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Biochemical composition and energy content of size-fractionated zooplankton east of the Kerguelen Islands

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Abstract

Food quality is recognized as a key parameter of food web functioning in which zooplankton plays a crucial role not only in linking lower to upper trophic levels but also in transforming the quality of the organic matter available to predators. The influence of size and taxonomic group composition of zooplankton in these processes was assessed in eastern Kerguelen waters (Southern Ocean) at the onset of the spring bloom in 2011. Biochemical (lipids, proteins and carbohydrates) and elemental (carbon and nitrogen) composition were measured in five size—fractions of bulk zooplankton ranging from 80 µm to > 2000 µm and in large copepods, euphausiids, annelids and salps, and energy content was derived from biochemical contents. Proteins were the dominant component of zooplankton dry weight (21.5% dw), followed by lipids (8.9% dw), soluble carbohydrates (2.2% dw) and insoluble carbohydrates (1.0% dw). A concentration increase with zooplankton size for all biochemical components was observed, particularly stronger for proteins and lipids. Copepods and salps provided, respectively, the highest and the lowest amount of lipids and energy. A four-fold increase in energy content was observed from the smallest to the largest fraction inducing a significant increase (> 10 kJ g−1 dw) in the quality of zooplankton matter. This may explain why large zooplankton represent a major food resource for numerous fish, seabirds and marine mammals in the Southern Ocean. Such unique results are required to better quantify energy dynamics in polar food webs.

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References

  • Arun Kumar M, Padmavati G, Anandavelu I (2013) Biochemical composition and calorific value of zooplankton from the coastal waters of South Andaman. Proc Int Acad Ecol Environ Sci 3:278–287

    CAS  Google Scholar 

  • Banse K (1995) Zooplankton: pivotal role in the control of ocean production. ICES J Mar Sci 52:265–277

    Article  Google Scholar 

  • Barnes C, Maxwell D, Reuman DC, Jennings S (2010) Global patterns in predator-prey size relationships reveal size dependency of trophic transfer efficiency. Ecology 91:222–232

    Article  PubMed  Google Scholar 

  • Beukema JJ (1997) Caloric values of marine invertebrates with an emphasis on the soft parts of marine bivalves. Oceanogr Mar Biol Ann Rev 35:387–414

    Google Scholar 

  • Bhat KL, Sreepada RA, Ansari ZA (1993) Biochemical composition of zooplankton from the northern Arabian sea. Pak J Mar Sci 2:17–22

    Google Scholar 

  • Blain S, Quéguiner B, Trull T (2008) The natural iron fertilization experiment KEOPS (Kerguelen Ocean Plateau Compared Study): an overview. Deep-Sea Res Pt II 55:559–565

    Article  Google Scholar 

  • Blanchard JL, Heneghan RF, Everett JD, Trebilco R, Richardson AJ (2017) From bacteria to whales: Using functional size spectra to model marine ecosystems. Trends Ecol Evol 32:174–186

    Article  PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Physiol Pharmacol 37:911–917

    CAS  Google Scholar 

  • Bocher P, Cherel Y, Labat JP, Mayzaud P, Razouls S, Jouventin P (2001) Amphipod-based food web: Themisto gaudichaudii caught in nets and by seabirds in Kerguelen waters, southern Indian Ocean. Mar Ecol Prog Ser 223:261–276

    Article  Google Scholar 

  • Bocher P, Cherel Y, Alonzo F, Razouls S, Labat JP, Mayzaud P, Jouventin P (2002) Importance of the large copepod Paraeuchaeta antarctica (Giesbrecht, 1902) in coastal waters and the diet of seabirds at Kerguelen, Southern Ocean. J Plankton Res 24:1317–1333

    Article  Google Scholar 

  • Bost CA, Cotté C, Bailleul F, Cherel Y, Charrassin JB, Guinet C, Ainley DG, Weimerskirch H (2009) The importance of oceanic fronts to marine birds and mammals of the southern oceans. J Mar Syst 78:363–376

    Article  Google Scholar 

  • Carlotti F, Krause M, Radach G (1993) Growth and development of Calanus finmarchicus related to the influence of temperature: experimental results and conceptual model. Limnol Oceanogr 38:1125–1134

    Article  Google Scholar 

  • Carlotti F, Giske J, Werner F (2000) Modelling zooplankton dynamics. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, San Diego, pp 571–667

    Chapter  Google Scholar 

  • Carlotti F, Jouandet MP, Nowaczyk A, Harmelin-Vivien M, Lefèvre D, Richard P, Zhu Y, Zhou M (2015) Mesozooplankton structure and functioning during the onset of the Kerguelen bloom during Keops2 survey. Biogeosciences 12:4543–4563

    Article  Google Scholar 

  • Cass CJ, Daly KL, Wakeham SG (2014) Assessment of storage lipid accumulation patterns in eucalanoid copepods from the eastern tropical Pacific Ocean. Deep-Sea Res Pt I 93:117–130

    Article  CAS  Google Scholar 

  • Cherel Y, Bocher P, Trouvé C, Weimerskirch H (2002) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:283–299

    Article  Google Scholar 

  • Cherel Y, Fontaine C, Richard P, Labat JP (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr 55:324–332

    Article  CAS  Google Scholar 

  • Cherel Y, Bost CA, Guinet C, Weimerskirch H (2005) Feeding habits of seabirds and marine mammals of the Kerguelen Archipelago. In: Palomares MLD, Pruvost P, Pitcher TJ, Pauly D (eds) Modeling Antarctic marine ecosystems. Fisheries Centre Research Reports, 13(7). Fisheries Centre, University of British Columbia, Vancouver, pp 31–36

  • Clarke A, Holmes LJ, Gore DJ (1992) Proximate and elemental composition of gelatinous zooplankton from the Southern Ocean. J Exp Mar Biol Ecol 155:55–68

    Article  Google Scholar 

  • Donnelly J, Stickney DG, Torres JJ (1993) Proximate and elemental composition and energy content of mesopelagic crustaceans from the Eastern Gulf of Mexico. Mar Biol 115:469–480

    Article  CAS  Google Scholar 

  • Donnelly J, Torres JJ, Hopkins TL, Lancraft TM (1994) Chemical composition of Antarctic zooplankton during austral fall and winter. Polar Biol 14:171–183

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Reber PA, Smith F (1956) Colorimetric method for determination of sugar and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Falk-Petersen S, Sargent JR, Loenne OJ, Timofeev S (1999) Functional biodiversity of lipids in Antarctic zooplankton: Calanoides acutus, Calanus propinquus, Thysanoessa macrura and Euphausia crystallorophias. Polar Biol 21:37–47

    Article  Google Scholar 

  • Färber-Lorda J, Gaudy R, Mayzaud P (2009) Elemental composition, biochemical composition and caloric value of Antarctic krill. Implications in energetics and carbon balances. J Mar Syst 78:518–524

    Article  Google Scholar 

  • Frederiksen M, Edwards M, Richardson AJ, Halliday NC, Wanless S (2006) From plankton to top predators: bottom-up control of a marine food web across four trophic levels. J Anim Ecol 75:1259–1268

    Article  PubMed  Google Scholar 

  • García-Comas C, Sastri AR, Ye L, Chang CY, Lin FS, Su MS, Gong GC, Hsieh CH (2016) Prey size diversity hinders biomass trophic transfer and predator size diversity promotes it in planktonic communities. Proc R Soc B 283:2015–2129

    Article  CAS  Google Scholar 

  • Goswami SC, Rao TSS, Matondkar P (1981) Biochemical composition of zooplankton from the Andaman Sea. Indian J Mar Sci 10:296–300

    CAS  Google Scholar 

  • Guinet C, Cherel Y, Ridoux V, Jouventin P (1996) Consumption of marine resources by seabirds and seals in Crozet and Kerguelen waters: Changes in relation to consumer biomass. 1962–1985. Antarct Sci 8:23–30

    Article  Google Scholar 

  • Guisande C (2006) Biochemical fingerprints in zooplankton. Limnetica 25:369–376

    Google Scholar 

  • Hagen W, Auel H (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton. Zoology 104:313–326

    Article  PubMed  CAS  Google Scholar 

  • Hansen B, Bjornsen PK, Hansen PJ (1994) The size ratio between planktonic predators and their prey. Limnol Oceanogr 39:395–403

    Article  Google Scholar 

  • Hindell MA, Bost CA, Charrassin JB, Gales N, Lea MA, Goldsworthy S, Page B, Robertson G, Wienecke W, O’Toole M, Guinet C (2011) Foraging habitats of top predators, and areas of ecological significance, on the Kerguelen plateau. In: Duhamel G, Welsford D (eds) The Kerguelen Plateau: marine ecosystem and fisheries. Société d’Ichtyologie, Paris, pp 203–215

    Google Scholar 

  • Huenerlage K, Buchholz F (2013) Krill of the northern Benguela Current and the Angola-Benguela frontal zone compared: physiological performance and short-term starvation in Euphausia hanseni. J Plankton Res 35:337–351

    Article  Google Scholar 

  • Ikeda T, Skjoldal HR (1989) Metabolism and elemental composition of zooplankton from the Barrents Sea during early Arctic summer. Mar Biol 100:173–183

    Article  CAS  Google Scholar 

  • Iverson SJ, Lang SLC, Cooper MH (2001) Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283–1287

    Article  PubMed  CAS  Google Scholar 

  • Jouandet MP, Jackson G, Carlotti F, Picheral M, Stemmann L, Blain S (2014) Rapid formation of large aggregates during the spring bloom of Kerguelen Island: observations and model comparisons. Biogeosciences 11:4949–4993

    Article  Google Scholar 

  • Kattner G, Hagen W, Lee RF, Campbell R, Deibel D, Falk-Petersen S, Graeve M, Hansen BW, Hirche HJ, Jónasdottir SH, Madsen ML, Mayzaud P, Müller-Navarra D, Nichols PD, Paffenhöfer GA, Pond D, Saito H, Stübing D, Virtue P (2007) Perspectives on marine zooplankton lipids. Can J Fish Aquat Sci 64:1628–1639

    Article  CAS  Google Scholar 

  • Lasbleiz M, Leblanc K, Blain S, Ras J, Cornet-Barthaux V, Hélias Nunige S, Quéguiner B (2014) Pigments, elemental composition (C, N, P, and Si), and stoichiometry of particulate matter in the naturally iron fertilized region of Kerguelen in the Southern Ocean. Biogeosciences 11:5931–5955

    Article  Google Scholar 

  • Lea MA, Nichols PD, Wilson G (2002) Fatty acid composition of lipid-rich myctophids and mackerel icefish (Chamsocephalus gunnari) - Southern Ocean food-web implications. Polar Biol 25:843–854

    Google Scholar 

  • Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Progr Ser 307:273–306

    Article  CAS  Google Scholar 

  • Legendre L, Legendre P (2012) Numerical ecology, 3rd edn. Elsevier, New York

    Google Scholar 

  • Lopes RM, Marcolin CR, Brandini FP (2015) Influence of oceanic fronts on mesozooplankton abundance and grazing during spring in the south-western Atlantic. Mar Freshw Res 67:626–635

    Article  Google Scholar 

  • Lowry O, Rosenbrough RJ, Farr L, Randall R (1951) Protein measurements with the Folin phenol sulfuric acid method. Water Res 7:741–746

    Google Scholar 

  • Mayzaud P, Martin JLM (1975) Some aspects of the biochemical and mineral composition of marine plankton. J Exp Mar Biol Ecol 17:297–310

    Article  CAS  Google Scholar 

  • Mayzaud P, Laureillard J, Merien D, Labat JP (2007) Zooplankton nutrition, storage and fecal lipid composition in different water masses associated with the Agulhas and Subtropical Fronts. Mar Chem 107:202–213

    Article  CAS  Google Scholar 

  • Mayzaud P, Lacombre S, Boutoute M (2011) Seasonal and growth stage changes in lipid and fatty acid composition in the multigeneration copepod Drepanus pectinatus from Iles Kerguelen. Antarct Sci 23:3–17

    Article  Google Scholar 

  • Nageswara Rao I, Ratna Kumari R (2002) Biochemical composition of zooplankton from Visakhapatnam harbour waters, east coast of India. Indian J Mar Sci 31:125–129

    Google Scholar 

  • Pakhomov EA, Perissinotto R, McQuaid CD (1996) Prey composition and daily rations of myctophid fishes in the Southern Ocean. Mar Ecol Prog Ser 134:1–14

    Article  Google Scholar 

  • Park YH, Durand I, Kestenare E, Rougier G, Zhou M, d’Ovidio F, Cotté C, Lee JH (2014) Polar Front around the Kerguelen Islands: An up-to-date determination and associated circulation of surface/subsurface waters. J Geophys Res Oceans 119:6575–6592

    Article  Google Scholar 

  • Pauthenet E, Roquet F, Madec G, Guinet C, Hindell M, McMahon CR, Harcourt R, Nerini D (2018) Seasonal meandering of the Polar Front upstream of the Kerguelen plateau. Geophys Res Lett. https://doi.org/10.1029/2018GL079614

    Article  Google Scholar 

  • Percy JA, Fife FJ (1981) The biochemical composition and energy content of Arctic marine macrozooplankton. Arctic 34:307–313

    Article  Google Scholar 

  • Postel L, Fock H, Hagen W (2000) Biomass and abundance. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic, San Diego, pp 82–192

    Google Scholar 

  • Pruvost P, Duhamel G, Palomares MLD (2005) An ecosystem model of the Kerguelen Islands’EEZ. In: Palomares MLD, Pruvost P, Pitcher TJ, Pauly D (eds) Modeling Antarctic marine ecosystems. Fisheries Centre Research Reports, 13(7). Fisheries Centre, University of British Columbia, Vancouver, pp 40–46

  • Raymont JEG, Srinivasagam RT, Raymont JKB (1971) The biochemical composition of Euphausia superba. J Mar Biol Assoc UK 51:581–588

    Article  CAS  Google Scholar 

  • Reinhardt SB, VanVleet ES (1986) Lipid composition of twenty-two species of Antarctic midwater zooplankton and fish. Mar Biol 91:149–159

    Article  CAS  Google Scholar 

  • Richoux N (2011) Trophic ecology of zooplankton at a frontal transition zone: fatty acid signatures at the subtropical convergence, Southern Ocean. J Plankton Res 33:491–505

    Article  Google Scholar 

  • Ridoux V (1994) The diets and dietary segregation of seabirds at the subantarctic Crozet Islands. Mar Ornithol 22:1–192

    Google Scholar 

  • Salonen K, Sarvala J, Hakala I, Viljanen ML (1976) The relation of energy to organic carbon in aquatic invertebrates. Limnol Oceanogr 21:724–730

    Article  CAS  Google Scholar 

  • Schmidt K, Atkinson A (2016) Feeding and food processing in Antarctic krill (Euphausia superba Dana). In: Siegel V (ed) Biology and Ecology of Antarctic krill, Euphausia superba Dana 1850. Springer, Cham, pp 175–224

    Google Scholar 

  • Schmidt K, Atkinson A, Pond DW, Ireland LC (2014) Feeding and overwintering of Antarctic krill across its major habitats: The role of sea ice cover, water depth, and phytoplankton abundance. Limnol Oceanogr 59:17–36

    Article  Google Scholar 

  • Sogawa S, Sugisaki H, Tadokoro K, Ono T, Sato E, Shimode S, Kikuchi T (2017) Feeding habits of six species of euphausiids (Decapoda: Euphausiacea) in the northwestern Pacific Ocean determined by carbon and nitrogen stable isotope ratios. J Crust Biol 37:29–36

    Article  Google Scholar 

  • Torres JJ, Donnelly J, Hopkins TL, Lancraft TM, Aarset AV, Ainley DG (1994) Proximate composition and overwintering strategies of Antarctic micronektonic Crustacea. Mar Ecol Prog Ser 113:221–232

    Article  Google Scholar 

  • Travers-Trolet M, Shin YJ, Jennings S, Cury P (2007) Towards end-to-end models for investigating the effects of climate and fishing in marine ecosystems. Prog Oceanogr 75:751–770

    Article  Google Scholar 

  • Trull TW, Davies DM, Dehairs F, Cavagna AJ, Lasbleiz M, Laurenceau-Cornec EC, d’Ovidio F, Planchon F, Leblanc K, Quéguiner B, Blain S (2015) Chemometric perspectives on plankton community responses to natural iron fertilization over and downstream of the Kerguelen Plateau in the Southern Ocean. Biogeosciences 12:1029–1056

    Article  CAS  Google Scholar 

  • Waluda CM, Hill SL, Peat HJ, Trathan PN (2012) Diet variability and reproductive performance of macaroni penguins Eudyptes chrysolophus at Bird Island, South Georgia. Mar Ecol Prog Ser 466:261–274

    Article  Google Scholar 

  • Ward P, Shreeve RS, Cripps GC (1996) Rhincalanus gigas and Calanus simillimus: lipid storage patterns of two species of copepod in the seasonally ice-free zone of the Southern Ocean. J Plankton Res 18:1439–1454

    Article  Google Scholar 

  • Woodson CB, Litvin SY (2014) Ocean fronts drive marine fishery production and biogeochemical cycling. Proc Natl Acad Sci USA 112:1710–1715

    Article  CAS  Google Scholar 

  • Yebra L, Kobari T, Sastri AR, Gusmão F, Hernández-León S (2017) Advances in biochemical indices of zooplankton production. Adv Mar Biol 76:157–240

    Article  PubMed  CAS  Google Scholar 

  • Yun MS, Lee DB, Kim BK, Kang JJ, Lee JH, Yang EJ, Park WG, Chung KH, Lee SH (2015) Comparison of phytoplankton macromolecular compositions and zooplankton proximate compositions in the northern Chukchi Sea. Deep Sea Res Pt II 120:82–90

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank S. Blain, project coordinator, B. Quéguiner chief scientist on board, and Captain B. Lassiette and the crew of the R/V Marion Dufresnes. Special thanks are due to M.P. Jouandet for her help in sample collection, M.F. Fontaine for biochemical analyzes, to L. Guillou and P. Richard (LIENSs Laboratory, La Rochelle University) for C and N analyzes, and to M. Paul, a native English speaker, for English correction. This work was supported by the French Research program of INSU-CNRS LEFE – CYBER (“Les enveloppes fluides et l’environnement-Cycles biogéochimiques, environnement et resources”), the French ANR (Agence Nationale de la Recherche, ANR-10-BLAN-0614 of SIMI-6 program, and ANR-09-CEXC-006–01 to M. Zhou and F. Carlotti), LABEX OT-MED (No. ANR-11-LABX-0061), the French CNES (Centre National d’Etudes Spatiales) and the French Polar Institute IPEV (Insitut Polaire Paul-Emile Victor). The project leading to this publication has received funding from European FEDER Fund under Project 1166-39417. Many thanks are addressed to the three reviewers for their constructive and helpful comments on an earlier version of the manuscript.

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  1. Aix Marseille Université, Université de Toulon, CNRS, IRD, Mediterranean Institute of Oceanography (MIO), UM 110, 13288, Marseille Cedex 09, France

    Mireille Harmelin-Vivien, Daniela Bӑnaru, Mélanie Ourgaud & François Carlotti

  2. UMR BOREA, CNRS 7208-MNHN-Sorbonne Université-UCN-IRD 207-UA, Laboratoire D’Excellence « CORAIL », Université Des Antilles, 97157, Pointe-à-Pitre, Guadeloupe

    Charlotte R. Dromard

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  1. Mireille Harmelin-Vivien
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Harmelin-Vivien, M., Bӑnaru, D., Dromard, C.R. et al. Biochemical composition and energy content of size-fractionated zooplankton east of the Kerguelen Islands. Polar Biol 42, 603–617 (2019). https://doi.org/10.1007/s00300-019-02458-8

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