Marine Biology

, Volume 156, Issue 6, pp 1241–1253

Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia

Original Paper

Abstract

Muscle tissue was collected for stable isotope analysis (SIA) from the main fish predators and their fish and cephalopod prey from oceanic waters off eastern Australia between 2004 and 2006. SIA of δ15N and δ13C revealed that the species examined could be divided into three main trophic groups. A “top predator” group consisted mainly of large billfish (Xiphias gladius and Tetrapturus audax), yellowfin (Thunnus albacares), bigeye (T. obesus) and southern bluefin (T. maccoyii) tunas and sharks; with mako (Isurus oxyrinchus) the highest. Below this tier was a second group composed of mid-trophic level fishes including albacore tuna (Thunnus alalunga), lancet fish (Alepisaurus ferox), mahi mahi (Coryphaena hippuris) and ommastrephid squid. Underlying both groups was a grouping of small fishes including myctophids, small scombrids and nomeids as well as surface fishes including macrorhamphosids. These groupings were based largely on mean animal size which showed a positive linear relation to δ15N (r2 = 0.58). Some species showed significant ontogenetic variation in either δ15N (swordfish, lancet fish, yellowfin and albacore tuna) or δ13C (mako shark). We also noted a consistent latitudinal change in δ15N and δ13C at ~28°S for the top predator species, particularly albacore and yellowfin tuna. The differences were consistent with a change from oligotrophic Coral Sea to nutrient rich Tasman Sea waters. These differences suggest that predatory fishes may have extended residence time in distinct regions off eastern Australia.

References

  1. Baird ME, Timko PG, Middleton JH, Mullaney TJ, Cox DR, Suthers IM (2008) Biological properties across the Tasman Front off southeast Australia. Deep Sea Res Part I Oceanogr Res Pap 55:1438–1455. doi:10.1016/j.dsr.2008.06.011 CrossRefGoogle Scholar
  2. Best PB, Schell DM (1996) Stable isotopes in Southern Right Whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Mar Biol (Berl) 124:483–494. doi:10.1007/BF00351030 CrossRefGoogle Scholar
  3. Caraveo-Patino J, Hobson K, Soto L (2007) Feeding ecol gray whales inferred from stable-carbon nitrogen isotopic anal baleen plates. Hydrobiologia 586:17–25CrossRefGoogle Scholar
  4. Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the southern ocean. Mar Ecol Prog Ser 329:281–287. doi:10.3354/meps329281 CrossRefGoogle Scholar
  5. Davenport SR, Bax NJ (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Can J Fish Aquat Sci 59:514–530. doi:10.1139/f02-031 CrossRefGoogle Scholar
  6. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi:10.1016/0016-7037(78)90199-0 CrossRefGoogle Scholar
  7. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. doi:10.1016/0016-7037(81)90244-1 CrossRefGoogle Scholar
  8. Estrada JA, Rice AN, Lutkavage ME, Skomal GB (2003) Predicting trophic position in sharks of the north–west Atlantic Ocean using stable isotope analysis. J Mar Biol Assoc UK 83:1347–1350. doi:10.1017/S0025315403008798 CrossRefGoogle Scholar
  9. Fry B, Quinones RB (1994) Biomass spectra and stable-isotope indicators of trophic level in zooplankton of the northwest Atlantic. Mar Ecol Prog Ser 112:201–204. doi:10.3354/meps112201 CrossRefGoogle Scholar
  10. Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47Google Scholar
  11. Graham BS, Grubbs D, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar Biol (Berl) 150:647–658. doi:10.1007/s00227-006-0360-y CrossRefGoogle Scholar
  12. Hynd JS (1974) Unusual bluefin tuna season in N.S.W. Aust Fish 33(4):9–11Google Scholar
  13. James AG (1988) Are clupeid microphagists herbivorous or omnivorous? A review of the diets of some commercially important clupeids. S Afr J Mar Sci 7:161–177Google Scholar
  14. Jennings S, Pinnegar JK, Polunin NVC, Boon TW (2001) Weak-cross species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. J Anim Ecol 70:934–944. doi:10.1046/j.0021-8790.2001.00552.x CrossRefGoogle Scholar
  15. Jennings S, Warr KJ, Mackinson S (2002) Use of size-based production and stable isotope analyses to predict trophic transfer efficiencies and predator–prey body mass ratios in food webs. Mar Ecol Prog Ser 240:11–20. doi:10.3354/meps240011 CrossRefGoogle Scholar
  16. Kurle CM, Worthy GAJ (2002) Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Mar Ecol Prog Ser 236:289–300. doi:10.3354/meps236289 CrossRefGoogle Scholar
  17. Lansdell M, Young JW (2007) Pelagic cephalopods from eastern Australia: species composition, horizontal and vertical distribution determined from the diets of pelagic fishes. Rev Fish Biol Fish 17:125–138. doi:10.1007/s11160-006-9024-8 CrossRefGoogle Scholar
  18. Lindsay DJ, Minagawa M, Mitani I, Kawaguchi K (1998) Trophic shift in the Japanese anchovy Engraulis japonicus in its early life history stages as detected by stable isotope ratios in Sagami Bay, Central Japan. Fish Sci 64:403–410Google Scholar
  19. MacDonald JS, Waiwood KG, Green RH (1982) Rates of digestion of different prey in Atlantic cod (Gadus morhua), ocean pout (Macrozoarces americanus), winter flounder (Pseudopleuronectes americanus), and American plaice (Hippoglossoides platessoides). Can J Fish Aquat Sci 39:651–659. doi:10.1139/f82-094 CrossRefGoogle Scholar
  20. MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:199–206. doi:10.3354/meps302199 CrossRefGoogle Scholar
  21. MacNeil MA, Drouillard KG, Fisk AT (2006) Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can J Fish Aquat Sci 63:345–353. doi:10.1139/f05-219 CrossRefGoogle Scholar
  22. Mahaffey C, Michaels AF, Capone DG (2005) The conundrum of marine N2 fixation. Am J Sci 305:546–595. doi:10.2475/ajs.305.6-8.546 CrossRefGoogle Scholar
  23. Mcclelland JW, Montoya JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83:2173–2180Google Scholar
  24. McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol (Berl) 53:257–262. doi:10.1007/BF00952434 CrossRefGoogle Scholar
  25. Menard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol (Berl) 153:141–152. doi:10.1007/s00227-007-0789-7 CrossRefGoogle Scholar
  26. Montoya JP, Horrigan SG, McCarthy JJ (1990) Natural abundance of 15N in particulate nitrogen and zooplankton in the Chesapeake Bay. Mar Ecol Prog Ser 65:35–61. doi:10.3354/meps065035 CrossRefGoogle Scholar
  27. Montoya JP, Holl CM, Zehr JP, Hansen A, Villareal TA, Capone DG (2004) High rates of N2 fixation by unicellular diazotrophs in the oligotrophic pacific ocean. Nature 430:1027–1031. doi:10.1038/nature02824 PubMedCrossRefGoogle Scholar
  28. Nichols P, Mooney B, Virtue P, Elliott N (1998) Nutritional value of Australian fish: oil, fatty acid and cholesterol of edible species. Final report, FRDC Project 95/122Google Scholar
  29. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. doi:10.1146/annurev.es.18.110187.001453 CrossRefGoogle Scholar
  30. Pinnegar JK, Polunin NVC (1999) Differential fractionation of 13C and 15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231. doi:10.1046/j.1365-2435.1999.00301.x CrossRefGoogle Scholar
  31. Popp BN, Graham BS, Olson RJ, Hannides CCS, Lott MJ, Lopez-Ibarra GA, Galvan-Magafia F, Fry B (2007) Insight into the trophic ecology of yellowfin tuna Thunnus albacares, from compound specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson TE, Siegwolf R (eds) Stable isotopes as indicators of ecological change. Academic press, ElsevierGoogle Scholar
  32. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  33. Rau GH, Takahashi T, Des Marais DJ (1989) Latitudinal variations in plankton δ13C: implications for CO2 and productivity in past oceans. Nature 341:516–518. doi:10.1038/341516a0 PubMedCrossRefGoogle Scholar
  34. Revelante N, Williams WT, Bunt JS (1982) Temporal and spatial distribution of diatoms, dinoflagellates and Trichodesmium in waters of the Great Barrier Reef. J Exp Mar Biol Ecol 63:27–45. doi:10.1016/0022-0981(82)90048-X CrossRefGoogle Scholar
  35. Sara G, Sara R (2007) Feeding habits and trophic levels of bluefin tuna Thunnus thynnus of different size classes in the Mediterranean Sea. J Appl Ichthyol 23:122–127. doi:10.1111/j.1439-0426.2006.00829.x CrossRefGoogle Scholar
  36. Shingu C (1978) Ecology and stock of Southern Bluefin Tuna. Japan Association of Fishery Resources Protection. Fisheries Study 31 (in Japanese). English translation in: CSIRO Division of Fisheries and Oceanography, Report No. 131 (1981)Google Scholar
  37. Vander Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467. doi:10.1038/46762 CrossRefGoogle Scholar
  38. Worm B, Duffy JE (2003) Biodiversity, productivity and stability in real food webs. Trends Ecol Evol 18:628–632. doi:10.1016/j.tree.2003.09.003 CrossRefGoogle Scholar
  39. Young JW, Lamb TD, Bradford R, Clementson L, Kloser R, Galea H (2001) Yellowfin tuna (Thunnus albacares) aggregations along the shelf break of southeastern Australia: links between inshore and offshore processes. Mar Freshw Res 52:463–474. doi:10.1071/MF99168 CrossRefGoogle Scholar
  40. Young JW, Lansdell MJ, Riddoch S, Revill AT (2006) Feeding ecology of broadbill swordfish, Xiphias gladius, off eastern Australia in relation to physical and environmental variables. Bull Mar Sci 79:793–810Google Scholar
  41. Young JW, Lansdell MJ, Hobday AJ, Dambacher JD, Cooper S, Griffiths SP, Kloser R, Nichols PD, Revill A (2009) Determining ecological effects of longline fishing in the Eastern Tuna and Billfish Fishery. FRDC Final Report 2004/063, pp 310Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Andrew T. Revill
    • 1
  • Jock W. Young
    • 1
  • Matt Lansdell
    • 1
  1. 1.CSIRO Marine and Atmospheric ResearchHobartAustralia

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