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Management and conservation of the kelp speciesLaminaria digitata : using genetic tools to explore the potentialexporting role of the MPA “Parc naturel marin d’Iroise”

Published online by Cambridge University Press:  24 October 2012

Lucía Couceiro ,
Marine Robuchon ,
Christophe Destombe  and
Myriam Valero
Lucía Couceiro
Affiliation:
UPMC, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France CNRS, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France
Marine Robuchon
Affiliation:
UPMC, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France CNRS, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France MNHN, UMR 7138, Systématique, adaptation, évolution, 57 rue Cuvier, 75231 Paris Cedex 05, France
Christophe Destombe
Affiliation:
UPMC, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France CNRS, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France
Myriam Valero*
Affiliation:
UPMC, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France CNRS, UMR 7144, Adaptation et diversité en milieu marin, Équipe BEDIM, Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France
*
a Corresponding author:[email protected]
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Abstract

Marine protected areas (MPAs) have been depicted as a useful tool for improving fisherymanagement and protecting biodiversity. For example, by acting as source populations, MPAsmay provide a spillover of adults/propagules, enhancing recruitment to surrounding,non-protected waters. However, such positive effect will depend on how a MPAs designmatches population biology and dispersal abilities of the target species. High levels ofintraspecific genetic diversity without pronounced structure have been found in manymarine organisms over large spatial scales (from hundreds to thousands kilometres) but donot hold for other ecologically and economically important species such as coral reeffishes, seagrasses and kelps. In particular, the limited potential for dispersal of manymacroalgae suggests the occurrence of self-sustaining, “closed” populations that contrastwith the “open” populations of many fishes and invertebrates. Consequently, the highresilience of fish/invertebrate populations cannot be generalized to the whole marinerealm. In the present work, we use genetic tools to explore the role of the MPAParc naturel marin d’Iroise in the management of the emblematic kelpLaminaria digitata. While kelps have received much more scientificattention than any other seaweed group, there is still critical baseline knowledge whichneeds to be addressed for their effective management. Our genetic survey of 12 L.digitata populations along the Brittany coast, four of them located within theboundaries of the Parc naturel marin d’Iroise, allowed us to assess theconservation value of these kelp populations. In particular, classical genetic metrics aswell as more recent clustering approaches were used to identify and characterizeManagement Units. Moreover, assignment tests were employed to determine contemporarymigration events and source/sink populations. Our results show that populations withinthis MPA have high conservation value. However, we also identify other populations ofconservation interest.

Keywords

Population genetic connectivityMicrosatellite markersGene flowGametophyte bankSeaweedLaminaria digitataMarine protected areaUshant frontAtlantic OceanDispersalKelpMarginal populationsManagement unitsGenetic diversitySourcesink
Type
Research Article
Information
Aquatic Living Resources , Volume 26 , Issue 2 , April 2013 , pp. 197 - 205
Copyright
© EDP Sciences, IFREMER, IRD 2012

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References

Références

Agardy, M.T., 1994, Advances in marine conservation : the role of marine protected areas. Trends Ecol. Evol. 9, 267–270. CrossRefGoogle Scholar
Airoldi, L., Beck, M.W., 2007, Loss, status and trends for coastal marine habitats of Europe. Oceanogr. Mar. Biol. Annu. Rev. 45, 345–405. Google Scholar
Alban, F., Frangoudes, K., Fresard, M., 2011, Kelp harvesting fleet dynamics and the fleet’s dependence on Laminaria forests in the Iroise Sea (North Finistere, France). Cah. Biol. Mar. 52, 507–516. Google Scholar
Alberto, F., Raimondi, P.T., Reed, D.C., Coelho, N.C., Leblois, R., Whitmer, A., Serrao, E.A., 2010, Habitat continuity and geographic distance predict population genetic differentiation in giant kelp. Ecology 91, 49–56. CrossRefGoogle ScholarPubMed
Almany, G.R., Berumen, M.L., Thorrold, S.R., Planes, S., Jones, G.P, 2007, Local replenishment of coral reef fish populations in a marine reserve. Science 316, 742–744. CrossRefGoogle Scholar
Arzel P., 1998, Les laminaires sur les côtes bretonnes. Evolution de l’exploitation et de la flottille de pêche, état actuel et perspectives. Ifremer edn.
Ayata, S.D., Lazure, P., Thiébaut, E., 2010, How does the connectivity between populations mediate range limits of marine invertebrates? A case study of larval dispersal between the Bay of Biscay and the English Channel (North-East Atlantic). Prog. Oceanogr. 87, 18–36. CrossRefGoogle Scholar
Bartsch, I., Wiencke, C., Bischof, K., Buchholz, C.M., Buck, B.H., Eggert, A., Feuerpfeil, P., Hanelt, D., Jacobsen, S., Karez, R., 2008, The genus Laminaria sensu lato : recent insights and developments. Eur. J. Phycol. 43, 1–86. CrossRefGoogle Scholar
Billot, C., Engel, C.R., Rousvoal, S., Kloareg, B., Valero, M., 2003, Current patterns, habitat discontinuities and population genetic structure : the case of the kelp Laminaria digitata in the English Channel. Mar. Ecol. Prog. Ser. 253, 111–121. CrossRefGoogle Scholar
Billot, C., Rousvoal, S., Estoup, A., Epplen, J.T., Saumitou Laprade, P., Valero, M., Kloareg, B., 1998, Isolation and characterization of microsatellite markers in the nuclear genome of the brown alga Laminaria digitata (Phaeophyceae). Mol. Ecol. 7, 1778–1780. CrossRefGoogle Scholar
Bolton, J.J., 2010, The biogeography of kelps (Laminariales, Phaeophyceae) : a global analysis with new insights from recent advances in molecular phylogenetics. Helgol. Mar. Res. 64, 263–279. CrossRefGoogle Scholar
Bridle, J.R., Vines, T.H, 2006, Limits to evolution at range margins : when and why does adaptation fail? Trends Ecol. Evol. 22, 140–147. CrossRefGoogle ScholarPubMed
Carney, L.T., Edwards, M.S., 2006, Cryptic processes in the sea : a review of delayed development in the microscopic life stages of marine macroalgae. Algae 21, 161–168. CrossRefGoogle Scholar
Carr, M.H., Neigel, J.E., Estes, J.A., Andelman, S., Warner, R.R., Largier, J.L., 2003, Comparing marine and terrestrial ecosystems : implications for the design of coastal marine reserves. Ecol. Appl. 13, S90–S107. CrossRefGoogle Scholar
Chapman A.R.O., 1986, Population and community ecology of seaweeds. In : Blaxter J.H.S., Southwood A.J. (Eds.) Advances in marine biology, London, Academic Press, pp. 1–16.
Charrier, G., Durand, J.D., Quiniou, L., Laroche, J., 2006, An investigation of the population genetic structure of pollack (Pollachius pollachius) based on microsatellite markers. ICES J. Mar. Sci. 63, 1705–1709. CrossRefGoogle Scholar
Clinchy, M., 1997, Does immigration “rescue” populations from extinction? Implications regarding movement corridors and the conservation of mammals. Oikos 80, 618–622. CrossRefGoogle Scholar
Coleman, M.A., Chambers, J., Knott, N.A., Malcolm, H.A., Harasti, D., Jordan, A., Kelaher, B.P., 2011, Connectivity within and among a network of temperate marine reserves. PLoS ONE 6, e20168. CrossRefGoogle ScholarPubMed
Corander, J., Marttinen, P., Sirén, J., Tang, J., 2008, Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinf. 9, e539. CrossRefGoogle ScholarPubMed
Cowen, R.K., Sponaugle, S., 2009, Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 1, 443–466. CrossRefGoogle ScholarPubMed
Crowder, L.B., Lyman, S.J., Figueira, W.F., Priddy, J., 2000, Source-sink population dynamics and the problem of siting marine reserves. Bull. Mar. Sci. 66, 799–820. Google Scholar
Dinter W., 2001, Biogeography of the OSPAR Maritime Area :a synopsis and synthesis of biogeographical distribution patterns described for the North-East Atlantic. Bonn, German Federal Agency for Nature Conservation.
Dring, M.J., Makarov, V., Schoschina, E., Lorenz, M., Lüning, K., 1996, Influence of ultraviolet-radiation on chlorophyll fluorescence and growth in different life-history stages of three species of Laminaria (Phaeophyta). Mar. Biol. 126, 183–191. CrossRefGoogle Scholar
Eckert, C.G., Samis, K.E., Lougheed, S.C., 2008, Genetic variation across species’ geographical ranges : the central-marginal hypothesis and beyond. Mol. Ecol. 17, 1170–1188. CrossRefGoogle ScholarPubMed
Frankham R., Ballou J.D., Briscoe D.A., 2004, A primer of conservation genetics. New York, Cambridge University Press.
Fraser, C.I., Thiel, M., Spencer, H.G, Waters, J.M., 2010, Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. BMC Evol. Biol. 10, e203. CrossRefGoogle ScholarPubMed
Goudet, J., 1995, FSTAT (Version 1.2) : a computer program to calculate F-statistics. J. Hered. 86, 485–486. CrossRefGoogle Scholar
Hoffmann, A.J., Santelices, B., 1991, Banks of algal microscopic forms : hypothesis on their functioning and comparisons with seed banks. Mar. Ecol. Prog. Ser. 79, 185–194. CrossRefGoogle Scholar
Jakobsson, M., Rosenberg, N.A., 2007, CLUMPP : a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806. CrossRefGoogle ScholarPubMed
Jolly, M.T., Jollivet, D., Gentil, F., Thiébaut, E., Viard, F., 2005, Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France. Heredity 94, 23–32. CrossRefGoogle Scholar
Jones, G.P., Srinivasan, M., Almany, G.R., 2007, Population connectivity and conservation of marine biodiversity. Oceanography 20, 100–111. CrossRefGoogle Scholar
Jones, G.P., Almany, G.R., Russ, G.R., Sale, P.F., Steneck, R.S., von Oppen, M.J.H., Willis, B.L., 2009, Larval retention and connectivity among populations of corals and reef fishes : history, advances and challenges. Coral Reefs 28, 307–325. CrossRefGoogle Scholar
Kalinowski, S.T., 2005, HP-RARE 1.0 : a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 5, 187–189. CrossRefGoogle Scholar
Kelleher G., 1999, Guidelines for Marine Protected Areas. Gland and Cambridge, IUCN.
Kinlan, B.P., Gaines, S.D., 2003, Propagule dispersal in marine and terrestrial environments : a community perspective. Ecology 84, 2007–2020. CrossRefGoogle Scholar
Kinlan, B.P., Gaines, S.D., Lester, S.E., 2005, Propagule dispersal and the scales of marine community process. Divers. Distrib. 11, 139–148. CrossRefGoogle Scholar
Koutsikopoulos, C., Le Cann, B., 1996, Physical processes and hydrological structures related to the Bay of Biscay anchovy. Sci. Mar. 60, 9–19. Google Scholar
Ladah, L.B., Zertuche-González, J.A., Hernández-Carmona, G., 1999, Giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997-1998. J. Phycol. 35, 1106–1112. CrossRefGoogle Scholar
Le Fèvre, J., 1986, Aspects of the biology of frontal systems. Adv. Mar. Biol. 23, 163–299. CrossRefGoogle Scholar
Lüning, K., 1981, Egg release in gametophytes of Laminaria saccharina : induction by darkness and inhibition by blue light and UV. Br. Phycol. J. 16, 379–393. CrossRefGoogle Scholar
Manel, S., Gaggiotti, O.E., Waples, R.S., 2005, Assignment methods : matching biological questions with appropriate techniques. Trends Ecol. Evol. 20, 136–142. CrossRefGoogle ScholarPubMed
Morizt, C., 1994, Defining “Evolutionary Significant Units” for conservation. Trends Ecol. Evol. 9, 373–375. Google Scholar
Oppliger, L.V., Correa, J.A., Engelen, A.H., Tellier, F., Vieira, V., Faugeron, S., Valero, M., Gomez, G., Destombe, C., 2012, Temperature effects on gametophyte life-history traits and geographic distribution of two cryptic kelp species. PLoS ONE 7, e39289. CrossRefGoogle ScholarPubMed
Paetkau, D., Slade, R., Burden, M., Estoup, A., 2004, Genetic assignment methods for the direct, real-time estimation of migration rate : a simulation-based exploration of accuracy and power. Mol. Ecol. 13, 55–65. CrossRefGoogle ScholarPubMed
Palumbi, S.R., 2004, Marine reserves and ocean neighborhoods : the spatial scale of marine populations and their management. Annu. Rev. Environ. Resour. 29, 31–68. CrossRefGoogle Scholar
Peakall, R., Smouse, P.E., 2006, GENALEX 6 : genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295. Google Scholar
Pingree, R., Pugh, P., Holligan, P., Forster, G., 1975, Summer phytoplankton blooms and red tides along the tidal fronts in the approaches of the English Channel. Nature 258, 672–677. CrossRefGoogle Scholar
Piry, S., Alapetite, A., Cornuet, J.M., Paetkau, D., Baudouin, L., Estoup, A., 2004, GENECLASS2 : a software for genetic assignment and first-generation migrant detection. J. Hered. 95, 536–539. CrossRefGoogle ScholarPubMed
Pritchard, J.K., Stephens, M., Donnelly, P., 2000, Inference of population structure using multilocus genotype data. Genetics 155, 945–959. Google ScholarPubMed
Procaccini, G., Olsen, J. L., Reusch, T.B.H., 2007, Contribution of genetics and genomics to seagrass biology and conservation. J. Exp. Mar. Biol. Ecol. 350, 234–259. CrossRefGoogle Scholar
Pulliam, H.R., 1988, Sources, sinks, and population regulation. Am. Nat. 132, 652–661. CrossRefGoogle Scholar
Rannala, B., Mountain, J.L., 1997, Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. USA 94, 9197–9201. CrossRefGoogle ScholarPubMed
Raymond, M., Rousset, F., 1995, GENEPOP (Version 1.2) : population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249. CrossRefGoogle Scholar
Rice, W.R., 1989, Analyzing tables of statistical tests. Evolution 43, 223–225. CrossRefGoogle ScholarPubMed
Roberts, C.M., 1997, Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457. CrossRefGoogle ScholarPubMed
Rosenberg, N.A., 2004, DISTRUCT : a program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138. CrossRefGoogle Scholar
Roughgarden, J., Gaines, S., Possingham, H., 1988, Recruitment dynamics in complex life cycles. Science 241, 1460–1466. CrossRefGoogle ScholarPubMed
Salm R.V., Done T., McLeod E., 2006, Marine protected area planning in a changing climate. In : Phinney J.T., Hoegh-Guldberg O., Kleypas J., Skirving W., Strong A. (Eds.) Coral reefs and climate change : science and management, Washington, American Geophysical Union, pp. 207–221.
Santelices, B., 1990, Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr. Mar. Biol. Annu. Rev. 28, 177–276. Google Scholar
Selkoe, K.A., Henzler, C.M., Gaines, S.D., 2008, Seascape genetics and the spatial ecology of marine populations. Fish Fish. 9, 363–377. CrossRefGoogle Scholar
Teske, P.R., Forget, F.R.G., Cowley, P.D., Heyden, S., Beheregaray, L.B., 2010, Connectivity between marine reserves and exploited areas in the philopatric reef fish Chrysoblephus laticeps (Teleostei : Sparidae). Mar. Biol. 157, 2029–2042. CrossRefGoogle Scholar
Thiel, M., Gutow, L., 2005, The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr. Mar. Biol. Annu. Rev. 43, 279–418. Google Scholar
Valero, M., Destombe, C., Mauger, S., Ribout, C., Engel, C.R., Daguin-Thiebaut, C., Tellier, F., 2011, Using genetic tools for sustainable management of kelps : a literature review and the example of Laminaria digitata. Cah. Biol. Mar. 52, 467–483. Google Scholar
Waples, R.S., Punt, A.E., Cope, J.M., 2008, Integrating genetic data into management of marine resources : how can we do it better? Fish Fish. 9, 423–449. CrossRefGoogle Scholar
Weir, B.S., Cockerham, C.C., 1984, Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370. Google ScholarPubMed