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Population differentiation and taxonomic status of the exploited limpet Patella candei in the Macaronesian islands (Azores, Madeira, Canaries)

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Abstract

There has been considerable confusion in the taxonomy of limpets of the North East Atlantic Ocean and Mediterranean Sea, particularly those from the Macaronesian islands. The present study compared populations of the intertidal limpet Patella candei d'Orbigny from the Azores, Madeira and the Canaries with those of P. caerulea Linnaeus and P. depressa Pennant from the European and African continental coasts. No major differences in radular morphology were detected between the three species. However, electrophoretic analysis of 15 enzyme loci gave overall genetic identity (I) values of ∼0.5 between the three species, indicating that they cannot be regarded as conspecific as previously thought, and suggesting that P. candei is endemic to the Macaronesian islands. Comparisons of P. candei within these islands showed that, although populations did not differ with respect to radular morphology and soft-body parts, populations from the Azores were distinct from those in Madeira and the Canaries in shell shape and gene frequencies. Individuals from the Azores had, no average, taller shells and longer radulae, while those in Madeira and the Canaries had a shallow, depressed and stellate shell form. This was interpreted as being due to the wider habitat distribution of the species in the Azores compared to Madeira and the Canaries. Electrophoretic results showed that P. candei from the Azores differed from P. candei in Madeira and the Canaries by almost 40% of the loci investigated (I=0.660), suggesting that the former is a separate endemic species. An I value of 0.969 between populations in Madeira and the Canaries was typical of conspecific populations.

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References

  • Abdel-Monem A, Fernandez LA, Boone GM (1975) K-Ar ages from the eastern Azores group (Santa Maria, S. Miguel and the Formigas islands). Lithos 8:247–254

    Google Scholar 

  • Anderson TW (1984) An introduction to multivariate statistical analysis. Wiley, New York

    Google Scholar 

  • Atchley WR, Nordheim EV, Gunsett FC, Crump PL (1982) Geometric and probabilistic aspects of statistical distance functions. Syst Zool 31:445–460

    Google Scholar 

  • Ayala FJ (1975) Genetic differentiation during the speciation process. Evolutionary Biol 8:1–78

    Google Scholar 

  • Ayala FJ (1983) Enzymes as taxonomic characters. In: Oxford GS, Rollinson D (eds) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, pp 3–26

    Google Scholar 

  • Beaumont AR, Wei JHC (1991) Morphological and genetic variation in the Antarctic limpet Nacella concinna (Strebel, 1908). J mollusc Stud 57:443–450

    Google Scholar 

  • Beaumont AR, Zouros ER (1991) Genetics of scallops. In: Shumway SE (ed) Scallops: biology, ecology and aquaculture. Elsevier Publishers, Amsterdam, pp 585–617

    Google Scholar 

  • Berggren WA, Hollister CD (1974) Paleogeography, paleobiogeography and the history of circulation in the Atlantic Ocean. Spec Publs Soc econ Paleont Miner, Tulsa 20:126–186

    Google Scholar 

  • Blackith RE, Reyment RA (1971) Multivariate morphometrics. Academic Press, London

    Google Scholar 

  • Bonnell ML, Selander RK (1974) Elephant seals: genetic variation and near extinction. Science, NY 184:908–909

    Google Scholar 

  • Bowman RS, Lewis JR (1977) Annual fluctuations in recruitment of P. vulgata. J mar biol Ass UK 57:799–815

    Google Scholar 

  • Branch CM (1981) The biology of limpets: physical factors, energy flow and ecological interactions. Oceanogr mar biol A Rev 19:235–380

    Google Scholar 

  • Brian MV, Owen G (1952) The relation of the radula fraction to the environment in Patella. J Anim Ecol 21:241–249

    Google Scholar 

  • Briggs JC (1970) A faunal history of the North Atlantic Ocean. Syst Zool 19:19–34

    Google Scholar 

  • Christiaens J (1973) Révision du genre Patella (Mollusca, Gastropoda). Bull Mus natn Hist nat, Paris 182:1305–1392

    Google Scholar 

  • Colognola R, Mastrurzo P, Russo GF, Scardi M, Vinci D, Fresi E (1986) Biometric and genetic analysis of the marine rissoid Rissoa auriscalpium (Gastropoda: Prosobranchia) and its ecological implications. Mar Ecol 7:265–285

    Google Scholar 

  • Cook LM, Cameron RAD, Lace LA (1990) Land snails of eastern Madeira: speciation, persistance and colonisation. Proc R Soc (Ser B) 239:35–79

    Google Scholar 

  • Côrte-Real HBSM (1992) Taxonomy and population genetics of exploited species of Patella in the Azores, Madeira and Canaries. Unpublished thesis. University of Liverpool, Port Erin, Isle of Man

    Google Scholar 

  • Côrte-Real HBSM, Hawkins SJ, Thorpe JP (1992) Genetic confirmation that intertidal and subtidal morphs of Patella ulyssiponensis aspera Röding (Mollusca: Gastropoda: Patellidae) are conspecific. Arquipélago 10:55–66

    Google Scholar 

  • Cretella M, Scillitani G, Toscano F, Turella P, Picariello D, Cataudo A (1994) Relationships between Patella ferruginea Gmelin, 1971 and other Tyrrhenian species of Patella (Gastropoda: Patellidae). J mollusc Stud 60:9–17

    Google Scholar 

  • Dautzenberg PH (1889) Contribution à la faune malacologique des Iles Açores. Résult Camp Scient Prince Albert I

  • Davies PS (1969) Effect of environment on metabolic activity and morphology of Mediterranean and British species of Patella. Pubbl Staz zool Napoli (I: Mar Ecol) 37:641–656

    Google Scholar 

  • Drouet H (1858) Mollusques marins des Iles Açores. Mém Soc acad Agric Sci Dép Aube 22

  • Ferguson A (1980) Biochemical systematics and evolution. Blackie, Glasgew

    Google Scholar 

  • Fischer-Piette E (1935) Systématique et biogéographie-les patelles d'Europe et d'Afrique du Nord. J Conch, Paris 79:5–66

    Google Scholar 

  • Fischer-Piette E (1938) The concept of species and geographical isolation in the case of North Atlantic Patellas. Proc Linn Soc Lond 150:268–275

    Google Scholar 

  • Gaffney PM (1980) On the number of Patella spp. in southwest England. J mar biol Ass UK 60:565–574

    Google Scholar 

  • Gould AA (1864) Expedition shells, described for the work of the United States Exploring Expedition. Boston

  • Gray JE (1954) List of the shells of the Canaries in the collection of the British Museum. British Museum, London

    Google Scholar 

  • Harris H, Hopkinson DA (1970) Handbook of enzyme electrophoresis in human genetics. North-Holland, Amsterdam

    Google Scholar 

  • Hawkins SJ, Burnay LP, Neto AI, Tristão da Cunha R, Frias Martins AM (1990a) A description of the zonation patterns of molluscs and other important biota on the south coast of São Miguel, Azores. Açforeana (Revta Estud açorean: Bolm Soc Estud açorean “Afonso Chaves”) Suppl: 21–38

  • Hawkins SJ, Còrte-Real HBSM, Martins HR, Santos RS, Frias Martins AM (1990b) A note on the identity of Patella in the Azores. Açoreana (Revta Estud açorean: Bolm Soc Estud açorean “Afonso Chaves”) Suppl: 167–173

  • Hawkins SJ, Watson DC, Hill AS, Harding SP, Kyriakides MA, Hutchinson S, Norton TA (1989) A comparison of feeding mechanisms in microphagous, herbivorous, intertidal, prosobranchs in relation to resource partitioning. J molluse Stud 55:151–165

    Google Scholar 

  • Hoelzel AR, Dover GA (1990) Molecular techniques for examining genetic variation and stock identity in cetacean species. Rep int Whal Commn Spec Iss II: 81–120 (SC/39/07)

  • Janson K (1987) Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol J Linn Soc 30:245–256

    Google Scholar 

  • Janson K, Sundberg P (1983) Multivariate morphometric analysis of two varieties of Littorina saxatilis from the Swedish west coast. Mar Biol 74:49–53

    Google Scholar 

  • Johnson MS, Black R (1984) The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp. Mar Biol 79:295–302

    Google Scholar 

  • Lamarck JBPA (1836) Histoire naturelle des animaux sans vertèbres. JB Bailliere, Paris

    Google Scholar 

  • Lessios HA (1992) Testing electrophoretic data for agreement with Hardy-Weinberg expectations. Mar Biol 112:517–523

    Google Scholar 

  • Linnaeus C von (1758) Systema naturae Xth ed. Regnum animale. Impensis Direct, Holmiae

    Google Scholar 

  • MacAndrew R (1954) On the geographical distribution of testaceous Mollusca in the North Atlantic and neighbouring seas. Greenwood, Liverpool

  • Martins HR, Santos RS, Hawkins SJ (1987) Exploitation of limpets (Patella spp.) in the Azores with a preliminary analysis of the stocks. Int Counc Explor Sea Comm Meet (Shellfish and Benthos Comm) K 53:1–18

    Google Scholar 

  • Minitab Inc. (1991) Release 8.1. State College, Pennsylvania

  • Moore HB (1934) The relationship of shell growth to environment in P. vulgata. Proc malac Soc Lond 21:217–222

    Google Scholar 

  • Morton BS (1967) Malacological report. In: Anonymous (ed) Chelsea College Azores Expedition, July–October 1965. Chelsea College, London, pp 30–39

    Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106: 283–292

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, Austin, Tex 89:583–590

    Google Scholar 

  • Nei M (1987) Genetic distance and molecular phylogeny. In: Ryman N, Utter F (eds) Population genetics and fishery management. Washington Sea Grant Program, Seattle, USA, pp 193–223

    Google Scholar 

  • Nei M, Roychoudhury AK (1974) Sampling variances of heterozygosity and genetic distance. Genetics, Austin, Tex 76:379–390

    Google Scholar 

  • Nobre A (1930) Materiais para o estudo da fauna dos Açores. Instituto de Zoologia da Universidade do Porto, Porto

    Google Scholar 

  • Nolan CP (1991) Size, shape and shell morphology of the Antartic limpet Nacella concinna at Signy Island, South Orkney Islands. J mollusc Stud 57:225–238

    Google Scholar 

  • Pilsbry H (1891) Patellidae, structure and systematics.In: Tyron GW (ed) Manual of conchology. National Academy of Science, Philadelphia, pp 1–195

    Google Scholar 

  • Powell A (1973) the patellid limpets of the world. Indo-Pacif Mollusca 3:75–99

    Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis — a handbook for animal systematics and population studies. Academic Press, London

    Google Scholar 

  • Sarich VM (1977) Electrophoresis in evolutionary studies: rates, sample sizes and the neutrality hypothesis. Nature, Lond 265: 24–28

    Google Scholar 

  • Schaal BA, Anderson WW (1974) An outline of techniques for starch gel electrophoresis of enzymes from the American oyster Crassostrea virginica Gmelin. Tech Rep Ser Ga mar Sci Cent Savannah 74:3–19

    Google Scholar 

  • Schmncke H-U (1973) Magmatic evolution and tectonic regime in the Canary, Madeira and Azores island groups. Bull geol Soc Am 84:633–648

    Google Scholar 

  • Selander RK (1970) Behaviour and genetic variation in natural populations. Am Zool 10:53–66

    Google Scholar 

  • Sella G (1976) Biometrical relationships between mesolittoral and infralittoral Patella populations in the Mediterranean. Pubbl Staz zool Napoli (I: Mar Ecol) 40:123–132

    Google Scholar 

  • Sella G, Robotti CA, Biglione V (1993) Genetic divergence among three sympatric species of Mediterranean Patella (Archaeogastropoda). Mar Biol 115:401–405

    Google Scholar 

  • Skibinski DOF, Ward RD (1982) Correlations between heterozygosity and evolutionary rates of proteins. Nature, Lond 298:490–492

    Google Scholar 

  • Smith PJ, Jamieson A, Birley AJ (1990) Electrophoresis studies and the stock concept in marine teleosts. J Cons int Explor Mer 47:231–245

    Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy — the principles and practice of numerical classification. Freeman, San Francisco

    Google Scholar 

  • Solé-Cava AM, Klautau M, Boury-Esnault N, Borojecic R, Thorpe JP (1991) Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genus Clathrina. Mar Biol 111:381–386

    Google Scholar 

  • Solé-Cava Am, Thorpe JP (1986) Genetic differentiation between morphotypes of the marine sponge Suberites ficus (Demospongiae: Hadromerida). Mar Biol 93:247–253

    Google Scholar 

  • Somers KM (1986) Multivariate allometry and removal of size with principal component analysis. Syst Zool 35:359–368

    Google Scholar 

  • Sundberg P (1988) Microgeographic variation in shell characters of Littorina saxatilis Olivi — a question mainly of size? Biol J Linn Soc 35:169–184

    Google Scholar 

  • Sverdrup HV, Johnson MW, Fleming RH (1946) The oceans. Prentice-Hall, Englewood Cliffs, New Jersey

    Google Scholar 

  • Swofford DL, Selander RK (1981) BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J Hered 72:281–283

    Google Scholar 

  • Thorpe JP (1979) Enzyme variation and taxonomy: the estimation of sampling errors in measurements of interspecific genetic similatity. Biol J Linn Soc 11:369–386

    Google Scholar 

  • Thorpe JP (1982) The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. A Rev Ecol Syst 13:139–168

    Google Scholar 

  • Thorpe JP (1983) Enzyme variation, genetic distance and evolutionary divergence in relation to levels of taxonomic separation. In: Oxford GS, Rollinson D (eds) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, pp 131–152

    Google Scholar 

  • Thorpe JP (1989) Possible effects of interprotein variation in mean rate of amino acid substitution on the relationship of genetic distance with time since evolutionary divergence. Biol J Linn Soc 37:335–344

    Google Scholar 

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

    Google Scholar 

  • Varvio S-L, Koehn RK, Väinölä R (1988) Evolutionary genetics of the Mytilus edulis complex in the North Atlantic region. Mar Biol 98:51–60

    Google Scholar 

  • Ward RD, Beardmore JA (1977) Protein variation in the plaice Pleuronectes platessa. Genet Res 30:45–62

    Google Scholar 

  • Ward RD, Skibinski DOF (1985) Observed relationships between protein heterozygosity and protein genetic distance, and comparisons with neutral expectations. Genet Res 45:315–340

    Google Scholar 

  • Webb PB, Berthelot S, d'Orbigny ACV (1839) Mollusques, échinodermes, foraminifères et polypiers, recueillis aux îles Canaries. In: Webb PB, Berthelot S & C (eds) Histoire naturelle des Iles Canaries, Vol II. Pt I. Paris

  • Zouros E (1987) On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine molluscs. Isozymes 15:225–270

    Google Scholar 

  • Zouros E, Foltz DW (1987) The use of allelic isozyme variation for the study of heterosis. Isozymes 13:1–59

    Google Scholar 

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Communicated by A. Rodríguez, Puerto Real

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Côrte-Real, H.B.S.M., Hawkins, S.J. & Thorpe, J.P. Population differentiation and taxonomic status of the exploited limpet Patella candei in the Macaronesian islands (Azores, Madeira, Canaries). Marine Biology 125, 141–152 (1996). https://doi.org/10.1007/BF00350768

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