Oceanography The Official Magazine of
The Oceanography Society
Volume 26 Issue 03

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Volume 26, No. 3
Pages 180 - 189

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Stable Isotopes Reveal Trophic Relationships and Diet of Consumers in Temperate Kelp Forest and Coral Reef Ecosystems

By Henry M. Page , Andrew J. Brooks, Michel Kulbicki , René Galzin, Robert J. Miller , Daniel C. Reed , Russell J. Schmitt, Sally J. Holbrook, and Craig Koenigs 
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Article Abstract

We explored the use of stable nitrogen (N) isotope analysis to assess trophic position of consumers in two marine ecosystems: the kelp forests of southern California and a coral atoll in the tropical Pacific. The δ15N values of consumers in both ecosystems increased from known herbivores (invertebrates and fish) to higher-level consumers (predatory invertebrates and fish). In the absence of data on trophic enrichment in 15N for our study species, we used the oft-cited value of +3.4‰ increase in δ15N value per trophic level and estimates of the δ15N producer baseline value to estimate trophic position. The trophic position of consumers computed using N isotopes compared favorably to published observations of diet. Nitrogen isotope analysis revealed that some of our higher-level fish consumers from rocky reefs (i.e., some rockfish) were feeding largely on invertebrates rather than on fish, as is often assumed. Our analysis also suggests that higher-level consumers on coral reefs may consume more herbivorous prey (i.e., both fishes and invertebrates) than previously reported. Our data support the use of nitrogen isotope values to assess trophic position and, thus, their utility as one metric with which to explore the effects of short- and longer-term natural and human-induced changes on kelp forest and coral reef food webs.

Citation

Page, H.M., A.J. Brooks, M. Kulbicki, R. Galzin, R.J. Miller, D.C. Reed, R.J. Schmitt, S.J. Holbrook, and C. Koenigs. 2013. Stable isotopes reveal trophic relationships and diet of consumers in temperate kelp forest and coral reef ecosystems. Oceanography 26(3):180–189, https://doi.org/10.5670/oceanog.2013.61.

References
    Adam, T.C., R.J. Schmitt, S.J. Holbrook, A.J. Brooks, P.J. Edmunds, R.C. Carpenter, and G. Bernardi. 2011. Herbivory, connectivity, and ecosystem resilience: Response of a coral reef to a large-scale perturbation. PloS One 6:e23717, https://doi.org/10.1371/journal.pone.0023717.
  1. Adjeroud, M., F. Michonneau, P.J. Edmunds, Y. Chancerelle, T. Lison de Loma, L. Penin, L. Thibaut, J. Vidal-Dupiol, B. Salvat, and R. Galzin. 2009. Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28:775–780, https://doi.org/10.1007/s00338-009-0515-7. 
  2. Byrnes, J.E., D.C. Reed, B.J. Cardinale, K.C. Cavanaugh, S.J. Holbrook, and R.J. Schmitt. 2011. Climate-driven increases in storm frequency simplify kelp forest food webs. Global Change Biology 17:2,513–2,524, https://doi.org/10.1111/j.1365-2486.2011.02409.x. 
  3. Cabana, G., and J.B. Rasmussen. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences of the United States of America 93:10,844–10,847.
  4. Carassou, L., M. Kulbicki, T.J.R. Nicola, and N.V.C. Polunin. 2008. Assessment of fish trophic status and relationships by stable isotope data in the coral reef lagoon of New Caledonia, Southwest Pacific. Aquatic Living Resources 12:1–12, https://doi.org/10.1051/alr:2008017.
  5. Caut, S., E. Angulo, and F. Courchamp. 2009. Variation in discrimination factors (Δ15N and Δ13C): The effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46:443–453.
  6. Dayton, P.K., M.J. Tegner, P.B. Edwards, and K. Riser. 1999. Temporal and spatial scales of kelp demography: The role of oceanographic climate. Ecological Monographs 69:219–250.
  7. de la Morinière, E.C., B.J.A. Pollux, I. Nagelkerken, M.A. Hemminga, A.H.L. Huiskes, and G. van der Velde. 2003. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuarine, Coastal and Shelf Science 57:1,079–1,089, https://doi.org/​10.1016/S0272-7714(03)00011-8.
  8. Duggins, D.O. 1981. Sea urchins and kelp: The effects of short term changes in urchin diet. Limnology and Oceanography 26:391–394.
  9. Fredriksen, S. 2003. Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Marine Ecology Progress Series 260:71–81.
  10. Froese, R., and D. Pauly, eds. 2013. FishBase. World Wide Web electronic publication, http://www.fishbase.org, version (04/2013).
  11. Fry, B. 1988. Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnology and Oceanography 33:1,182–1,190.
  12. Fry, B. 2006. Stable Isotope Ecology. Springer, New York, USA, 308 pp.
  13. Galván, D.E., C.J. Sweeting, and W.D.K. Reid. 2010. Power of stable isotope techniques to detect size-based feeding in marine fishes. Marine Ecology Progress Series 407:271–278, https://doi.org/10.3354/meps08528.
  14. Hanson, K. 2011. Planktivorous fish link coral reef and oceanic food webs: Causes and consequences of landscape-level patterns in fish behavior, diet and growth. PhD Dissertation, University of California, San Diego.
  15. Hatcher, B.G. 1988. Coral reef primary productivity: A beggar’s banquet. Trends in Ecology and Evolution 3:106–111, https://doi.org/​10.1016/0169-5347(88)90117-6.
  16. Hentschel, B.T. 1998. Intraspecific variations in δ13C indicate ontogenetic diet changes in deposit-feeding polychaetes. Ecology 79:1,357–1,370.
  17. Hobson, K.A., and H.E. Welch. 1992. Determination of trophic relationships within a high Arctic marine food web using delta-13 C and delta-15 N analysis. Marine Ecology Progress Series 84:9–18.
  18. Jack, L., and S.R. Wing. 2011. Individual variability in trophic position and diet of a marine omnivore is linked to kelp bed habitat. Marine Ecology Progress Series 443:129–139, https://doi.org/10.3354/meps09468.
  19. Kayal, M., J. Vercelloni, T. Lison de Loma, P. Bosserelle, Y. Chancerelle, S. Geoffroy, C. Stievenart, F. Michonneau, L. Penin, S. Planes, and others. 2012. Predator Crown-of-thorns Starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PloS One 7:e47363, https://doi.org/10.1371/journal.pone.0047363.
  20. Kulbicki, M., Y. Bozec, P. Labrosse, Y. Letourneur, G. Mou-Tham, and L. Wantiez. 2005. Diet composition of carnivorous fishes from coral reef lagoons of New Caledonia. Aquatic Living Resources 18:213–250.
  21. Layman, C.A., M.S. Araujo, R. Boucek, C.M. Hammerschlag-Peyer, E. Harrison, Z.R. Jud, P. Matich, A.E. Rosenblatt, J.J. Vaudo, L.A. Yeager, and others. 2012. Applying stable isotopes to examine food-web structure: An overview of analytical tools. Biological Reviews 87:454–562, https://doi.org/​10.1111/j.1469-185X.2011.00208.x.
  22. Lecchini, D., L. Carassou, B. Frédérich, Y. Nakamura, S.C. Mills, and R. Galzin. 2012. Effects of alternate reef states on coral reef fish habitat associations. Environmental Biology of Fishes 94:421–429, https://doi.org/10.1007/s10641-011-9958-0. 
  23. Leighton, D.L. 1966. Studies of food preference in algivorous invertebrates of Southern California kelp beds. Pacific Science 20:104–113.
  24. Lindegren, M., C. Möllmann, A. Nielsen, K. Brander, B.R. MacKenzie, and N. Chr. Stenseth. 2010. Ecological forecasting under climate change: The case of Baltic cod. Proceedings of the the Royal Society B 277:2,121–2,130, https://doi.org/​10.1098/rspb.2010.0353.
  25. Mann, K.H. 2000. Ecology of Coastal Waters. Blackwell Science, Malden, MA, 322 pp.
  26. McCauley, D.J., F. Micheli, H.S. Young, D.P. Tittensor, D.R. Brumbaugh, E.M.P. Madin, K.E. Holmes, J.E. Smith, H.K. Lotze, P.A. DeSalles, and others. 2010. Acute effects of removing large fish from a near-pristine coral reef. Marine Biology 157:2,739–2,750, https://doi.org/10.1007/s00227-010-1533-2.
  27. McCutchan, J.H., W.M. Lewis, C. Kendall, C. Claire, J.H. McCutchan Jr., W.M. Lewis Jr., and C.C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390.
  28. Minagawa, M., and E. Wada. 1984. Stepwise enrichment of δ15N along food chains: Further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48:1,135–1,140, https://doi.org/​10.1016/0016-7037(84)90204-7.
  29. Moore, J.C., and P.C. de Ruiter. 2012. Energetic Food Webs: An Analysis of Real and Model Ecosystems. Oxford University Press, Oxford, UK, 344 pp.
  30. Morris, R.H., D.P. Abbott, and E.C. Haderlie. 1980. Intertidal Invertebrates of California. Stanford University Press, Stanford, CA, 690 pp.
  31. Naiman, R.J., J.R. Alldredge, D.A. Beauchamp, P.A. Bisson, J. Congleton, C.J. Henny, N. Huntly, E.R. Lamberson, C. Levings, E.N. Merrill, and others. 2012. Developing a broader scientific foundation for river restoration: Columbia River food webs. Proceedings of the National Academy of Sciences of the United States of America 109:21,201–21,207, https://doi.org/10.1073/pnas.1213408109.
  32. Olive, P.J.W., J.K. Pinnegar, N.V.C. Polunin, G. Richards, and R. Welch. 2003. Isotope trophic-step fraction: A dynamic equilibrium model. Journal of Animal Ecology 72:608–617, https://doi.org/​10.1046/j.1365-2656.2003.00730.x.
  33. Page, H.M., D.C. Reed, M.A. Brzezinski, J.M. Melack, and J.E. Dugan. 2008. Assessing the importance of land and marine sources of organic matter to kelp forest food webs. Marine Ecology Progress Series 360:47–62, https://doi.org/10.3354/meps07382.
  34. Parrish, J.D. 1987. The trophic biology of snappers and groupers. Pp. 405–464 in Tropical Snappers and Groupers: Biology and Fishery Management. J.J. Polovina and S. Ralston, eds, Westview Press, Boulder, CO.
  35. Peterson, B.J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293–320, https://doi.org/​10.1146/annurev.es.18.110187.001453.
  36. Planes, S., R. Galzin, J.-P. Bablet, and P.F. Sale. 2005. Stability of coral reef fish assemblages impacted by nuclear tests. Ecology 86:2,578–2,585, https://doi.org/10.1890/04-0774.
  37. Post, D.M., M.L. Pace, and N.G. Hairston Jr. 2000. Ecosystem size determines food-chain length in lakes. Nature 405:1,047–1,049, https://doi.org/10.1038/35016565.
  38. Post, D.M. 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83:703–718, https://doi.org/10.1890/0012-9658(2002)083​[0703:USITET]2.0.CO;2. 
  39. Pratchett, M.S., M.L. Berumen, M.J. Marnane, J.V. Eagle, and D.J. Pratchett. 2008. Habitat associations of juvenile versus adult butterflyfishes. Coral Reefs 27:541–551, https://doi.org/10.1007/s00338-008-0357-8.
  40. Randall, J.E. 2005. Reef and Shore Fishes of the South Pacific: New Caledonia to Tahiti and the Pitcairn Islands. University of Hawaii Press, Honolulu, HI, 707 pp.
  41. Reed, D.C., A. Rassweiler, M.H. Carr, K.C. Cavanaugh, D.P. Malone, and D.A. Siegel. 2011. Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92:2,108–2,116.
  42. Steneck, R.S., J. Vavrinec, and A.V. Leland. 2004. Accelerating trophic-level dysfunction in kelp forest ecosystems of the western North Atlantic. Ecosystems 7:323–332, https://doi.org/10.1007/s10021-004-0240-6.
  43. Sweeting, C.J., J. Barry, C. Barnes, N.V.C. Polunin, and S. Jennings. 2007. Effects of body size and environment on diet-tissue δ15N fractionation in fishes. Journal of Experimental Marine Biology and Ecology 340:1–10, https://doi.org/​10.1016/j.jembe.2006.07.023. 
  44. Vander Zanden, M.J., and J.B. Rasmussen. 2001. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography 46:2,061–2,066, https://doi.org/10.4319/lo.2001.46.8.2061.
  45. Wyatt, A.S.J., A.M. Waite, and S. Humphries. 2010. Variability in isotope discrimination factors in coral reef fishes: Implications for diet and food web reconstruction. PloS One 5:e13682, https://doi.org/10.1371/journal.pone.0013682.
  46. Wyatt, A.S.J., A.M. Waite, and S. Humphries. 2012. Stable isotope analysis reveals community-level variation in fish trophodynamics across a fringing coral reef. Coral Reefs 31:1,029–1,044, https://doi.org/10.1007/s00338-012-0923-y. 
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