Skip to main content
SpringerLink
Log in

Using stable isotopes to assess carbon and nitrogen turnover in the Arctic sympagic amphipod Onisimus litoralis

  • Physiological Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Food web studies based on stable C and N isotope ratios usually assume isotopic equilibrium between a consumer and its diet. In the Arctic, strong seasonality in food availability often leads to diet switching, resulting in a consumer’s isotopic composition to be in flux between different food sources. Experimental work investigating the time course and dynamics of isotopic change in Arctic fauna has been lacking, although these data are crucial for accurate interpretation of food web relationships. We investigated seasonal (ice-covered spring vs. ice-free summer) and temperature (1 vs. 4°C) effects on growth and stable C and N isotopic change in the common nearshore Arctic amphipod Onisimus litoralis following a diet switch and while fasting in the laboratory. In spring we found no significant temperature effect on N turnover [half-life (HL) estimates: HL-N = 20.4 at 4°C, 22.4 days at 1°C] and a nonsignificant trend for faster growth and C turnover at the higher temperature (HL-C = 13.9 at 4°C, 18.7 days at 1°C). A strong seasonal effect was found, with significantly slower growth and C and N turnover in the ice-free summer period (HL-N = 115.5 days, HL-C = 77.0 days). Contrary to previous studies, metabolic processes rather than growth accounted for most of the change in C and N isotopic composition (84–89 and 67–77%, respectively). This study provides the first isotopic change and metabolic turnover rates for an Arctic marine invertebrate and demonstrates the risk of generalizing turnover rates based on taxon, physiology, and environment. Our results highlight the importance of experimental work to determine turnover rates for species of interest.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–h
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arndt CE, Beuchel F (2006) Life history and population dynamics of the Arctic sympagic amphipods Onisimus nanseni Sars and O. glacialis Sars (Gammaridea: Lysianassidae). Polar Biol 29:239–248

    Article  Google Scholar 

  • Attkinson A, Meyer B, Stübing D, Hagen W, Schmidt K, Bathmann UV (2002) Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter. II. Juveniles and adults. Mar Ecol Prog Ser 160:63–76

    Article  Google Scholar 

  • Bluhm BA, Gradinger R (2008) Regional variability in food availability for Arctic marine mammals. Ecol Appl 18[Suppl]:77–96

    Article  Google Scholar 

  • Bosley KL, Witting DA, Chambers RC, Wainright SC (2002) Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Mar Ecol Prog Ser 236:233–240

    Article  Google Scholar 

  • Boudrias MA, Carey AG Jr (1988) Life history patterns of Pseudolibrotus litoralis (Crustacea: Amphipoda) on the inner continental shelf, SW Beaufort Sea. Mar Ecol Prog Ser 49:249–257

    Article  Google Scholar 

  • Bradstreet SW, Cross WE (1982) Trophic relationships at high ice edges. Arctic 35:1–12

    Google Scholar 

  • Carey AG Jr (1992) The ice fauna in the shallow southwestern Beaufort Sea, Arctic Ocean. J Mar Syst 3:225–236

    Article  Google Scholar 

  • Carey AG Jr, Boudrias MA (1987) Feeding ecology of Pseudolibrotus (=Onisimus) litoralis Kröyer (Crustacea: Amphipoda) on the Beaufort Sea inner continental shelf. Polar Biol 8:29–33

    Article  Google Scholar 

  • Chapelle G, Peck LS (1995) The influence of acclimation and substratum on the metabolism of the Antarctic amphipods Waldeckia obesa (Chevreux 1905) and Bovallia gigantea (Pfeffer 1888). Polar Biol 15:225–232

    Article  Google Scholar 

  • Collie JS (1985) Life history and production of three amphipod species on Georges Bank. Mar Ecol Prog Ser 22:229–238

    Article  Google Scholar 

  • Dower KM, Lucas MI, Phillips R, Dieckmann G, Robinson DH (1996) Phytoplankton biomass, P–I relationships and primary production in the Weddell Sea, Antarctica, during the austral autumn. Polar Biol 16:41–52

    Google Scholar 

  • Frazer TK (1996) Stable isotopes composition (δ13C and δ15N) of larval krill, Euphausia superba, and two of its potential food sources in winter. J Plankton Res 18:1413–1426

    Article  CAS  Google Scholar 

  • Frazer TK, Ross RM, Quentin LB, Montoya JP (1997) Turnover of carbon and nitrogen during growth of larval krill, Euphausia superba Dana: a stable isotope approach. J Exp. Mar Biol Ecol 212:259–257

    Article  Google Scholar 

  • Fry B, Arnold C (1982) Rapid 13C/12C turnover during growth of brown shrimp (Panaeus aztecus). Oecologia 54:200–204

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gorokhova E, Hansson S (1999) An experimental study on variations in stable carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Can J Fish Aquat Sci 56:2203–2210

    Article  Google Scholar 

  • Gradinger RR (2002) Sea ice microorganisms. In: Bitten G (ed) Encyclopedia of environmental microbiology. Wiley, Hoboken, N.J., pp 2833–2844

    Google Scholar 

  • Gradinger R (2008) Sea ice algae: major contributors to primary production and algal biomass in the Chukchi and Beaufort Sea. Deep Sea Res (in press)

  • Gradinger RR, Bluhm BA (2004) In situ observations on the distribution and behavior of amphipods and Arctic cod (Boreogadus saida) under the sea ice of the high Arctic Canadian Basin. Polar Biol 27:595–603

    Article  Google Scholar 

  • Gradinger RR, Bluhm BA (2005) Susceptibility of sea ice biota to disturbances in the shallow Beaufort Sea. Phase 1: Biological coupling of sea ice with the pelagic and benthic realms. Final report, OCS Study MMS 2005–062

  • Graeve M, Kattner G, Piepenburg D (1997) Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol 18:53–61

    Article  Google Scholar 

  • Haddon M (2001) Modeling and quantitative methods in fisheries. Chapman and Hall, Boca Raton

    Google Scholar 

  • Herzka SZ, Holt JG (2000) Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Can J Fish Aquat Sci 57:137–147

    Article  Google Scholar 

  • Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulfur, carbon and nitrogen in tissue of the growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C and δ15N. Can J Fish Aquat Sci 50:2071–2076

    Article  CAS  Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188

    Article  Google Scholar 

  • Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using delta-13°C and delta-15 N analysis. Mar Ecol Prog Ser 84:9–18

    Article  CAS  Google Scholar 

  • Hobson KA, Alisauskas RT, Clark RG (1993) Stable isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analysis of diet. Condor 95:388–394

    Article  Google Scholar 

  • Hochachka P, Somero G (2002) Biochemical adaptation, mechanism and physical evolution. Oxford University Press, New York

    Google Scholar 

  • Horner RS, Ackley F, Dieckmann GS, Gulliksen B, Hoshiai T, Legendre L, Melnikov IA, Reeburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota, 1: Habitat, terminology, and methodology. Polar Biol 12:417–427

    Article  Google Scholar 

  • Horner R (1985) Sea ice biota. CRC, Boca Raton

    Google Scholar 

  • Iken K, Bluhm BA, Gradinger R (2005) Food web structure in the high Arctic Canada Basin: evidence from δ13C and δ15N analysis. Polar Biol 28:238–249

    Article  Google Scholar 

  • Jardine TD, MacLatchy DL, Fairchild WL, Cunjak RA, Brown SB (2004) Rapid carbon turnover during growth of Atlantic Salmon (Salmo salar) smolts in sea water, and evidence for reduced food consumption by growth-stunts. Hydrobiologia 527:63–73

    Article  Google Scholar 

  • Lovvorn JR, Cooper LW, Brooks ML, De Ruyck CC, Bump JK, Grebmeier JM (2005) Organic matter pathways to zooplankton and benthos under pack ice in late winter and open water in late summer in the north-central Bering Sea. Mar Ecol Prog Ser 291:135–150

    Article  CAS  Google Scholar 

  • MacAvoy SE, Macko SA, Garman GC (2001) Isotopic turnover in aquatic predators: quantifying the exploitation of migratory prey. Can J Fish Aquat Sci 58:923–932

    Article  CAS  Google Scholar 

  • MacAvoy SE, Macko SA, Arneson LS (2005) Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can J Zool 83:631–641

    Article  CAS  Google Scholar 

  • Maruyama M, Yamada Y, Rusuwa B, Yuma M (2001) Change in stable nitrogen isotope ratio in the muscle tissue of a migratory goby, Rhinogobius sp., in a natural setting. Can J Fish Aquat Sci 58:2125–2128

    Article  Google Scholar 

  • McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • McIntyre PB, Flecker AS (2006) Rapid turnover of tissue nitrogen in primary consumers in tropical freshwaters. Oecologia 148:12–21

    Article  PubMed  Google Scholar 

  • McMahon KW, Ambrose WG, Johnson BJ, Sun M, Lopez GR, Clough LM, Carroll ML (2006) Benthic community response to ice algae and phytoplankton in Ny Alesund, Svalbard. Mar Ecol Prog Ser 310:1–14

    Article  Google Scholar 

  • McWhinnie MA (1964) Temperature responses and tissue respiration in Antarctic crustacea with particular reference to the krill, Euphaasia superba. Antarct Res Ser 1:63–72

    Google Scholar 

  • Peck L (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40

    Article  Google Scholar 

  • Percy JA (1993) Energy consumption and metabolism during starvation in the Arctic hyperiid amphipod Themisto libellula. Polar Biol 13:549–555

    Google Scholar 

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

    Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Rakusa-Suszczewski S (1972) The biology of Paramoera walkeri Stebbing (amphipoda) and the antarctic sub-fast ice community. Polar Arch Hydrobiol 19:11–36

    Google Scholar 

  • Robertson RF, El-Haj AJ, Peck LS, Taylor EW (2001) The effects of temperature on metabolic rate and protein synthesis following a meal in the isopod Glyptonotus antarcticus Eights (1852). Polar Biol 24:677–686

    Google Scholar 

  • Sainte-Marie B (1986) Foraging by lysianassid amphipods. PhD thesis, Dalhousie University, Halifax

  • Sainte-Marie B, Percy JA, Shea JR (1989) A comparison of meal size and feeding rate of the lysianassid amphipods Anonyx nugax, Onisimus (= Pseudalibrotus) litoralis and Orchomenella pinguis. Mar Biol 102:361–368

    Article  Google Scholar 

  • Sakano H, Fujiwara E, Nohara S, Ueda H (2005) Estimation of nitrogen stable isotope turnover rate of Onchorynchus nerka. Environ Biol Fishes 72:13–18

    Article  Google Scholar 

  • Sakshaug E (2004) Primary and secondary production in the Arctic seas. In: Stein R, Macdonald RW (eds) The organic carbon cycle in the Arctic Ocean. Springer, New York, pp 57–81

    Google Scholar 

  • 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

    Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can J Fish Aquat Sci 62:671–678

    Google Scholar 

  • Tamelander T, Renaud PE, Hop H, Carroll ML, Ambrose WG, Hobson KA (2006) Trophic relationships and pelagic–benthic coupling during summer in the Barents Sea marginal ice zone, revealed by stable carbon and nitrogen isotope measurements. Mar Ecol Prog Ser 310:33–46

    Article  CAS  Google Scholar 

  • Tieszen LL, Boutton TW, TeSDahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37

    Article  Google Scholar 

  • Tominaga O, Ono N, Seikai T (2003) Influence of diet shift from formulated feed to live mysids on the carbon and nitrogen stable isotope ratio (δ13C and δ15N) in dorsal muscles of juvenile Japanese flounders, Paralichthys olivaceus. Aquaculture 218:265–276

    Google Scholar 

  • Weingartner TJ, Okkonen SR, Danielson SL (2005) Circulation and water property variations in the nearshore Alaskan Beaufort Sea. Final report. OCS study MMS 2005–028

  • Werner I (2000) Faecal pellet production by Arctic under-ice amphipods—transfer of organic matter through the ice/water interface. Hydrobiologia 426:89–96

    Article  CAS  Google Scholar 

  • Werner I, Auel H (2005) Seasonal variability in abundance, respiration and lipid composition of under ice amphipods. Mar Ecol Prog Ser 292:251–262

    Article  Google Scholar 

  • Witting DA, Chambers RC, Bosley KL, Wainright SC (2004) Experimental evaluation of ontogenetic diet transitions in summer flounder (Paralichthys dentatus), using stable isotopes as diet tracers. Can J Aquat Sci 61:2069–2084

    Article  CAS  Google Scholar 

  • Yokoyama H, Tamaki A, Harada K, Shimoda K, Koyama K, Ishihi K (2005) Variability of diet-tissue isotopic fractionation in estuarine macrobenthos. Mar Ecol Prog Ser 296:115–128

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This publication is the result of research sponsored by Alaska Sea Grant with funds from the National Oceanic and Atmospheric Administration Office of Sea Grant, Department of Commerce under grant no. NA 16RG2321 (project no. R/101-04) and from the University of Alaska with funds appropriated by the state. Additional funding was provided by the Center for Global Change. We want to thank S. Sugai for her special attention and interest in the successful completion of this project. We are grateful to the staff of the Barrow Arctic Science Consortium who greatly simplified field logistics and to S. Story, S. Lee, K. Meiners, and M. Kaufman for their field assistance. T. Howe and N. Haubenstock at the Alaska Stable Isotope Facility analyzed the many stable isotope samples collected for this research. We also want to thank the School of Fisheries and Ocean Sciences and its office staff, with special thanks to C. Neumann, for their support and assistance. M. Castellini and M. Wooller are thanked for their very helpful suggestions and valuable contributions to the Master’s thesis by M. Nielson-Kaufman, which is the basis for this manuscript. The experiments conducted during this study were in compliance with current United States laws governing ethical conduct and the care and use of animals in research.

Author information

Authors and Affiliations

  1. School of Fisheries and Ocean Sciences, University of Alaska, Fairbanks, 245 O’Neill Building, Fairbanks, AK, 99775, USA

    Mette R. Kaufman, Rolf R. Gradinger & Bodil A. Bluhm

  2. Institute of Arctic Biology, University of Alaska, Fairbanks, 902 North Koyukuk Drive, Fairbanks, AK, 99775, USA

    Diane M. O’Brien

Authors
  1. Mette R. Kaufman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rolf R. Gradinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bodil A. Bluhm
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Diane M. O’Brien
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mette R. Kaufman.

Additional information

Communicated by Marc Mangel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaufman, M.R., Gradinger, R.R., Bluhm, B.A. et al. Using stable isotopes to assess carbon and nitrogen turnover in the Arctic sympagic amphipod Onisimus litoralis . Oecologia 158, 11–22 (2008). https://doi.org/10.1007/s00442-008-1122-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1122-y

Keywords

Search

Navigation