Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Equivalence of trophic structure between a tropical and temperate mangrove ecosystem in the Indo-Pacific

Debashish Mazumder A D , Neil Saintilan B , Fatimah M. Yusoff C and Jeffrey J. Kelleway B
+ Author Affiliations
- Author Affiliations

A Australian Nuclear Science and Technology Organisation, Locked Bag 2001, Kirrawee DC, NSW 2232, Australia.

B Department of Environmental Sciences, Macquarie University, Sydney, NSW 2109, Australia.

C Institute of Bioscience, Department of Aquaculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia.

D Corresponding author. Email: debashish.mazumder@ansto.gov.au

Marine and Freshwater Research 70(10) 1436-1444 https://doi.org/10.1071/MF18072
Submitted: 27 February 2018  Accepted: 7 March 2019   Published: 22 May 2019

Abstract

In this study we compared ecosystem trophic structure between a tropical mangrove forest at Matang, Malaysia, and a temperate mangrove forest near mangrove poleward limits at Towra Point in south-east Australia. These forests are separated by 8500 km of ocean over 45° of latitude and are of contrasting size, productivity and diversity. However, we observed a marked degree of similarity in food chain length (approximately four trophic levels in both forests), the taxonomy of key intermediate members of the food chain and the isotope signature of primary carbon sources, suggesting a strong contribution of surface organic matter rather than mangrove detritus. Common families were represented among dominant grazing herbivores, zooplanktivorous fishes, decapod crustaceans and top predators. These similarities suggest that there is some consistency in trophic interactions within two mangroves on opposite sides of the Indo-Pacific, despite a degree of evolutionary divergence in the assemblage.

Additional keywords: food chain length, carbon isotope, coevolution, fisheries, phylogenetic.


References

Abrantes, K., and Sheaves, M. (2009). Food web structure in a near-pristine mangrove area of the Australian Wet Tropics. Estuarine, Coastal and Shelf Science 82, 597–607.
Food web structure in a near-pristine mangrove area of the Australian Wet Tropics.Crossref | GoogleScholarGoogle Scholar |

Arnaud‐Haond, S., Teixeira, S., Massa, S., Billot, C., Saenger, P., Coupland, G., Duarte, C., and Serrao, E. (2006). Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Molecular Ecology 15, 3515–3525.
Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations.Crossref | GoogleScholarGoogle Scholar | 17032254PubMed |

Ashton, E. C. (2002). Mangrove sesarmid crab feeding experiments in Peninsular Malaysia. Journal of Experimental Marine Biology and Ecology 273, 97–119.
Mangrove sesarmid crab feeding experiments in Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |

Ashton, E. C., Macintosh, D. J., and Hogarth, P. J. (2003). A baseline study of the diversity and community ecology of crab and molluscan macrofauna in the Sematan mangrove forest, Sarawak, Malaysia. Journal of Tropical Ecology 19, 127–142.
A baseline study of the diversity and community ecology of crab and molluscan macrofauna in the Sematan mangrove forest, Sarawak, Malaysia.Crossref | GoogleScholarGoogle Scholar |

Bazzaz, F., and Pickett, S. (1980). Physiological ecology of tropical succession: a comparative review. Annual Review of Ecology and Systematics 11, 287–310.
Physiological ecology of tropical succession: a comparative review.Crossref | GoogleScholarGoogle Scholar |

Bersier, L.-F., and Kehrli, P. (2008). The signature of phylogenetic constraints on food-web structure. Ecological Complexity 5, 132–139.
The signature of phylogenetic constraints on food-web structure.Crossref | GoogleScholarGoogle Scholar |

Bouillon, S., Raman, A., Dauby, P., and Dehairs, F. (2002). Carbon and nitrogen stable isotope ratios of subtidal benthic invertebrates in an estuarine mangrove ecosystem (Andhra Pradesh, India). Estuarine, Coastal and Shelf Science 54, 901–913.
Carbon and nitrogen stable isotope ratios of subtidal benthic invertebrates in an estuarine mangrove ecosystem (Andhra Pradesh, India).Crossref | GoogleScholarGoogle Scholar |

Carrasco, N. K., Perissinotto, R., and Nel, H. A. (2012). Diet of selected fish species in the freshwater-deprived St Lucia Estuary, South Africa, assessed using stable isotopes. Marine Biology Research 8, 701–714.
Diet of selected fish species in the freshwater-deprived St Lucia Estuary, South Africa, assessed using stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Cattin, M.-F., Bersier, L.-F., Banašek-Richter, C., Baltensperger, R., and Gabriel, J.-P. (2004). Phylogenetic constraints and adaptation explain food-web structure. Nature 427, 835–839.
Phylogenetic constraints and adaptation explain food-web structure.Crossref | GoogleScholarGoogle Scholar | 14985761PubMed |

Chong, V. (2007). Mangroves-fisheries linkages – the Malaysian perspective. Bulletin of Marine Science 80, 755–772.

Chong, V., and Sasekumar, A. (1981). Food and feeding habits of the white prawn Penaeus merguiensis. Marine Ecology Progress Series 5, 185–191.
Food and feeding habits of the white prawn Penaeus merguiensis.Crossref | GoogleScholarGoogle Scholar |

Cohen, J. E., and Newman, C. M. (1991). Community area and food-chain length: theoretical predictions. American Naturalist 138, 1542–1554.
Community area and food-chain length: theoretical predictions.Crossref | GoogleScholarGoogle Scholar |

DeNiro, M. J., and Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.
Influence of diet on the distribution of nitrogen isotopes in animals.Crossref | GoogleScholarGoogle Scholar |

Duke, N. C. (1992). Mangrove floristics and biogeography. Tropical Mangrove Ecosystems 41, 63–100.
Mangrove floristics and biogeography.Crossref | GoogleScholarGoogle Scholar |

Duke, N., Ball, M., and Ellison, J. (1998). Factors influencing biodiversity and distributional gradients in mangroves. Global Ecology and Biogeography Letters 7, 27–47.
Factors influencing biodiversity and distributional gradients in mangroves.Crossref | GoogleScholarGoogle Scholar |

Gong, W.-K., and Ong, J.-E. (1990). Plant biomass and nutrient flux in a managed mangrove forest in Malaysia. Estuarine, Coastal and Shelf Science 31, 519–530.
Plant biomass and nutrient flux in a managed mangrove forest in Malaysia.Crossref | GoogleScholarGoogle Scholar |

Hashimoto, T. R., Saintilan, N., and Haberle, S. G. (2006). Mid‐Holocene development of mangrove communities featuring Rhizophoraceae and geomorphic change in the Richmond River Estuary, New South Wales, Australia. Geographical Research 44, 63–76.
Mid‐Holocene development of mangrove communities featuring Rhizophoraceae and geomorphic change in the Richmond River Estuary, New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Hesslein, R. H., Hallard, K., and Ramlal, P. (1993). Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50, 2071–2076.
Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N.Crossref | GoogleScholarGoogle Scholar |

Hollingsworth, A., and Connolly, R. M. (2006). Feeding by fish visiting inundated subtropical saltmarsh. Journal of Experimental Marine Biology and Ecology 336, 88–98.
Feeding by fish visiting inundated subtropical saltmarsh.Crossref | GoogleScholarGoogle Scholar |

Holt, R. D. (1996). ‘Food Webs; Integration of Patterns and Dynamics.’ (Chapman and Hall: New York, NY, USA.)

Kelleway, J., Mazumder, D., Wilson, G. G., Saintilan, N., Knowles, L., Iles, J., and Kobayashi, T. (2010). Trophic structure of benthic resources and consumers varies across a regulated floodplain wetland. Marine and Freshwater Research 61, 430–440.
Trophic structure of benthic resources and consumers varies across a regulated floodplain wetland.Crossref | GoogleScholarGoogle Scholar |

Kelleway, J. J., Saintilan, N., Macreadie, P. I., Skilbeck, C. G., Zawadzki, A., and Ralph, P. J. (2016). Seventy years of continuous encroachment substantially increases ‘blue carbon’ capacity as mangroves replace intertidal salt marshes. Global Change Biology 22, 1097–1109.
Seventy years of continuous encroachment substantially increases ‘blue carbon’ capacity as mangroves replace intertidal salt marshes.Crossref | GoogleScholarGoogle Scholar | 26670941PubMed |

Kelleway, J. J., Mazumder, D., Baldock, J. A., and Saintilan, N. (2018). Carbon isotope fractionation in the mangrove Avicennia marina has implications for food web and blue carbon research. Estuarine, Coastal and Shelf Science 205, 68–74.
Carbon isotope fractionation in the mangrove Avicennia marina has implications for food web and blue carbon research.Crossref | GoogleScholarGoogle Scholar |

Laegdsgaard, P., and Johnson, C. R. (1995). Mangrove habitats as nurseries: unique assemblages of juvenile fish in subtropical mangroves in eastern Australia. Marine Ecology Progress Series 126, 67–81.
Mangrove habitats as nurseries: unique assemblages of juvenile fish in subtropical mangroves in eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Lai, S.-M., Liu, W.-C., and Jordán, F. (2012). On the centrality and uniqueness of species from the network perspective. Biology Letters 8, 570–573.
On the centrality and uniqueness of species from the network perspective.Crossref | GoogleScholarGoogle Scholar | 22357938PubMed |

Legendre, P., and Legendre, L. F. (2012). ‘Numerical Ecology.’ (Elsevier: Amsterdam, Netherlands.)

Luczkovich, J. J., Borgatti, S. P., Johnson, J. C., and Everett, M. G. (2003). Defining and measuring trophic role similarity in food webs using regular equivalence. Journal of Theoretical Biology 220, 303–321.
Defining and measuring trophic role similarity in food webs using regular equivalence.Crossref | GoogleScholarGoogle Scholar | 12468282PubMed |

Mazumder, D. (2009). ‘Ecology of Burrowing Crabs in Temperate Saltmarsh of South-east Australia.’ (CSIRO Publishing: Melbourne, Vic., Australia.)

Mazumder, D., and Saintilan, N. (2010). Mangrove leaves are not an important source of dietary carbon and nitrogen for crabs in temperate Australian mangroves. Wetlands 30, 375–380.
Mangrove leaves are not an important source of dietary carbon and nitrogen for crabs in temperate Australian mangroves.Crossref | GoogleScholarGoogle Scholar |

Mazumder, D., Saintilan, N., and Williams, R. J. (2005). Temporal variations in fish catch using pop nets in mangrove and saltmarsh flats at Towra Point, NSW, Australia. Wetlands Ecology and Management 13, 457–467.
Temporal variations in fish catch using pop nets in mangrove and saltmarsh flats at Towra Point, NSW, Australia.Crossref | GoogleScholarGoogle Scholar |

Mazumder, D., Saintilan, N., and Williams, R. J. (2006a). Fish assemblages in three tidal saltmarsh and mangrove flats in temperate NSW, Australia: a comparison based on species diversity and abundance. Wetlands Ecology and Management 14, 201–209.
Fish assemblages in three tidal saltmarsh and mangrove flats in temperate NSW, Australia: a comparison based on species diversity and abundance.Crossref | GoogleScholarGoogle Scholar |

Mazumder, D., Saintilan, N., and Williams, R. J. (2006b). Trophic relationships between itinerant fish and crab larvae in a temperate Australian saltmarsh. Marine and Freshwater Research 57, 193–199.
Trophic relationships between itinerant fish and crab larvae in a temperate Australian saltmarsh.Crossref | GoogleScholarGoogle Scholar |

Mazumder, D., Williams, R. J., Reid, D., Saintilan, N., and Szymczak, R. (2008). Variability of stable isotope ratios of glassfish (Ambassis jacksoniensis) from mangrove/saltmarsh environments in southeast Australia and implications for choosing sample size. Environmental Bioindicators 3, 114–123.
Variability of stable isotope ratios of glassfish (Ambassis jacksoniensis) from mangrove/saltmarsh environments in southeast Australia and implications for choosing sample size.Crossref | GoogleScholarGoogle Scholar |

Mazumder, D., Iles, J., Kelleway, J., Kobayashi, T., Knowles, L., Saintilan, N., and Hollins, S. (2010). Effect of acidification on elemental and isotopic compositions of sediment organic matter and macro-invertebrate muscle tissues in food web research. Rapid Communications in Mass Spectrometry 24, 2938–2942.
Effect of acidification on elemental and isotopic compositions of sediment organic matter and macro-invertebrate muscle tissues in food web research.Crossref | GoogleScholarGoogle Scholar | 20872625PubMed |

Mazumder, D., Saintilan, N., Williams, R. J., and Szymczak, R. (2011). Trophic importance of a temperate intertidal wetland to resident and itinerant taxa: evidence from multiple stable isotope analyses. Marine and Freshwater Research 62, 11–19.
Trophic importance of a temperate intertidal wetland to resident and itinerant taxa: evidence from multiple stable isotope analyses.Crossref | GoogleScholarGoogle Scholar |

McPhee, J. J., Freewater, P., Gladstone, W., Platell, M. E., and Schreider, M. J. (2015). Glassfish switch feeding from thalassinid larvae to crab zoeae after tidal inundation of saltmarsh. Marine and Freshwater Research 66, 1037–1044.
Glassfish switch feeding from thalassinid larvae to crab zoeae after tidal inundation of saltmarsh.Crossref | GoogleScholarGoogle Scholar |

Melville, A. J., and Connolly, R. (2003). Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136, 499–507.
Spatial analysis of stable isotope data to determine primary sources of nutrition for fish.Crossref | GoogleScholarGoogle Scholar | 12774226PubMed |

Menge, B. A., and Sutherland, J. P. (1987). Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. American Naturalist 130, 730–757.
Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment.Crossref | GoogleScholarGoogle Scholar |

Micheli, F. (1993). Feeding ecology of mangrove crabs in north eastern Australia: mangrove litter consumption by Sesarma messa and Sesarma smithii. Journal of Experimental Marine Biology and Ecology 171, 165–186.
Feeding ecology of mangrove crabs in north eastern Australia: mangrove litter consumption by Sesarma messa and Sesarma smithii.Crossref | GoogleScholarGoogle Scholar |

Nagelkerken, I., Blaber, S., Bouillon, S., Green, P., Haywood, M., Kirton, L., Meynecke, J.-O., Pawlik, J., Penrose, H., and Sasekumar, A. (2008). The habitat function of mangroves for terrestrial and marine fauna: a review. Aquatic Botany 89, 155–185.
The habitat function of mangroves for terrestrial and marine fauna: a review.Crossref | GoogleScholarGoogle Scholar |

Odum, E. P. (1959). ‘Fundamentals of Ecology.’ (WB Saunders Company: Philadelphia, PA, USA.)

Phillips, D. L., and Gregg, J. W. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.
Source partitioning using stable isotopes: coping with too many sources.Crossref | GoogleScholarGoogle Scholar | 12759813PubMed |

Pinnegar, J., and Polunin, N. (1999). Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.
Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions.Crossref | GoogleScholarGoogle Scholar |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |

Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J., Montaña, C. G., and Rosenheim, J. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.
Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses.Crossref | GoogleScholarGoogle Scholar | 17225157PubMed |

Qin, H., Sheng, Q., Chu, T., Wang, S., and Wu, J. (2015). Import and export fluxes of macrozooplankton are taxa- and season-dependent at Jiuduansha Marsh, Yangtze River estuary. Estuarine, Coastal and Shelf Science 163, 254–264.
Import and export fluxes of macrozooplankton are taxa- and season-dependent at Jiuduansha Marsh, Yangtze River estuary.Crossref | GoogleScholarGoogle Scholar |

Resetarits, W. J., and Chalcraft, D. R. (2007). Functional diversity within a morphologically conservative genus of predators: implications for functional equivalence and redundancy in ecological communities. Functional Ecology 21, 793–804.
Functional diversity within a morphologically conservative genus of predators: implications for functional equivalence and redundancy in ecological communities.Crossref | GoogleScholarGoogle Scholar |

Ricardo, G. F., Davis, A. R., Knott, N. A., and Minchinton, T. E. (2014). Diel and tidal cycles regulate larval dynamics in salt marshes and mangrove forests. Marine Biology 161, 769–784.
Diel and tidal cycles regulate larval dynamics in salt marshes and mangrove forests.Crossref | GoogleScholarGoogle Scholar |

Robertson, A. (1986). Leaf-burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora spp.) in northeastern Australia. Journal of Experimental Marine Biology and Ecology 102, 237–248.
Leaf-burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora spp.) in northeastern Australia.Crossref | GoogleScholarGoogle Scholar |

Rodelli, M. R., Gearing, J., Gearing, P., Marshall, N., and Sasekumar, A. (1984). Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61, 326–333.
Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems.Crossref | GoogleScholarGoogle Scholar | 28311057PubMed |

Saintilan, N. (2004). Relationships between estuarine geomorphology, wetland extent and fish landings in New South Wales estuaries. Estuarine, Coastal and Shelf Science 61, 591–601.
Relationships between estuarine geomorphology, wetland extent and fish landings in New South Wales estuaries.Crossref | GoogleScholarGoogle Scholar |

Sasekumar, A., and Chong, V. C. (1987). ‘Mangroves and Prawns: Further Perspectives.’ (University of Malaya: Kuala Lumpur, Malaysia.)

Schoener, T. W. (1989). Food webs from the small to the large: the Robert H. MacArthur Award Lecture. Ecology 70, 1559–1589.
Food webs from the small to the large: the Robert H. MacArthur Award Lecture.Crossref | GoogleScholarGoogle Scholar |

Skov, M. W., and Hartnoll, R. G. (2002). Paradoxical selective feeding on a low-nutrient diet: why do mangrove crabs eat leaves? Oecologia 131, 1–7.
Paradoxical selective feeding on a low-nutrient diet: why do mangrove crabs eat leaves?Crossref | GoogleScholarGoogle Scholar | 28547499PubMed |

Thompson, J. N. (1999). Specific hypotheses on the geographic mosaic of coevolution. American Naturalist 153, S1–S14.
Specific hypotheses on the geographic mosaic of coevolution.Crossref | GoogleScholarGoogle Scholar |

Weiss, C., Weiss, J., Boy, J., Iskandar, I., Mikutta, R., and Guggenberger, G. (2016). Soil organic carbon stocks in estuarine and marine mangrove ecosystems are driven by nutrient colimitation of P and N. Ecology and Evolution 6, 5043–5056.
Soil organic carbon stocks in estuarine and marine mangrove ecosystems are driven by nutrient colimitation of P and N.Crossref | GoogleScholarGoogle Scholar | 27547332PubMed |

Zamora, R. (1999). Conditional outcomes of interactions: the pollinator–prey conflict of an insectivorous plant. Ecology 80, 786–795.

Zamora, R. (2000). Functional equivalence in plant–animal interactions: ecological and evolutionary consequences. Oikos 88, 442–447.
Functional equivalence in plant–animal interactions: ecological and evolutionary consequences.Crossref | GoogleScholarGoogle Scholar |