Abstract
The diversity–stability relationship is the subject of a long-standing debate in ecology, but the genetic component of diversity has seldom been explored. In this study, we analyzed the interplay between genetic diversity and demographic responses to environmental pressures. This analysis included 30 meadows formed by the Mediterranean endemic seagrass, Posidonia oceanica, showing a wide range of population dynamics ranging from a near equilibrium state to steep decline due to strong environmental pressures close to aquaculture installations. Our results show that sedimentation rates are much better predictors of mortality than clonal or genetic components. An unexpected positive trend was observed between genotypic diversity and mortality, along with a negative relationship between allelic richness and net population growth. Yet such trends disappeared when excluding the most extreme cases of disturbance and mortality, suggesting the occurrence of a threshold below which no relationship exists. These results contrast with the positive relationship between genotypic diversity and resistance or resilience observed in previous manipulative experiments on seagrass. We discuss the reasons for this discrepancy, including the difficulties in designing experiments reflecting the complexity of natural meadows.
Similar content being viewed by others
References
Alberto, F., L. Correia, S. Arnaud-Haond, C. Billot, C.M. Duarte, and E.A. Serrão. 2003. New microsatellites markers for the endemic Mediterranean seagrass Posidonia oceanica. Molecular Ecology Notes 3: 253–255.
Arnaud-Haond, S., and K. Belkhir. 2007. GenClone 1.0: A new program to analyse genetics data on clonal organisms. Molecular Ecology Notes 7: 15–17.
Arnaud-Haond, S., F. Alberto, S. Teixeira, G. Procaccini, E.A. Serrao, and C.M. Duarte. 2005. Assessing genetic diversity in clonal organisms: Low diversity or low resolution? Combining power and cost efficiency in selecting markers. Journal of Heredity 96: 434–440.
Arnaud-Haond, S., C.M. Duarte, F. Alberto, and E.A. Serrão. 2007a. Standardizing methods to address clonality in population studies. Molecular Ecology 16: 5115–5139.
Arnaud-Haond, S., M. Migliaccio, E. Diaz-Almela, S. Teixeira, M.S. van de Vliet, F. Alberto, G. Procaccini, C.M. Duarte, and E.A. Serrao. 2007b. Vicariance patterns in the Mediterranean Sea: East–west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. Journal of Biogeography 34: 963–976.
Belkhir K, Borsa P, Chikhi L, N.Raufaste, Bonhomme F (1996–2001) GENETIX 4.02, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome et Populations, Interactions, Adaptations, CNRS UMR5000, Université Montpellier II, Montpellier, France
Blomqvist, S., and L. Hakanson. 1981. A review on sediment traps in aquatic environments. Archiv Fur Hydrobiologie 91: 101–132.
The R Development Core Team (2004) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-00-3. http://www.r-project.org/.
Diaz-Almela, E., S. Arnaud-Haond, M.S. Vliet, E. Alvarez, N. Marba, C.M. Duarte, and E.A. Serrao. 2007. Feed-backs between genetic structure and perturbation-driven decline in seagrass (Posidonia oceanica) meadows. Conservation Genetics 8: 1377–1391.
Diaz-Almela, E., N. Marba, E. Alvarez, R. Santiago, M. Holmer, A. Grau, S. Mirto, R. Danovaro, A. Petrou, and M. Argyrou. 2008. Benthic input rates predict seagrass (Posidonia oceanica) fish farm-induced decline. Marine Pollution Bulletin 56: 1332–1342.
Dorken, M.E., J. Friedman, and S.C.H. Barrett. 2002. The evolution and maintenance of monoecy and dioecy in Sagittaria latifolia (Alismataceae). Evolution 56: 31–41.
Doyle, J.J., and J.L.I. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 11: 11–15.
Ehlers, A., B. Worm, and T.B.H. Reusch. 2008. Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Marine Ecology. Progress Series 355: 1–7.
Frankel, O.H. 1974. Genetic conservation: Our responsibility. Genetics 78: 53–56.
Frankel, O.H., and M.E. Soulé. 1981. Conservation and evolution. Cambridge: Cambridge University Press.
Frankham, R. 1995. Conservation genetics. Annual Review of Genetics 29: 305–327.
Frankham, R. 2005. Genetics and extinction. Biological Conservation 126: 131–140.
Frederiksen, M.S., M. Holmer, M. Perez, R.J.M. Invers, and B.B. Knudsen. 2008. Effect of increased sediment sulfide concentrations on the composition of stable sulfur isotopes (delta S-34) and sulfur accumulation in the seagrasses Zostera marina and Posidonia oceanica. Journal of Experimental Marine Biology and Ecology 358: 98–109.
Gacia, E., T.C. Granata, and C.M. Duarte. 1999. An approach to measurement of particle flux and sediment retention within seagrass (Posidonia oceanica) meadows. Aquatic Botany 65: 255–268.
Hämmerli, A., and T.B.H. Reusch. 2003. Inbreeding depression influences genet size distribution in a marine angiosperm. Molecular Ecology 12: 619–629.
Harada, Y., S. Kawano, and Y. Iwasa. 1997. Probability of clonal identity: Inferring the relative success of sexual versus clonal reproduction from spatial genetic patterns. Journal of Ecology 85: 591–600.
Hargrave, B.T., and N.M. Burns. 1979. Assessment of sediment trap collection efficiency. Limnology and Oceanography 24: 1124–1136.
Holmer, M., M. Argyrou, T. Dalsgaard, R. Danovaro, E. Diaz-Almela, C.M. Duarte, M. Frederiksen, A. Grau, I. Karakassis, and N. Marba. 2008. Effects of fish farm waste on Posidonia oceanica meadows: Synthesis and provision of monitoring and management tools. Marine Pollution Bulletin 56: 1618–1629.
Hughes, A.R., and J.J. Stachowicz. 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. PNAS 101: 8998–9002.
Hughes, A.R., B.D. Inouye, M.T. Johnson, N. Underwood, and M. Vellend. 2008. Ecological consequences of genetic diversity. Ecology Letters 11: 609–623.
Huston, M. 1979. General hypothesis of species-diversity. American Naturalist 113: 81–101.
Johnson, K.H., K.A. Vogt, H.J. Clark, O.J. Schmitz, and D.J. Vogt. 1996. Biodiversity and the productivity and stability of ecosystems. Trends in Ecology & Evolution 11: 372–377.
Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
Koroleff, F. 1983. Determination of nutrients. In Methods of seawater analysis, ed. K. Grasshof MEaKK, 125–139. Weinheim: Verlag Chemie.
Lande, R. 1995. Mutation and conservation. Conservation Biology 9: 782–791.
Loreau, M., S. Naeem, P. Inchausti, J. Bengtsson, J.P. Grime, A. Hector, D.U. Hooper, M.A. Huston, D. Raffaelli, B. Schmid, D. Tilman, and D.A. Wardle. 2001. Ecology—Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294: 804–808.
Lynch, M., J. Conery, and R. Burger. 1995. Mutational meltdowns in sexual populations. Evolution 49: 1067–1080.
Marbà, N., C.M. Duarte, J. Cebrian, M.E. Gallegos, B. Olesen, and K. SandJensen. 1996. Growth and population dynamics of Posidonia oceanica on the Spanish Mediterranean coast: Elucidating seagrass decline. Marine Ecology. Progress Series 137: 203–213.
Marbà, N., C.M. Duarte, E. Diaz-Almela, J. Terrados, E. Alvarez, R. Martiinez, R. Santiago, E. Gacia, and A.M. Grau. 2005. Direct evidence of imbalanced seagrass (Posidonia oceanica) shoot population dynamics in the Spanish Mediterranean. Estuaries 28: 53–62.
Mascaro, O., T. Valdemarsen, M. Holmer, M. Perez, and J. Romero. 2009. Experimental manipulation of sediment organic content and water column aeration reduces Zostera marina (eelgrass) growth and survival. Journal of Experimental Marine Biology and Ecology 373: 26–34.
McCann, K.S. 2000. The diversity–stability debate. Nature 405: 228–233.
Naeem, S., and S.B. Li. 1997. Biodiversity enhances ecosystem reliability. Nature 390: 507–509.
Newman, D., and D. Pilson. 1997. Increased probability of extinction due to decreased genetic effective population size: Experimental populations of Clarkia pulchella. Evolution 51: 354–362.
Orth, R.J., T.J.B. Carruthers, W.C. Dennison, C.M. Duarte, J.W. Fourqurean, K.L. Heck, A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, S. Olyarnik, F.T. Short, M. Waycott, and S.L. Williams. 2006. A global crisis for seagrass ecosystems. Bioscience 56: 987–996.
Parks, J.C., and C.R. Werth. 1993. A study of spatial features of clones in a population of Bracken Fern, Pteridium aquilinum (Dennstaedtiaceae). American Journal of Botany 80: 537–544.
Pfisterer, A.B., and B. Schmid. 2002. Diversity-dependent production can decrease the stability of ecosystem functioning. Nature 416: 84–86.
Procaccini, G., and L. Piazzi. 2001. Genetic polymorphism and transplantation success in the Mediterranean seagrass Posidonia oceanica. Restoration Ecology 9: 332–338.
Reusch, T.B.H. 2006. Does disturbance enhance genotypic diversity in clonal organisms? A field test in the marine angiosperm Zostera marina. Molecular Ecology 15: 277–286.
Reusch, T.B.H., C. Bostrom, W.T. Stam, and J.L. Olsen. 1999. An ancient eelgrass clone in the Baltic. Marine Ecology. Progress Series 183: 301–304.
Reusch, T.B.H., A. Ehlers, A. Hammerli, and B. Worm. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. PNAS 102: 2826–2831.
Saccheri, I., M. Kuussaari, M. Kankare, P. Vikman, W. Fortelius, and I. Hanski. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392: 491–494.
Spielman, D., B.W. Brook, and R. Frankham. 2004. Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America 101: 15261–15264.
Storey, J.D. 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society, Series B 64: 479–498.
Storey, J.D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America 100: 9440–9445.
Storey, J.D., J.E. Taylor, and D. Siegmund. 2004. Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: A unified approach. Journal of the Royal Statistical Society Series B-Statistical Methodology 66: 187–205.
Tibayrenc, M., F. Kjellberg, and F. Ayala. 1990. A clonal theory of parasitic protozoa: The population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. PNAS 87: 2414–2418.
Worm, B., E.B. Barbier, N. Beaumont, J.E. Duffy, C. Folke, B.S. Halpern, J.B.C. Jackson, H.K. Lotze, F. Micheli, S.R. Palumbi, E. Sala, K.A. Selkoe, J.J. Stachowicz, and R. Watson. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787–790.
Young, A.G., J.H. Hill, B.G. Murray, and R. Peakall. 2002. Breeding system, genetic diversity and clonal structure in the sub-alpine forb Rutidosis leiolepis F. Muell. (Asteraceae). Biological Conservation 106: 71–78.
Acknowledgments
This research was funded by projects M&MS (EVK3-CT-2000-00044) and MedVeg (Q5RS-2001-02456 of FP5), a project funded by the BBVA Foundation, the Portuguese Fundação para a Ciência e a Tecnologia (FCT) and FEDER through project DIVSTAB-(POCI 2010) and a FCT and FSE postdoctoral fellowship (S.A.-H.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Arnaud-Haond, S., Marbà, N., Diaz-Almela, E. et al. Comparative Analysis of Stability—Genetic Diversity in Seagrass (Posidonia oceanica) Meadows Yields Unexpected Results. Estuaries and Coasts 33, 878–889 (2010). https://doi.org/10.1007/s12237-009-9238-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-009-9238-9