Marine Biology

, Volume 156, Issue 11, pp 2313–2323 | Cite as

Lower genetic diversity in the limpet Patella caerulea on urban coastal structures compared to natural rocky habitats

  • Cécile FauvelotEmail author
  • Francesca Bertozzi
  • Federica Costantini
  • Laura Airoldi
  • Marco Abbiati
Original Paper


Human-made structures are increasingly found in marine coastal habitats. The aim of the present study was to explore whether urban coastal structures can affect the genetic variation of hard-bottom species. We conducted a population genetic analysis on the limpet Patella caerulea sampled in both natural and artificial habitats along the Adriatic coast. Five microsatellite loci were used to test for differences in genetic diversity and structure among samples. Three microsatellite loci showed strong Hardy–Weinberg disequilibrium likely linked with the presence of null alleles. Genetic diversity was significantly higher in natural habitat than in artificial habitat. A weak but significant differentiation over all limpet samples was observed, but not related to the type of habitat. While the exact causes of the differences in genetic diversity deserve further investigation, these results clearly point that the expansion of urban structures can lead to genetic diversity loss at regional scales.


Null Allele Allelic Richness Artificial Structure Heterozygote Deficiency Null Allele Frequency 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the EU projects DELOS (EVK3-CT-2000-00041) and EUMAR (EVK3CT2001-00048) and by the project MedRed (Bilateral Projects Italy–Israel, Italian Ministry of the Environment). We thank F. Bacchiocchi, C. Papetti, and M. Virgilio for help at various stages of the work. We are grateful to M. Coleman and anonymous reviewers whose comments greatly improved this manuscript.


  1. Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol 45:345–405Google Scholar
  2. Airoldi L, Abbiati M, Beck MW, Hawkins SJ, Jonsson PR, Martin D, Moschella PS, Sundelöf A, Thompson RC, Åberg P (2005a) An ecological perspective on the deployment and design of low crested and other hard coastal defence structures. Coast Eng 52:1073–1087CrossRefGoogle Scholar
  3. Airoldi L, Bacchiocchi F, Cagliola C, Bulleri F, Abbiati M (2005b) Impact of recreational harvesting on assemblages in artificial rocky habitats. Mar Ecol Prog Ser 299:55–66CrossRefGoogle Scholar
  4. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  5. Bacchiocchi F, Airoldi L (2003) Distribution and dynamics of epibiota on hard structures for coastal protection. Estuar Coast Shelf Sci 56:1157–1166CrossRefGoogle Scholar
  6. Bacci G, Sella G (1970) Correlations between characters and environmental conditions in Patella of caerulea group. Pubbl Staz Zool Napoli 38:1–17Google Scholar
  7. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) Genetix 404 A windows program for population genetics. Montpellier: Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, France. Available at Accessed 23 June 2009
  8. Bradshaw CJA, Isagi Y, Kaneko S, Brook BW, Bowman DMJS, Frankham R (2007) Low genetic diversity in the bottlenecked population of endangered non-native banteng in northern Australia. Mol Ecol 16:2998–3008PubMedCrossRefGoogle Scholar
  9. Buckland-Nicks J, Gibson G, Koss R (2002) Phylum Mollusca: Gastropoda. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic Press, San Diego, pp 261–287Google Scholar
  10. Bulleri F (2005) Role of recruitment in causing differences between intertidal assemblages on seawalls and rocky shores. Mar Ecol Prog Ser 287:53–65CrossRefGoogle Scholar
  11. Bulleri F, Airoldi L (2005) Artificial marine structures facilitate the spread of a non-indigenous green alga, Codium fragile spp. tomentosoides, in the north Adriatic Sea. J Appl Ecol 42:1063–1072CrossRefGoogle Scholar
  12. Bulleri F, Chapman MG (2004) Intertidal assemblages on artificial and natural habitats in marinas on the north-west coast of Italy. Mar Biol 145:381–391CrossRefGoogle Scholar
  13. Cencini C (1998) Physical processes and human activities in the evolution of the Po delta, Italy. J Coast Res 14:774–793Google Scholar
  14. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  15. Colson I, Hughes RN (2004) Rapid recovery of genetic diversity of dog whelk (Nucella lapillus L.) populations after local extinction and recolonization contradicts predictions from life-history characteristics. Mol Ecol 13:2223–2233PubMedCrossRefGoogle Scholar
  16. Connell SD (2001) Urban structures as marine habitats: an experimental comparison of the composition and abundance of subtidal epibiota among pilings, pontoons and rocky reefs. Mar Environ Res 52:115–125PubMedCrossRefGoogle Scholar
  17. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  18. Côrte-Real HBSM, Hawkins SJ, Thorpe JP (1996) Population differentiation and taxonomic status of the exploited limpet Patella candei in the Macaronesian islands (Azores, Madeira, Canaries). Mar Biol 125:141–152CrossRefGoogle Scholar
  19. Costantini F, Fauvelot C, Abbiati M (2007) Fine-scale genetic structuring in Corallium rubrum (L.): evidences of inbreeding and limited effective larval dispersal. Mar Ecol Prog Ser 340:109–119CrossRefGoogle Scholar
  20. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509PubMedCrossRefGoogle Scholar
  21. Davis J, Levin L, Walther S (2002) Artificial armoured shorelines: sites for open-coast species in a southern California bay. Mar Biol 140:1249–1262CrossRefGoogle Scholar
  22. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38Google Scholar
  23. Dethier MN, McDonald KM, Strathmann RR (2003) Colonization and connectivity of habitat patches for coastal marine species distant from source populations. Conserv Biol 17:1024–1035CrossRefGoogle Scholar
  24. Dodd JM (1957) Artificial fertilisation, larval development and metamorphosis in Patella vulgata L. and Patella caerulea L. Pubbl Staz Zool Napoli 29:172–186Google Scholar
  25. Dondi L, Rizzini A, Rossi P (1985) Recent geological evolution of the Adriatic Sea. In: Stanley DJ, Wezel FC (eds) Geological evolution of the Mediterranean basin. Springer, New York, pp 195–214Google Scholar
  26. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839CrossRefGoogle Scholar
  27. Espinosa F, Guerra-Garcia JM, Fa D, Garcia-Gomez JC (2006) Effects of competition on an endangered limpet Patella ferruginea (Gastropoda: Patellidae): implications for conservation. J Exp Mar Biol Ecol 330:482–492CrossRefGoogle Scholar
  28. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  29. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50Google Scholar
  30. Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evol Int J Org Evol 57:1571–1583Google Scholar
  31. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  32. Glasby TM, Connell SD (1999) Urban structures as marine habitats. Ambio 28:595–598Google Scholar
  33. Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  34. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices Version 2.9.3 [updated from Goudet (1995)]. Available at Accessed 23 June 2009
  35. Goudet J, Raymond M, de-Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  36. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623PubMedCrossRefGoogle Scholar
  37. Hurst CD, Skibinski DOF (1995) Comparison of allozyme and mitochondrial DNA spatial differentiation in the limpet Patella vulgata. Mar Biol 122:257–263Google Scholar
  38. Imron, Jeffrey B, Hale P, Degnan BM, Degnan SM (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Mol Ecol 16:289–304PubMedCrossRefGoogle Scholar
  39. Jenkins SR, Coleman RA, Della Santina P, Hawkins SJ, Burrows MT, Hartnoll RG (2005) Regional scale differences in the determinism of grazing effects in the rocky intertidal. Mar Ecol Prog Ser 287:77–86CrossRefGoogle Scholar
  40. Johnson MS, Black R (1984) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evol Int J Org Evol 38:1371–1383Google Scholar
  41. Koike K (1996) The countermeasures against coastal hazards in Japan. Geojournal 38:301–312CrossRefGoogle Scholar
  42. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228PubMedCrossRefGoogle Scholar
  43. Martin D, Bertasi F, Colangelo MA, de Vries M, Frost M, Hawkins SJ, Macpherson E, Moschella PS, Satta MP, Thompson RC, Ceccherelli VU (2005) Ecological impact of coastal defence structures on sediment and mobile fauna: evaluating and forecasting consequences of unavoidable modifications of native habitats. Coast Eng 52:1027–1051CrossRefGoogle Scholar
  44. Mauro A, Parrinello N, Arculeo M (2001) Artificial environmental conditions can affect allozymes genetic structure of the marine gastropod Patella caerulea. J Shellfish Res 20:1059–1063Google Scholar
  45. McElroy TC, Kandl KL, Garcia J, Trexler JC (2003) Extinction–colonization dynamics structure genetic variation of spotted sunfish (Lepomis punctatus) in the Florida Everglades. Mol Ecol 12:355–368PubMedCrossRefGoogle Scholar
  46. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260CrossRefGoogle Scholar
  47. Moreira J, Chapman MG, Underwood AJ (2006) Seawalls do not sustain viable populations of limpets. Mar Ecol Prog Ser 322:179–188CrossRefGoogle Scholar
  48. Moschella PS, Abbiati M, Åberg P, Airoldi L, Anderson JM, Bacchiocchi F, Bulleri F, Dinesen GE, Frost M, Gacia E, Granhag L, Jonsson PR, Satta MP, Sundelof A, Thompson RC, Hawkins SJ (2005) Low-crested coastal defence structures as artificial habitats for marine life: using ecological criteria in design. Coast Eng 52:1053–1071CrossRefGoogle Scholar
  49. Nei M (1987) Molecular evolutionary genetics. Columbia Univ Press, New YorkGoogle Scholar
  50. O’Reilly PT, Canino MF, Bailey KM, Bentzen P (2004) Inverse relationship between FST and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure. Mol Ecol 13:1799–1814PubMedCrossRefGoogle Scholar
  51. Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520PubMedCrossRefGoogle Scholar
  52. Peijnenburg KTCA, Fauvelot C, Breeuwer JAJ, Menken SBJ (2006) Spatial and temporal genetic structure of the planktonic Sagitta setosa (Chaetognatha) in European seas as revealed by mitochondrial and nuclear DNA markers. Mol Ecol 15:3319–3338PubMedCrossRefGoogle Scholar
  53. Pérez M, Branco M, Llavona A, Ribeiro PA, Santos AM, Hawkins SJ, Dàvila JA, Presa P, Alexandrino P (2007) Development of microsatellite loci for the black-footed limpet, Patella depressa, and cross-amplification in two other Patella species. Conserv Genet 8:739–742CrossRefGoogle Scholar
  54. Perkol-Finkel S, Shashar N, Benayahu Y (2006) Can artificial reefs mimic natural reef communities? The roles of structural features and age. Mar Env Res 61:121–135CrossRefGoogle Scholar
  55. Poulain PM (2001) Adriatic Sea surface circulation as derived from drifter data between 1990 and 1999. J Mar Syst 29:3–32CrossRefGoogle Scholar
  56. Raymond M, Rousset F (1995) GENEPOP: a population genetic software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  57. Reusch TBH, Ehlers A, Hammerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831PubMedCrossRefGoogle Scholar
  58. Rice WR (1989) Analysing tables of statistical tests. Evol Int J Org Evol 43:223–225Google Scholar
  59. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedCrossRefGoogle Scholar
  60. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386Google Scholar
  61. Sá-Pinto A, Branco M, Sayanda D, Alexandrino P (2008) Patterns of colonization, evolution and gene flow in species of the genus Patella in the Macaronesian Islands. Mol Ecol 17:519–532PubMedGoogle Scholar
  62. Spencer CC, Neigel JE, Leberg PL (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol Ecol 9:1517–1528PubMedCrossRefGoogle Scholar
  63. Thiede J (1978) A glacial Mediterranean. Nature 276:680–683CrossRefGoogle Scholar
  64. Vellend M (2006) The consequences of genetic diversity in competitive communities. Ecology 87:304–311PubMedCrossRefGoogle Scholar
  65. Virgilio M, Fauvelot C, Costantini F, Abbiati M, Backeljau T (2009) Deep phylogenetic splits and disjunct haplotype distribution suggest cryptic speciation in Hediste diversicolor (Polychaeta: Nereididae). Mol Ecol 18:1980–1994PubMedCrossRefGoogle Scholar
  66. Weir BS (1996) Genetic data analysis II. Sinauer Associates, SunderlandGoogle Scholar
  67. Wilson AB (2006) Genetic signature of recent glaciations on populations of a near-shore marine fish species (Syngnathus leptorhynchus). Mol Ecol 15:1857–1871PubMedCrossRefGoogle Scholar
  68. Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407PubMedCrossRefGoogle Scholar
  69. Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Cécile Fauvelot
    • 1
    • 2
    Email author
  • Francesca Bertozzi
    • 1
  • Federica Costantini
    • 1
  • Laura Airoldi
    • 1
  • Marco Abbiati
    • 1
  1. 1.Dipartimento di Biologia Evoluzionistica Sperimentale, Centro Interdipartimentale di Ricerca per le Scienze AmbientaliUniversity of BolognaRavennaItaly
  2. 2.Institut de Recherche pour le Développement (IRD), UR128, Centre de Biologie et d’Ecologie Tropicale et MéditerranéenneUniversité de PerpignanPerpignan CedexFrance

Personalised recommendations