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Influence of Environmental Factors on the Distribution of Pteropods Limacina helicina (Phipps, 1774) in Siberian Arctic Seas

  • MARINE BIOLOGY
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Abstract

Analysis of zooplankton collected on five cruises (2007–2016) in the Kara and Laptev seas has revealed considerable heterogeneity in the spatial distribution of the biomass of the pteropod Limacina helicina, one of the important components of the Arctic zooplankton. The biomass and abundance of mollusks in 2014–2016 were significantly lower than in the previous period, in 2007 and 2011. The existence of persistent aggregations of L. helicina in the area of the continental slope of the Kara Sea (St. Anna Trough) with a biomass an order of magnitude higher than in the adjacent areas has been shown. Such aggregations of L. helicina were related to a combination of favorable factors: high salinity (≥33 psu), optimal temperature range (1–5°C), and local hydrophysical processes associated with the slope frontal zone. Results of the General Linear Mixed Model (GLMM) have shown that the biomass of pteropods is primarily related to salinity and temperature. No relationship between the biomass of pteropods and the average chlorophyll concentration in the upper layer has been found. However, within L. helicina aggregations, the biomass of mollusks correlated with the concentration of chlorophyll a in the layer of its maximum.

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REFERENCES

  1. E. G. Arashkevich, M. V. Flint, A. B. Nikishina, et al., “The role of zooplankton in the transformation of the organic matter in the Ob estuary, on the shelf, and in the deep regions of the Kara Sea,” Oceanology (Engl. Transl.) 50, 780–792 (2010).

  2. M. E. Vinogradov and E. A. Shushkina, Activity of Planktonic Communities of the Ocean Epipelagial (Nauka, Moscow, 1987) [in Russian].

    Google Scholar 

  3. A. V. Drits, E. G. Arashkevich, A. B. Nikishina, et al., “Mesozooplankton grazing impact on phytoplankton in the northern regions of the Kara Sea in autumn,” Oceanology (Engl. Transl.) 55, 595–605 (2015).

  4. A. F. Pasternak, A. V. Drits, and M. V. Flint, “Feeding, egg production, and respiration rate of pteropods Limacina in Arctic seas,” Oceanology (Engl. Transl.) 57, 122–129 (2017).

  5. K. A. Rogachev, “Formation of dense agglomerations of pelagic mollusks (Limacina helicina) in the Academy Bay, Sea of Okhotsk,” Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr. 166, 200–207 (2011).

    Google Scholar 

  6. I. N. Sukhanova, M. V. Flint, E. I. Druzhkova, et al., “Phytoplankton in the northwestern Kara Sea,” Oceanology (Engl. Transl.) 55, 547–560 (2015). https://doi.org/10.1134/S0001437015040141

  7. I. N. Sukhanova, M. V. Flint, E. G. Sakharova, et al., “Phytocenoses of the Ob estuary and Kara Sea shelf in the late spring season,” Oceanology (Engl. Transl.) 58, 802–816 (2018).

  8. M. V. Flint, “Cruise 54th of the research vessel Akademik Mstislav Keldysh in the Kara Sea,” Oceanology (Engl. Transl.) 50, 637–642 (2010).

  9. M. V. Flint, T. N. Semenova, E. G. Arashkevich, et al., “Structure of the zooplankton communities in the region of the Ob River’s estuarine frontal zone,” Oceanology (Engl. Transl.) 50, 766–779 (2010).

  10. M. V. Flint, S. G. Poyarkov, A. G. Timonin, and K. A. Soloviev, “The structure of the mesoplankton community in the area of the continental slope of the St. Anna Trough (Kara Sea),” Oceanology (Engl. Transl.) 55, 583–594 (2015). https://doi.org/10.1134/S0001437015040062

  11. L. L. Chislenko, Nomograms for Determining the Weight of Aquatic Organisms by the Size and Shape of the Body (Nauka, Leningrad, 1968) [in Russian].

    Google Scholar 

  12. A. Accornero, C. Manno, F. Esposito, and M. C. Gambi, “The vertical flux of particulate matter in the polynya of Terra Nova Bay. Part II. Biological components,” Antarct. Sci. 15, 175–188 (2003).

    Article  Google Scholar 

  13. A. Atkinson, R. S. Shreeve, E. A. Pakhomov, et al., “Zooplankton response to a phytoplankton bloom near South Georgia, Antarctica,” Mar. Ecol.: Prog. Ser. 144, 195–210 (1996).

    Article  Google Scholar 

  14. U. V. Bathmann, T. T. Noji, and B. von Bodungen, “Sedimentation of pteropods in the Norwegian Sea in autumn,” Deep-Sea Res., Part A 38 (10), 1341–1360 (1991).

    Article  Google Scholar 

  15. E. Bauerfeind, E. M. Nöthig, A. Beszczynska, et al., “Particle sedimentation patterns in the eastern Fram Strait during 2000–2005: results from the Arctic long-term observatory HAUSGARTEN,” Deep Sea Res., Part I 56 (9), 1471–1487 (2009).

    Article  Google Scholar 

  16. E. Bauerfeind, E.-M. Nöthig, B. Pauls, et al., “Variability in pteropod sedimentation and corresponding aragonite flux at the Arctic deep-sea long-term observatory HAUSGARTEN in the eastern Fram Strait from 2000 to 2009,” J. Mar. Syst. 132, 95–105 (2014).

    Article  Google Scholar 

  17. A. W. H. Bé and R. W. Gilmer, “A zoogeographic and taxonomic review of euthecosomatous Pteropoda,” in Oceanic Micropalaeontology, Ed. by M. A. Ali (Academic, London, 1977), pp. 773–808.

    Google Scholar 

  18. N. Bednaršek, G. A. Tarling, S. Fielding, and D. C. E. Baker, “Population dynamics and biogeochemical significance of Limacina helicina antarctica in the Scotia sea (Southern Ocean),” Deep Sea Res., Part II 59–60, 105–116 (2012).

    Article  Google Scholar 

  19. N. Bednaršek, R. A. Feely, N. Tolimieri, et al., “Exposure history determines pteropod vulnerability to ocean acidification along the US West Coast,” Sci. Rep. 7, 4526 (2017). https://doi.org/10.1038/s41598-017-03934-z

    Article  Google Scholar 

  20. K. S. Bernard, PhD Thesis (Rhodes University, Grahamstown, 2006), p. 196.

  21. K. S. Bernard and P. W. Froneman, “The sub-Antarctic euthecosome pteropod, Limacina retroversa: distribution patterns and trophic role,” Deep Sea Res., Part I 56, 582–598 (2009). https://doi.org/10.1016/j.dsr.2008.11.007

    Article  Google Scholar 

  22. B. Bolker, Ecological Models and Data in R (Princeton University Press, Princeton, NJ, 2007).

    Google Scholar 

  23. K. Busch, E. Bauerfeind, and E.-M. Nöthig, “Pteropod sedimentation patterns in different water depths observed with moored sediment traps over a 4-year period at the LTER station HAUSGARTEN in eastern Fram Strait,” Polar Biol. 38 (6), 845–859 (2015). https://doi.org/10.1007/s00300-015-1644-9

    Article  Google Scholar 

  24. C. Chen, “Zoogeography of thecosomatous pteropods in the West Antarctic Ocean,” Nautilus 81, 94–100 (1968).

    Google Scholar 

  25. S. Comeau, R. Jeffree, J.-L. Teyssie, et al., “Response of the Arctic pteropod Limacina helicina to projected future environmental conditions,” PLoS One 5 (6). e11362 (2010). https://doi.org/10.1371/journal.pone.0011362

    Article  Google Scholar 

  26. F. Cribari-Neto and A. Zeileis, “Beta regression in R,” J. Stat. Software 34 (2), 1–24 (2010). http://www.jstatsoft.org/v34/i02/.

    Article  Google Scholar 

  27. C. Gannefors, B. Marco, K. Gerhard, et al., “The Arctic sea butterfly Limacina helicina: lipids and life strategy,” Mar. Biol. 147, 169–177 (2005).

    Article  Google Scholar 

  28. R. W. Gilmer and G. R. Harbison, “Diet of Limacina helicina (Gastropoda: Thecosomata) in Arctic waters in midsummer,” Mar. Ecol.: Prog. Ser. 77, 125–134 (1991).

    Article  Google Scholar 

  29. T. L. Hopkins, “Midwater food web in McMurdo Sound, Ross Sea, Antarctica,” Mar. Biol. 96, 93–106 (1987).

    Article  Google Scholar 

  30. W. R. Howard, D. Roberts, A. D. Moy, et al., “Distribution, abundance and seasonal flux of pteropods in the Sub-Antarctic zone,” Deep Sea Res., Part II 58, 2293–2300 (2011).

    Article  Google Scholar 

  31. B. P. V. Hunt, E. A. Pakhomov, G. W. Hosie, et al., “Pteropods in Southern Ocean ecosystems,” Prog. Oceanogr. 78, 193–221 (2008).

    Article  Google Scholar 

  32. P. Kacprzak, A. Panasiuk, J. Wawrzynek, and A. Weydmann, “Distribution and abundance of pteropods in the western Barents Sea,” Oceanol. Hydrobiol. Stud. 46 (4), 393–404 (2017). https://doi.org/10.1515/ohs-2017-0039

    Article  Google Scholar 

  33. S. Lischka, J. Büdenbender, T. Boxhammer, and U. Riebesell, “Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth,” Biogeosciences 8, 919–932 (2011). https://doi.org/10.5194/bg-8-919-2011

    Article  Google Scholar 

  34. A. E. Maas, L. E. Elder, H. M. Dierssen, and B. A. Seibel, “Metabolic response of Antarctic pteropods (Mollusca: Gastropoda) to food deprivation and regional productivity,” Mar. Ecol.: Prog. Ser. 441, 129–139 (2011).

    Article  Google Scholar 

  35. D. L. Mackas and M. D. Galbraith, “Pteropod time-series from the NE Pacific,” ICES J. Mar. Sci. 69, 448–459 (2012).

    Article  Google Scholar 

  36. C. Manno, V. Tirelli, A. Accornero, and S. Fonda Umani, “Importance of the contribution of Limacina helicina faecal pellets to the carbon pump in Terra Nova Bay (Antarctica),” J. Plankton Res. 34, 145–152 (2010).

    Article  Google Scholar 

  37. Y. Nishizawa, H. Sasaki, and K. Takahashi, “Interannual variability in shelled pteropods (Limacina spp.) in the Indian sector of the Southern Ocean during austral summer,” Antarct. Rec. 60, 35–48 (2016).

    Google Scholar 

  38. T. T. Noji, U. V. Bathmann, B. von Bodungen, et al., “Clearance of picoplankton-sized particles and formation of rapidly sinking aggregates by the pteropod, Limacina retroversa,” J. Plankton Res. 19, 863–875 (1997).

    Article  Google Scholar 

  39. M. D. Ohman, B. E. Lavaniegos, and A. W. Townsend, “Multidecadal variations in calcareous holozooplankton in the California Current System: thecosome pteropods, heteropods, and foraminifera,” Geophys. Res. Lett. 36, L18608 (2009).

    Article  Google Scholar 

  40. E. A. Pakhomov, P. W. Froneman, P. Wassmann, et al., “Contribution of algal sinking and zooplankton grazing to downward flux in the Lazarev Sea (Southern Ocean) during the onset of phytoplankton bloom: a Lagrangian study,” Mar. Ecol. Prog. Ser. 233, 73–88 (2002).

    Article  Google Scholar 

  41. R Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2019). https://www.R-project.org/.

  42. B. A. Seibel and H. M. Dierssen, “Cascading trophic impacts of reduced biomass in the Ross Sea, Antarctica: Just the tip of the iceberg?” Biol. Bull. 205, 93–97 (2003).

    Article  Google Scholar 

  43. B. A. Seibel, A. E. Maas, and H. M. Dierssen, “Energetic plasticity underlies a variable response to ocean acidification in the pteropod, Limacina helicina antarctica,” PLoS One 7, e30464 (2012).

    Article  Google Scholar 

  44. M. Tsurumi, D. L. Mackas, F. A. Whitney, et al., “Pteropods, eddies, carbon flux, and climate variability in the Alaska Gyre,” Deep Sea Res., Part II 52, 1037–1053 (2005).

    Article  Google Scholar 

  45. K. Wang, B. P. V. Hunt, C. Liang, et al., “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 (7), 1906–1920 (2017). https://doi.org/10.1093/icesjms/fsx014

    Article  Google Scholar 

  46. B. Winter, Linear models and linear mixed effects models in R with linguistic applications, 2013. arXiv:1308.5499

  47. A. Zeileis and T. Hothorn, “Diagnostic checking in regression relationships,” R News 2 (3), 7–10 (2002). https://CRAN.R-project.org/doc/Rnews/.

    Google Scholar 

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Funding

Field studies were carried out under the state assignment of Ministry of Science and Higher Education of the Russian Federation (theme No. № 0149-2019-0008, (topic no. 0149-2019-0008). Sample processing and combined evaluation of findings were supported by the Russian Foundation for Basic Research (project no. 18-05-60069 Arctic); analysis of the obtained data was supported by the Russian Foundation for Basic Research (project no. 19-05-00022); preparation and writing of the article was supported by the Russian Foundation for Basic Research (project no. 19-04-00322).

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Authors and Affiliations

  1. Shirshov Institute of Oceanology, Russian Academy of Science, Moscow, Russia

    A. F. Pasternak, A. V. Drits & M. V. Flint

  2. Severtsov Institute of Ecology and Evolution, Moscow, Russia

    M. V. Gopko

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  1. A. F. Pasternak
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  2. A. V. Drits
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  3. M. V. Gopko
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Correspondence to A. F. Pasternak.

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Translated by T. Kuznetsova

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Pasternak, A.F., Drits, A.V., Gopko, M.V. et al. Influence of Environmental Factors on the Distribution of Pteropods Limacina helicina (Phipps, 1774) in Siberian Arctic Seas. Oceanology 60, 490–500 (2020). https://doi.org/10.1134/S0001437020040177

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