Skip to main content
Log in

Patterns of genetic and morphometric diversity in the marbled crab (Pachygrapsus marmoratus, Brachyura, Grapsidae) populations across the Tunisian coast

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

The present study reports on population structure analysis of the marbled crab Pachygrapsus marmoratus (Fabricius, 1787) from the Tunisian coast, an appropriate location to study biogeographical processes because of the presence of a well-known discontinuous biogeographic area (the Siculo-Tunisian Strait). Patterns of morphological and genetic variation of this highly dispersive and continuously distributed decapod species were assessed among its geographically close populations which cover almost the entire Tunisian coastline. A total of 386 specimens from nine sites were collected and examined for morphometric variability at 14 morphometric traits. The results of multivariate analyses of linear morphometric traits showed the existence of sexual dimorphism in this species by PERMANOVA (Permutational multivariate analysis of variance). In addition, both CDA (Canonical discriminant analysis) and NPMANOVA (Non parametric MANOVA test) analyses revealed statistically significant differences among the studied locations for both sexes. Overall, the outcome of CDA analysis showed that over 87% of individuals could be assigned correctly to three regional groups in both sexes (North, Center and South). Specifically, SIMPER (Similarity Percentages) analysis showed that carapace length, carapace width and merus length were major contributors to the morphometric separation between populations. The pattern of phenotypic variation suggested by morphometric analyses was found to be highly discordant with that suggested by the analysis of a mitochondrial marker (cytochrome oxidase I, COI). Indeed, the results inferred from restriction fragment analysis of the COI in 180 crabs, suggested high genetic homogeneity. Very low levels of haplotype diversity (h) were found in almost all the studied populations, associated with non significant genetic distances for nearly all population comparisons. Explanations to these morphometric and mtDNA patterns as well as the discrepancy between them are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anastasiadou C, Leonardos I D. 2008. Morphological variation among populations of Atyaephyra desmarestii (Millet, 1831) (Decapoda: Caridea: Atyidae) from freshwater habitats of northwestern Greece. Journal of Crustacean Biology, 28(2): 240–247

    Article  Google Scholar 

  • Anderson M J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1): 32–46

    Google Scholar 

  • Anderson M J. 2005. Permanova-Permutational multivariate analysis of variance [dissertation]. Auckland: Department of Statistics University of Auckland

    Google Scholar 

  • Anderson M J, Ter Braak C J F. 2003. Permutation tests for multifactorial analysis of variance. Journal of Statistical Computation and Simulation, 73(2): 85–113

    Article  Google Scholar 

  • Arnaud-Haond S, Migiaccio M, Diaz-Almela E, et al. 2007. Vicariance patterns in the Mediterranean Sea: east-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. Journal of Biogeography, 34(6): 963–976

    Article  Google Scholar 

  • Avise J C. 2000. Phylogeography: the History and Formation of Species. Cambridge, Massachusetts: Harvard University Press, 464

    Google Scholar 

  • Bahri-Sfar L, Lemaire C, Hassine O K B, et al. 2000. Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. The Royal Society Publishing: Proceedings B, 267(1446): 929–935

    Article  Google Scholar 

  • Barber P H, Erdmann M V, Palumbi S R. 2006. Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the coral triangle. Evolution, 60(9): 1825–1839

    Article  Google Scholar 

  • Bell M A, Aguirre W E, Buck N J. 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution, 58(4): 814–824

    Article  Google Scholar 

  • Bentley M G, Clare A S, Scott C L, et al. 2002. A1.10-Multi-level analyses of endocrine disruption in shore crabs from estuarine and coastal environments. Comparative Biochemistry and Physiology Part A, 132: S1–S12

    Article  Google Scholar 

  • Borsa P, Blanquer A, Berrebi P. 1997. Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Marine Biology, 129(2): 233–246

    Article  Google Scholar 

  • Brian J V. 2005. Inter-population variability in the reproductive morphology of the shore crab (Carcinus maenas): evidence of endocrine disruption in a marine crustacean? Marine Pollution Bulletin, 50(4): 410–416

    Article  Google Scholar 

  • Brian J V, Fernandes T, Ladle R J, et al. 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(1): 47–54

    Article  Google Scholar 

  • Brooker A L, Benzie J A H, Blair D, et al. 2000. Population structure of the giant tiger prawn Penaeus monodon in Australian waters, determined using microsatellite markers. Marine Biology, 136(1): 149–157

    Article  Google Scholar 

  • Burrows M T, Harvey R, Robb L. 2008. Wave exposure indices from digital coastlines and the prediction of rocky shore community structure. Marine Ecology Progress Series, 353: 1–12

    Article  Google Scholar 

  • Cadrin S X. 1995. Discrimination of 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(12): 2712–2723

    Article  Google Scholar 

  • Cannicci S, Gomei M, Boddi B, et al. 2002. Feeding habits and natural diet of the intertidal crab Pachygrapsus marmoratus: opportunistic browser or selective feeder? Estuarine, Coastal and Shelf Science, 54(6): 983–1001

    Article  Google Scholar 

  • Cannicci S, Gomei M, Dahdouh-Guebas F, et al. 2007. Influence of seasonal food abundance and quality on the feeding habits of an opportunistic feeder, the intertidal crab Pachygrapsus marmoratus. Marine Biology, 151(4): 1331–1342

    Article  Google Scholar 

  • Cannicci S, Paula J, Vannini M. 1999. Activity pattern and spatial strategy in Pachygrapsus marmoratus (Decapoda: Grapsidae) from Mediterranean and Atlantic shores. Marine Biology, 133(3): 429–435

    Article  Google Scholar 

  • Cassone B J, Boulding E G. 2006. Genetic structure and phylogeography of the lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts. Marine Biology, 149(2): 213–226

    Article  Google Scholar 

  • Clarke K R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18(1): 117–143

    Article  Google Scholar 

  • Cuesta J A, Rodriguez A. 2000. Zoeal stages of the intertidal crab Pachygrapsus marmoratus (Fabricius, 1787) (Brachyura, Grapsidae) reared in the laboratory. Hydrobiologia, 436(1–3): 119–130

    Article  Google Scholar 

  • Darling J A, Bagley M J, Roman J, et al. 2008. Genetic patterns across multiple introductions of the globally invasive crab genus (Carcinus). Molecular Ecology, 17(23): 4992–5007

    Article  Google Scholar 

  • Debuse V J, Addison J T, Reynolds J D. 2001. Morphometric variability in UK populations of the European lobster. Journal of the Marine Biological Association of the United Kingdom, 81(3): 469–474

    Article  Google Scholar 

  • Deli T, Said K, Chatti N. 2014. Morphological differentiation among geographically close populations of the green crab Carcinus aestuarii Nardo, 1847 (Brachyura, Carcinidae) from the Tunisian coast. Crustaceana, 87(3): 257–283

    Article  Google Scholar 

  • Duarte C M, Dennison W C, Orth R J W, et al. 2008. The charisma of coastal ecosystems: addressing the imbalance. Estuaries and Coasts, 31(2): 233–238

    Article  Google Scholar 

  • Duffy J E. 1996. Species boundaries, specialization, and the radiation of sponge-dwelling alpheid shrimp. Biological Journal of the Linnean Society, 58(3): 307–324

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S. 2005. Arlequin ver.3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1: 47–50

    Google Scholar 

  • Ferreira Silva A C, Brazão S, Hawkins S J, et al. 2009. Abundance, population structure and claw morphology of the semi-terrestrial crab Pachygrapsus marmoratus (Fabricius, 1787) on shores of differing wave exposure. Marine Biology, 156(12): 2591–2599

    Article  Google Scholar 

  • Flores A A V, Paula J. 2002. Population dynamics of the shore crab Pachygrapsus marmoratus (Brachyura: Grapsidae) in the central Portuguese coast. Journal of the Marine Biological Association of the United Kingdom, 82(2): 229–241

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, et al. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5): 294–299

    Google Scholar 

  • Fratini S, Ragionieri L, Cutuli G, et al. 2013. Pattern of genetic isolation in the crab Pachygrapsus marmoratus within the Tuscan Archipelago (Mediterranean Sea). Marine Ecology Progress Series, 478: 173–183

    Article  Google Scholar 

  • Fratini S, Schubart C D, Ragionieri L. 2011. Population genetics in the rocky shore crab Pachygrapsus marmoratus from the western Mediterranean and eastern Atlantic: complementary results from mtDNA and microsatellites at different geographic scales. In: Held C, Koenemann S, Schubart C D, eds. Crustacean Issues 19: Phylogeography and Population Genetics in Crustacea. Boca Raton, Florida: Taylor & Francis/CRC Press, 191–213

    Chapter  Google Scholar 

  • Fratini S, 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(1): 103–116

    Article  Google Scholar 

  • Fratini S, Zane L, Ragionieri L, et al. 2008. Relationship between heavy metal accumulation and genetic variability decrease in the intertidal crab Pachygrapsus marmoratus (Decapoda; Grapsidae). Estuarine, Coastal and Shelf Science, 79(4): 679–686

    Article  Google Scholar 

  • Freire J, Sampedro M P, González-Gurriarán E. 1996. Influence of morphometry and biomechanics on diet selection in three portunid crabs. Marine Ecology Progress Series, 137: 111–121

    Article  Google Scholar 

  • Hammer Ø, Harper D A T, Ryan P D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 9

    Google Scholar 

  • Hobbs R C, Botsford L W, Thomas A. 1992. Influence of hydrographic conditions and wind forcing on the distribution and abundance of Dungeness crab, Cancer magister, larvae. Canadian Journal of Fisheries and Aquatic Sciences, 49(7): 1379–1388

    Article  Google Scholar 

  • Hopkins M J, Thurman C L. 2010. The geographic structure of morphological variation in eight species of fiddler crabs (Ocypodidae: genus Uca) from the eastern United States and Mexico. Biological Journal of the Linnean Society, 100(1): 248–270

    Article  Google Scholar 

  • Hunt A. 1993. Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Pateriella calcar and P. exigua. Marine Ecology Pro-gress Series, 92: 179–186

    Article  Google Scholar 

  • Ingle R W. 1980. British Crabs. British Museum (Natural History). London: Oxford University Press, 222

    Google Scholar 

  • Johnson D F, Botsford L W, Methot R D Jr, et al. 1986. Wind stress and cycles in Dungeness crab (Cancer magister) catch off California, Oregon, and Washington. Canadian Journal of Fisheries and Aquatic Sciences, 43(4): 838–845

    Article  Google Scholar 

  • Johnson D R, Hester B S, McConaugha J R. 1984. Studies of a wind mechanism influencing the recruitment of blue crabs in the Middle Atlantic Bight. Continental Shelf Research, 3(4): 425–437

    Article  Google Scholar 

  • Jørstad K E, Prodöhl P A, Agnalt A-L, et al. 2004. Sub-arctic populations of European lobster, Homarus gammarus, in northern Norway. Environmental Biology of Fishes, 69(1–4): 223–231

    Article  Google Scholar 

  • Kimura M, Weiss G H. 1964. The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics, 49: 561–576

    Google Scholar 

  • Lee S Y, Seed R. 1992. Ecological implications of cheliped size in crabs: some data from Carcinus maenas and Liocarcinus holsatus. Marine Ecology Progress Series, 84: 151–160

    Article  Google Scholar 

  • Lye C M, Bentley M G, Clare A S, et al. 2005. Endocrine disruption in the shore crab Carcinus maenas-a biomarker for benthic marine invertebrates? Marine Ecology Progress Series, 288: 221–232

    Article  Google Scholar 

  • Mense D J, Posey M H, West T, et al. 1995. Settlement of brachyuran postlarvae along the North Carolina coast. Bulletin of Marine Science, 57(3): 793–806

    Google Scholar 

  • Narum S R. 2006. Beyond Bonferroni: less conservative analyses for conservation genetics. Conservation Genetics, 7(5): 783–787

    Article  Google Scholar 

  • Nei M. 1987. Molecular Evolutionary Genetics. New York: Columbia University Press, 512

    Google Scholar 

  • Nikula R, Väinölä R. 2003. Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Marine Biology, 143(2): 339–350

    Article  Google Scholar 

  • Orr M R, Smith T B. 1998. Ecology and speciation. Trends Ecol Evol, 13(12): 502–506

    Article  Google Scholar 

  • Pfeiler E, Hurtado L A, Knowles L L, et al. 2005. Population genetics of the swimming crab Callinectes bellicosus (Brachyura: Portunidae) from the eastern Pacific Ocean. Marine Biology, 146(3): 559–569

    Article  Google Scholar 

  • Quesada H, Beynon C M, Skibinski D O F. 1995. A mitochondrial DNA discontinuity in the mussel Mytilus Galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Molecular Biology and Evolution, 12(3): 521–524

    Google Scholar 

  • Reist J D. 1985. An empirical evaluation of several univariate methods that adjust for size variation in mor-phometric data. Canadian Journal of Zoology, 63(6): 1429–1439

    Article  Google Scholar 

  • Roman J, Palumbi S R. 2004. A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Molecular Ecology, 13(10): 2891–2898

    Article  Google Scholar 

  • Schluter D. 2000. Ecological character displacement in adaptive radiation. Amer Nat, 156(S4): S4–S16

    Article  Google Scholar 

  • Schubart C D, Cuesta J A, Rodriguez A. 2001. Molecular phylogeny of the crab genus Brachynotus (Brachyura: Varunidae) based on the 16S rRNA gene. Hydrobiologia, 449(1–3): 41–46

    Article  Google Scholar 

  • Serena F. 2005. Field identification guide to the sharks and rays of the Mediterranean and Black Sea. FAO Species Identification Guide for Fishery Purposes. Rome: FAO, 97

    Google Scholar 

  • Shirley S M, Shirley T C, Rice S D. 1987. Latitudinal variation in the Dungeness crab, Cancer magister: zoeal morphology explained by incubation temperature. Marine Biology, 95(3): 371–376

    Article  Google Scholar 

  • Silva I C, Mesquita N, 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(1): 28–46

    Article  Google Scholar 

  • Silva I C, Mesquita N, Schubart C D, et al. 2009. Genetic patchiness of the shore crab Pachygrapsus marmoratus along the Portuguese coast. Journal of Experimental Marine Biology and Ecology, 378(1–2): 50–57

    Article  Google Scholar 

  • Silva I C, Paula J. 2008. Is there a better chela to use for geometric morphometric differentiation in brachyuran crabs? A case study using Pachygrapsus marmoratus and Carcinus maenas. Journal of the Marine Biological Association of the United Kingdom, 88(5): 941–953

    Article  Google Scholar 

  • Slatkin M, Barton N H. 1989. A comparison of three indirect methods for estimating average levels of gene flow. International Journal of Organic Evolution, 43(7): 1349–1368

    Article  Google Scholar 

  • Slatkin M, Maddison W P. 1990. Detecting isolation by distance using phylogenies of genes. Genetics, 126(1): 249–260

    Google Scholar 

  • Spivak E D, Schubart C D. 2003. Species status in question: a morphometric and molecular comparison of Cyrtograpsus affinis and C. altimanus (Decapoda, Brachyura, Varunidae). Journal of Crustacean Biology, 23(1): 212–222

    Article  Google Scholar 

  • Spotte S. 1997. Sexual and regional variation in the morphology of the spotted anemone shrimp Periclimenes yucatanicus (Decapoda: Caridea: Palaemonidae). Journal of Crustacean Biology, 17(3): 389–397

    Article  Google Scholar 

  • Stamatis C, Triantafyllidis A, Moutou K A, et al. 2004. Mitochondrial DNA variation in Northeast Atlantic and Mediterranean populations of Norway lobster Nephrops norvegicus. Molecular Ecology, 13(6): 1377–1390

    Article  Google Scholar 

  • Stamatis C, Triantafyllidis A, Moutou K A, et al. 2006. Allozymic variation in Northeast Atlantic and Mediterranean populations of Norway lobster Nephrops norvegicus. ICES Journal of Marine Science, 63(5): 875–882

    Article  Google Scholar 

  • StatSoft, Inc. 1993. STATISTICA (data analysis software system: for the windows operating system reference for statistical procedures), version 4.5. www.statsoft.com

    Google Scholar 

  • Triantafyllidis A, Apostolidis A P, Katsares V, et al. 2005. Mitochondrial DNA variation in the European lobster (Homarus gammarus) throughout the range. Marine Biology, 146(2): 223–235

    Article  Google Scholar 

  • Weber L I, Hartnoll R G, Thorpe J P. 2000. Genetic divergence and larval dispersal in two spider crabs (Crustacea: Decapoda). Hydrobiologia, 420(1): 211–219

    Article  Google Scholar 

  • Weber L I, Levy J A. 2000. Genetic population structure of the swimming crab Callinectes danae (Crustacea: Decapoda) in southern Brazil. Hydrobiologia, 420(1): 203–210

    Article  Google Scholar 

  • Weetman D, Ruggiero A, Mariani S, et al. 2007. Hierarchical population genetic structure in the commercially exploited shrimp Crangon crangon identified by AFLP analysis. Marine Biology, 151(2): 565–575

    Article  Google Scholar 

  • Wright S. 1950. The genetical structure of populations. Nature, 166(4215): 247–249

    Article  Google Scholar 

  • Zitari-Chatti R, Chatti N, Elouaer A, et al. 2008. Genetic variation and population structure of the caramote prawn Penaeus kerathurus (Forskäl) from the eastern and western Mediterranean coasts in Tunisia. Aquaculture Research, 39(1): 70–76

    Article  Google Scholar 

  • Zitari-Chatti R, Chatti N, Fulgione D, et al. 2009. Mitochondrial DNA variation in the caramote prawn Penaeus (Melicertus) kerathurus across a transition zone in the Mediterranean Sea. Genetica, 136(3): 439–447

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Temim Deli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deli, T., Bahles, H., Said, K. et al. Patterns of genetic and morphometric diversity in the marbled crab (Pachygrapsus marmoratus, Brachyura, Grapsidae) populations across the Tunisian coast. Acta Oceanol. Sin. 34, 49–58 (2015). https://doi.org/10.1007/s13131-015-0687-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-015-0687-7

Key words

Navigation