Coral Reefs

, Volume 31, Issue 4, pp 1029–1044 | Cite as

Stable isotope analysis reveals community-level variation in fish trophodynamics across a fringing coral reef



In contrast to trophodynamic variations, the marked zonation in physical and biological processes across coral reefs and the concomitant changes in habitat and community structure are well documented. In this study, we demonstrate consistent spatial changes in the community-level trophodynamics of 46 species of fish across the fringing Ningaloo Reef, Western Australia, using tissue stable isotope and fatty acid analyses. Increasing nitrogen (δ15N) and decreasing carbon (δ13C) isotope ratios in the tissues of herbivores, planktivores and carnivores with increasing proximity to the ocean were indicative of increased reliance on oceanic productivity. In contrast, detritivores and corallivores displayed no spatial change in δ15N or δ13C, indicative of the dependence on reef-derived material across the reef. Higher δ13C, as well as increased benthic- and bacterial-specific fatty acids, suggested reliance on reef-derived production increased in back-reef habitats. Genus-level analyses supported community- and trophic group-level trends, with isotope modelling of species from five genera (Abudefduf sexfasciatus, Chromis viridis, Dascyllus spp., Pomacentrus spp. and Stegastes spp.), demonstrating declining access to oceanic zooplankton and, in the case of Pomacentrus spp. and Stegastes spp., a switch to herbivory in the back-reef. The spatial changes in fish trophodynamics suggest that the relative roles of oceanic and reef-derived nutrients warrant more detailed consideration in reef-level community ecology.


Carbon Ningaloo Reef Nitrogen Particulate organic matter Recycling Stable isotope analysis 



F. McGregor and K. Brooks provided valuable sampling assistance. Sample grinding facilities were generously made available by P. Grierson, West Australian Biogeochemistry Centre. Isotope analysis was performed by J. Tranter, Natural Isotopes/Edith Cowan University. Fatty acid analysis was performed by S. Wang, ChemCentre, Perth. Funding was provided by a Natural Environment Research Council Advanced Fellowship (NE/B500690/1) and a grant from the British Ecological Society to SH; grants from The University of Western Australia, the Faculty of Engineering, Computing and Mathematical Sciences and the Western Australian Marine Science Institution (Node 3) to AMW; an Australian Research Council (ARC) Discovery Grant #DP0663670 to AMW et al.; an Australian Coral Reef Society Fellowship to ASJW; and CSIRO Wealth from Oceans funding to AMW and to ASJW. The authors would like to acknowledge the support provided by the Australian-American Fulbright Commission during manuscript preparation in the form of a Fulbright Western Australia Scholarship to ASJW. The manuscript was improved by comments from P. Munday and four anonymous reviewers.

Supplementary material

338_2012_923_MOESM1_ESM.doc (468 kb)
Supplementary material 1 (DOC 467 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46Google Scholar
  2. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  3. Atkinson MJ, Falter JL (2003) Coral reefs. In: Black K, Shimmield G (eds) Biogeochemistry of marine systems. CRC Press, Boca Raton, pp 40–64Google Scholar
  4. Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst 42:411–440CrossRefGoogle Scholar
  5. Carassou L, Kulbicki M, Nicola TJR, Polunin NVC (2008) Assessment of fish trophic status and relationships by stable isotope data in the coral reef lagoon of New Caledonia, southwest Pacific. Aquat Living Resour 21:1–12CrossRefGoogle Scholar
  6. Cocheret de la Moriniere E, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Mar Ecol-Prog Ser 246:279–289CrossRefGoogle Scholar
  7. Cummings DO, Booth DJ, Lee RW, Simpson SJ, Pile AJ (2010) Ontogenetic diet shifts in the reef fish Pseudanthias rubrizonatus from isolated populations on the North-West Shelf of Australia. Mar Ecol-Prog Ser 419:211–222CrossRefGoogle Scholar
  8. Deb D (1997) Trophic uncertainty vs parsimony in food web research. Oikos 78:191–194CrossRefGoogle Scholar
  9. Elsdon TS, Ayvazian S, McMahon KW, Thorrold SR (2010) Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Mar Ecol Prog Ser 408:195–205CrossRefGoogle Scholar
  10. Frederich B, Fabri G, Lepoint G, Vandewalle P, Parmentier E (2009) Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Recif of Toliara, Madagascar. Ichthyol Res 56:10–17CrossRefGoogle Scholar
  11. Friedlander AM, Sandin SA, DeMartini EE, Sala E (2010) Spatial patterns of the structure of reef fish assemblages at a pristine atoll in the central Pacific. Mar Ecol-Prog Ser 410:219–231CrossRefGoogle Scholar
  12. Froese R, Pauly D (2009) FishBase., Accessed: Aug 2009
  13. Fry B, Lutes R, Northam M, Parker PL, Ogden J (1982) A C-13/C-12 comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 14:389–398CrossRefGoogle Scholar
  14. Fry B, Cieri M, Hughes J, Tobias C, Deegan LA, Peterson B (2008) Stable isotope monitoring of benthic-planktonic coupling using salt marsh fish. Mar Ecol-Prog Ser 369:193–204CrossRefGoogle Scholar
  15. Gerber R, Marshall N (1974) Reef pseudoplankton in the lagoon trophic systems. Proc 2nd Int Coral Reef Symp: 105–110Google Scholar
  16. Greenwood NDW, Sweeting CJ, Polunin NVC (2010) Elucidating the trophodynamics of four coral reef fishes of the Solomon Islands using delta N-15 and delta C-13. Coral Reefs 29:785–792CrossRefGoogle Scholar
  17. Grol MGG, Nagelkerken I, Rypel AL, Layman CA (2011) Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish. Oecologia 165:79–88PubMedCrossRefGoogle Scholar
  18. Hammerschlag-Peyer CM, Layman CA (2010) Intrapopulation variation in habitat use by two abundant coastal fish species. Mar Ecol-Prog Ser 415:211–220CrossRefGoogle Scholar
  19. Hamner WM, Jones MS, Carleton JH, Hauri IR, Williams DM (1988) Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Bull Mar Sci 42:459–479Google Scholar
  20. Hamner WM, Colin PL, Hamner PP (2007) Export-import dynamics of zooplankton on a coral reef in Palau. Mar Ecol-Prog Ser 334:83–92CrossRefGoogle Scholar
  21. Hanson CE, Pattiaratchi CB, Waite AM (2005) Sporadic upwelling on a downwelling coast: Phytoplankton responses to spatially variable nutrient dynamics off the Gascoyne region of Western Australia. Cont Shelf Res 25:1561–1582CrossRefGoogle Scholar
  22. Hanson CE, Hyndes GA, Wang SF (2010) Differentiation of benthic marine primary producers using stable isotopes and fatty acids: Implications to food web studies. Aquat Bot 93:114–122CrossRefGoogle Scholar
  23. Hata H, Umezawa Y (2011) Food habits of the farmer damselfish Stegastes nigricans inferred by stomach content, stable isotope, and fatty acid composition analyses. Ecol Res 26:809–818CrossRefGoogle Scholar
  24. Hata H, Kudo S, Yamano H, Kurano N, Kayanne H (2002) Organic carbon flux in Shiraho coral reef (Ishigaki Island, Japan). Mar Ecol-Prog Ser 232:129–140CrossRefGoogle Scholar
  25. Hernaman V, Probert PK, Robbins WD (2009) Trophic ecology of coral reef gobies: interspecific, ontogenetic, and seasonal comparison of diet and feeding intensity. Mar Biol 156:317–330CrossRefGoogle Scholar
  26. Ho CT, Kao SJ, Dai CF, Hsieh HL, Shiah FK, Jan RQ (2007) Dietary separation between two blennies and the Pacific gregory in northern Taiwan: evidence from stomach content and stable isotope analyses. Mar Biol 151:729–736CrossRefGoogle Scholar
  27. Ho CT, Fu YC, Sun CL, Kao SJ, Jan RQ (2009) Plasticity of feeding habits of two Plectroglyphidodon damselfishes on coral reefs in southern Taiwan: evidence from stomach content and stable isotope analyses. Zool Stud 48:649–656Google Scholar
  28. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia (Berl) 120:314–326CrossRefGoogle Scholar
  29. Hussey NE, Brush J, McCarthy ID, Fisk AT (2010) delta N-15 and delta C-13 diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comp Biochem Physiol A-Mol Integr Physiol 155:445–453PubMedCrossRefGoogle Scholar
  30. Imbs AB, Yakovleva IM, Pham LQ (2010) Distribution of lipids and fatty acids in the zooxanthellae and host of the soft coral Sinularia sp. Fish Sci 76:375–380CrossRefGoogle Scholar
  31. Kolasinski J, Frouin P, Sallon A, Rogers K, Bruggemann HJ, Potier M (2009) Feeding ecology and ontogenetic dietary shift of yellowstripe goatfish Mulloidichthys flavolineatus (Mullidae) at Reunion Island, SW Indian Ocean. Mar Ecol Prog Ser 386:181–195CrossRefGoogle Scholar
  32. Kulbicki M, Bozec YM, Labrosse P, Letourneur Y, Mou-Tham G, Wantiez L (2005) Diet composition of carnivorous fishes from coral reef lagoons of New Caledonia. Aquat Living Resour 18:231–250CrossRefGoogle Scholar
  33. Kuo SR, Shao KT (1991) Feeding habits of damselfishes (Pomacentridae) from the southern part of Taiwan. J Fish Soc Taiwan 18:165–176Google Scholar
  34. Lebreton B, Richard P, Galois R, Radenac G, Pfleger C, Guillou G, Mornet F, Blanchard GF (2011) Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: Evidence from stable isotope and fatty acid analyses. Estuar Coast Shelf Sci 92:140–153CrossRefGoogle Scholar
  35. Logan JM, Lutcavage ME (2008) A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems. Rapid Commun Mass Spectrom 22:1081–1086PubMedCrossRefGoogle Scholar
  36. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390CrossRefGoogle Scholar
  37. McMahon KW, Berumen ML, Mateo I, Elsdon TS, Thorrold SR (2011) Carbon isotopes in otolith amino acids identify residency of juvenile snapper (Family: Lutjanidae) in coastal nurseries. Coral Reefs 30:1135–1145CrossRefGoogle Scholar
  38. Minagawa M, Wada E (1984) Stepwise enrichment of 15 N along food chains: Further evidence and the relation between [delta]15 N and animal age. Geochim Cosmochim Acta 48:1135–1140CrossRefGoogle Scholar
  39. Mumby PJ, Edwards AJ, Arias-Gonzalez JE, Lindeman KC, Blackwell PG, Gall A, Gorczynska MI, Harborne AR, Pescod CL, Renken H, Wabnitz CCC, Llewellyn G (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536PubMedCrossRefGoogle Scholar
  40. Nagelkerken I, Bothwell J, Nemeth RS, Pitt JM, van der Velde G (2008) Interlinkage between Caribbean coral reefs and seagrass beds through feeding migrations by grunts (Haemulidae) depends on habitat accessibility. Mar Ecol-Prog Ser 368:155–164CrossRefGoogle Scholar
  41. Nagelkerken I, van der Velde G, Wartenbergh SLJ, Nugues MM, Pratchett MS (2009) Cryptic dietary components reduce dietary overlap among sympatric butterflyfishes (Chaetodontidae). J Fish Biol 75:1123–1143PubMedCrossRefGoogle Scholar
  42. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: Coping with too much variation. PLoS ONE 5:e9672PubMedCrossRefGoogle Scholar
  43. Parrish JD (1989) Fish communities of interacting shallow-water habitats in tropical oceanic regions. Mar Ecol-Prog Ser 58:143–160CrossRefGoogle Scholar
  44. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  45. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189PubMedCrossRefGoogle Scholar
  46. Pratchett MS, Gust N, Goby G, Klanten SO (2001) Consumption of coral propagules represents a significant trophic link between corals and reef fish. Coral Reefs 20:13–17CrossRefGoogle Scholar
  47. Sotiropoulos MA, Tonn WM, Wassenaar LI (2004) Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies. Ecol Freshw Fish 13:155–160CrossRefGoogle Scholar
  48. Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20:595–601PubMedCrossRefGoogle Scholar
  49. van Duyl F, Moodley L, Nieuwland G, van Ijzerloo L, van Soest R, Houtekamer M, Meesters E, Middelburg J (2011) Coral cavity sponges depend on reef-derived food resources: stable isotope and fatty acid constraints. Mar Biol 158:1653–1666CrossRefGoogle Scholar
  50. Vander Zanden MJ, Rasmussen JB (2001) Variation in delta N-15 and delta C-13 trophic fractionation: Implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066CrossRefGoogle Scholar
  51. Verweij MC, Nagelkerken I, Hans I, Ruseler SM, Mason PRD (2008) Seagrass nurseries contribute to coral reef fish populations. Limnol Oceanogr 53:1540–1547CrossRefGoogle Scholar
  52. Ward EJ, Semmens BX, Schindler DE (2010) Including source uncertainty and prior information in the analysis of stable isotope mixing models. Environ Sci Technol 44:4645–4650PubMedCrossRefGoogle Scholar
  53. Wells RJD, Cowan JH, Fry B (2008) Feeding ecology of red snapper Lutjanus campechanus in the northern Gulf of Mexico. Mar Ecol-Prog Ser 361:213–225CrossRefGoogle Scholar
  54. Wilson SK, Depczynski M, Fisher R, Holmes TH, O’Leary RA, Tinkler P (2010) Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae. PLoS ONE 5:e15185PubMedCrossRefGoogle Scholar
  55. Wyatt ASJ (2011) Oceanographic ecology of coral reefs: the role of oceanographic processes in reef-level biogeochemistry and trophic ecology. Ph.D. Thesis, The University of Western Australia, p 349Google Scholar
  56. Wyatt ASJ, Waite AM, Humphries S (2010a) Variability in isotope discrimination factors in coral reef fishes: Implications for diet and food web reconstruction. PLoS ONE 5:e13682. doi: 10.1371/journal.pone.0013682 PubMedCrossRefGoogle Scholar
  57. Wyatt ASJ, Lowe RJ, Humphries S, Waite AM (2010b) Particulate nutrient fluxes over a fringing coral reef: relevant scales of phytoplankton production and mechanisms of supply. Mar Ecol-Prog Ser 405:113–130CrossRefGoogle Scholar
  58. Wyatt ASJ, Falter JL, Lowe RJ, Humphries S, Waite AM (2012) Oceanographic forcing of nutrient uptake and release over a fringing coral reef. Limnol Oceanogr 57:401–419CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • A. S. J. Wyatt
    • 1
    • 2
    • 3
    • 4
  • A. M. Waite
    • 1
    • 2
  • S. Humphries
    • 5
  1. 1.The Oceans InstituteThe University of Western AustraliaCrawleyAustralia
  2. 2.School of Environmental Systems EngineeringThe University of Western AustraliaCrawleyAustralia
  3. 3.Scripps Institution of OceanographyUniversity of California, San DiegoLa JollaUSA
  4. 4.Marine Biogeochemistry Laboratory, Department of Chemical Oceanography, Atmosphere and Ocean Research InstituteThe University of TokyoKashiwaJapan
  5. 5.Department of Biological SciencesUniversity of HullKingston-upon-HullUK

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