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Interindividual variability in metal status in the shore crab Carcinus maenas: the role of physiological condition and genetic variation

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Abstract

The relations between genetic variation, physiological condition, size and metal status in the shore crab Carcinus maenas (L.) were investigated. Shore crabs were collected at three sites around the island of Funen, Denmark, and carapace width, colour, moulting stage and major ions and protein in the haemolymph were determined. Concentrations of water, cadmium, copper and zinc in midgut glands, muscles and gills were measured, and allozyme variation at 15 loci was studied. Generally, tissue water content and copper, zinc and cadmium concentrations decreased from the moulting stages C3 over C4 to D crabs, whereas the opposite was true for copper and zinc concentrations in gills and muscle. However, the water content of the tissues increased with the size of the crabs. Since tissue water contents changed consistently over moulting stages, conclusions on changes in metal concentrations sometimes diverged when expressed on a dry versus wet weight basis. Regarding allozymes, esterase, malate dehydrogenase and phosphoglucomutase were polymorphic. The crabs showed a low level of genetic variability for both polymorphism (0.14) and for heterozygosity (0.07) at the three sites. Allelic frequencies showed very low levels of differentiation among the samples, no evidence of inbreeding and no population subdivision. Multilocus heterozygosity was positively correlated with size. Concentrations of copper and zinc in midgut gland, muscle tissue and gill were not correlated with genotype, whereas a weak correlation between phosphoglucomutase genotypes and concentrations of cadmium in the midgut gland was found.

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References

  • Avise JC (1974) Systematic value of electrophoretic data. Syst Zool 23:465–481

    Google Scholar 

  • Ben-Shlomo R, Nevo E (1988) Isozyme polymorphism as monitoring of marine environments—the interactive effect of cadmium and mercury pollution on the shrimp, Palaemon elegans. Mar Pollut Bull 19:314–317

    Article  CAS  Google Scholar 

  • Benton MJ, Guttman SI (1990) Relationship of allozyme genotype to survivorship of mayflies (Stenonema femoratum) exposed to copper. J N Am Benthol Soc 9:271–276

    Google Scholar 

  • Benton MJ, Guttman SI (1992a) Allozyme genotype and differential resistance to mercury pollution in the caddisfly, Nectopsyche albida. 1. Single-locus genotypes. Can J Fish Aquat Sci 49:142–146

    Google Scholar 

  • Benton MJ, Guttman SI (1992b) Allozyme genotype and differential resistance to mercury pollution in the caddisfly, Nectopsyche albida. 2. Multilocus genotypes. Can J Fish Aquat Sci 49:147–149

    Google Scholar 

  • Bjerregaard P (1982) Accumulation of cadmium and selenium and their mutual interaction in the shore crab Carcinus maenas (L). Aquat Toxicol (Amst) 2:113–125

    Google Scholar 

  • Bjerregaard P (1988) Effect of selenium on cadmium uptake in selected benthic invertebrates. Mar Ecol Prog Ser 48:17–28

    CAS  Google Scholar 

  • Bjerregaard P (1990) Influence of physiological condition on cadmium transport from hemolymph to hepatopancreas in Carcinus maenas. Mar Biol 106:199–209

    CAS  Google Scholar 

  • Bjerregaard P (1991) Relationship between physiological condition and cadmium accumulation in Carcinus maenas (L). Comp Biochem Physiol A Physiol 99:75–83

    Article  Google Scholar 

  • Bjerregaard P, Depledge MH (1994) Cadmium accumulation in Littorina littorea, Mytilus edulis and Carcinus maenas—the influence of salinity and calcium-ion concentrations. Mar Biol 119:385–395

    CAS  Google Scholar 

  • Bjerregaard P, Depledge MH (2002) Trace metal concentrations and contents in the tissues of the shore crab Carcinus maenas: effects of size and tissue hydration. Mar Biol 141:741–752

    Article  CAS  Google Scholar 

  • Bjerregaard P, Vislie T (1986) Effect of copper on ion-regulation and osmoregulation in the shore crab Carcinus maenas. Mar Biol 91:69–76

    CAS  Google Scholar 

  • Bondgaard M, Nørum U, Bjerregaard P (2000) Cadmium accumulation in the female shore crab Carcinus maenas during the moult cycle and ovarian maturation. Mar Biol 137:995–1004

    Article  CAS  Google Scholar 

  • Brown AHD (1970) The estimation of Wright’s fixation index from genotypic frequencies. Genetica (Dordr) 41:399–406

  • Bulnheim HP, Bahns S (1996) Genetic variation and divergence in the genus Carcinus (Crustacea, Decapoda). Int Rev Gesamten Hydrobiol 81:611–619

    Google Scholar 

  • Burton RS (1983) Protein polymorphisms and genetic differentiation of marine invertebrate populations. Mar Biol Lett 4:193–206

    Google Scholar 

  • Burton RS, Feldman MW, Curtsinger JW (1979) Population-genetics of Tigriopus californicus (Copepoda, Harpacticoida). 1. Population-structure along the central California coast. Mar Ecol Prog Ser 1:29–39

    CAS  Google Scholar 

  • Chan HM, Rainbow PS (1993) The accumulation of dissolved zinc by the shore crab Carcinus maenas (L). Ophelia 38:13–30

    Google Scholar 

  • Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed  Google Scholar 

  • Crisp DJ (1978) Genetic consequences of different reproductive strategies in marine invertebrates. In: Battaglia B, Beardmore JA (ed) Marine organisms. Genetics, ecology and evolution. Plenum, New York, pp 257–269

  • Crothers JH (1967) The biology of the shore crab Carcinus maenas (L.). I. The background—anatomy, growth and life history. Field Stud 2:407–434

    Google Scholar 

  • Crothers JH (1968) The biology of the shore crab Carcinus maenas (L.). II. The life of the adult crab. Field Stud 2:579–614

    Google Scholar 

  • De Nicola M, Gambardella C, Guarino SM (1992) Interactive effects of cadmium and zinc pollution on Pgi and Pgm polymorphisms in Idotea baltica. Mar Pollut Bull 24:619–621

    Article  Google Scholar 

  • Devescovi M, Lucu C (1995) Seasonal-changes of the copper level in shore crabs Carcinus mediterraneus. Mar Ecol Prog Ser 120:169–174

    CAS  Google Scholar 

  • Diehl WJ, Biesiot PM (1994) Relationships between multilocus heterozygosity and morphometric indexes in a population of the deep-sea red crab Chaceon quinquedens (Smith). J Exp Mar Biol Ecol 182:237–250

    Article  Google Scholar 

  • Gaffney PM, Scott TM, Koehn RK, Diehl WJ (1990) Interrelationships of heterozygosity, growth-rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics 124:687–699

    CAS  PubMed  Google Scholar 

  • Garton DW, Haag WR (1991) Heterozygosity, shell length and metabolism in the European mussel, Dreissena polymorpha, from a recently established population in Lake Erie. Comp Biochem Physiol A Physiol 99:45–48

    Article  Google Scholar 

  • Gentili MR, Beaumont AR (1988) Environmental-stress, heterozygosity, and growth-rate in Mytilus edulis. l. J Exp Mar Biol Ecol 120:145–153

    Article  Google Scholar 

  • Hedgecock D, Tracey ML, Nelson K (1982) Genetics. In: Abele LG (ed) The biology of Crustacea, vol 2. Embryology, morphology and genetics. Academic, New York, pp 283–403

  • Hillis DM (1987) Molecular versus morphological approaches to systematics. Annu Rev Ecol Syst 18:23–42

    Article  Google Scholar 

  • Huang S, Shih JT (1995) Microgeographic genetic-structure of the fiddler-crab, Uca arcuata de Haan (Ocypodidae) in Taiwan. Hydrobiologia 295:67–74

    CAS  Google Scholar 

  • Hvilsom MM (1983) Copper-induced differential mortality in the mussel Mytilus edulis. Mar Biol 76:291–295

    CAS  Google Scholar 

  • Kerkut GA, Moritz PM, Munday KA (1961) Variations of copper concentrations in Carcinus maenas. Cah Biol Mar 2:399–408

    Google Scholar 

  • Kittiwattanawong K (2001) Correlation of multilocus heterozygosity to growth rate, oxygen consumption, and morphological characteristics in Cerastoderma edule (Bivalvia: Cardiidae). Phuket Mar Biol Center Spec Publ 25:323–341

    Google Scholar 

  • Koehn RK, Gaffney PM (1984) Genetic heterozygosity and growth-rate in Mytilus edulis. Mar Biol 82:1–7

    Google Scholar 

  • Koehn RK, Diehl WJ, Scott TM (1988) The differential contribution by individual enzymes of glycolysis and protein catabolism to the relationship between heterozygosity and growth-rate in the coot clam, Mulinia lateralis. Genetics 118:121–130

    CAS  PubMed  Google Scholar 

  • Lavery S, Fielder DR (1993) Low allozyme variation in the coconut crab Birgus latro. Comp Biochem Physiol B Biochem Mol Biol 104:353–359

    Article  Google Scholar 

  • Lavie B, Nevo E (1986) Genetic selection of homozygote allozyme genotypes in marine gastropods exposed to cadmium pollution. Sci Total Environ 57:91–98

    Article  CAS  PubMed  Google Scholar 

  • McGaw IJ, Naylor E (1992a) Distribution and rhythmic locomotor patterns of estuarine and open-shore populations of Carcinus maenas. J Mar Biol Assoc UK 72:599–609

    Google Scholar 

  • McGaw IJ, Naylor E (1992b) Salinity preference of the shore crab Carcinus maenas in relation to coloration during intermolt and to prior acclimation. J Exp Mar Biol Ecol 155:145–159

    Article  Google Scholar 

  • McGaw IJ, Kaiser MJ, Naylor E, Hughes RN (1992) Intraspecific morphological variation related to the molt-cycle in color forms of the shore crab Carcinus maenas. J Zool 228:351–359

    Google Scholar 

  • Mulley JC, Latter BDH (1980) Genetic-variation and evolutionary relationships within a group of 13 species of penaeid prawns. Evolution 34:904–916

    CAS  Google Scholar 

  • Nelson K, Hedgecock D (1980) Enzyme polymorphism and adaptive strategy in the decapod Crustacea. Am Nat 116:238–280

    Article  CAS  Google Scholar 

  • Nevo E (1978) Genetic-variation in natural-populations—Patterns and theory. Theor Popul Biol 13:121–177

    CAS  PubMed  Google Scholar 

  • Nevo E, Perl T, Beiles A, Wool D (1981) Mercury selection of allozyme genotypes in shrimps. Experientia 37:1152–1154

    CAS  Google Scholar 

  • Nevo E, Ben-Shlomo R, Lavie B (1984) Mercury selection of allozymes in marine organisms—Prediction and verification in nature. Proc Natl Acad Sci USA 81:1258–1259

    CAS  Google Scholar 

  • Nevo E, Noy R, Lavie B, Beiles A, Muchtar S (1986) Genetic diversity and resistance to marine pollution. Biol J Linn Soc 29:139–144

    Google Scholar 

  • Nørum U, Bondgaard M, Bjerregaard P (2003) Copper and zinc handling during the moult cycle of male and female shore crabs Carcinus maenas. Mar Biol 142:757–769

    Google Scholar 

  • Patarnello T, Guinez R, Battaglia B (1991) Effects of pollution on heterozygosity in the barnacle Balanus amphitrite (Cirripedia, Thoracica). Mar Ecol Prog Ser 70:237–243

    Google Scholar 

  • Reid DG, Abello P, McGaw IJ, Naylor E (1989) Phenotypic variation in sympatric crab populations. In: Aldrich JC (ed) Phenotypic responses and individuality in aquatic ectotherms. JAPAGA, Ashford, Wicklow, Ireland, pp 89–96

  • Reid DG, Abello P, Kaiser MJ, Warman CG (1997) Carapace colour, inter-moult duration and the behavioural and physiological ecology of the shore crab Carcinus maenas. Estuar Coast Shelf Sci 44:203–211

    Article  Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. Academic, New York

  • Sherburne SW (1976) Phosphoglucomutase polymorphism in green crab, Carcinus maenas. J Fish Res Board Can 33:2826–2829

    Google Scholar 

  • Siegismund HR (1994) G-Stat, ver. 3. Genetical statistical programs for the analysis of population data. The Arboretum, Royal Veterinary and Agricultural University, Hoersholm, Denmark

  • Simonsen V, Damgaard BM, Larsen B, Lohi O (1992) Genetic-polymorphism of esterase in plasma of American mink (Mustela vison L). Anim Genet 23:553–555

    CAS  PubMed  Google Scholar 

  • Singh SM, Zouros E (1978) Genetic-variation associated with growth-rate in American oyster (Crassostrea virginica). Evolution 32:342–353

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. The principles and practice of statistics in biological research, 2nd edn. Freeman, New York

  • Stevens PM (1991) A genetic-analysis of the pea crabs (Decapoda, Pinnotheridae) of New-Zealand. 2. Patterns and intensity of spatial population-structure in Pinnotheres atrinicola. Mar Biol 108:403–410

    Google Scholar 

  • Styrishave B, Petersen MF, Andersen O (2000) Influence of cadmium accumulation and dietary status on fatty acid composition in two colour forms of shore crabs, Carcinus maenas. Mar Biol 137:423–433

    Article  CAS  Google Scholar 

  • Tchernigovtzeff C (1965) Multiplication cellulaire et régénération au cours du cycle d’intermue des crustacés décapodes. Arch Zool Exp Gen 106:377–497

    Google Scholar 

  • Theede H (1969) Some new aspects in osmoregulation of Carinus maenas. Mar Biol 2:114–120

    CAS  Google Scholar 

  • Thorpe JP, Solé-Cava AM (1994) The use of allozyme electrophoresis in invertebrate systematics. Zool Scr 23:3–18

    Google Scholar 

  • Toro JE, Vergara AM, Gallegillos R (1996) Multiple-locus heterozygosity, physiology and growth at two different stages in the life cycle of the Chilean oyster Ostrea chilensis. Mar Ecol Prog Ser 134:151–158

    Google Scholar 

  • Tracey ML, Nelson K, Hedgecock D, Shleser RA, Pressick ML (1975a) Biochemical genetics of lobsters—Genetic-variation and structure of American lobster (Homarus americanus) populations. J Fish Res Board Can 32:2091–2101

    CAS  Google Scholar 

  • Tracey ML, Bellet NF, Gravem CD (1975b) Excess allozyme homozygosity and breeding population structure in mussel Mytilus californianus. Mar Biol 32:303–311

    CAS  Google Scholar 

  • Van Wormhoudt A, Bourreau G, Lemoullac G (1995) Amylase polymorphism in Crustacea decapoda—Electrophoretic and immunological studies. Biochem Syst Ecol 23:139–149

    Article  Google Scholar 

  • Zouros E, Romerodorey M, Mallet AL (1988) Heterozygosity and growth in marine bivalves—Further data and possible explanations. Evolution 42:1332–1341

    Google Scholar 

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Acknowledgements

This investigation was supported by grants from the Danish Natural Science Research Council and The Danish Environmental Research Program.

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Authors and Affiliations

  1. Ecotoxicology Group, Institute of Biology, University of Southern Denmark, Campusvej 55, 5230, Odense M, Denmark

    L. R. Nissen & P. Bjerregaard

  2. Department of Terrestrial Ecology, National Environmental Research Institute, P.O. Box 314, 8600, Silkeborg, Denmark

    V. Simonsen

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  1. L. R. Nissen
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  2. P. Bjerregaard
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Correspondence to P. Bjerregaard.

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Communicated by M. Kühl, Helsingør

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Nissen, L.R., Bjerregaard, P. & Simonsen, V. Interindividual variability in metal status in the shore crab Carcinus maenas: the role of physiological condition and genetic variation. Marine Biology 146, 571–580 (2005). https://doi.org/10.1007/s00227-004-1455-y

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