[en] The discrepancy between the ecological significance of amphipods in the Antarctic and our poor knowledge of their ecofunctional role calls for a more detailed investigation of their trophic status in this ecosystem. A total of 12 amphipod species from suspension feeder to scavenger have been considered in this study. Our objective was to investigate whether the combination of fatty-acid and stable-isotope signatures into a 2-dimensional trophic biomarker assay would increase accuracy in the identification of Antarctic benthic amphipod trophic position. Amphipod isotopic averages ranged from -29.3 parts per thousand (delta(13)C) and 4.1 parts per thousand (delta(15)N) for the suspension feeder Ampelisca richardsoni to -21.7 parts per thousand (delta(13)C) and 11.9 parts per thousand (delta(15)N) for the high predator Iphimediella sp. Cluster analysis of the fatty-acid composition separated the amphipod species into 4 trophic groups: suspension feeders, macroherbivores, omnivores and scavengers. The suspension feeder was isolated due to an important proportion of 18:4(n-3), a fatty-acid biomarker of phytoplankton. Macro-herbivores were found to rely heavily on macroalgal carbon, containing a high percentage of arachidonic acid (20:4(n-6)). Scavenger amphipods revealed a unique fatty-acid composition dominated by 1 single fatty acid, 18:1(n-9), probably the result of a very intensive de novo biosynthesis to cope with starvation periods. Our data emphasise the need to combine different types of information to be able to draw the right conclusions regarding trophic ecology. Indeed, in some cases, the exclusive use of 1 type of tracing method, fatty acids or stable isotopes, would have resulted in misleading/false conclusions in the trophic classification of amphipods. Therefore, a 2-dimensional biomarker assay is a useful tool to elucidate the trophic positions of benthic amphipods.
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture SSTC - Services Fédéraux des Affaires Scientifiques, Techniques et Culturelles
Adams TS, Sterner RW (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45:601-607
Albers CS, Kattner G, Hagen W (1996) The compositions of wax esters, triacylglycerols and phospholipids in Arctic and Antarctic copepods: evidence of energetic adaptations. Mar Chem 55:347-358
Auel H, Harjes M, da Rocha R, Stübing D, Hagen W (2002) Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biol 25:374-383
Bell MV, Sargent JR (1985) Fatty acid analyses of phosphoglycerides from tissues of the clam Chlamys islandica (Muller) and the starfish Ctenodiscus crispatus (Retzius) from Balsfjorden, northern Norway. J Exp Mar Biol Ecol 87:31-40
Burns JM, Trumble SJ, Castellini MA, Testa JW (1998) The diet of the Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol 19:272-282
Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis: an interpretation. Plymouth Marine Laboratory, Plymouth
Cook EJ, Bell MV, Black KD, Kelly MS (2000) Fatty acid compositions of gonadal material and diets of the sea urchin, Psammechinus miliaris: trophic and nutritional implications. J Exp Mar Biol Ecol 255:261-274
Dalsgaard J, St John M, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225-340
Dauby P, Scailteur Y, Chapelle G, De Broyer C (2001a) Impact of the main benthic amphipod species populations on the eastern Weddell Sea shelf ecosystem. Polar Biol 24:657-662
Dauby P, Scailteur Y, De Broyer C (2001b) Trophic diversity within eastern Weddell Sea amphipod community. Hydrobiologia 443:69-86
Dauby P, Nyssen F, De Broyer C (2003) Amphipods as food sources for higher trophic levels in the Southern Ocean: a synthesis. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys Publ, Leiden, p 129-134
De Broyer C, Jazdzewski K (1996) Biodiversity of the Southern Ocean: towards a new synthesis for the Amphipoda (Crustacea). Boll Mus Civ Stor Nat Verona 20:547-568
De Broyer C, Rauschert M, Scailteur Y (1999) Structural and ecofunctional biodiversity of the benthic amphipod taxocoenoses In: Arntz W, Gutt J (eds) The expedition ANTARKTIS XV/3 (EASIZ II) of 'Polarstern' in 1998. Ber Polarforsch 301:163-174
De Broyer C, Scailteur Y, Chapelle G, Rauschert M (2001) Diversity of epibenthic habitats of gammaridean amphipods in the eastern Weddell Sea. Polar Biol 24:744-753
De Broyer C, Dauby P, Nyssen F, Martin P (2003a) Biodiversity, molecular phylogeny and trophodynamics of amphipod crustaceans in the Antarctic deep-sea. In: Fütterer DK, Brandt A, Poore GCB (eds) ANDEEP I and II: ANtarctic benthic DEEP-sea biodiversity - colonization history and recent community patterns. Ber Polarforsch 470:81-85
De Broyer C, Jazdzewski K, Dauby P (2003b) Biodiversity of the Southern Ocean: lessons from Crustacea. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys Publ, Leiden, p 201-214
DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261-263
DeNiro MJ, Epstein S (1978) Influence of the diet on the distribution of the carbon isotopes in animals. Geochim Cosmochim Acta 42:495-506
DeNiro MJ, Epstein S (1981) Influence of the diet on the distribution of the nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341-351
Dunton KH (2001) δ15N and δ13C measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41:99-112
Falk-Petersen S, Hopkins CCE, Sargent JR (1990) Trophic relationships in the pelagic arctic food web. In: Barnes M, Gibson RN (eds) Trophic relationships in the marine environment. Proc 24th Eur Mar Biol Symp. Aberdeen University Press, Aberdeen, p 315-333
Fantle MS, Dittel AI, Schwalm SM, Epifiano CE, Fogel ML (1999) A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120:416-426
Folch J, Lees N, Sloan-Stanley GH (1957) A simple method for the isolation and purification of total lipids. J Biol Chem 226:497-509
Fullarton JG, Dando PR, Sargent JR, Southward AJ, Southward EC (1995) Fatty acid of hydrothermal vent Ridgeia piscesae and inshore bivalves containing symbiotic bacteria. J Mar Biol Assoc UK 75:455-468
Gannes LZ, O'Brien DM, del Rio CM (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271-1276
Graeve M (1993) Umsatz und Verteilung von Lipiden in arktischen marinen Organismen unter besonderer Berücksichtigung unterer trophischer Stufen. Rep Polar Res 124:1-141
Graeve M, Kattner G, Hagen W (1994a) Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: experimental evidence of trophic markers. J Exp Mar Biol Ecol 182:97-110
Graeve M, Hagen W, Kattner G (1994b) Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods. Deep-Sea Res 41:915-924
Graeve M, Kattner G, Piepenburg D (1997) Lipids in Arctic benthos: Does fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol 18:53-61
Graeve M, Dauby P, Scailteur Y (2001) Combined lipid, fatty acid and digestive tract content analyses: a penetrating approach to estimate feeding modes of Antarctic amphipods. Polar Biol 24:853-862
Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicators for phylogenetic and trophic relationships. Mar Ecol Prog Ser 231:67-74
Gutt J, Sirenko BI, Arntz W, Smirnov I, De Broyer C (2000) Biodiversity of the Weddell Sea: macrozoobenthic species (demersal fish included) sampled during the expedition ANT XIII/3 (EASIZ I) with RV 'Polarstern'. Ber Polarforsch 372:1-103
Hagen W (1988) On the significance of lipids in Antarctic zooplankton. Ber Polarforsch 49:1-117
Hagen W, Kattner G (1998) Lipid metabolism of the Antarctic euphausiid Thysanoessa macrura and its ecological implications. Limnol Oceanogr 43:1894-1901
Hagen W, Kattner G, Graeve M (1993) Calanoides acutus and Calanus propinquus, Antarctic copepods with different lipid storage modes via wax esters or triacylglycerols. Mar Ecol Prog Ser 97:135-142
Hagen W, Kattner G, Friedrich C (2000) The lipid compositions of five Antarctic fish species with different life strategies. Polar Biol 23:785-791
Harrington GW, Beach DH, Dunham JE, Holz GG (1970) The polyunsaturated fatty acids of dinoflagellates. J Protozool 17:213-219
Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9-18
Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388-394
Hobson KA, Ambrose WG Jr, Renaud PE (1995) Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13C and δ15N analysis. Mar Ecol Prog Ser 128:1-10
Hobson KA, Schell D, Renouf D, Noseworthy E (1996) Stable-carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528-533
Hobson KA, Sease JL, Merrick RL, Piatt JF (1997) Investigating trophic relationships of pinnipeds in Alaska and Washington using stable isotope ratios of nitrogen and carbon. Mar Mamm Sci 13:114-132
Howell KL, Pond DW, Billett DSM, Tyler PA (2003) Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty-acid biomarker approach. Mar Ecol Prog Ser 255:193-206
Iverson SJ, Frost KJ, Lang SLC (2002) Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Mar Ecol Prog Ser 241:161-181
Jarre-Teichmann A, Brey T, Bathmann UV, Dahm C and 8 others (1997) Trophic flows in the benthic communities of the eastern Weddell Sea, Antarctica. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. University Press, Cambridge, p 118-134
Jazdzewski K, Weslawski JM, De Broyer C (1996) A comparison of the amphipod faunal diversity in two polar fjords: Admiralty Bay, King George Island (Antarctic) and Hornsund, Spitsbergen (Arctic). Pol Arch Hydrobiol 42:367-384
Kattner G, Fricke HSG (1986) Simple gas-liquid chromatographic method for the simultaneous determination of fatty acids and alcohol in wax esters of marine organisms. J Chromatogr 361:263-268
Kattner G, Graeve M, Hagen W (1994) Ontogenetic and seasonal changes in lipid and fatty acid/alcohol compositions of the dominant Antarctic copepods Calanus propinquus, Calanoides acutus and Rhincalanus gigas. Mar Biol 118:637-644
Kayama M, Araki S, Sato S (1989) Lipids of marine plants. In: Ackman RG (ed) Marine biogenic lipids, fats and oils, Vol 2. CRC Press, Boca Raton, FL, p 3-48
Kharlamenko VI, Kiyashko SI, Imbs AB, Vyshkvartzev (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Mar Ecol Prog Ser 220:103-117
Klages M (1991) Biologische und populationsdynamische Untersuchungen an ausgewählten Gammariden (Crustacea: Amphipoda) des südöstlichen Weddellmeeres, Antarktis. PhD thesis, University of Bremen
Lee RF, Nevenzel JC, Paffenhöfer GA (1971) Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Mar Biol 9:99-108
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136:513-518
Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic foodwebs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental sciences. Blackwell Science, London, p 138-157
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135-1140
Nelson MM, Mooney BD, Nichols PD, Phleger CF (2001) Lipids of Antarctic Ocean amphipods: food chain interactions and the occurrence of novel biomarkers. Mar Chem 73:53-64
Nichols PD, Skerratt JH, Davidson A, Burton H, McMeekin TA (1991) Lipids of cultured Phaeocystis pouchetii: signatures for food-web, biogeochemical and environmental studies in Antarctica and the Southern Ocean. Phytochemistry 30:3209-3214
Nyssen F, Brey T, Lepoint G, Bouquegneau JM, De Broyer C, Dauby P (2002) A stable isotope approach to the eastern Weddell Sea trophic web: focus on benthic amphipods. Polar Biol 25:280-287
Peterson BJ, Fry B (1987) Stable isotopes in ecosystems studies. Annu Rev Ecol Syst 18:293-320
Phleger CF, Nichols PD, Virtue P (1998) Lipids and trophodynamics of Antarctic zooplankton. Comp Biochem Physiol 120B:311-323
Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fishes tissues: implications for the study of trophic relationships. Funct Ecol 13:225-231
Rau GH, Hopkins TL, Torres JJ (1991a) 15N/14N and 13C/12C in Weddell Sea invertebrates: implications for feeding diversity. Mar Ecol Prog Ser 77:1-6
Rau GH, Sullivan CW, Gordon LJ (1991b) δ13C and δ15N variations in Weddell Sea particulate organic matter. Mar Chem 35:355-369
Rau GH, Ainley DG, Bengston JL, Torres JJ, Hopkins TL (1992) 15N/14N and 13C/12C in Weddell Sea birds, seals and fish: implications for diet and trophic structure. Mar Ecol Prog Ser 84:1-8
Reinhardt SB, Van Vleet ES (1986) Lipid composition of twenty-two species of Antarctic midwater zooplankton and fishes. Mar Biol 91:149-159
Sargent JR (1976) The structure, metabolism and function of lipids in marine organisms. In: Malins DC, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology. Academic Press, New York, p 149-212
Sargent JR, Henderson RJ (1986) Lipids. In: Corner EDS, O'Hara S (eds) Biological chemistry of marine copepods. Oxford University Press, Oxford, p 59-108
Sargent JR, Whittle KJ (1981) Lipids and hydrocarbons in the marine food web. In: Longhurst A (ed) Analysis of marine ecosystems. Academic Press, London, p 491-533
Scherrer B (1984) Biostatistiques. Gaétan Morin, Québec
Schmidt K, Atkinson A, Stübing D, McClelland JW, Montoya JP, Voss M (2003) Trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnol Oceanogr 48:277-289
Swadling KM, Nichols PD, Gibson JAE, Ritz DA (2000) Role of lipid in the life cycles of ice-dependent and ice-independent populations of the copepod Paralabidocera antarctica. Mar Ecol Prog Ser 208:171182
Tieszen LL, Boutton TW, Tesdahl KG, Slade NH (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for 13C analysis of diet. Oecologia 57:32-37
Ulanowicz RE (2000) Growth and development: ecosystems phenomenology. Excel Press, San Jose
Wada E, Terazaki M, Kabaya Y, Nemoto T (1987) 15N and 13C abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Res 34:829-841
