Abstract
Intertidal crabs are abundant, key components of tropical estuaries whose trophic interactions provide a direct and identifiable link within the ecosystem. Our study investigated spatial variability in food resource use of intertidal crabs, using stable isotope (δ13C and δ15N) values. This was done for two genera with contrasting feeding strategies (specialist Uca vs. generalist Metopograpsus) within and among locations in North Queensland, Australia. Uca coarctata, Uca seismella, Metopograpsus frontalis, and Metopograpsus latifrons occupied distinct isotopic niches, as quantified by standard ellipse areas. Bayesian mixing models suggested a diet supported by microphytobenhos for Uca species and a more depleted source for Metopograpsus species. Evidence for opportunistic feeding at higher trophic levels by Metopograpsus spp. was reflected by higher δ15N values compared to Uca species. Differences in diet between Uca and Metopograpsus, based on isotopic data, were maintained among ten locations across five estuaries. Food resource use was more variable for Metopograpsus spp. compared to Uca spp. among locations, reflecting the opportunistic feeding of the former. Sewage pollution was echoed in augmented δ15N values of all species. Results revealed separate trophic niches for both generalist and specialist feeding intertidal crab species across the estuarine landscape. The isotopic patterns of Uca spp. and Metopograpsus spp. fitted within the wider intertidal crab community, with generally low overlap among species within individual habitats. The greater flexibility in food resource use by generalists among locations could potentially provide a buffer against changes in food availability. We argue that patterns in food-resource use need to be considered in response to anthropogenic changes in the estuarine landscape.
Similar content being viewed by others
References
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.
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.
Abrantes KG, Johnston R, Connolly RM, Sheaves M (2014) Importance of mangrove carbon from aquatic food webs in wet-dry tropical estuaries. Estuaries and Coasts
Albano, M.J., P.C. Lana, C. Bremec, R. Elias, C.C. Martins, N. Venturini, P. Muniz, S. Rivero, E.A. Vallarino, and S. Obenat. 2013. Macrobenthos and multi-molecular markers as indicators of environmental contamination in a South American port (Mar del Plata, Southwest Atlantic). Marine Pollution Bulletin 73: 102–114.
Alongi, D.M. 2002. Present state and future of the world’s mangrove forests. Environmental Conservation 29: 331–349.
Alongi, D.M. 2008. Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuarine, Coastal and Shelf Science 76: 1–13.
Arruda Bezerra, L.E., C.B. Dias, G.X. Santana, and H. Matthews-Cascon. 2006. Spatial distribution of fiddler crabs (genus Uca) in a tropical mangrove of northeast Brazil. Scientia marina 70: 759–766.
Bartolini, F., G. Penha-Lopes, S. Limbu, J. Paula, and S. Cannicci. 2009. Behavioural responses of the mangrove fiddler crab (Uca annulipes and U. inversa) to urban sewage loadings: results of a mesocosm approach. Marine Pollution Bulletin 58: 1860–1867.
Batschelet, E. 1981. Circular statistics in biology. London: Academic Press.
Bearhop, S., C.E. Adams, S. Waldron, R.A. Fuller, and H. Macleod. 2004. Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73: 1007–1012.
Bouillon, S., N. Koedam, A.V. Raman, and F. Dehairs. 2002. Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130: 441–448.
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.
Cannicci, S., S. Ritossa, R.K. Ruwa, and M. Vannini. 1996. Tree fidelity and hole fidelity in the tree crab Sesarma leptosoma (Decapoda, Grapsidae). Journal of Experimental Marine Biology and Ecology 196: 299–311.
Cannicci, S., S. Fratini, and M. Vannini. 1999. Use of time, space and food resources in the mangrove climbing crab Selatium elongatum (Grapsidae, Sesarmidae). Marine Biology 135: 335–339.
Cannicci, S., F. Bartolini, F. Dahdouh-Guebas, S. Fratini, C. Litulo, A. Macia, E.J. Mrabu, G. Penha-Lopes, and J. Paula. 2009. Effects of urban wastewater on crab and mollusc assemblages in equatorial and subtropical mangroves of East Africa. Estuarine, Coastal and Shelf Science 84: 305–317.
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.
Cloern, J.E., E.A. Cannuel, and D. Harris. 2002. Stable carbon and nitrogen composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47: 7113–7729.
Costanza, R., R. d'Arge, R. de Groot, S. Farberk, M. Grazzo, B. Hannon, K. Limburg, S. Naeem, R.V. O'Neill, J. Paruelo, R.G. Raskin, P. Sutton, and M. van den Belt. 1997. The value of the world’s ecosystem services and natural capital. Nature 387: 253–260.
DeNiro, M.J., and S. Epstein. 1978. Influence of diet in the distribution of carbon isotopes in animals. Geochimica et Cosmochimica 42: 495–506.
Duke, N.C., J.O. Meynecke, S. Dittmann, A.M. Ellison, K. Anger, U. Berger, S. Cannicci, K. Diele, K.C. Ewel, C.D. Field, N. Koedam, S.Y. Lee, C. Marchand, I. Nordhaus, and F. Dahdouh-Guebas. 2007. A world without mangroves. Science 317: 41–42.
Fausch, K.D., C.E. Torgersen, C.V. Baxter, and H.W. Li. 2002. Landscapes to riverscapes: bridging the gap between research and conservation of stream fishes. BioScience 52: 483–498.
Fratini, S., S. Cannicci, L.M. Abincha, and M. Vannini. 2000. Feeding, temporal and spatial preferences of Metopograpsus thukuhar (Decapoda; Graspidae): an opportunistic mangrove dweller. Journal of Crustacean Biology 20: 326–333.
Fry, B. 1981. Natural stable carbon isotope tag traces Texas shrimp migrations. Fishery Bulletin 79: 337–345.
Fry, B., M. Cieri, C. Tobias, L.A. Deegan, and B. Peterson. 2008. Stable isotope monitoring of benthic–planktonic coupling using salt marsh fish. Marine Ecology Progress Series 369: 193–204.
Guest, M., R.M. Connolly, and N. Loneragan. 2004. Within and among site variability in δ13C and δ15N for three estuarine producers, Sporobolus virginicus, Zostera capricorni, and epiphytes of Z. capricorni. Aquatic Botany 79: 87–94.
Hsieh, H., C. Chen, Y. Chen, and H. Yang. 2002. Diversity of benthic organic matter flows through polychaetes and crabs in a mangrove estuary: δ13C and δ34S signals. Marine Ecology Progress Series 227: 145–155.
Icely, J.D., and D.A. Jones. 1978. Factors affecting the distribution of the genus Uca (Crustacea: Ocypodidae) on an East African shore. Estuarine and Coastal Marine Science 6: 315–325.
Jackson, A.L., R. Inger, A.C. Parnell, and S. Bearhop. 2011. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.
Koch, V., and M. Wolff. 2002. Energy budget and ecological role of mangrove epibenthos in the Caeté estuary, North Brazil. Marine Ecology Progress Series 228: 119–130.
Kristensen, E. 2008. Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. Journal of Sea Research 59: 30–43.
Kristensen, D.K., E. Kristensen, and P. Mangion. 2010. Food partitioning of leaf-eating mangrove crabs (Sesarminae): experimental and stable isotope (13C and 15 N) evidence. Estuarine, Coastal and Shelf Science 87: 583–590.
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.
Lim, S., and S. Kalpana. 2011. Maxilliped-setation adaptations to habitat and sexual dimorphism of feeding claws in Uca perplexa and U. vomeris. Journal of Crustacean Biology 31: 406–412.
Mazumder, D., and N. Saintilan. 2010. Mangrove leaves are not an important source of dietary carbon and nitrogen for crabs in temperate Australian mangroves. Wetlands 30: 375–380.
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 implications for choosing sample size. Bioindicators 3: 114–123.
McCutchan, J.H., W.M. Lewis, C. Kendall, and C.C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102: 378–390.
Meziane, T., and M. Tsuchiya. 2000. Fatty acids as tracers of organic matter in the sediment and food web of a mangrove/intertidal flat ecosystem, Okinawa, Japan. Marine Ecology Progress Series 200: 49–57.
Meziane, T., M.C. Sanabe, and M. Tsuchiya. 2002. Role of fiddler crabs of a subtropical intertidal flat on the fate of sedimentary fatty acids. Journal of Experimental Marine Biology and Ecology 270: 191–201.
Minagawa, M., and E. Wada. 1984. Stepwise enrichment of d15N along food chains: further evidence and the relation between d15N and animal age. Geochimica et Cosmochimica 48: 1135–1140.
Ng, P.K.L., D. Guinot, and P.J.F. Davie. 2008. Systema Brachyurorum: Part I. An annotated checklist of extant Brachyuran crabs of the world. The Raffles Bulletin of Zoology 17: 1–286.
Nordhaus, I. 2004. Feeding ecology of the semi-terrestrial crab Ucides cordatus cordatus (Decapoda: Brachyura) in a mangrove forest in northern Brazil. ZMT contributions 18: 1–198.
Nordhaus, I., T. Salewski, and T.C. Jennerjahn. 2011. Food preferences of mangrove crabs related to leaf nitrogen compounds in the Segara Anakan Lagoon, Java, Indonesia. Journal of Sea Research 65: 414–426.
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.
Parnell AC, Inger R, Bearhop S, Jackson AL (2008) SIAR: Stable isotope analysis in R. Available at: http://cran.r-project.org/web/packages/siar
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: 1–5.
Penha-Lopes, G., F. Bartolini, S. Limbu, S. Cannicci, E. Kristensen, and J. Paula. 2009. Are fiddler crabs potentially useful ecosystem engineers in mangrove wastewater wetlands? Marine Pollution Bulletin 58: 1694–1703.
Poon, D.Y.N., B.K.K. Chan, and G.A. Williams. 2010. Spatial and temporal variation in diets of the crabs Metopograpsus frontalis (Grapsidae) and Perisesarma bidens (Sesarmidae): implications for mangrove food webs. Hydrobiologia 638: 29–40.
Ronnback, P. 1999. The ecological basis for economic value of seafood production supported by mangrove ecosystems. Ecological Economics 29: 235–252.
Seto, K.C. 2011. Exploring the dynamics of migration to mega-delta cities in Asia and Africa: contemporary drivers and future scenario. Global Environmental Change 21S: 94–107.
Shaw, M., and I.R. Tibbetts. 2004. Grazing by Metopograpsus frontalis (Decapoda: Grapsidae) on intertidal rock walls of Moreton Bay. Proceedings of the Royal Society of Queensland 111: 95–101.
Sheaves, M., and B. Molony. 2000. Short-circuit in the mangrove food chain. Marine Ecology Progress Series 199: 97–109.
Sheaves, M., R. Johnston, B. Molony, and G. Shepard. 2007. The effect of impoundments on the structure and function of fish fauna in a highly regulated dry tropical estuary. Estuaries and Coasts 30: 507–517.
Sheaves, M., R. Baker, I. Nagelkerken, and R.M. Connolly. 2014a. True value of estuarine and coastal nurseries for fish: incorporating complexity and dynamics. Estuaries and Coasts 1–14.
Sheaves, M., J. Brookes, R. Coles, M. Freckelton, P. Groves, R. Johnston, and P. Winberg. 2014b. 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.
Takeda, S. 2003. Mass wandering in the reproductive season by the fiddler crab Uca perplexa (Decapoda: Ocypodidae). Journal of Crustacean Biology 23: 723–728.
Thrush, S.F., J. Halliday, J.E. Hewitt, and A.M. Lohrer. 2008. The effects of habitat loss, fragmentation, and community homogenization on resilience in estuaries. Ecological Applications 18: 12–21.
Valiela, I., J.L. Bowen, and J.K. York. 2001. Mangrove forests: one of the world’s threatened major tropical environments. BioScience 51: 807–815.
Vermeiren, P., and M. Sheaves. 2014a. Predictable habitat associations of four crab species across the low intertidal landscape of a tropical estuary over time. Estuaries and Coasts. doi:10.1007/s12237-014-9799-0.
Vermeiren, P., and M. Sheaves. 2014b. A remote photographic technique for high replication, large scale understanding of spatial distribution patterns of intertidal crabs. Hydrobiologia 724: 79–89.
Vermeiren, P., and M. Sheaves. 2014c. Predicting habitat associations of five intertidal crab species among estuaries. Estuarine, Coastal and Shelf Science 149: 133–142.
Vermeiren, P., and M. Sheaves. 2014d. Modeling intertidal crab distribution patterns using photographic mapping among tropical Australian estuaries. Estuaries and coasts. doi:10.1007/s12237-014-9897-z.
Werry, J., and S.Y. Lee. 2005. Graspid carbs mediate link between mangrove litter production and estuarine planktonic food chains. Marine Ecology Progress Series 293: 165–176.
Yamaguchi, T., and S. Tabata. 2005. Territory usage and defence of the fiddler crab, Uca lactea (De Haan) (Decapoda, Brachyura, Ocypodidae). Crustaceana 77: 1055–1080.
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.
Zeil, J. 1998. Homing of fiddler crabs (Uca lactea annulipes and Uca vomeris: Ocypodidae). Journal of Comparative Physiology Part A 183: 367–377.
Zeil, J., and J.M. Hemmi. 2006. The visual ecology of fiddler crabs. Journal of Comparative Physiology 192: 1–25.
Acknowledgments
We thank members of the Estuary and Tidal Wetland Ecosystems Research Group for their assistance in the field, Dr. Ron Baker for his insights in stable isotope analysis, and Cynthia Camacho-Muňoz for her assistance in the lab. We also like to acknowledge the feedback of two anonymous reviewers on earlier versions of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Kenneth Dunton
Electronic supplementary material
Below is the link to the electronic supplementary material.
Appendix 1
Bayesian mixing model solutions for the proportions of mangrove, plankton, and microphytobenthos (MPB) material to the diets of crab species within Ross River downstream location. Boxes indicate 50, 75, and 95 % Bayesian credibility intervals (JPEG 1351 kb)
Appendix 2
Photographs of the four main study species (JPEG 75 kb)
Appendix 3
Bayesian mixing model estimates (mode of percentage contribution, 95 % Confidence interval) for contribution of mangrove, plankton, and microphytobenthos (MPB) material to the diet of for all species within Ross River downstream location. n = the number of individuals analyzed (DOC 41 kb)
Rights and permissions
About this article
Cite this article
Vermeiren, P., Abrantes, K. & Sheaves, M. Generalist and Specialist Feeding Crabs Maintain Discrete Trophic Niches Within and Among Estuarine Locations. Estuaries and Coasts 38, 2070–2082 (2015). https://doi.org/10.1007/s12237-015-9959-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-015-9959-x