Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol 45:345–405

    Google Scholar 

  • 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 52:1073–1087

    Article  Google Scholar 

  • 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 299:55–66

    Article  Google Scholar 

  • Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30

    Article  Google Scholar 

  • Bacchiocchi F, Airoldi L (2003) Distribution and dynamics of epibiota on hard structures for coastal protection. Estuar Coast Shelf Sci 56:1157–1166

    Article  Google Scholar 

  • Bacci G, Sella G (1970) Correlations between characters and environmental conditions in Patella of caerulea group. Pubbl Staz Zool Napoli 38:1–17

    Google Scholar 

  • 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 http://www.genetix.univ-montp2.fr/genetix/intro.htm#abstract. Accessed 23 June 2009

  • 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 16:2998–3008

    Article  PubMed  Google Scholar 

  • 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 261–287

    Google Scholar 

  • Bulleri F (2005) Role of recruitment in causing differences between intertidal assemblages on seawalls and rocky shores. Mar Ecol Prog Ser 287:53–65

    Article  Google Scholar 

  • 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 42:1063–1072

    Article  Google Scholar 

  • Bulleri F, Chapman MG (2004) Intertidal assemblages on artificial and natural habitats in marinas on the north-west coast of Italy. Mar Biol 145:381–391

    Article  Google Scholar 

  • Cencini C (1998) Physical processes and human activities in the evolution of the Po delta, Italy. J Coast Res 14:774–793

    Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  PubMed  CAS  Google Scholar 

  • 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 13:2223–2233

    Article  PubMed  CAS  Google Scholar 

  • 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 52:115–125

    Article  PubMed  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • 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 125:141–152

    Article  Google Scholar 

  • 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 340:109–119

    Article  CAS  Google Scholar 

  • Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  PubMed  CAS  Google Scholar 

  • Davis J, Levin L, Walther S (2002) Artificial armoured shorelines: sites for open-coast species in a southern California bay. Mar Biol 140:1249–1262

    Article  Google Scholar 

  • Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38

    Google Scholar 

  • Dethier MN, McDonald KM, Strathmann RR (2003) Colonization and connectivity of habitat patches for coastal marine species distant from source populations. Conserv Biol 17:1024–1035

    Article  Google Scholar 

  • Dodd JM (1957) Artificial fertilisation, larval development and metamorphosis in Patella vulgata L. and Patella caerulea L. Pubbl Staz Zool Napoli 29:172–186

    Google Scholar 

  • 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 195–214

    Google Scholar 

  • 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 92:832–839

    Article  Google Scholar 

  • 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 330:482–492

    Article  Google Scholar 

  • 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 131:479–491

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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 57:1571–1583

    CAS  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Glasby TM, Connell SD (1999) Urban structures as marine habitats. Ambio 28:595–598

    Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • 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 http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 23 June 2009

  • Goudet J, Raymond M, de-Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    PubMed  CAS  Google Scholar 

  • Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623

    Article  PubMed  Google Scholar 

  • Hurst CD, Skibinski DOF (1995) Comparison of allozyme and mitochondrial DNA spatial differentiation in the limpet Patella vulgata. Mar Biol 122:257–263

    CAS  Google Scholar 

  • 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 16:289–304

    Article  PubMed  CAS  Google Scholar 

  • 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 287:77–86

    Article  Google Scholar 

  • 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 38:1371–1383

    Google Scholar 

  • Koike K (1996) The countermeasures against coastal hazards in Japan. Geojournal 38:301–312

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • 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 52:1027–1051

    Article  Google Scholar 

  • Mauro A, Parrinello N, Arculeo M (2001) Artificial environmental conditions can affect allozymes genetic structure of the marine gastropod Patella caerulea. J Shellfish Res 20:1059–1063

    Google Scholar 

  • 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 12:355–368

    Article  PubMed  CAS  Google Scholar 

  • McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260

    Article  Google Scholar 

  • Moreira J, Chapman MG, Underwood AJ (2006) Seawalls do not sustain viable populations of limpets. Mar Ecol Prog Ser 322:179–188

    Article  Google Scholar 

  • 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 52:1053–1071

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia Univ Press, New York

    Google Scholar 

  • 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 13:1799–1814

    Article  PubMed  Google Scholar 

  • Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520

    Article  PubMed  CAS  Google Scholar 

  • 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 15:3319–3338

    Article  PubMed  CAS  Google Scholar 

  • 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 8:739–742

    Article  Google Scholar 

  • 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 61:121–135

    Article  CAS  Google Scholar 

  • Poulain PM (2001) Adriatic Sea surface circulation as derived from drifter data between 1990 and 1999. J Mar Syst 29:3–32

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP: a population genetic software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reusch TBH, Ehlers A, Hammerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831

    Article  PubMed  CAS  Google Scholar 

  • Rice WR (1989) Analysing tables of statistical tests. Evol Int J Org Evol 43:223–225

    Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • 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 365–386

    Google Scholar 

  • 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 17:519–532

    PubMed  Google Scholar 

  • Spencer CC, Neigel JE, Leberg PL (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol Ecol 9:1517–1528

    Article  PubMed  CAS  Google Scholar 

  • Thiede J (1978) A glacial Mediterranean. Nature 276:680–683

    Article  Google Scholar 

  • Vellend M (2006) The consequences of genetic diversity in competitive communities. Ecology 87:304–311

    Article  PubMed  Google Scholar 

  • 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 18:1980–1994

    Article  PubMed  CAS  Google Scholar 

  • Weir BS (1996) Genetic data analysis II. Sinauer Associates, Sunderland

    Google Scholar 

  • Wilson AB (2006) Genetic signature of recent glaciations on populations of a near-shore marine fish species (Syngnathus leptorhynchus). Mol Ecol 15:1857–1871

    Article  PubMed  CAS  Google Scholar 

  • Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407

    Article  PubMed  CAS  Google Scholar 

  • Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cécile Fauvelot.

Additional information

Communicated by T. Reusch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fauvelot, C., Bertozzi, F., Costantini, F. et al. Lower genetic diversity in the limpet Patella caerulea on urban coastal structures compared to natural rocky habitats. Mar Biol 156, 2313–2323 (2009). https://doi.org/10.1007/s00227-009-1259-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1259-1

Keywords

Navigation