Tracing carbon flow through coral reef food webs using a compound-specific stable isotope approach
- 1.7k Downloads
Coral reefs support spectacularly productive and diverse communities in tropical and sub-tropical waters throughout the world’s oceans. Debate continues, however, on the degree to which reef biomass is supported by new water column production, benthic primary production, and recycled detrital carbon (C). We coupled compound-specific stable C isotope ratio (δ13C) analyses with Bayesian mixing models to quantify C flow from primary producers to coral reef fishes across multiple feeding guilds and trophic positions in the Red Sea. Analyses of reef fishes with putative diets composed primarily of zooplankton (Amblyglyphidodon indicus), benthic macroalgae (Stegastes nigricans), reef-associated detritus (Ctenochaetus striatus), and coral tissue (Chaetodon trifascialis) confirmed that δ13C values of essential amino acids from all baseline C sources were both isotopically diagnostic and accurately recorded in consumer tissues. While all four source end-members contributed to the production of coral reef fishes in our study, a single-source end-member often dominated dietary C assimilation of a given species, even for highly mobile, generalist top predators. Microbially reworked detritus was an important secondary C source for most species. Seascape configuration played an important role in structuring resource utilization patterns. For instance, Lutjanus ehrenbergii showed a significant shift from a benthic macroalgal food web on shelf reefs (71 ± 13 % of dietary C) to a phytoplankton-based food web (72 ± 11 %) on oceanic reefs. Our work provides insights into the roles that diverse C sources play in the structure and function of coral reef ecosystems and illustrates a powerful fingerprinting method to develop and test nutritional frameworks for understanding resource utilization.
KeywordsAmino acids Bayesian mixing model Diet Fish Red Sea
This research was based on work supported by Awards USA 00002 and KSA 00011 from King Abdullah University of Science and Technology (KAUST); additional funding was provided by the Woods Hole Oceanographic Institution (WHOI), a KAUST-WHOI award (SPCF-7000000104), and KAUST baseline research funds. We thank E. Mason and the Dream Divers crew for boat and dive operation support, C. Braun for creating the site map, and the following people for field assistance: C. Braun, T. Sinclair-Taylor, M. Priest, G. Nanninga, N. desRosiers, P. de la Torre, J. Bouwmeester, L.-L. Hamady. We also thank two anonymous reviewers and the handling editor for valuable comments on this paper.
Author contribution statement
K. W. M., S. R. T., and M. L. B. conceived of and designed the study; K. W. M. and M. L. B. conducted the fieldwork; K. W. M. and L. A. H. conducted the laboratory analyses; K. W. M. and S. R. T. analyzed the data and wrote the manuscript; M. L. B. and L. A. H. revised and edited the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Alongi DDM (1988) Detritus in coral reef ecosystems: fluxes and fates. Proc 6th Int Coral Reef Symp 1:29–36Google Scholar
- Chen L-S (2002) Post-settlement diet shift of Chlorurus sordidus and Scarus schlegeli (Pisces: Scaridae). Zool Stud 41:47–58Google Scholar
- 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 246:279–289. doi: 10.3354/meps246279 CrossRefGoogle Scholar
- Darwin C (1842) The structure and distribution of coral reefs. Appleton, New YorkGoogle Scholar
- Emery A (1973) Comparative ecology and functional osteology of fourteen species of damselfish (Pices: Pomacentridae) at Alligator Reef, Florida Keys. Bull Mar Sci 23:649–770Google Scholar
- Hamner WM, Jones MS, Carleton JH, Hauri IR, Williams DM (1988) Zooplankton, planktivorous fishes, and water currents on a windward reef face: Great Barrier reef, Australia. Bull Mar Sci 42:459–479Google Scholar
- Hayes JM (2001) Fractionation of the isotopes of carbon and hydrogen in biosynthetic processes. In: Cole DR, Valley JW (eds) Reviews in mineralogy and geochemistry 43, stable isotope geochemistry. The Mineralogical Society of America, Washington, pp 225–277Google Scholar
- Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365. doi: 10.1016/j.cub.2006.12.049 CrossRefPubMedGoogle Scholar
- JMP (2013) Graphic builder, version 11. SAS Institute, Cary, NC, URL http://www.jmp.com/software/jmp
- Lammens EHRR, de Nie HW, Vijverberg J, van Densen WLT (1985) Resource partitioning and niche shifts of bream (Abramis brama) and eel (Anguilla Anguilla) mediated by predation of smelt (Osmerus eperlanus) on Daphnia hyaline. Can J Fish Aquat Sci 42:1342–1351. doi: 10.1139/f85-169 CrossRefGoogle Scholar
- Larsen T, Bach LT, Salvatteci R, Wang YV, Andersen N, Ventura M, McCarthy MD (2015) Assessing the potential of amino acid δ13C patterns as a carbon source tracer in marine sediments: effects of algal growth conditions and sedimentary diagenesis. Biogeosci Discuss 12:1613–1651. doi: 10.5194/bgd-12-1613-2015 CrossRefGoogle Scholar
- Letourneur Y, Lison De Loma T, Richard P, Harmelin-Vivien ML, Cresson P, Banaru D, Fontaine MF, Gref T, Planes S (2013) Identifying carbon sources and trophic position of coral reef fishes using diet and stable isotope (δ15N and δ13C) analyses in two contrasted bays in Moorea, French Polynesia. Coral Reefs 32:1091–1102. doi: 10.1007/s00338-013-1073-6 CrossRefGoogle Scholar
- Lieske E, Myers RF (2004) Coral reef guide: Red Sea. Harper Collins, OxfordGoogle Scholar
- McCarthy DM, Benner R, Lee C, Hedges JL, Fogel ML (2004) Amino acid carbon isotopic fractionation patterns in oceanic dissolved organic matter: an unaltered photoautotrophic source for dissolved organic nitrogen in the ocean? Mar Chem 92:123–134. doi: 10.1016/j.marchem.2004.06.021 CrossRefGoogle Scholar
- McMahon KW, Hamady L-L, Thorrold SR (2013) Ocean ecogeochemistry: a review. Oceanogr Mar Biol Annu Rev 51:327–374Google Scholar
- Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Collins Johnson N, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600. doi: 10.1111/j.1461-0248.2004.00606.x CrossRefGoogle Scholar
- R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, URL http://www.R-project.org
- Schiff JT, Batista FC, Sherwood OA, Guilderson TP, Hill TM, Ravelo AC, McMahon KW, McCarthy MD (2014) Compound specific amino acid δ13C patterns in a deep-sea proteinaceous coral: implications for reconstructing detailed δ13C records of exported primary production. Mar Chem 166:82–91CrossRefGoogle Scholar
- Sheppard CRC, Sheppard ALS (1991) Corals and coral communities of Arabia. Fauna Saudi Arabia 12:7–192Google Scholar
- Sommer C, Schneider W, Poutiers JM (1996) FAO species identification field guide for fishery purposes. The living marine resources of Somalia. Food and Agricultural Organization of the United Nations, RomeGoogle Scholar
- Uthicke S (1999) Sediment bioturbation and impact of feeding activity of Holothuria (Halodeima) atra and Stichopus chloronotus, two sediment feeding holothurians, at Lizard Island, Great Barrier Reef. Bull Mar Sci 64:129–141Google Scholar