Importance of Mangrove Carbon for Aquatic Food Webs in Wet–Dry Tropical Estuaries

Estuaries and Coasts

Volumn 38, Issue 1, 2015, Pages 383-399

  Abrantes, Kátya G ^a   Johnston, Ross ^a   Connolly, Rod M ^b   Sheaves, Marcus ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

Bayesian mixing models; Estuaries; Food webs; Mangroves; Stable isotope analysis; 13C

Indexed keywords

EID: 84939894790     PISSN: 15592723     EISSN: 15592731     Source Type: Journal    
DOI: 10.1007/s12237-014-9817-2     Document Type: Article

References (98)

1. Abrantes, K., and M. Sheaves. 2008. Incorporation of terrestrial wetland material into aquatic food webs in a tropical estuarine wetland. Estuarine, Coastal and Shelf Science 80: 401–412.
2. Abrantes, K., and M. Sheaves. 2009a. Food web structure in a near-pristine mangrove area of the Australian Wet Tropics. Estuarine, Coastal and Shelf Science 82: 597–607.
3. Abrantes, K., and M. Sheaves. 2009b. Sources of nutrition supporting juvenile penaeid prawns in an Australian dry tropics estuary. Marine and Freshwater Research 60: 949–959.
4. Abrantes, K.G., and M. Sheaves. 2010. Importance of freshwater flow in terrestrial-aquatic energetic connectivity in intermittently connected estuaries of tropical Australia. Marine Biology 157: 2071–2086.
5. Abrantes, K. G, Barnett, A, Marwick, T. R, Bouillon S. 2013. Importance of terrestrial subsidies for estuarine food webs in contrasting east African catchments. Ecosphere 4:Art14
6. Al-Maslamani, I., M. Walton, H. Kennedy, M. Al-Mohannadi, and L. Le Vay. 2013. Are mangroves in arid environments isolated systems? Life-history and evidence of dietary contribution from inwelling in a mangrove-resident shrimp species. Estuarine, Coastal and Shelf Science 124: 56–63.
7. Alongi, D.M. 1988. Bacterial productivity and microbial biomass in tropical mangrove sediments. Microbial Ecology 15: 59–79.
8. Alongi, D.M. 1994. Zonation and seasonality of benthic primary production and community respiration in tropical mangrove forests. Oecologia 98: 320–327.
9. Alongi, D.M., P. Christoffersen, and F. Tirendi. 1993. The influence of forest type on microbial-nutrient relationships in tropical mangrove sediments. Journal of Experimental Marine Biology and Ecology 171: 201–223.
10. Baker, R., and M. Sheaves. 2009. Refugees or ravenous predators: detecting predation on new recruits to tropical estuarine nurseries. Wetlands Ecology and Management 17: 317–330.
11. Barnes, C., C.J. Sweeting, S. Jennings, J.T. Barry, and N.V.C. Polunin. 2007. Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Functional Ecology 21: 356–362.
12. Beck, M.W., K.L. Heck Jr., K.W. Able, D.L. Childers, D.B. Eggleston, B.M. Gillanders, B. Halpern, C.G. Hays, K. Hoshino, T.J. Minello, R.J. Orth, P.F. Sheridan, and M.P. Weinstein. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51: 633–641.
13. Blanchard, G.F., J.-M. Guarini, P. Richard, P. Gros, and F. Mornet. 1996. Quantifying the short-term temperature effect on light-saturated photosynthesis of intertidal microphytobenthos. Marine Ecology Progress Series 134: 309–313.
14. Bond, A.L., and A.W. Diamond. 2011. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21: 1017–1023.
15. Boon, P.I., F.L. Bird, and S.E. Bunn. 1997. Diet of the intertidal callianassid shrimps Biffarius arenosus and Trypea australiensis (Decapoda:Thalassinidea) in Western Port (southern Australia), determined with multiple stable-isotope analyses. Marine and Freshwater Research 48: 503–511.
16. Bouillon, S., P.C. Mohan, N. Sreenivas, and F. Dehairs. 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: 79–92.
17. Bouillon, S., T. Moens, I. Overmeer, N. Koedam, and F. Dehairs. 2004. Resource utilization patterns of epifauna from mangrove forests with contrasting inputs of local versus imported organic matter. Marine Ecology Progress Series 278: 77–88.
18. Bouillon, S., J.J. Middelburg, F. Dehairs, A.V. Borges, G. Abril, M.R. Flindt, S. Ulomi, and E. Kristensen. 2007. Importance of intertidal sediment processes and porewater exchange on the water column biogeochemistry in a pristine mangrove creek (Ras Dege, Tanzania). Biogeosciences 4: 311–322.
19. Bouillon, S., R.M. Connolly, and S.Y. Lee. 2008. Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research 59: 44–58.
20. Bouillon, S., R.M. Connolly, and D.P. Gillikin. 2011. Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. In Treatise on Estuarine and Coastal Science, ed. E. Wolanski and D.S. McLusky. Waltham: Academic Press.
21. Boys, C.A., F.J. Kroon, T.M. Glasby, and K. Wilkinson. 2012. Improved fish and crustacean passage in tidal creeks following floodgate remediation. Journal of Applied Ecology 49: 223–233.
22. Buchheister, A., and R.J. Latour. 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Canadian Journal of Fisheries and Aquatic Sciences 67: 445–461.
23. 13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Animal Ecology 46: 443–453.
24. Cerling, T.E., J.M. Harris, B.J. MacFadden, M.G. Leakey, J. Quade, V. Eisenmann, and J.R. Ehleringer. 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature 389: 153–158.
25. Chanton, J., and F.G. Lewis. 2002. Examination of coupling between primary and secondary production in a river-dominated estuary: Apalachicola Bay, Florida, USA. Limnology and Oceanography 47: 683–697.
26. Chong, V.C., C.B. Low, and T. Ichikawa. 2001. Contribution of mangrove detritus to juvenile prawn nutrition: a dual stable isotope study in a Malaysian mangrove forest. Marine Biology 138: 77–86.
27. Clementz, M.T., and P.L. Koch. 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129: 461–472.
28. Cloern, J.E., E.A. Canuel, and D. Harris. 2002. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47: 713–729.
29. Clough, B. 1998. Mangrove forest productivity and biomass accumulation in Hinchinbrook Channel, Australia. Mangroves and Salt Marshes 2: 191–198.
30. Cole, J.J., S.R. Carpenter, M.L. Pace, M.C. Van de Bogert, J.L. Kitchell, and J.R. Hodgson. 2006. Differential support of lake food webs by three types of terrestrial organic carbon. Ecology Letters 9: 558–568.
31. Dahlgren, C.P., G. Kellison, A.J. Adams, B.M. Gillanders, M.S. Kendall, C.A. Layman, J.A. Ley, I. Nagelkerken, and J.E. Serafy. 2006. Marine nurseries and effective juvenile habitats: concepts and applications. Marine Ecology Progress Series 312: 291–295.
32. De’ath, G., and K.E. Fabricius. 2000. Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81: 3178–3192.
33. DeNiro, M.J., and S. Epstein. 1978. Influence of diet in the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495–506.
34. Elsdon, T.S., S. Ayvazian, K.W. McMahon, and S.R. Thorrold. 2010. Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Marine Ecology Progress Series 408: 195–205.
35. Erskine, W.D., M.J. Saynor, L. Erskine, K.G. Evans, and D.R. Moliere. 2005. A preliminary typology of Australian tropical rivers and implications for fish community ecology. Marine and Freshwater Research 56: 253–267.
36. Finlayson, B., and T. McMahon. 1988. Australia vs the world: a comparative analysis of streamflow characteristics. In Fluvial Geomorphology of Australia, ed. R. Werner. Sydney: Academic Press.
37. France, R.L. 1996. Scope for use of stable carbon isotopes in discerning the incorporation of forest detritus into aquatic foodwebs. Hydrobiologia 325: 219–222.
38. Fry, B. 1981. Natural stable carbon isotope tag traces Texas shrimp migrations. Fishery Bulletin 79: 337–345.
39. Fry, B. 2002. Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25: 264–271.
40. Fry, B., and K.C. Ewel. 2003. Using stable isotopes in mangrove fisheries research—a review and outlook. Isotopes in Environmental and Health Studies 39: 191–196.
41. Giarrizzo, T., R. Schwamborn, and U. Saint-Paul. 2011. Utilization of carbon sources in a northern Brazilian mangrove ecosystem. Estuarine Coastal and Shelf Science 95: 447–457.
42. 13C-DIC and phytoplankton. Organic Geochemistry 37: 1371–1382.
43. Gorokhova, E., and S. Hansson. 1999. An experimental study on variations in stable carbon and nitrogen fractionation during growth of Mysis mixta and Neomysis integer. Canadian Journal of Fisheries and Aquatic Sciences 56: 2203–2210.
44. 15N in different tissues of juvenile sand goby Pomatoschistus minutus: a laboratory diet-switch experiment. Marine Ecology Progress Series 341: 205–215.
45. 15N for three estuarine producers, Sporobolus virginicus, Zostera capricorni, and epiphytes of Z. capricorni. Aquatic Botany 79: 87–94.
46. Haywood, M.D.E., and D.J. Staples. 1993. Field estimates of growth and mortality of juvenile banana prawns (Penaeus merguiensis). Marine Biology 116: 407–416.
47. Heithaus, E.R., P.A. Heithaus, M.R. Heithaus, D. Burkholder, and C.A. Layman. 2011. Trophic dynamics in a relatively pristine subtropical fringing mangrove community. Marine Ecology Progress Series 428: 49–61.
48. Hemminga, M.A., and M.A. Mateo. 1996. Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Marine Ecology Progress Series 140: 285–298.
49. Hoover, R.S., D. Hoover, M. Miller, M.R. Landry, E.H. DeCarlo, and F.T. Mackenzie. 2006. Zooplankton response to storm runoff in a tropical estuary: bottom-up and top-down controls. Marine Ecology Progress Series 318: 187–201.
50. Igulu, M., I. Nagelkerken, G. van der Velde, and Y. Mgaya. 2013. Mangrove fish production is largely fuelled by external food sources: a stable isotope analysis of fishes at the individual, species, and community levels from across the globe. Ecosystems 16: 1336–1352.
51. Jennerjahn, T.C., and V. Ittekkot. 2002. Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89: 23–30.
52. Kristensen, E., S. Bouillon, T. Dittmar, and C. Marchand. 2008. Organic carbon dynamics in mangrove ecosystems: a review. Aquatic Botany 89: 201–219.
53. Lancaster, J., and S. Waldron. 2001. Stable isotope values of lotic invertebrates: sources of variation, experimental design, and statistical interpretation. Limnology and Oceanography 46: 723–730.
54. Layman, C.A. 2007. What can stable isotope ratio reveal about mangroves as fish habitat? Bulletin of Marine Science 80: 513–527.
55. Lin, H.-J., W.-Y. Kao, and Y.-T. Wang. 2007. Analyses of stomach contents and stable isotopes reveal food sources of estuarine detritivorous fish in tropical/subtropical Taiwan. Estuarine, Coastal and Shelf Science 73: 527–537.
56. Loneragan, N.R., S.E. Bunn, and D.M. Kellaway. 1997. Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable-isotope study. Marine Biology 130: 289–300.
57. Lotze, H.K., H.S. Lenihan, B.J. Bourque, R.H. Bradbury, R.G. Cooke, M.C. Kay, S.M. Kidwell, M.X. Kirby, C.H. Peterson, and J.B.C. Jackson. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312: 1806–1809.
58. Maher, D.T., I.R. Santos, L. Golsby-Smith, J. Gleeson, and B.D. Eyre. 2013. Groundwater-derived dissolved inorganic and organic carbon exports from a mangrove tidal creek: the missing mangrove carbon sink? Limnology and Oceanography 58: 475–488.
59. Marczak, L.B., R.M. Thompson, and J.S. Richardson. 2007. Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88: 140–148.
60. Mavuti, K.M., J.A. Nyunja, and E.O. Wakwabi. 2007. Trophic ecology of some common juvenile fish species in Mtwapa Creek, Kenya. West Indian Ocean Journal of Marine Science 3: 179–188.
61. Mazumder, D., R.J. Williams, D. Reir, N. Saintilan, and R. Szymczak. 2008. Variability of stable isotope ratios of glassfish (Ambassis jacksoniensis) from mangrove/saltmarsh environments in southeast Australia and emplications for choosing sample size. Environmental Bioindicators 3: 114–123.
62. McCutchan, J.H., W.M. Lewis Jr., C. Kendall, and C.C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102: 378–390.
63. Nagelkerken, I., and G. van der Velde. 2004. Are Caribbean mangroves important feeding grounds for juvenile reef fish from adjacent seagrass beds? Marine Ecology Progress Series 274: 143–151.
64. Newell, R.I.E., N. Marshall, A. Sasekumar, and V.C. Chong. 1995. Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Marine Biology 123: 595–606.
65. Nyunja, J., M. Ntiba, J. Onyari, K. Mavuti, K. Soetaert, and S. Bouillon. 2009. Carbon sources supporting a diverse fish community in a tropical coastal ecosystem (Gazi Bay, Kenya). Estuarine, Coastal and Shelf Science 83: 333–341.
66. Parnell, A.C., R. Inger, S. Bearhop, and A.L. Jackson. 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5: e9672.
67. Peel, M.C., B.L. Finlayson, and T.A. McMahon. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences Discussions 4: 439–473.
68. Peterson, B.J., R.W. Howarth, and R.H. Garritt. 1986. Sulfur and carbon isotopes as tracers of salt-marsh organic matter flow. Ecology 67: 865–874.
69. Polis, G.A., W.B. Anderson, and R.D. Holt. 1997. Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28: 289–316.
70. Post, D.M. 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83: 703–718.
71. Post, D.M., C.A. Layman, D.A. Arrington, G. Takimoto, J. Quattrochi, and C.G. Montanã. 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189.
72. Ridd, P.V., and T. Stieglitz. 2002. Dry season salinity changes in arid estuaries fringed by mangroves and saltflats. Estuarine, Coastal and Shelf Science 54: 1039–1049.
73. Ridd, P., R. Sam, S. Hollins, and G. Brunskill. 1997. Water, salt and nutrient fluxes of tropical tidal salt flats. Mangroves and Salt Marshes 1: 229–238.
74. Robertson, A.I. 1988. Abundance, diet and predators of juvenile banana prawns, Penaeus merguiensis, in a tropical mangrove estuary. Australian Journal of Marine & Freshwater Research 39: 467–478.
75. Robertson, A.I., and S.J.M. Blaber. 1992. Plankton, epibenthos and fish communities. In Tropical Mangrove Ecossystems, Book 41, ed. A.I. Robertson and D.M. Alongi. Washington, DC: American Geophysical Union.
76. Robertson, A.I., and N.C. Duke. 1990. Recruitment, growth and residence time of fishes in a tropical Australian mangrove system. Estuarine, Coastal and Shelf Science 31: 723–743.
77. Robertson, A.I., P. Dixon, and P.A. Daniel. 1988. Zooplankton dynamics in mangrove and other nearshore habitats in tropical Australia. Marine Ecology Progress Series 43: 139–150.
78. Rodelli, M.R., J.N. Gearing, P.J. Gearing, N. Marshall, and A. Sasekumar. 1984. Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61: 326–333.
79. Schlacher, T.A., A.J. Skillington, R.M. Connolly, W. Robinson, and T.F. Gaston. 2008. Coupling between marine plankton and freshwater flow in the plumes off a small estuary. International Review of Hydrobiology 93: 641–658.
80. Schlacher, T.A., R.M. Connolly, A.J. Skillington, and T.F. Gaston. 2009. Can export of organic matter from estuaries support zooplankton in nearshore, marine plumes? Aquatic Ecology 43: 383–393.
81. Sheaves, M. 1996. Do spatial differences in the abundance of two serranid fishes in estuaries of tropical australia reflect long-term salinity patterns? Marine Ecology Progress Series 137: 39–49.
82. Sheaves, M., and R. Johnston. 2009. Ecological drivers of spatial variability among fish fauna of 21 tropical Australian estuaries. Marine Ecology Progress Series 385: 245–260.
83. Sheaves, M., and R. Johnston. 2010. Implications of spatial variability of fish assemblages for monitoring of Australia’s tropical estuaries. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 348–356.
84. Sheaves, M., and B. Molony. 2000. Short-circuit in the mangrove food chain. Marine Ecology Progress Series 199: 97–109.
85. Sheaves, M., R. Johnston, and R. Connolly. 2010. Temporal dynamics of fish assemblages of natural and artificial tropical estuaries. Marine Ecology Progress Series 410: 143–157.
86. Sheaves, M., R. Johnston, and R.M. Connolly. 2012. Fish assemblages as indicators of estuary ecosystem health. Wetlands Ecology and Management 20: 477–490.
87. Sheaves, M., R. Johnston, A. Johnson, R. Baker, and R. Connolly. 2013. Nursery function drives temporal patterns in fish assemblage structure in four tropical estuaries. Estuaries and Coasts 36: 893–905.
88. Sheaves, M., J. Brookes, R. Coles, M. Freckelton, P. Groves, R. Johnston, and P. Winberg. 2014. Repair and revitalisation of Australia's tropical estuaries and coastal wetlands: opportunities and constraints for the reinstatement of lost function and productivity. Marine Policy 47: 23–38.
89. Suring, E., and S.R. Wing. 2009. Isotopic turnover rate and fractionation in multiple tissues of red rock lobster (Jasus edwardsii) and blue cod (Parapercis colias): consequences for ecological studies. Journal of Experimental Marine Biology and Ecology 370: 56–63.
90. Vance, D.J., M.D.E. Haywood, D.S. Heales, R.A. Kenyon, N.R. Loneragan, and R.C. Pendrey. 1996. How far do prawns and fish move into mangroves? Distribution of juvenile banana prawns Penaeus merguiensis and fish in a tropical mangrove forest in northern Australia. Marine Ecology Progress Series 131: 115–124.
91. 13C trophic fractionation: implication for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.
92. Vaslet, A., D.L. Phillips, C. France, I.C. Feller, and C.C. Baldwin. 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 434–435: 81–93.
93. Wai, T.-C., J.S. Ng, K.M. Leung, D. Dudgeon, and G.A. Williams. 2008. The source and fate of organic matter and the significance of detrital pathways in a tropical coastal ecosystem. Limnology and Oceanography 53: 1479–1492.
94. Wai, T.-C., K.M.Y. Leung, S.Y.T. Sin, A. Cornish, D. Dudgeon, and G.A. Williamsa. 2011. Spatial, seasonal, and ontogenetic variations in the significance of detrital pathways and terrestrial carbon for a benthic shark, Chiloscyllium plagiosum (Hemiscylliidae), in a tropical estuary. Limnology and Oceanography 56: 1035–1053.
95. 13C addition. Canadian Journal of Fisheries and Aquatic Sciences 68: 387–399.
96. Wilson, J.P., and M. Sheaves. 2001. Short-term temporal variations in taxonomic composition and trophic structure of a tropical estuarine fish assemblage. Marine Biology 139: 787–796.
97. Yokoyama, H., A. Tamaki, K. Harada, K. Shimoda, K. Koyama, and Y. Ishihi. 2005. Variability of diet-tissue isotopic fractionation in estuarine macrobenthos. Marine Ecology Progress Series 296: 115–128.
98. Zagars, M., K. Ikejima, A. Kasai, N. Arai, and P. Tongnunui. 2013. Trophic characteristics of a mangrove fish community in Southwest Thailand: Important mangrove contribution and intraspecies feeding variability. Estuarine Coastal and Shelf Science 119: 145–152.