Abstract
Thecosome pteropods form an important part of marine food webs, especially in polar ecosystems, and are the focus of research on ocean acidification. Although the larval stages of species in the genus Limacina often form major components of zooplankton communities, little is known of their population dynamics. We report high Limacina spp. abundance in March 2000 during surface zooplankton community sampling via a Continuous Plankton Recorder (CPR; 270-µm mesh) in a large area within the seasonal ice zone of the Southern Ocean. Regions with high Limacina spp. abundances extended to 600 nautical miles (ca 1110 km). Annual variability in Limacina spp. abundance and shell size is evaluated using North Pacific standard net (100-µm mesh) data from the same area and sampling periods (March) from 1997 to 2006. Although the relative total abundance of Limacina spp. in 2000 was the highest in the study period, its overall abundance was lower than the mean value for that period. Mean shell size for most years ranged 160–300 µm, while a relatively large mean size (444.7 µm) occurred in 2000. We conclude that a CPR with 270-µm mesh could catch large Limacina individuals that dominated in March 2000. The timing of reproduction and growth of the new generation may influence Limacina abundance throughout the sampling area.
Similar content being viewed by others
Data availability
All raw data on which this study is based are available at the Australian Antarctic Data Centre via the home page of the Southern Ocean Continuous Plankton Recorder (SO-CPR) Survey (http://data.aad.gov.au.aadc/cpr/).
References
Arbuckle JL (2014) Amos 23.0 user′s guide. Chicago, IBM SPSS 1–702
Bednaršek N, Tarling GA, Bakker DCE, Fielding S, Jones EM, Venables HJ, Ward P, Kuzirian A, Lézé B, Feely RA, Murphy EJ (2012a) Extensive dissolution of live pteropods in the Southern Ocean. Nat Geogr 5:881–885. https://doi.org/10.1038/ngeo1635
Bednaršek N, Tarling GA, Fielding S, Bakker DCE (2012b) Population dynamics and biogeochemical significance of Limacina helicina antarctica in the Scotia Sea (Southern Ocean). Deep-Sea Res II 59–60:105–116. https://doi.org/10.1016/j.dsr2.2011.08.003
Bednaršek N, Harvey CJ, Kaplan IC, Feely RA, Možina J (2016) Pteropods on the edge: cumulative effects of ocean acidification, warming, and deoxygenation. Prog Oceanogr 145:1–24. https://doi.org/10.1016/j.pocean.2016.04.002
Boissonnot L, Kohnert P, Ehrenfels B, Søreide JE, Graeve M, Stübner E, Schrödl M, Niehoff B (2021) Year-round population dynamics of Limacina spp. early stages in a high-Arctic fjord (Adventfjorden, Svalbard). Polar Biol 44:1605–1618. https://doi.org/10.1007/s00300-021-02904-6
Brierley AS, Thomas DN (2002) Ecology of Southern Ocean pack ice. In: Southward AJ et al (eds) Advances in marine biology, vol 43. Academic Press, London, pp 171–276
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth
Clark RA, Frid CLJ, Batten S (2001) A critical comparison of the two long-term zooplankton time series from the central west North Sea. J Plankton Res 23:27–39. https://doi.org/10.1093/plankt/23.1.27
Conroy JA, Steinberg DK, Thibodeau PS, Schofield O (2020) Zooplankton diel vertical migration during Antarctic summer. Deep-Sea Res I 162:103324. https://doi.org/10.1016/j.dsr.2020.103324
Dupont S, Thorndyke MC (2009) Impact of CO2-driven ocean acidification on invertebrate′s early life-history-what we know, what we need to know and what we can do. Biogeosci Discuss 6:3109–3131. https://doi.org/10.5194/bgd-6-3109-2009
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Mar Sci 65:414–432. https://doi.org/10.1093/icesjms/fsn048
Field JG, Clarke KR, Warwick RM (1982) A practical strategy for analysing multispecies distribution patterns. Mar Ecol Prog Ser 8:7–52. https://doi.org/10.3354/meps008037
Fukuchi M, Hattori H (1987) Surface water monitoring system installed on board the icebreaker Shirase. Proc NIPR Symp Polar Biol 1:7–55
Gannefors C, Böer M, Kattner G, Graeve M, Eiane K, Gulliksen B, Hop H, Falk-Petersen S (2005) The Arctic sea butterfly Limacina helicina lipids and life strategy. Mar Biol 147:169–177. https://doi.org/10.1007/s00227-004-1544-y
Gardner J, Manno C, Bakker DCE, Peck VL, Tarling GA (2018) Southern Ocean pteropods at risk from ocean warming and acidification. Mar Biol 165:8. https://doi.org/10.1007/s00227-017-3261-3
Hopkins TL (1971) Zooplankton standing crop in the Pacific sector of the Antarctic. In: Llano GA, Wallen IE (eds) Biology of the Antarctic Seas. American Geophysical Union, Washington, D. C, pp 347–367
Hopkins TL (1987) Midwater food web in McMurdo Sound, Ross Sea, Antarctica. Mar Biol 96:93–106. https://doi.org/10.1007/BF00394842
Hosie GW, Fukuchi M, Kawaguchi S (2003) Development of the Southern Ocean Continuous Plankton Recorder survey. Prog Oceanogra 58:263–284. https://doi.org/10.1016/j.pocean.2003.08.007
Hosie GW, Mormède S, Kitchener J, Takahashi K, Raymond B (2014) Chapter 10.3. Near-surface zooplankton communities. In: De Broyer C, Koubbi P et al (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 422–430
Hunt BPV, Hosie GW (2003) The Continuous Plankton Recorder in the Southern Ocean: a comparative analysis of zooplankton communities sampled by the CPR and vertical net hauls along 140°E. J Plankton Res 24:1561–1579. https://doi.org/10.1093/plankt/fbg108
Hunt BPV, Hosie GW (2005) Zonal structure of zooplankton communities in the Southern Ocean south of Australia: results from a 2150 km continuous plankton recorder transect. Deep-Sea Res I 52:1241–1271. https://doi.org/10.1016/j.dsr.2004.11.019
Hunt BPV, Hosie GW (2006) The seasonal succession of zooplankton in the Southern Ocean south of Australia, part I: the seasonal ice zone. Deep-Sea Res I 53:1182–1202. https://doi.org/10.1016/j.dsr.2006.05.001
Hunt BPV, Pakhomov EA, Hosie GW, Siegel V, Ward P, Bernard K (2008) Pteropods in Southern Ocean ecosystems. Prog Oceanogr 78:193–221. https://doi.org/10.1016/j.pocean.2008.06.001
Hunt BPV, Strugnell J, Bednarsek N, Linse K, Nelson RJ, Pakhomov E, Seibel B, Steinke D, Wurzberg L (2010) Poles apart: the ′′Bipolar′′ Pteropod species Limacina helicina is genetically distinct between the Arctic and Antarctic Oceans. PLoS ONE 5:e9835. https://doi.org/10.1371/journal.pone.0009835
Janssen AW, Bush SL, Bednaršek N (2019) The shelled pteropods of the northeast Pacific Ocean (Mollusca: Heterobranchia, Pteropoda). Zoosymposia 13:305–346. https://doi.org/10.11646/zoosymposia.13.1.22
John EH, Batten SD, Harris RP, Hays GC (2001) Comparison between zooplankton data collected by the Continuous Plankton Recorder survey in the English Channel and by WP-2 nets at station L4, Plymouth (UK). J Sea Res 46:223–232. https://doi.org/10.1016/S1385-1101(01)00085-5
Johnston NM, Murphy EJ, Atkinson A, Constable AJ, Cotté C, Cox M, Daly KL, Driscoll R, Flores H, Halfter S, Henschke N, Hill SL, Höfer J, Hunt BPV, Kawaguchi S, Lindsay D, Liszka C, Loeb V, Manno C, Meyer B, Pakhomov EA, Pinkerton MH, Reiss CS, Richerson K, Smith WO Jr, Steinberg DK, Swadling KM, Tarling GA, Thorpe SE, Veytia D, Ward P, Weldrick CK, Yang G (2022) Status, change, and futures of zooplankton in the Southern Ocean. Front Ecol Evol 9:624692. https://doi.org/10.3389/fevo.2021.624692
Lalli CM, Wells FE (1978) Reproduction in genus Limacina (Opisthobranchia Thecosomata). J Zool 186:95–108. https://doi.org/10.1111/j.1469-7998.1978.tb03359.x
Lalli CM, Gilmer RW (1989) Pelagic snails: the biology of holopanktonic gastropod mollusks. Stanford University Press, Palo Alto
Mackey A, Atkinson A, Hill S, Ward P, Cunningham N, Johnston NM, Murphy EJ (2012) Antarctica microzooplankton of the southwest Atlantic sector and Bellingshausen Sea: historical distributions: relationships with food; and implications for ocean warming. Deep-Sea Res II 59–60:130–146. https://doi.org/10.1016/j.dsr2.2011.08.011
Makabe R, Tanimura A, Fukuchi M (2012) Comparison of mesh size effects on mesozooplankton collection efficiency in the Southern Ocean. J Plankton Res 34:432–436. https://doi.org/10.1093/plankt/fbs014
Manno C, Sandrini S, Tositti L, Accornero A (2007) First stages of degradation of Limacina helicina shells observed above the aragonite chemical lysocline in Terra Nova Bay (Antarctica). J Mar Syst 68:91–102. https://doi.org/10.1016/j.jmarsys.2006.11.002
Manno C, Accornero A, Umani SF (2010) Importance of the contribution of Limacina helicina faecal pellets to the carbon pump in Terra Nova Bay (Antarctica). J Plankton Res 32:145–152. https://doi.org/10.1093/plankt/fbp108
Manno C, Morata N, Primicerio R (2012) Limacina retroversa′s response to combined effects of ocean acidification and sea water freshening. Estuar Coast Shelf Sci 113:163–171. https://doi.org/10.1016/j.ecss.2012.07.019
Manno C, Peck VL, Tarling GA (2016) Pteropod eggs released at high pCO2 lack resilience to ocean acidification. Sci Rep 6:25752. https://doi.org/10.1038/srep25752
Manno C, Giglio F, Stowasser G, Fielding S, Enderlein P, Tarling GA (2018) Threatened species drive the strength of the carbonate pump in the northern Scotia Sea. Nat Commun 9:4592. https://doi.org/10.1038/s41467-018-07088-y
Mekkes L, Sepúlveda-Rodríguez G, Bielkinaitë G, Wall-Palmer D, Brumme G-JA, Dämmer LK, Huisman J, van Loon E, Renema W, Peijnenburg KTCA (2021) Effects of ocean acidification on calcification of the Sub-Antarctic Pteropod Limacina retroversa. Front Mar Sci 8:581432. https://doi.org/10.3389/fmars.2021.581432
Nishizawa Y, Sasaki H, Takahashi KT (2016) Interannual variability in shelled pteropods (Limacina spp.) in the Indian sector of the Southern Ocean during austral summer. Antarct Rec 60:35–48. https://doi.org/10.15094/00012672
Ojima M, Takahashi KT, Iida T, Odate T, Fukuchi M (2013) Distribution patterns of micro- and meso-zooplankton communities in sea ice regions of Lützow-Hom Bay, East Antarctica. Polar Biol 36:1293–1304. https://doi.org/10.1007/s00300-013-1348-y
Ojima M, Takahashi KT, Tanimura A, Odate T, Fukuchi M (2015) Spatial distribution of micro- and meso-zooplankton in the seasonal ice zone of east Antarctica during 1983–1995. Polar Sci 9:319–326. https://doi.org/10.1016/j.polar.2015.05.002
Orsi AH, Whitworth T III, Nowlin WD Jr (1995) On the meridional extent and fronts of the Antarctic Circumpolar Current. Deep-Sea Res 42:641–673. https://doi.org/10.1016/0967-0637(95)00021-W
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. https://doi.org/10.1038/nature04095
Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press Inc., New York
Pinkerton MH, Décima M, Kitchener JA, Takahashi KT, Robinson KV, Stewart R, Hosie GW (2020) Zooplankton in the Southern Ocean from the continuous plankton recorder: Distributions and long-term change. Deep-Sea Res I 162:103303. https://doi.org/10.1016/j.dsr.2020.103303
Seibel BA, Dierssen HM (2003) Cascading trophic impacts of reduced biomass in the Ross Sea Antarctica: just the tip of the iceberg? Biol Bull 205:93–97. https://doi.org/10.2307/1543229
Sokolov S, Rintoul SR (2002) Structure of Southern Ocean fronts at 140°E. J Mar Syst 37:151–184. https://doi.org/10.1016/S0924-7963(02)00200-2
Steinberg DK, Ruck KE, Gleiber MR, Garzio LM, Cope JS, Bernard KS (2015) Long-term (1993–2013) changes in macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res I 101:54–70. https://doi.org/10.1016/j.dsr.2015.02.009
Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. J Oceanogra 46:190–194. https://doi.org/10.1007/BF02125580
Takahashi KT, Hosie GW (2021)The status and trends of Southern Ocean zooplankton based on the SCAR Southern Ocean Continuous Plankton Recorder (SO-CPR) survey. SCAR Bulletin, No. 206, p 97
Takahashi KT, Hosie GW, Kitchener JA, McLeod DJ, Odate T, Fukuchi M (2010) Comparison of zooplankton distribution patterns between four seasons in the Indian Ocean sector of the Southern Ocean. Polar Sci 4:317–331. https://doi.org/10.1016/j.polar.2010.05.002
Takahashi KT, Hosie GW, Kitchener JA, McLeod DJ, Stevens C, Robinson K, Jonas T, Fukuchi M (2011) Report on “Southern Ocean CPR Standards Workshop -SCAR Expert Group on CPR Research-.” Nankyoku Shiryô (antarctic Record) 55:277–284
Takahashi KT, Ojima M, Tanimura A, Odate T, Fukuchi M (2017) The vertical distribution and abundance of copepod nauplii and other micro- and mesozooplankton in the seasonal ice zone of Lützow−Holom Bay during austral summer 2009. Polar Biol 40:79–93. https://doi.org/10.1007/s00300-016-1925-y
Thibodeau PS, Steinberg DK, Stammerjohn SE, Hauri C (2019) Environmental controls on pteropod biogeography along the Western Antarctic Peninsula. Limnol Oceanogr 64:S240–S256. https://doi.org/10.1002/lno.11041
Thibodeau PS, Steinberg DK, McBride CE, Conroy JA, Keul N, Ducklow HW (2020) Long-term observations of pteropod phynology along the Western Antarctic Peninsula. Deep-Sea Res I 166:103363. https://doi.org/10.1016/j.dsr.2020.103363
Thibodeau PS, Song B, Moreno CM, Steinberg DK (2022) Feeding ecology and microbiome of the pteropod Limacina helicina antarctica. Aquat Microb Ecol 88:19–24. https://doi.org/10.3354/ame01981
Wang K, Hunt BPV, Liang C, Pauly D, Pakhomov EA (2017) Reassessment of the life cycle of the pteropod Limacina helicina from a high resolution interannual time series in the temperate North Pacific. ICES J Mar Sci 74:1906–1920. https://doi.org/10.1093/icesjms/fsx014
Weldrick CK, Trebilco R, Davies DM, Swadling KM (2019) Trophodynamics of Southern Ocean pteropods on the southern Kerguelen Plateau. Ecol Evol 9:8119–8132. https://doi.org/10.1002/ece3.5380
Weldrick CK, Makabe R, Mizobata K, Moteki M, Odate T, Takao S, Trebilco R, Swadling KM (2021) The use of swimmers from sediment traps to measure summer community structure of Southern Ocean pteropods. Polar Biol 44:457–472. https://doi.org/10.1007/s00300-021-02809-4
Acknowledgements
We express our heartfelt appreciation to all members of the 38–47th Japanese Antarctic Research Expeditions, who collected the samples and oceanographic data used in this study. We would like to thank Patricia Thibodeau and one anonymous reviewer for their constructive comments on an earlier version of this manuscript. We are also grateful to the officers and crew of the icebreaker Shirase for their assistance during the cruise. We thank Edanz (https://jp.edanz.com/ac), for editing a draft of this manuscript.
Funding
This research was supported in part by the National Institute of Polar Research (NIPR) through Project Research no. KP-308, and a Grant-in-Aid for Science (No. 16H02970) to K.T. Takahashi from the Japan Society for the Promotion of Science. The study is also part of the Science Program of JARE AMB-0902.
Author information
Authors and Affiliations
Contributions
KTT directed the JARE monitoring program and wrote the manuscript. HU carried out field sampling aboard the icebreaker Shirase and processed the samples.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Takahashi, K.T., Umeda, H. The variability in abundance and shell size of the thecosome pteropods Limacina spp. in the seasonal ice zone of the Southern Ocean in March. Polar Biol 46, 523–537 (2023). https://doi.org/10.1007/s00300-023-03141-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-023-03141-9