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Phylogeography of the Christmas Island blue crab, Discoplax celeste (Decapoda: Gecarcinidae) on Christmas Island, Indian Ocean

Published online by Cambridge University Press:  25 May 2012

Lucy M. Turner*
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, University of Plymouth, Drake Circus, Plymouth, Devon PL4 8AA, UK
J. Paul Hallas
Affiliation:
School of Applied Sciences, University of Glamorgan, Upper Glyntaff, Pontypridd CF37 4AT, UK
Michael J. Smith
Affiliation:
Department of the Environment, Water, Heritage and the Arts, Christmas Island National Park, PO Box 867, Christmas Island, Indian Ocean 6798, Australia
Stephen Morris
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
*
Correspondence should be addressed to: L.M. Turner, Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, University of Plymouth, Drake Circus, Plymouth, Devon PL4 8AA, UK email: lucy.m.turner@plymouth.ac.uk

Abstract

The land crab, Discoplax celeste (Gecarcinidae) is endemic to Christmas Island in the Indian Ocean. Due to a freshwater-dependant life history, in which the megalopae migrate from the ocean up freshwater streams to their adult terrestrial/freshwater habitat, D. celeste inhabits only a few isolated locations on the island. This restricted distribution is one of a number of factors which has previously highlighted the vulnerability of this species to outside threats. A number of anthropogenic factors including the introduction of multiple invasive species and habitat destruction have led to drastic ecosystem change on Christmas Island. The aim of this study was to investigate whether the restricted geographical distributions of D. celeste populations contribute to significant genetic structuring across Christmas Island, with an objective to inform future conservation strategies for this species on Christmas Island. Fragments of the mitochondrial cytochrome oxidase I gene and the control region were sequenced from 95 individuals collected from all five locations on Christmas Island known to be inhabited by D. celeste. Analyses using analysis of molecular variance revealed no evidence of population sub-structuring, indicating that despite any geographical isolation, there is a single population of D. celeste on Christmas Island. This lack of population differentiation is probably explained by the oceanic dispersal of larvae, rather than terrestrial migration of D. celeste. Therefore, based on these results, for conservation purposes, D. celeste on Christmas Island can be considered a single management unit.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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Footnotes

Professor Morris died on 11 August 2009 before this work was completed. This paper is dedicated to his memory.

References

REFERENCES

Adamczewska, A.M. and Morris, S. (1996) The respiratory gas transport, acid–base state, ion and metabolite status of the Christmas Island blue crab, Cardisoma hirtipes (Dana) assessed in situ with respect to immersion. Physiological Zoology 69, 6792.Google Scholar
Alcock, A. (1900) Materials for a carcinological fauna of India. No. 6. The Brachyura Catometopa or Grapsoidea. Journal of the Asiatic Society of Bengal 69, 279486.Google Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403410.Google Scholar
Anger, K., Torres, G., Charmantier-Daures, M. and Charmantier, G. (2008) Adaptive diversity in congeneric coastal crabs: ontogenetic patterns of osmoregulation match life-history strategies in Armases spp. (Decapoda, Sesarmidae). Journal of Experimental Marine Biology and Ecology 367, 2836.CrossRefGoogle Scholar
Avise, J.C. (2000) Phylogeography: the history and formation of species. 1st edition. Cambridge, MA: Harvard University Press.Google Scholar
Barrett, P.J. (2001) Searching for water on Christmas Island. Helictite 37, 3739.Google Scholar
Chambers, P. (2011) Society has been defended: following the shifting shape of state through Australia's Christmas Island. International Political Sociology 5, 1834.Google Scholar
Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.Google Scholar
Cook, B.D., Pringle, C.M. and Hughes, J.M. (2008) Phylogeography of an island endemic, the Puerto Rican freshwater crab (Epilobocera sinuatifrons). Journal of Heredity 99, 157164.Google Scholar
Cumberlidge, N. and Ng, P.K.L. (2009) Systematics, evolution and biogeography of the freshwater crabs. In Martin, J.W., Crandall, K.A. and Felder, D.L. (eds) Crustacean Issues 18: Decapod Crustacean Phylogenetics. Volume 18. Boca Raton, FL: Taylor and Francis, pp. 491508.Google Scholar
Cumberlidge, N., Ng, P.K.L., Yeo, D.C.J., Magalhaes, C., Campos, M.R., Alvarez, F., Naruse, T., Daniels, S.R., Esser, L.J., Attipoe, F.Y.K., Clotilde-Ba, F.-L., Darwall, W., McIvor, A., Baillie, J.E.M., Collen, B. and Ram, M. (2009) Freshwater crabs and the biodiversity crisis: importance, threats, status, and conservation challenges. Biological Conservation 142, 16651673.CrossRefGoogle Scholar
Davies, C. and Beckley, L.E. (2010) Zooplankton from the inshore waters of Christmas Island (Indian Ocean) with reference to larvae of the red land crab, Gecarcoidea natalis . Journal of the Royal Society of Western Australia 93, 4350.Google Scholar
Dela-Cruz, J. (1998) Ion and water regulation in Cardisoma (Brachyura, Gecarcinidae). MSc thesis. University of Sydney, Australia.Google Scholar
Dela-Cruz, J. and Morris, S. (1997a) Respiratory, acid–base, and metabolic responses of the Christmas Island blue crab, Cardisoma hirtipes (Dana), during simulated environmental conditions. Physiological Zoology 70, 100115.Google Scholar
Dela-Cruz, J. and Morris, S. (1997b) Water and ion balance and nitrogenous excretion as limitations to terrestrial excursion in the Christmas Island blue crab, Cardisoma hirtipes (Dana). Journal of Experimental Zoology 279, 537548.Google Scholar
Dittel, A.I. and Epifanio, C.E. (2009) Invasion biology of the Chinese mitten crab Eriochier sinensis: a brief review. Journal of Experimental Marine Biology and Ecology 374, 7992.CrossRefGoogle Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.Google Scholar
Environment Australia (2004) Pulu Keeling National Park Management Plan. Darwin: Commonwealth of Australia.Google Scholar
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google Scholar
Excoffier, L., Smouse, P.E. and Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoen, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
Forward, R.B. (2009) Larval biology of the crab Rhithropanopeus harrisii (Gould): a synthesis. Biological Bulletin. Marine Biological Laboratory, Woods Hole 216, 243256.Google Scholar
Frankham, R., Ballou, J.D. and Briscoe, D.A. (2002) Introduction to conservation genetics. 1st edition. Cambridge: Cambridge University Press.Google Scholar
Fu, X.Y. (1997) Statistic test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915925.Google Scholar
Gibson-Hill, C.A. (1947) Field notes on the terrestrial crabs. Bulletin of the Raffles Museum, Singapore 18, 4352.Google Scholar
Gray, H.S. (1995) Christmas Island naturally: the natural history of an isolated oceanic island the Australian territory of Christmas Island Indian Ocean. 2nd edition. Christmas Island, Indian Ocean: Christmas Island Natural History Association.Google Scholar
Greenaway, P. (1989) Sodium-balance and adaptation to fresh-water in the amphibious crab Cardisoma hirtipes. Physiological Zoology 62, 639653.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Harpending, R.C. (1994) Signature of ancient population growth in low resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591600.Google Scholar
Hartnoll, R.G. (1988) Evolution, systematics, and geographical distribution. In Burggren, W.W. and McMahon, B.R. (eds) Biology of the land crabs. Cambridge: Cambridge University Press, pp. 654.Google Scholar
Hicks, J.W. (1985) The breeding behaviour and migrations of the terrestrial crab Gecarcoidea natalis (Decapoda: Brachyura). Australian Journal of Zoology 33, 127142.Google Scholar
Hicks, J., Rumpff, H. and Yorkston, H. (1990) Christmas crabs. 1st edition. Christmas Island, Indian Ocean: Christmas Island Natural History Association.Google Scholar
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Lopez-Victoria, M. and Werding, B. (2008) Ecology of the endemic land crab Johngarthia malpilensis (Decapoda: Brachyura: Gecarcinidae), a poorly known species from the tropical eastern Pacific. Pacific Science 62, 483493.Google Scholar
MacArthur, R.H. and Wilson, E.O. (1967) The theory of island biogeography. 1st edition. Princeton, NJ: Princeton University Press.Google Scholar
Morris, S. (2005) Respiratory and acid–base responses during migration and to exercise by the terrestrial crab Discoplax (Cardisoma) hirtipes, with regard to season, humidity and behaviour. Journal of Experimental Biology 208, 43334343.Google Scholar
Morris, S. and Dela-Cruz, J. (1998) The ecophysiological significance of lung-air retention during submersion by the air-breathing crabs Cardisoma carnifex and Cardisoma hirtipes. Experimental Biology Online 3, 119.Google Scholar
Mousset, S., Derome, N. and Veuille, M. (2004) A test of neutrality and constant population size based on the mismatch distribution. Molecular Biology and Evolution 21, 724731.CrossRefGoogle ScholarPubMed
Navid, D. (1984) International cooperation for wetland conservation—the Ramsar Convention. Transactions of the North American Wildlife and Natural Resources Conference 49, 3341.Google Scholar
Nei, M. (1987) Molecular evolutionary genetics. 1st edition. New York: Columbia University Press.Google Scholar
Ng, P.K.L. and Davie, P.J.F. (2012) The blue crab of Christmas Island, Discoplax celeste, new species (Crustacea: Decapoda: Brachyura: Gecarcinidae). Raffles Bulletin of Zoology 60, 89100.Google Scholar
Ng, P.K.L. and Guinot, D. (2001) On the land crabs of the genus Discoplax A. Milne Edwards, 1867 (Crustacea: Decapoda: Brachyura: Gecarcinidae), with description of a new cavernicolous species from the Philippines. Raffles Bulletin of Zoology 49, 311338.Google Scholar
O'Dowd, D.J. and Lake, P.S. (1989) Red crabs in rain forest, Christmas Island: removal and relocation of leaf-fall. Journal of Tropical Ecology 5, 337348.Google Scholar
O'Dowd, D.J., Green, P.T. and Lake, P.S. (2003) Invasional ‘meltdown' on an oceanic island. Ecology Letters 6, 812817.Google Scholar
Oliveira-Neto, J.F., Pie, M.R., Boeger, W.A., Ostrensky, A. and Baggio, R.A. (2007) Population genetics and evolutionary demography of Ucides cordatus (Decapoda: Ocypodidae). Marine Ecology 28, 460469.Google Scholar
Oliveira-Neto, J.F., Pie, M.R., Chammas, M.A., Ostrensky, A. and Boeger, W.A. (2008) Phylogeography of the blue land crab, Cardisoma guanhumi (Decapoda: Gecarcinidae) along the Brazilian coast. Journal of the Marine Biological Association of the United Kingdom 88, 14171423.Google Scholar
Perger, R., Vargas, R. and Wall, A. (2011) Johngarthia cocoensis, a new species of Gecarcinidae MacLeay, 1838 (Crustacea, Decapoda, Brachyura) from Cocos Island, Costa Rica. Zootaxa 2911, 5768.CrossRefGoogle Scholar
Posada, D. and Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.Google Scholar
Posada, D. and Crandall, K.A. (2001) Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution 16, 3745.Google Scholar
Ragionieri, L., Cannicci, S., Schubart, C.D. and Fratini, S. (2010) Gene flow and demographic history of the mangrove crab Neosarmatium meinerti: a case study from the western Indian Ocean. Estuarine, Coastal and Shelf Science 86, 179188.CrossRefGoogle Scholar
Ramírez-Soriano, A., Ramos-Onsins, S.E., Rozas, J., Calafell, F., Navarro, A. (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179, 555567.Google Scholar
Rogers, A.J. and Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552569.Google ScholarPubMed
Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstruction of phylogenetic trees. Molecular Biology and Evolution 4, 406425.Google Scholar
Schneider, S. and Excoffier, L. (1999) Estimation of demographic parameters from distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152, 10721089.Google Scholar
Schubart, C.D., Santl, T. and Koller, P. (2008) Mitochondrial patterns of intra- and interspecific differentiation among endemic freshwater crabs of ancient lakes in Sulawesi. Contributions to Zoology 77, 8390.Google Scholar
Shih, H.T., Hung, H.C., Schubart, C.D., Chen, C.L.A. and Chang, H.W. (2006) Intraspecific genetic diversity of the endemic freshwater crab Candidiopotamon rathbunae (Decapoda, Brachyura, Potamidae) reflects five million years of the geological history of Taiwan. Journal of Biogeography 33, 980989.Google Scholar
Shokita, S. and Shikatani, N. (1990) Complete larval development of the land-crab, Cardisoma hirtipes Dana (Brachyura: Gecarcinidae) reared in the laboratory. Researches on Crustacea 18, 114.Google Scholar
Silva, I.C., Mesquita, N. and Paula, J. (2010) Genetic and morphological differentiation of the mangrove crab Perisesarma guttatum (Brachyura: Sesarmidae) along an East African latitudinal gradient. Biological Journal of the Linnean Society 99, 2846.Google Scholar
Slatkin, M. and Hudson, R.R. (1999) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555562.Google Scholar
Sokolov, E.P. (2000) An improved method for DNA isolation from mucopolysaccharide-rich molluscan tissues. Journal of Molluscan Studies 66, 573575.Google Scholar
Sotelo, G., Morán, P. and Posada, D. (2008) Genetic identification of the north-eastern Atlantic spiny spider crab as Maja brachydactyla Balss, 1922. Journal of Crustacean Biology 28, 7681.Google Scholar
Swofford, D.L. (2002) PAUP*, Version 4b10. Sunderland, MA: Sinauer Associates Inc.Google Scholar
Tajima, F. (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.Google Scholar
Tajima, F. (1989b) The effect of change in population size on DNA polymorphism. Genetics 123, 597601.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Templeton, A.R., Crandall, K.A. and Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619633.Google Scholar
Torres, G., Anger, K. and Gimenez, L. (2006) Effects of reduced salinities on metamorphosis of a freshwater-tolerant sesarmid crab, Armases roberti: is upstream migration in the megalopa stage constrained by increasing osmotic stress? Journal of Experimental Marine Biology and Ecology 338, 134139.Google Scholar
Triantis, K.A., Borges, P.A.V., Ladle, R.J., Hortal, J., Cardoso, P., Gaspar, C., Dinis, F., Mendonça, E., Silveira, L.M.A., Gabriel, R., Melo, C., Santos, A.M.C., Amorim, I.R., Ribeiro, S.P., Serrano, A.R.M., Quartau, J.A. and Whittaker, R.J. (2010) Extinction debt on oceanic islands. Ecography 33, 285294.Google Scholar
Turner, L.M. (2010) A role for crustacean hyperglycaemic hormone (CHH) in the regulation of kidney-like function in freshwater land crabs: a study of the Christmas Island blue Crab, Discoplax hirtipes. PhD thesis. University of Bristol, UK.Google Scholar
Turner, L.M., Hallas, J.P. and Morris, S. (2011) Population structure of the Christmas Island blue Crab, Discoplax hirtipes (Decapoda: Brachyura: Gecarcinidae) on Christmas Island, Indian Ocean. Journal of Crustacean Biology 31, 450457.Google Scholar
Tweedie, M.W.F. (1950) The fauna of the Cocos Keeling Islands, Brachyura and Stomatopoda. Bulletin of the Raffles Museum, Singapore 22, 105148.Google Scholar
Vannini, M. and Cannicci, S. (1995) Homing behaviour and possible cognitive maps in crustacean decapods. Journal of Experimental Marine Biology and Ecology 193, 6791.Google Scholar
Wan, Q-H., Wu, H., Fujihara, T. and Fang, S-G. (2004) Which genetic marker for which conservation genetics issue? Electrophoresis 25, 21652176.Google Scholar
Xia, X. and Xie, Z. (2001) DAMBE: data analysis in molecular biology and evolution. Journal of Heredity 92, 371373.Google Scholar
Xia, X., Xie, Z., Salemi, M., Chen, L. and Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 17.Google Scholar