of pteropods as prey

Predator species Source Limacina spp. Limacina helicinaantarctica

PlanktonThemisto gaudichaudii 2Themisto gaudichaudii Pers. Obs. Up to 20–80% of food

bolusEuphausia superba 11 10%FOSalpa thompsoni 11 18–44%FOSalpa thompsoni 13 13%FO

BenthosNauticaris marionis 5

Pelagic fishElectrona antarctica 7Electron antarctica 9 1.4%PNElectrona paucirastra 9 20%PNElectron subaspera 9 41.7%PNMetelectron harwigi 9 25%PNProtomyctophum normani 9 0.5%PNDiaphus taaningi 9 2.6%PNDiaphus hudsoni 9 1.6%PNGymnoscopleus nicolsi 9 0.2%PNCeratoscopelus warmingi 9 3.3%PNSymbolophorus boops 9 1.3%PNBathylagus antarcticus 11Electrona antarctica 11Protomyctophum tenisoni 13 9%FO

Demersal fishNotothenia rossi 1Notothenia rossi 1Lepinotonothen squamifrons 1Lepinotonothen squamifrons 1

Trematomus scotti, juveniles 3 1.5%FO; 0.7%PTremanomus hansoni,juveniles

3 100%FO; 4%P

Lepidonotothen squamifrons 4Lepidonotothen larseni 6Gobionotothen marionensis 6Trematomus lepidorchinus 8Trematomus lepidorchinus 8Trematomus lepidorchinus 8Chaenodraco wilsoni 8Lepidonotothen kempi 8Lepidonotothen kempi 8Lepidonotothen kempi 8Pleuragramma antarcticum 8 0.7%FO; <0.1%PTrematomus hansoni 8Trematomus hansoni 8Trematomus hansoni 8Trematomu eulepidotus 8

Trematomu eulepidotus 8

Trematomu eulepidotus 8Pagothenia borchgrevinki 10 63%PNTrematomus bernacchii 10 20%PNTrematomus hansoni 10 90%PNTrematomus ctentronotus 10 70%PN

BirdsHalobaena caerulea 12

%FO – percentage frequency of occurrence; %P – percentage importance by mass; %PN –1. Chechun (1984); 2. Pakhomov and Perissinotto (1996); 3. Pakhomov et al. (1995); 4.(1979); 8. Pakhomov (1991); 9. Pakhomov et al. (1996); 10. Foster and Montgomery (19(1991).

the diet of zooplankton as well as pelagic and demersal fish, withone reported occurrence in the blue petrel Halobaena caerulea.Thecosome pteropods therefore provide an avenue for transfer ofprimary production to longer lived carbon sources. It should benoted that due to the production of fish anti-feedants by SouthernOcean gymnosome pteropods, they are likely to experience mini-mal fish predation (Section 3.2.3).

Limacina retroversaaustralis


Pteropods

6.3–100%FO; 5–100%P

6.3%FO; 1.3%P

7.9%FO; 2.9%P

14%FO7–21%FO

6.3-6.7%FO; 1.4–2.7%P0.3-0.8%FO; 0.1–0.2%P2.6–3.8%FO; 0.3–1.5%P8.9–62.7%FO; 4.7–29.8%P

Up to 30%P5.7%FO; 0.4%P2.4%FO; <0.1%P

44.4%FO; 42.9%P4.2%FO; 0.3%P4.8%FO; 0.2%P0.5%FO; 0.02%P

2.2%FO; 0.1%P0.8%FO; 0.1%P1%FO; 0.2%P

2.2%FO; 0.2%P14.3%FO; 1.5%P0.6%FO; 0.3%P6.4%FO; 0.3%P

2.9–68.8%FO; 0.2–49.2%P1.4–32.4%FO; 2.6–20.6%P12%FO; 5.6%P

2%FO

percentage of total prey number.Pakhomov (1993); 5. Pakhomov et al. (1999); 6. Bushula et al. (2005); 7. Rowedder93); 11. Hopkins and Torres (1989); 12. Steele and Klages (1986); 13. Lancraft et al.


The aragonite shells produced by thecosome pteropods contrib-ute at least 12% to global carbonate flux (Berner and Honjo, 1981).However, due to their relatively high solubility, a function of depth,temperature and pH (pCO2), the aragonite saturation horizon be-low which this form of carbonate is thermodynamically unstableis relatively shallow. Consequently, sediments containing >30%pteropod shells (‘‘pteropod ooze”) are found predominantly inthe tropics and sub-tropics, at <2800 m depth in the Atlantic and<500 m in the Pacific, and none are present in the Southern Ocean.Overall, only�2.4% of the Atlantic Ocean sea floor comprises ptero-pod ooze. Although not contributing substantially to sediments theproduction and export of CaCO3 pteropod shells is an importantregulating mechanism for the transport of carbon to the deepocean (Francois et al., 2002). The sinking rate of empty L. helicinashells has been calculated as between 864 and 1210 m d�1

(Lalli and Gilmer, 1989). Due to their high density and ballastingcapacity shells also facilitate rapid transfer of organic carbon(Francois et al., 2002) and inorganic carbon (Honjo, 2004) to thedeep ocean when pteropods die.

Sediment trap studies have shown that south of the PolarFront, pteropods (predominantly Limacina) are the major sourceof carbonate flux (>50%) to the ocean interior, while in the Sub-Antarctic Zone coccolithophores and foraminiferan tests dominate(Honjo et al., 2000; Honjo, 2004). In 1996–1998 carbonate exportsouth of the SAF was 11–13 g m�2 y�1, equivalent to the midNorth Atlantic Ocean (Honjo et al., 2000). Some caution needsto be used when analyzing sediment trap data as pteropods havebeen demonstrated to collect in traps as ‘‘swimmers”, at least atshallow depths, possibly due to their sinking escape behavior(Gilmer and Harbison, 1986). Conversely, traps may significantlyunderestimate flux volumes due to shell dissolution in trap jars(Betzer et al., 1984). A single cup trap deployed in the Ross Seain 1983–1984 found that pteropods constituted >50% of CaCO3

mass (Dunbar, 1984). Subsequent sediment trap data collectedin the Ross Sea found that the contribution of dead L. helicina ant-arctica was <5% of organic carbon from winter through to January,but increased to over 56–96% of organic carbon and 78–100% ofCaCO3 flux in April–June (Collier et al., 2000; Accornero et al.,2003). This increased contribution to flux in autumn was attrib-uted to a pteropod die off. A study in the seasonal ice zone northof Prydz Bay, East Antarctica, observed large numbers of empty L.helicina antarctica tests in traps between approximately April andOctober 1999 but did not quantify them (Pilskaln et al., 2004).There is no record of pteropod tests in Weddell Sea sediment trapstudies with foraminiferans being the only mentioned contribu-tors to CaCO3 flux (Fischer et al., 1988; Bathmann et al., 1991b;Wefer and Fischer, 1991). It is possible that acidity in trap cupscaused dissolution of shells prior to retrieval. The data from theRoss Sea and Prydz Bay, however, demonstrate that pteropodscan be seasonally major contributors to both inorganic and organ-ic carbon flux in the Southern Ocean. One of the possible conse-quences of a shoaling aragonite saturation horizon with acontinued rise in CO2 emissions may be the reduction in the trans-fer of inorganic carbon to the deep ocean. Coupled to this is areduction in the ballasting effect of thecosome shells, resulting inshallower re-mineralization of organic carbon and a reduction inthe recycling time of CO2 to the atmosphere (Feely et al., 2004).

4. Summary and directions for future research

Pteropods are ubiquitous components of Southern Ocean zoo-plankton communities. Regionally they are extremely abundantand can contribute substantially to communities in both the meso-and macrozooplankton size fractions. Densities vary substantiallybetween species and regions, being dominated by L. retroversa aus-

tralis in the sub-Antarctic mesozooplankton, L. helicina antarctica inthe Antarctic mesozooplankton, and L. helicina antarctica and C.pyramidata in the Antarctic macrozooplankton. Sub-Antarctic sam-pling was largely limited to the Prince Edward Islands, but in theAntarctic there was more substantial spatial coverage with thewestern sector of the Southern Ocean, between 180�W and90�W, being a conspicuous gap. In the area covered, South Georgia,East Antarctica south of Australia and the Ross Sea were hotspotsin terms of both pteropod densities and proportional contributionto zooplankton communities. Data reporting on the densities ofpteropods in the Weddell Sea are few, but indications are that theycan be highly abundant there too. Regional and inter-annual vari-ation in primary production is probably the major determinant ofspatial and temporal variability in pteropod densities (Comisoet al., 1993; Seibel and Dierssen, 2003).

Despite their numerical importance, the life cycle of pteropodsin the Southern Ocean has been little researched. There is an urgentneed for studies on population structure and its seasonal variation.However, future population studies of Southern Ocean pteropodsshould note that there may be considerable spatial and seasonallife cycle variation, including size at maturity and maximum sizeattained. Seasonal variation in size at maturity has already beendemonstrated in the Southern Ocean for L. retroversa australis (Da-don and de Cidre, 1992). In the northern hemisphere the maximumsize attained by L. helicina has variously been recoded as 3.7 mm incentral Arctic Ocean (Kobayashi, 1974), 6 mm in northwest Atlan-tic (Van der Spoel, 1967), and 11 mm at Baffin Island and Kongsf-jorden (Lalli and Wells, 1978; Gannefors et al., 2005). Thisvariation in size has significant implications for female fecundity(Lalli and Gilmer, 1989).

The variation in population size structure and reproductive tim-ing observed in the northern hemisphere is most likely related tothe seasonal cycle of primary production and indicates consider-able life cycle flexibility. The regional variation in primary produc-tion demonstrated by satellite imagery may translate to similarscale variation in thecosome life cycles in the Southern Ocean(e.g. Comiso et al., 1993). An additional factor that needs to be con-sidered in the Southern Ocean is growth and life cycle variation be-tween the different forms of L. helicina antarctica (f. rangi and f.antarctica) and C. pyramidata (f. antarctica and f. sulcata). The twoforms of both species are biogeographically distinct (Section 3.1)yet they are typically not differentiated in the literature. An impor-tant yet poorly understood component of pteropod life cycles isseasonal variation in vertical distribution. Our data indicate thatthe densities of pteropods are substantially reduced in winterand, at least in the macrozooplankton size fraction, there is evi-dence for both migration to deeper in the water column and winterfeeding in the surface layers.

An essential component to understanding the life cycle of ptero-pods and their role in Southern Ocean ecosystems is their trophicecology. A combination of gut content, lipid and stable isotopesanalyses indicate that thecosome pteropods are predominantlyherbivorous. However, more detailed studies are required to inves-tigate diet selectivity and the effect of phytoplankton biomass andcomposition on growth and reproduction, and its regional and sea-sonal variation. Although predominantly herbivorous, carnivoryclearly plays a dietary role, particularly in large thecosome ptero-pods. It is possible that there is a shift to increased carnivory withincreasing size, and it may be important for thecosome winter sur-vival (Conover and Lalli, 1974). The contribution of carnivory tothecosome diets needs to be quantified in order to accurately alignthis pteropod group within Southern Ocean trophic models. Inaddition to trophic studies, metabolic data may provide valuableinsights in this regard. Gymnosome pteropods have a well definedrole as specialist predators on thecosome species. Due to chemicaldefenses their consumption by fish is likely to be low, but studies


in the Arctic have shown that at times they can be important fortop predators (Lalli and Gilmer, 1989). Thecosomes, however,befitting their higher densities, can be important prey items forzooplankton, and pelagic and demersal fish, and have also been re-corded in the diets of seabirds. Pteropods therefore play a role asboth consumers and prey items.

Thecosomes have amongst the highest ingestion rates recordedfor Southern Ocean zooplankton, with C. pyramidata and L. helicinaantarctica rivaling that of the tunicate S. thompsoni. The few com-munity grazing studies that have included thecosomes have foundthat their contribution to grazing impact can be substantial butvariable on the regional scale. In view of their regionally high graz-ing impact, thecosome pteropods are potentially important con-tributors to vertical carbon flux in the Southern Ocean. They maycontribute to the vertical flux of organic carbon through the pro-duction of fast sinking faecal pellets, mucous flocs, and rapid set-tling out of dead animals due to the ballast provided by theiraragonite shells (Section 3.5). However, much of the data requiredto quantify these contributions are not available, including mucousweb production rates, egestion rates, assimilation efficiencies, met-abolic rates, and the relationship of these to food quality. With theincreasing number of sediment trap studies being conducted in theSouthern Ocean, data on faecal pellet morphology would enablequantification of pteropod contribution to faecal pellet flux. Inaddition to vertical carbon flux, pteropods potentially have a sig-nificant influence on dimethyl sulphide (DMS) dynamics in surfacewaters (Levasseur et al., 1994).

It is predicted that if a business as usual approach to CO2 emis-sions is adopted, Southern Ocean surface waters will begin to be-come undersaturated with respect to aragonite by 2050 (Orret al., 2005). As highlighted in the introduction this predictedchange in ocean chemistry may result in a decline in SouthernOcean pteropod densities and ultimately a northward shift in theirdistribution. This may first impact on species in the high Antarctic,including C. pyramidata sulcata, L. helicina antarctica and C. piatkow-skii, and their gymnosome predators C. limacina antarctica and S.australis. The data presented here demonstrate that pteropodsare important components of Southern Ocean ecosystems in termsof density and biomass, trophic role, and contribution to carbonflux. A decline in pteropod densities due to ocean acidificationmay therefore have a significant ecological impact. In view of thelimited data available for Southern Ocean pteropods, there isclearly a need for focused research on this zooplankton group in or-der to quantify the ecosystem impacts resulting directly from spe-cies loss, as well as the impacts resulting from a breakdown ofinter-specific community relationships.

Acknowledgements

Voyages 1–7 were completed during the German SouthernOcean GLOBEC program (Table 1); Voyages 9–18 were collectedby the Southern Scientific Research Institute of Marine Fisheriesand Oceanography; Voyages 19–33 were completed with supportof the South African National Antarctic Program and the Depart-ment of Environmental Affairs and Tourism; Voyages 8 and 34–44 were collected by the British Antarctic Survey; Voyage 46 andthe CPR Survey with completed with the support of the AustralianAntarctic Division and the National Institute of Polar Research(Japan). Finally, we would like to note that all authors contributeddata to this review.

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Pteropods in Southern Ocean ecosystems