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Pathways of organic matter in an estuarine mangrove trophic network assessed by carbon and nitrogen stable isotopes

Published online by Cambridge University Press:  03 August 2017

Yves Letourneur*
Affiliation:
Institut ISEA and LABEX ‘Corail’,Université de la Nouvelle-Calédonie, BP R4, 98851 Nouméa cedex, New Caledonia
Marine J. Briand
Affiliation:
Institut ISEA and LABEX ‘Corail’,Université de la Nouvelle-Calédonie, BP R4, 98851 Nouméa cedex, New Caledonia
Gaël Guillou
Affiliation:
Département Littoral Environnement et Sociétés, Université de La Rochelle, UMR CNRS 6250 LIENSs, Bât. Marie Curie, Rue Olympe de Gouges, 17042 La Rochelle cedex 1, France
*
Correspondence should be addressed to: Y. Letourneur, Institut ISEA and LABEX ‘Corail’, Université de la Nouvelle-Calédonie, BP R4, 98851 Nouméa cedex, New Caledonia email: [email protected]

Abstract

Carbon and nitrogen stable isotopes were used to describe an estuarine mangrove food web in New Caledonia, SW Pacific. Isotopic values were measured for all components of the ecosystem, from various organic matter (OM) sources to predators. Primary producers showed δ13C values from −32.29‰ (Bruguiera gymnorhiza) to −24.67‰ (mouth particulate organic matter), whereas δ15N values ranged from 1.48‰ (Avicennia marina) to 10.17‰ (Eichomia crassipes). Two potential organic matter sources, i.e. the mangrove species and E. crassipes, appeared not to be directly used by consumers although were indirectly entering the food web through particulate and sedimentary organic matter pools (POM and SOM). Overall, invertebrates showed C-depleted and N-depleted values compared with fish, highlighting their lower trophic level. The highest trophic levels in this estuarine mangrove were represented by carangids (δ15N of 11.24‰ for Caranx sp. and 10.81‰ for Carangoides fulvoguttatus) and gerrids (δ15N of 10.42‰ for Gerres filamentosus). Two main pathways of organic matter were identified from sources of OM to end-members, i.e. from estuarine POM and SOM toward gerrids and from marine POM towards carangids. The food chain comprised three or four trophic levels, depending on the pathway of organic matter. The position of some consumer species within the reconstructed food web might imply that an important source of organic matter was probably missing, i.e. microphytobenthos. Despite an obvious connection, the role of river inputs as potential drivers of mangrove food web dynamics appeared important only during the wet season.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Abrantes, K.G., Barnett, A. and Bouillon, S. (2014) Stable isotope-based community metrics as a tool to identify patterns in food web structure in east African estuaries. Functional Ecology 28, 270282.Google Scholar
Abrantes, K.G., Johnston, R., Connolly, R.M. and Sheaves, M. (2015) Importance of mangrove carbon for aquatic food webs in wet–dry tropical estuaries. Estuaries and Coasts 38, 383399.Google Scholar
Abrantes, K.G. and Sheaves, M. (2008) Incorporation of terrestrial wetland material into aquatic food webs in a tropical estuarine wetland. Estuarine Coastal and Shelf Science 80, 401412.Google Scholar
Abrantes, K.G. and Sheaves, M. (2009) Food web structure in a near-pristine mangrove area of the Australian wet tropics. Estuarine Coastal and Shelf Science 82, 597607.Google Scholar
Abrantes, K.G. and Sheaves, M. (2010) Importance of freshwater flow in terrestrial–aquatic energetic connectivity in intermittently connected estuaries of tropical Australia. Marine Biology 157, 20712086.Google Scholar
Alongi, D.M. (1998) Coastal ecosystem processes. Boca Raton, FL: CRC Press.Google Scholar
Alongi, D.M. (2008) Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuarine Coastal and Shelf Science 76, 113.Google Scholar
Bautista-Vega, A.A., Letourneur, Y., Harmelin-Vivien, M.L. and Salen-Picard, C. (2008) Difference in diet and size-related trophic level in two sympatric fish species, the red mullets Mullus barbatus and M. surmuletus, in the Gulf of Lions (NW Mediterranean). Journal of Fish Biology 73, 24022420.Google Scholar
Bond, A.L. and Diamond, A.W. (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21, 10171023.Google Scholar
Bouillon, S., Chandra Mohan, P., Sreenivas, N. and Dehairs, F. (2000) Sources of suspended organic matter and selective feeding by zooplankton in an estuarine mangrove ecosystem as traced by stable isotopes. Marine Ecology Progress Series 208, 7992.Google Scholar
Bouillon, S., Koedam, N., Raman, A. and Dehairs, F. (2002) Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130, 441448.Google Scholar
Briand, M.J., Bonnet, X., Goiran, C., Guillou, G. and Letourneur, Y. (2015) Major sources of organic matter in a complex coral reef lagoon: identification from isotopic signatures (δ13C and δ15N). PLoS ONE 10, e0131555.Google Scholar
Brunel, J.P. (1979) Mesures de débit d’étiage sur la côte ouest de Nouvelle-Calédonie. Technical Report ORSTOM, 117 pp.Google Scholar
Cocheret de la Morinière, E., Pollux, B.J.A., Negelkerken, I., Hemminga, M.A., Huiskes, A.H.L. and van der Velde, G. (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut content analysis. Marine Ecology Progress Series 246, 279289.Google Scholar
Cresson, P., Ruitton, S., Fontaine, M.F. and Harmelin-Vivien, M.L. (2012) Spatio-temporal variation of suspended and sedimentary organic matter quality in the Bay of Marseilles (NW Mediterranean) assessed by biochemical and isotopic analyses. Marine Pollution Bulletin 64, 11121121.Google Scholar
De Niro, M.J. and Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica Cosmochimica Acta 42, 495506.Google Scholar
Dixon, R.K., Solomon, A.M., Brown, S., Houghton, R.A., Trexier, M.C. and Wisniewski, J. (1994) Carbon pools and flux of global forest ecosystems. Science 263, 185190.Google Scholar
Dubois, S.F. and Colombo, F. (2014) How picky can you be? Temporal variations in trophic niches of co-occurring suspension-feeding species. Food Webs 1, 19.Google Scholar
Duke, N.C., Meynecke, J.O., Dittmann, S., Ellison, A.M., Anger, K., Berger, U., Cannicci, S., Diele, K., Ewel, K.C., Field, C.D., Koedam, N., Lee, S.Y., Marchand, C., Nordhaus, I. and Dahdouh-Guebas, F. (2007) A world without mangroves? Science 317, 4142.Google Scholar
Faye, D., Tito de Morais, L., Raffray, J., Sadio, O., Thiaw, O.T. and Le Loc'h, F. (2011) Structure and seasonal variability of fish food webs in an estuarine tropical marine protected area (Senegal): evidence from stable isotope analysis. Estuarine Coastal and Shelf Science 92, 607617.Google Scholar
Frangoulis, C., Skliris, N., Lepoint, G., Elkalay, K., Goffart, A., Pinnegar, J.K. and Hecq, J.H. (2011) Importance of copepod carcasses versus faecal pellets in the upper water column of an oligotrophic area. Estuarine Coastal and Shelf Science 92, 456463.Google Scholar
Fry, B. (2008) Stable isotope ecology. Baton Rouge, LA: Springer.Google Scholar
Hackney, C.T. and Haines, E.B. (1980) Stable carbon isotope composition of fauna and organic matter collected in a Mississippi estuary. Estuarine Coastal and Shelf Science 10, 703708.Google Scholar
Harmelin-Vivien, M.L., Loizeau, V., Mellon, C., Beker, B., Arlhac, D., Bodiguel, X., Ferraton, F., Hermand, R., Philippon, X. and Salen-Picard, C. (2008) Comparison of C and N stable isotope ratios between surface particulate organic matter and microphytoplankton in the Gulf of Lions (NW Mediterranean). Continental Shelf Research 28, 19111919.Google Scholar
Hogarth, P.J. (1999) The biology of mangroves. Oxford: Oxford University Press.Google Scholar
Honda, K., Nakamura, Y., Nakaoka, M., Uy, W.H. and Fortes, M.D. (2013) Habitat use by fishes in coral reefs, seagrass beds and mangrove habitats in the Philippines. PLoS ONE 8, e65735.Google Scholar
Howarth, R.B. and Farber, S. (2002) Accounting for the value of ecosystem services. Ecological Economics 41, 421429.Google Scholar
Huxham, M., Kimani, E., Newton, J. and Augley, J. (2007) Stable isotope records from otoliths as tracers of fish migration in a mangrove system. Journal of Fish Biology 70, 15541567.Google Scholar
Imbert, D., Rousteau, A. and Labbe, P. (1998) Ouragans et diversité biologique dans les forêts tropicales, l'exemple de la Guadeloupe. Acta OEcologica 19, 251262.Google Scholar
Jouon, A., Douillet, P., Ouillon, S. and Fraunié, P. (2006) Calculations of hydrodynamic time parameters in a semi-opened coastal zone using a 3D hydrodynamic model. Continental Shelf Research 26, 13951415.Google Scholar
Kon, K., Kurokura, H. and Hayashizaki, K. (2007) Role of microhabitats in food webs of benthic communities in a mangrove forest. Marine Ecology Progress Series 340, 5562.Google Scholar
Kulbicki, M., Bozec, Y.M., Labrosse, P., Letourneur, Y., Mou-Tham, G. and Wantiez, L. (2005) Diet composition of carnivorous fishes from coral reef lagoons of New Caledonia. Aquatic Living Resources 18, 231250.Google Scholar
Leopold, A., Marchand, C., Deborde, J. and Allenbach, M. (2015) Temporal variability of CO2 fluxes at the sediment-air interface in mangroves (New Caledonia). Science of the Total Environment 502, 617626.Google Scholar
Letourneur, Y., Lison de Loma, T., Richard, P., Harmelin-Vivien, M.L., Cresson, P., Banaru, D., Fontaine, M.F., Gref, T. and 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, 10911102.Google Scholar
Lugendo, B.R., Nagelkerken, I., Kruitwagen, G., van der Velde, G. and Mgaya, Y.D. (2007) Relative importance of mangroves as feeding habitats for fishes: a comparison between mangrove habitats with different settings. Bulletin of Marine Sciences 80, 497512.Google Scholar
Lugendo, B.R., Nagelkerken, I., Van Der Velde, G. and Mgaya, Y.D. (2006) The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. Journal of Fish Biology 69, 16391661.Google Scholar
Marchand, C., Albéric, P., Lallier-Vergès, E. and Baltzer, F. (2006) Distribution and characteristics of dissolved organic matter in mangrove sediment pore waters along the coastline of French Guiana. Biogeochemistry 81, 5975.Google Scholar
Molnar, N., Welsh, D.T., Marchand, C., Deborde, J. and Meziane, T. (2013) Impacts of shrimp farm effluent on water quality, benthic metabolism and N-dynamics in a mangrove forest (New Caledonia). Estuarine Coastal and Shelf Science 117, 1221.Google Scholar
Mumby, P.J., Edwards, A.J., Ernesto Arias-Gonzalez, J., Lindeman, K.C., Blackwell, P.G., Gall, A., Gorczynska, M.I., Harborne, A.R., Pescod, C.L., Renken, H., Wabnitz, C. and Llewellyn, G. (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427, 533536.Google Scholar
Nagelkerken, I., Blaber, S.J.M., Bouillon, S., Green, P., Haywood, M., Kirton, L.G., Meynecke, J.O., Pawlik, J., Penrose, H.M., Sasekumar, A. and Somerfield, P.J. (2008) The habitat function of mangroves for terrestrial and marine fauna: a review. Aquatic Botany 89, 155185.Google Scholar
Nagelkerken, I., Dorenbosch, M., Verberk, W.C.E., Cocheret de la Morinière, E. and van der Velde, G. (2000) Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Marine Ecology Progress Series 202, 175192.Google Scholar
Nagelkerken, I. and van der Velde, G. (2004) Are Caribbean mangroves important feeding grounds for juvenile reef fish from adjacent seagrass beds? Marine Ecology Progress Series 274, 143151.Google Scholar
Ostrom, P.H. and Fry, B. (1993) Sources and cycling of organic matter within modern and prehistoric food webs. In Engel, M.H. and Macko, S.A. (eds) Organic geochemistry. New York, NY: Plenum Press, pp. 785798.Google Scholar
Parnell, A.C., Inger, R., Bearhop, S. and Jackson, A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5, e9672.Google Scholar
Phillips, D.L. (2001) Mixing models in analyses of diet using multiple isotopes: a critique. Oecologia 127, 166170.Google Scholar
Phillips, D.L. and Gregg, J.W. (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261269.Google Scholar
Pinnegar, J. and Polunin, N.V.C. (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225231.Google Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703710.Google Scholar
Rau, G.H., Teyssie, J.-L., Rassoulzadegan, F. and Fowler, S.W. (1990) 13C/12C and 15N/14N variations among size-fractionated marine particles: implications for their origin and trophic relationships. Marine Ecology Progress Series 59, 3338.Google Scholar
Rodelli, M.R., Gearing, J.N., Gearing, P.J., Marshall, N. and Sasekumar, A. (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61, 326333.Google Scholar
Rolff, C. and Elmgren, R. (2000) Use of riverine organic matter in plankton food webs of the Baltic Sea. Marine Ecology Progress Series 197, 81101.Google Scholar
Rozas, L.P. and Minello, T.J. (2006) Nekton use of Vallisneria americana Michx. (Wild celery) beds and adjacent habitats in Coastal Louisiana. Estuaries and Coasts 29, 297310.Google Scholar
Sepúlveda-Lozada, A., Mendoza-Carranza, M., Wolff, M., Saint-Paul, U. and Ponce-Mendoza, A. (2015) Differences in food web structure of mangroves and freshwater marshes: evidence from stable isotope studies in the Southern Gulf of Mexico. Wetlands Ecology and Management 23, 293314.Google Scholar
Serafy, J.E., Shideler, G.S., Araújo, R.J. and Nagelkerken, I. (2015) Mangroves enhance reef fish abundance at the Caribbean regional scale. PLoS ONE 10, e0142022.Google Scholar
Sheaves, M. and Molony, B. (2000) Short-circuit in the mangrove food chain. Marine Ecology Progress Series 199, 97109.Google Scholar
Tesi, T., Miserocchi, S., Goñi, M.A., Langone, L., Boldrin, A. and Turchetto, M. (2007) Organic matter origin and distribution in suspended particulate materials and surficial sediments from the western Adriatic Sea (Italy). Estuarine Coastal and Shelf Science 73, 431446.Google Scholar
Thimdee, W., Deein, G., Sangrungruang, C. and Matsunaga, K. (2004) Analysis of primary food sources and trophic relationships of aquatic animals in a mangrove-fringed estuary, Khung Krabaen Bay (Thailand) using dual stable isotope techniques. Wetlands Ecology and Management 12, 135144.Google Scholar
Thollot, P. (1992) Les poissons de mangrove du lagon sud-ouest de Nouvelle-Calédonie. PhD thesis. Université Aix-Marseille 2, Marseille, France.Google Scholar
Vaslet, A., Phillips, D.L., France, C.A.M., Feller, I.C. and Baldwin, C.C. (2012) The relative importance of mangroves and seagrass beds as feeding areas for resident and transient fishes among different mangrove habitats in Florida and Belize: evidence from dietary and stable-isotope analyses. Journal of Experimental Marine Biology and Ecology 434, 8193.Google Scholar
Vaslet, A., Phillips, D.L., France, C.A.M., Feller, I.C. and Baldwin, C.C. (2015) Trophic behaviour of juvenile reef fishes inhabiting interlinked mangrove–seagrass habitats in offshore mangrove islets. Journal of Fish Biology 87, 256273.Google Scholar
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