Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-29T13:11:14.031Z Has data issue: false hasContentIssue false
  • English
  • Français

Is there a better chela to use for geometric morphometric differentiation in brachyuran crabs? A case study using Pachygrapsus marmoratus and Carcinus maenas

Published online by Cambridge University Press:  25 July 2008

Inês C. Silva  and
José Paula
Inês C. Silva*
Affiliation:
IMAR—Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Estrada do Guincho, 2750-374 Cascais, Portugal
José Paula
Affiliation:
IMAR—Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Estrada do Guincho, 2750-374 Cascais, Portugal
*
Correspondence should be addressed to: Inês Cristóvão Silva Laboratório Marítimo da GuiaFaculdade de Ciências da Universidade de LisboaEstrada do Guincho, 2750-374 CascaisPortugal email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Landmark-based geometric morphometric methods were used to test which chela is most suitable to use in population differentiation of brachyuran crabs. Two species were analysed: Pachygrapsus marmoratus, a homochelous species, and Carcinus maenas, a heterochelous species. Variance analysis of shape variables and of each chela was calculated to determine which claw presents less variation within populations. The results showed that the right chela of P. marmoratus is more appropriate to use when the goal is to differentiate populations. In C. maenas, the males major chela and females right chela are more suitable to use, probably due to its heterochely. To test these results, specimens from different geographical locations were compared. Pachygrapsus marmoratus populations presented significant differences in manus shape, and C. maenas populations had differences in polex size and shape. Differences in carapace shape were also encountered between populations of both species. This phenotypic variation was not corroborated with genetic data, which were obtained using the mitochondrial DNA gene cytochrome oxidase I as a marker. These opposite results suggest that environmental factors, such as diet and parasitism, can be determining shape differentiation.

Keywords

chelageometric morphometric differentiationbrachyuran crabsPachygrapsus marmoratusCarcinus maenas
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 88 , Issue 5 , August 2008 , pp. 941 - 953
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abby-Kalio, N.J. and Warner, G.F. (1989) Heterochely and handedness in the shore crab Carcinus maenas (L.) (Crustacea: Brachyura). Zoological Journal of the Linnean Society 96, 19–26.CrossRefGoogle Scholar
Abelló, P., Pertierra, J.P. and Reid, D.G. (1990) Sexual size dimorphism, relative growth and handedness in Liocarcinus depurator and Macropipus tuberculatus (Brachyura: Portunidae). Scientia Marina 54, 195–202.Google Scholar
Adams, D.C., Rohlf, F.J. and Slice, D.E. (2004) Geometric morphometrics: ten years of progress following the ‘Revolution’. Italian Journal of Zoology 71, 5–16.CrossRefGoogle Scholar
Ahmed, M. (1978) Development of asymmetry in the fiddler crab Uca cumulanta Crane, 1943 (Decapoda, Brachyura). Crustaceana 34, 294–300.CrossRefGoogle Scholar
Andrade, S.C.S., Magalhães, C.A. and Solferini, V.N. (2003) Patterns of genetic variability in Brazilian Littorinids (Mollusca): a macrogeographic approach. Journal of Zoological Systematics and Evolutionary Research 41, 249–255.CrossRefGoogle Scholar
Barnwell, F.H. (1982) The prevalence of male right-handedness in the Indo-West Pacific fiddler crabs Uca vocans (Linnaeus) and U. tetragonon (Herbst) (Decapoda: Ocypodidae). Journal of Crustacean Biology 2, 70–83.CrossRefGoogle Scholar
Brian, J.V., Fernandes, T., Ladle, R.J. and Todd, P.A. (2006) Patterns of morphological and genetic variability in UK populations of the shore crab, Carcinus maenas Linnaeus, 1758 (Crustacea: Decapoda: Brachyura). Journal of Experimental Marine Biology and Ecology 329, 47–54.CrossRefGoogle Scholar
Brown, S.C., Cassuto, S. and Loos, R.W. (1979) Biomechanics of chelipeds in some decapod crustaceans. Journal of Zoology 188, 143–159.CrossRefGoogle Scholar
Cadrin, S.X. (1995) Discrimination of the American lobster (Homarus americanus) stocks off southern New England on the basis of secondary sex character allometry. Canadian Journal of Fisheries and Aquatic Sciences 52, 2712–2723.CrossRefGoogle Scholar
Cannicci, S., Gomei, M., Boddi, B. and Vannini, M. (2002) Feeding habitats and natural diet of the intertidal crab Pachygrapsus marmoratus: opportunistic browser or selective feeder? Estuarine, Coastal and Shelf Science 54, 983–1001.CrossRefGoogle Scholar
Cannicci, S., Paula, J. and Vannini, M. (1999) Activity pattern and spatial strategy in Pachygrapsus marmoratus (Decapoda: Grapsidae) from Mediterranean and Atlantic shores. Marine Biology 133, 429–435.CrossRefGoogle Scholar
Carrol, S.P. and Dingle, H. (1996) The biology of post-invasion events. Biological Conservation 78, 207–214.CrossRefGoogle Scholar
Cavalcanti, M.J., Monteiro, L.R. and Lopes, P.R.D. (1999) Landmark-based morphometric analysis in selected species of serranid fishes (Perciformes: Teleostei). Zoological Studies 38, 287–294.Google Scholar
Clark, P.F. (1986) North-east Atlantic crabs; an atlas of distribution. Ross-on-Wye: Marine Conservation Society.Google Scholar
Clark, P.F., Neale, M. and Rainbow, P.S. (2001) A morphometric analysis of regional variation in Carcinus Leach, 1814 (Brachyura: Portunidae: Carcininae) with particular reference to the status of the two species C. maenas (Linnaeus, 1758) and C. aestuarii Nardo, 1847. Journal of Crustacean Biology 21, 288–303.CrossRefGoogle Scholar
Coen, L.D. (1988) Herbivory by crabs and the control of algal epibionts on Caribbean host corals. Oecologia 75, 198–203.CrossRefGoogle ScholarPubMed
Cook, B.D., Bunn, S.E. and Hughes, J.M. (2002) Genetic structure and dispersal of Macrobrachium australiense (Decapoda: Palaemonidae) in Western Queensland, Australia. Freshwater Biology 47, 2098–2112.CrossRefGoogle Scholar
Crane, J. (1975) Fiddler crabs of the world. Princeton, New Jersey: Princeton University Press.Google Scholar
Cuesta, J.A. and Schubart, C.D. (1998) Morphological and molecular differentiation between three allopatric populations of the littoral crab Pachygrapsus transversus (Gibbs, 1850) (Brachyura: Grapsidae). Journal of Natural History 32, 1449–1508.CrossRefGoogle Scholar
Elner, R.W. (1981) Diet of the green crab Carcinus maenas (L.) from Port Herbert, Southwestern Nova Scotia. Journal of Shellfish Research 1, 89–94.Google Scholar
Excoffier, L. and Smouse, P.E. (1994) Using allele frequencies and geographic subdivisions to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136, 343–359.CrossRefGoogle ScholarPubMed
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, 479–491.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Fratini, S. and Vannini, M. (2002) Genetic differentiation in the mud crab Scylla serrata (Decapoda: Portunidae) within the Indian Ocean. Journal of Experimental Marine Biology and Ecology 272, 103–116.CrossRefGoogle Scholar
Grosholz, E.D. and Ruiz, G.M. (1995) Spread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California. Marine Biology 122, 239–247.CrossRefGoogle Scholar
Haley, S.R. (1969) Relative growth and sexual maturity of the Texas ghost crab, Ocypode quadrata (Fabr.) (Brachyura, Ocypodidae). Crustaceana 17, 285–297.CrossRefGoogle Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence aligment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hamilton, P.V., Nishimoto, R.T. and Halusky, G.J. (1976) Cheliped laterality in Callinectes sapidus (Rathbun). Biological Bulletin. Marine Biological Laboratory, Woods Hole 150, 393–401.CrossRefGoogle Scholar
Hartnoll, R.G. (1982) Growth. In Abele, L.G. (ed.) The biology of Crustacea 2. London: Academic Press, pp. 111–196.Google Scholar
Hillis, D.M., Mable, B.K., Larson, A., Davis, S.K. and Zimmer, E.A. (1996) Nucleic acids IV: sequencing and cloning. In Hillis, D.M., Moritz, C. and Mable, K. (eds) Molecular systematics. 2nd edition. Sunderland, MA: Sinauer Associates, pp. 385–407.Google Scholar
Hines, A.H. (1986) Larval patterns in the life histories of brachyuran crabs (Crustacea: Decapoda, Brachyura). Bulletin of Marine Science 39, 444–466.Google Scholar
Hunt, A. (1993) Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Marine Ecology Progress Series 92, 179–186.CrossRefGoogle Scholar
Ingle, R.W. and Clark, P.F. (2006) First reported occurrences of the marbled crab, Pachygrapsus marmoratus (Crustacea: Brachyura: Grapsoidea) in southern coastal waters of the British Isles. Journal of the Marine Biological Association of the United Kingdom 2 – Biodiversity Records, published online.Google Scholar
Kassam, D.D., Adams, D.C., Hori, M. and Yamaoka, K. (2003) Morphometric analysis on ecomorphologically equivalent cichlid species from Lakes Malawi and Tanganyika. Journal of Zoology 260, 153–157.CrossRefGoogle Scholar
Kaiser, M.J., Hughes, R.N. and Reid, D.G. (1990) Chelal morphology, prey-size selection and aggressive competition in green and red forms of Carcinus maenas (L.). Journal of Experimental Marine Biology and Ecology 140, 121–134.CrossRefGoogle Scholar
Lavery, S., Moritz, C. and Fielder, D.R. (1996) Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro. Molecular Ecology 5, 557–570.CrossRefGoogle Scholar
Le Roux, P.J., Branch, G.M. and Joska, M.A.P. (1990) On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L.) along the South African Coast. South African Journal of Marine Science 9, 85–93.CrossRefGoogle Scholar
Lee, S.Y. (1995) Cheliped size and structure: the evolution of a multifunctional decapod organ. Journal of Experimental Marine Biology and Ecology 193, 161–176.CrossRefGoogle Scholar
Levinton, J.S., Judge, M.L. and Kurdziel, J.P. (1995) Functional differences between the major and the minor claws of fiddler crabs (Uca, family Ocypodidae, Order Decapoda, Subphylum Crustacea): a result of selection or developmental constraint? Journal of Experimental Marine Biology and Ecology 193, 147–160.CrossRefGoogle Scholar
Macholán, M. (2006) A geometric morphometric analysis of the shape of the first upper molar in mice of the genus Mus (Muridae, Rodentia). Journal of Zoology 270, 672–681.CrossRefGoogle Scholar
Mathews, L.M., Schubart, C.D., Neigel, J.E. and Felder, D.L. (2002) Genetic, ecological, and behavioural divergence between two sibling snapping shrimp species (Crustacea: Decapoda: Alpheus). Molecular Ecology 11, 1427–1437.CrossRefGoogle ScholarPubMed
Nei, M. (1987) Molecular evolutionary genetics. New York: Columbia University Press.CrossRefGoogle Scholar
Neigel, J.E. (1994) Analysis of rapidly evolving molecules and DNA sequence variants: alternative approaches for detecting genetic structure in marine populations. California Cooperative Oceanic Fisheries Investigations Reports 35, 82–89.Google Scholar
Ng, P.K.L. and Tan, L.W.H. (1985) Right handedness in heterochelous calappoid and xanthoid crabs—suggestion for a functional advantage. Crustaceana 48, 98–100.CrossRefGoogle Scholar
Paula, J., Silva, I.C., Francisco, S.M. and Flores, A.A.V. (2006) The use of artificial benthic collectors for assessment of spatial patterns of settlement of megalopae of Carcinus maenas (L.) (Brachyura: Portunidae) in the lower Mira Estuary, Portugal. Hydrobiologia 557, 69–77.CrossRefGoogle Scholar
Quan, J., Lü, X., Zhuang, Z., Dai, J., Deng, J. and Zhang, Y. (2001) Low genetic variation of Penaeus chinensis as revealed by mitochondrial COI and 16S rRNA gene sequences. Biochemical Genetics 39, 279–284.CrossRefGoogle ScholarPubMed
Queiroga, H. (1996) Distribution and drift of the crab Carcinus maenas (L.) (Decapoda, Portunidae) larvae over the continental shelf off northern Portugal in April 1991. Journal of Plankton Research 18, 1981–2000.CrossRefGoogle Scholar
Rohlf, F.J. (2005) TpsRegr, version 1.31. Stony Brook, New York: Department of Ecology & Evolution, State University of New York.Google Scholar
Rohlf, F.J. (2006a) TpsDig2, version 2.05. Stony Brook, New York: Department of Ecology & Evolution, State University of New York.Google Scholar
Rohlf, F.J. (2006b) TpsRelw, version 1.44. Stony Brook, New york: Department of Ecology & Evolution, State University of New York.Google Scholar
Rohlf, F.J. and Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology and Evolution 8, 129–132.CrossRefGoogle Scholar
Rohlf, F.J. and Slice, D.E. (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39, 40–59.CrossRefGoogle Scholar
Roman, J. and Palumbi, S.R. (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Molecular Ecology 13, 2891–2998.CrossRefGoogle ScholarPubMed
Rosenberg, M.S. (1997) Evolution of shape differences between the major and the minor chelipeds of Uca pugnax (Decapoda: Ocypodidae). Journal of Crustacean Biology 17, 52–59.CrossRefGoogle Scholar
Rosenberg, M.S. (2001) The systematics and taxonomy of fiddler crabs: a phylogeny of the genus Uca. Journal of Crustacean Biology 21, 839–869.CrossRefGoogle Scholar
Rosenberg, M.S. (2002) Fiddler crab claw shape variation: a geometric morphometric analysis across the genus Uca (Crustacea: Brachyura: Ocypodidae). Biological Journal of the Linnean Society 75, 147–162.Google Scholar
Rufino, M.M., Abelló, P. and Yule, A.B. (2004) Male and female carapace shape differences in Liocarcinus depurator (Decapoda, Brachyura): an application of geometric morphometric analysis to crustaceans. Italian Journal of Zoology 71, 79–83.CrossRefGoogle Scholar
Rufino, M.M., Abelló, P. and Yule, A.B. (2006a) Geographic and gender shape differences in the carapace of Liocarcinus depurator (Brachyura: Portunidae) using geometric morphometrics and the influence of a digitizing method. Journal of Morphology 269, 458–465.Google Scholar
Rufino, M.M., Gaspar, M.B., Pereira, A.M. and Vasconcelos, P. (2006b) Use of shape to distinguish Chamelea gallina and Chamelea striatula (Bivalvia: Veneridae): linear and geometric morphometric methods. Journal of Morphology 267, 1433–1440.CrossRefGoogle ScholarPubMed
Schenk, S.C. and Wainwright, P. (2001) Dimorphism and the functional basis of claw strength in six brachyuran crabs. Journal of Zoology 255, 105–119.CrossRefGoogle Scholar
Schizas, N.V., Street, G.T. and Coull, B.C. (1999) Molecular population of the marine benthic copepod Microarthridion littorale along the southeastern and Gulf coasts of the USA. Marine Biology 135, 399–405.CrossRefGoogle Scholar
Schneider, S., Roessli, D. and Excoffier, L. (2000) ARLEQUIN: a software for population genetics data analysis. Genetics and Biometry Laboratory, Department of Anthropology and Ecology, University of Geneva, Geneva.Google Scholar
Schubart, C.D., Reimer, J. and Diesel, R. (1998) Morphological and molecular evidence for a new endemic freshwater crab, Sesarma ayatum sp. n., (Grapsidae, Sesarminae) from Eastern Jamaica. Zoologica Scripta 27, 373–380.CrossRefGoogle Scholar
Skilleter, G.A. and Anderson, D.T. (1986) Functional morphology of the chelipeds, mouthparts and gastric mill of Ozius truncates (Milne-Edwards) (Xanthidae) and Leptograpsus variegatus (Fabricius) (Grapsidae) (Brachyura). Australian Journal of Marine and Freshwater Research 37, 67–79.CrossRefGoogle Scholar
Smith, L.D. (2004) Biogeographic differences in claw size and performance in an introduced crab predator Carcinus maenas. Marine Ecology Progress Series 276, 209–222.CrossRefGoogle Scholar
Smith, L.D. and Palmer, A. (1994) Effects of manipulated diet on size and performance of brachyuran crab claws. Science 254, 710–712.CrossRefGoogle Scholar
Sotka, E.E., Wares, J.P., Barth, J.A., Grosberg, R.K. and Palumbi, S.R. (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Molecular Ecology 13, 2143–2156.CrossRefGoogle ScholarPubMed
Sousa, R., Freire, R., Rufino, M., Méndez, J., Gaspar, M., Antunes, C. and Guilhermino, L. (2007) Genetic and shell morphological variability of the invasive bivalve Corbicula fluminea (Müller, 1774) in two Portuguese estuaries. Estuarine, Coastal and Shelf Science 74, 166–174.CrossRefGoogle Scholar
Taylor, G.M., Palmer, A.R. and Barton, A.C. (2000) Variation in safety factors of claws within and among six species of Cancer crabs (Decapoda: Brachyura). Biological Journal of the Linnean Society 70, 37–62.CrossRefGoogle Scholar
Trapani, J. (2003) Geometric morphometric analysis of body-form variability in Cichlasoma minckleyi, the Cuatro Cienegas cichlid. Environmental Biology of Fishes 68, 357–369.CrossRefGoogle Scholar
Tresher, R., Proctor, C., Ruiz, G., Gurney, R., MacKinnon, C., Walton, W., Rodriguez, L. and Bax, N. (2003) Invasion dynamics of the European shore crab, Carcinus maenas, in Australia. Marine Biology 142, 867–876.CrossRefGoogle Scholar
Trott, T.J. (1987) The prevalence of left-handedness in the painted ghost crab Ocypode gaudichaudii H. Milne-Edwards & Lucas (Decapoda, Ocypodidae). Crustaceana 52, 213–215.CrossRefGoogle Scholar
Weissburg, M. (1991) Morphological correlates of male claw asymmetry in the foddler crab Uca pugnax (Smith) (Decapoda, Brachyura). Crustaceana 61, 11–20.CrossRefGoogle Scholar
Wilding, C.S., Mill, P.J. and Grahame, J. (1999) Partial sequence of the mitochondrial genome of Littorina saxatilis: relevance to gastropod phylogenetics. Journal of Molecular Evolution 48, 348–359.CrossRefGoogle ScholarPubMed
Yamada, S.B. and Boulding, E.G. (1998) Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs. Journal of Experimental Marine Biology and Ecology 220, 191–211.CrossRefGoogle Scholar
Yamaguchi, T. and Tokunaga, S. (1995) Cheliped handedness in four species of Charybdis, Portunus and Thalamita (Brachyura: Portunidae). Crustacean Research 24, 33–38.CrossRefGoogle Scholar
Zeidler, W. (1978) Note on the occurrence of the European shore crab Carcinus maenas (Linn., 1758) in Australia. South Australian Naturalist 52, 11–12.Google Scholar
Zelditch, M.L., Swiderski, D.L., Sheets, H.D. and Fink, W.L. (2004) Geometric morphometrics for biologists—a primer. San Diego, California: Elsevier Academic Press.Google Scholar