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Mangrove-Exported Nutrient Incorporation by Sessile Coral Reef Invertebrates

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Abstract

Coastal mangrove forests were historically considered as a source of organic matter (OM) for adjacent marine systems due to high net primary production; yet recent research suggesting little uptake through the food web because of low nutritional quality, challenges the concept of trophic linkage between mangrove forests and coral reefs. To examine the importance of mangrove forests to coral reef nutrient availability, we examined sessile reef-forming invertebrate consumers including hard corals, sponges, a bivalve mollusc, polychaete annelid and tunicate, and potential sources of OM (decaying mangrove leaves, microalgae, macroalgae, and seagrass) in Bocas del Toro, Panama. Using stable isotope analyses of δ34S and δ13C and a concentration-dependent version of the IsoSource mixing model, we were able to discriminate among and determine the range of potential contributions of our four OM sources to consumers. Contributions of microalgae and macroalgae were often indeterminate due to high variability, yet seagrass and mangrove contributions were often substantial. Mangrove OM ranged across sites and species of filter feeders from 0 to 57%, 7 to 41%, and 18 to 52% for sponges, file clams, and feather duster worms, respectively. Mangrove contribution to corals (Acropora cervicornis, Agaricia fragilis, Agaricia tenuifolia, Montastrea annularis, Diploria sp.) ranged from 0 to 44%. To examine whether OM contribution varied with distance from mangroves, we conducted a sponge transplant experiment that demonstrated declining mangrove contribution across three sponge species with increasing distance from the shore. These results supported the hypothesis of mangrove-coral reef nutrient linkages, providing the first evidence that mangrove inputs of OM to sessile invertebrates are substantial, accounting for 0–57% of the composition.

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References

  • Alongi, DM. 1990. Effects of mangrove detrital outwelling on nutrient regeneration and oxygen fluxes in coastal sediments of the central Great Barrier Reef lagoon. Estuar Coast Shelf Sci 31:581–98.

    Article  CAS  Google Scholar 

  • Ambler JW, Alcala-Herrera J, Burke R. 1994. Trophic roles of particle feeders and detritus in a mangrove island prop root ecosystem. Hydrobiologia 292–293:437–46.

    Google Scholar 

  • Benstead JP, March JG, Fry B, Ewel KC, Pringle CM. 2006. Testing IsoSource: stable isotope analysis of a tropical fishery with diverse organic matter sources. Ecology 87:326–33.

    Article  PubMed  Google Scholar 

  • Bouillon S, Borges AV, Castaneda-Moya E, Diele K, Dittmar T, Duke NC, Kristensen E, Lee SY, Marchand C, Middelburg JJ, Rivera-Monroy VH, Smith TJ III, Twilley RR. 2008. Mangrove production and carbon sinks: a revision of global budget estimates. Global Biogeochem Cycles 22 (GB2013)

  • Bouillon S, Koedam N, Raman AV, Dehairs F. 2002. Primary producers sustaining macroinvertebrate communities in intertidal mangrove forests. Oecologia 130:441–8.

    Article  Google Scholar 

  • Bouillon S, Mohan PC, Sreenivas N, Dehairs F. 2000. Sources of suspended organic matter and selective feeding by zooplankton in an estuarine mangrove ecosystem as traced by stable isotopes. Mar Ecol Prog Ser 208:79–92.

    Article  Google Scholar 

  • Cocheret dela Moriniere EC, 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 246:279–89.

    Article  Google Scholar 

  • Connell JH, Hughes TP, Wallace CC. 1997. A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67: 461–88.

    Google Scholar 

  • Deegan LA. 1993. Nutrient and energy transport between estuaries and coastal marine ecosystems by fish migration. Can J Fish Aquat Sci 50:74–9.

    Article  Google Scholar 

  • Duarte CM, Cebrian J. 1996. The fate of marine autotrophic production. Limnol Oceanogr 41:1758–66.

    CAS  Google Scholar 

  • Ellison AM, Farnsworth EJ, Twilley RR. 1996. Facultative mutualism between red mangroves and root-fouling sponges in Belizean mangal. Ecology 77:2431–44.

    Article  Google Scholar 

  • France R. 1998. Estimating the assimilation of mangrove detritus by fiddler crabs in Laguna Joyuda, Puerto Rico, using dual stable isotopes. J Trop Ecol 14:413–25.

    Article  Google Scholar 

  • France RL, Peters RH. 1997. Ecosystem differences in the trophic enrichment of 13C in aquatic food webs. Can J Fish Aquat Sci 54:1255–8.

    Article  Google Scholar 

  • Fry B, Smith TJ, III. 2002. Stable isotope studies of red mangroves and filter feeders from the Shark River estuary, Florida. Bull Mar Sci 70:871–90.

    Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE. 2006. Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–9.

    Article  PubMed  CAS  Google Scholar 

  • Heikoop JM, Dunn JJ, Risk MJ. 1998. Relationship between light and the d15N of coral tissue: examples from Jamaica and Zanzibar. Limnol Oceanogr 43:909–20.

    CAS  Google Scholar 

  • Jennerjahn TC, Ittekkot V. 1997. Organic matter in sediments in the mangrove areas and adjacent continental margins of Brazil. Oceanol Acta 20:359–69.

    CAS  Google Scholar 

  • JennerjahnTC, Ittekkot V. 2002. Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89:23–30.

    Article  PubMed  CAS  Google Scholar 

  • Lee SY. 1995. Mangrove outwelling: a review. Hydrobiologia 295:203–12.

    Article  Google Scholar 

  • Loneragan NR, Bunn SE, Kellaway DM. 1997. Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable-isotope study. Mar Biol 130:289–300.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Meyer JL, Schultz ET, Helfman GS. 1983. Fish schools: an asset to corals. Science 220:1047–9.

    Article  PubMed  CAS  Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR. 1989. Resource partitioning by reef corals as determined from stable isotope composition. Mar Biol 100:185–93.

    Article  Google Scholar 

  • Nagelkerken I, van der Velde G. 2004a. Are Caribbean mangroves important feeding grounds for juvenile reef fish from adjacent seagrass beds? Mar Ecol Prog Ser 274:143–51.

    Article  Google Scholar 

  • Nagelkerken I, van der Velde G. 2004b. Relative importance of interlinked mangroves and seagrass beds as feeding habitats for juvenile reef fish on a Caribbean island. Mar Ecol Prog Ser 274:153–9.

    Article  Google Scholar 

  • Newell RIE, Marshall N, Sasekumar A, Chong VC. 1995. Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Mar Biol 123:595–606.

    Article  Google Scholar 

  • Odum WE, Heald EJ. 1972. Trophic analyses of an estuarine mangrove community. Bull Mar Sci 22:671–738.

    Google Scholar 

  • Odum WE, Heald EJ. 1975. The detritus-based food web of an estuarine mangrove community. In: Cronin LE, Ed. Estuarine research. New York: Academic Press. pp 265–86.

    Google Scholar 

  • Porter JW. 1976. Autotrophy, heterotrophy and resource partitioning in Caribbean reef-building corals. Am Nat 110: 731–42.

    Article  Google Scholar 

  • Phillips DL, Gregg JW. 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–9.

    Article  PubMed  Google Scholar 

  • Phillips DL, Koch PL. 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–25.

    Google Scholar 

  • Suchanek TH, Carpenter RC, Whitman JD, Harvell CD. 1983. Sponges as important space competitors in deep Caribbean coral reef communities. In: Reaka ML (ed). The ecology of deep and shallow coral reefs. Symposia series for undersea research. Rockville, MD: NOAA Undersea Research Program. pp 55–60.

    Google Scholar 

  • Sheaves M, Molony B. 2000. Short-circuit in the mangrove food chain. Mar Ecol Prog Ser 199:97–109.

    Article  Google Scholar 

  • Twilley RT. 1985. The exchange of organic carbon in basin mangrove forests in a southwest Florida estuary. Estuar Coast Shelf Sci 20:543–57.

    Article  CAS  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB. 2001. Variation in d15N and d13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–6.

    CAS  Google Scholar 

  • Weis VM., Reynolds WS, deBoer MD, Krupp DA. 2001. Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20: 301–8.

    Article  Google Scholar 

  • Werry J, Lee SY. 2005. Grapsid crabs mediate link between mangrove litter production and estuarine planktonic food chains. Mar Ecol Prog Ser 293:165–76.

    Article  Google Scholar 

  • Wulff JL. 1997. Mutualisms among species of coral reef sponges. Ecology 78:146–59.

    Article  Google Scholar 

  • Wulff JL. 2000. Functional roles of sponges on coral reefs. Washington, DC: USAID.

    Google Scholar 

  • Yahel G. 2003. Feeding on ultraplankton and dissolved organic carbon in coral reefs: from the individual grazer to the community. PhD Dissertation. Hebrew University, Jerusalem, Israel

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Acknowledgments

We thank C. Diaz, B. Fry, B. Griffis, R. Brooks, S. Silva, R. Doucett, C. Kendall, S. Perez, V. Weis, and B. Hungate for their ideas, suggestions, interpretations, and assistance with the sample processing. We also thank K. Purcell, K. Frasier, N. Ehlers, A. Amat, and M. Brown for their assistance in the lab and field. This manuscript was significantly improved through discussions and input from V. Weis, B. Menge, J. Lubchenco, J. Benstead, and two anonymous reviewers. Funding for this study was provided by a Fulbright Fellowship, an NSF-GRF, an Oregon State University Aquaculture Collaborative Research Support Program Fellowship, The David and Lucile Packard Foundation, a Smithsonian Tropical Research Institution—Supplemental Research Award, an Anchor Environmental Scholarship, OSU URISC and IURP Fellowships, a Department of Zoology Research Fellowship from Oregon State University, and in-kind support from the USGS Menlo Park Laboratory and the US EPA National Health and Environmental Effects Laboratory, Western Ecology Division. This manuscript has been subjected to US EPA’s peer and administrative review, and it has been approved for publication as an EPA document. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

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  1. Elise F. Granek

    Present address: Environmental Sciences and Management, Portland State University, P.O. Box 751, Portland, Oregon, 97207, USA

Authors and Affiliations

  1. Department of Zoology, Oregon State University, Corvallis, Oregon, 97331, USA

    Elise F. Granek

  2. Western Ecology Division, US Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Corvallis, Oregon, 97333, USA

    Jana E. Compton & Donald L. Phillips

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  1. Elise F. Granek
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  2. Jana E. Compton
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  3. Donald L. Phillips
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Correspondence to Elise F. Granek.

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Author Contributions

EFG conceived of study, performed all field research, conducted data analysis and wrote the first draft of the manuscript. JEC assisted with study design, methods for sample processing, data analysis, and writing of the manuscript. DLP contributed new isotope models, assisted with data analysis, and contributed to writing of the manuscript.

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Granek, E.F., Compton, J.E. & Phillips, D.L. Mangrove-Exported Nutrient Incorporation by Sessile Coral Reef Invertebrates. Ecosystems 12, 462–472 (2009). https://doi.org/10.1007/s10021-009-9235-7

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