Scientia Marina, Vol 78, No 1 (2014)

Mitochondrial DNA markers of loggerhead marine turtles (Caretta caretta) (Testudines: Cheloniidae) nesting at Kyparissia Bay, Greece, confirm the western Greece unit and regional structuring


https://doi.org/10.3989/scimar.03865.27B

Carlos Carreras
Marine Turtle Research Group, College of Life and Environmental Sciences, University of Exeter , United Kingdom

ALan F. Rees
Marine Turtle Research Group, College of Life and Environmental Sciences, University of Exeter , United Kingdom

Annette C. Broderick
Marine Turtle Research Group, College of Life and Environmental Sciences, University of Exeter , United Kingdom

Brendan J. Godley
Marine Turtle Research Group, College of Life and Environmental Sciences, University of Exeter , United Kingdom

Dimitris Margaritoulis
ARCHELON, the Sea Turtle Protection Society of Greece , Greece

Abstract


Genetic markers have been widely used in marine turtles to assess population structuring and origin of individuals in common feeding grounds, which are key elements for understanding their ecology and for developing conservation strategies. However, these analyses are very sensitive to missing information, especially from abundant nesting sites. Kyparissia Bay (western Greece) hosts the second largest Mediterranean nesting aggregation of the loggerhead turtle (Caretta caretta), but the genetic profile of this nesting site has not, as yet, been described using the extended version of the historically used mitochondrial DNA (mtDNA) marker. This marker was genotyped for 36 individuals nesting at Kyparissia Bay and haplotype frequencies obtained were compared with published data from other Mediterranean nesting sites. The results confirmed the connection between Kyparissia and other western Greek nesting sites and the isolation of this western Greek group from other Mediterranean nesting areas. As a consequence of this isolation, this abundant group of nesting aggregations (almost 30% of the Mediterranean stock) is not likely to significantly contribute to the recovery of other declining Mediterranean units.

Keywords


population structure; endangered species; conservation; Caretta; Mediterranean; mitochondrial DNA

Full Text:


HTML PDF XML

References


Abreu-Grobois A., Horrocks J., Formia A., Leroux R., Velez-Zuazo X., Dutton P.H., Soares L., Meylan A., Browne D. 2006. New mtDNA d-loop primers which work for a variety of marine turtle species may increase the resolution capacity of mixed stock analysis. Proceedings of the 26th Annual Symposium on Sea Turtle Biology and Conservation, p. 179.

Álvarez de Quevedo I., Cardona L., De Haro A., Pubill E., Aguilar A. 2010. Sources of bycatch of loggerhead sea turtles in the western Mediterranean other than drifting longlines. ICES J. Mar. Sci. 67: 677-685. http://dx.doi.org/10.1093/icesjms/fsp278

Baez J.C., Real R., Macias D., de la Serna J.M., Bellido J.J., Cami-as J.A. 2010. Captures of swordfish Xiphias gladius (Linnaeus 1758) and loggerhead sea turtles Caretta caretta (Linnaeus 1758) associated with different bait combinations in the Western Mediterranean surface longline fishery. J. Appl. Ichthyol. 26: 126-127. http://dx.doi.org/10.1111/j.1439-0426.2009.01342.x

Bentivegna F., Treglia G., Hochscheid S. 2008. The first report of a loggerhead turtle Caretta caretta nest on the central Tyrrhenian coast (western Mediterranean). Mar. Biodiv. Rec. 1: 1-3.

Bolker B.M., Okuyama T., Bjorndal K.A., Bolten A.B. 2007. Incorporating multiple mixed stocks in mixed stock analysis: 'many-to-many' analyses. Mol. Ecol. 16: 685-695. http://dx.doi.org/10.1111/j.1365-294X.2006.03161.x PMid:17284204

Bolten A.B., Bjorndal K.A., Martins H.R., Dellinger T., Biscoito M.J., Encalada S.E., Bowen B.W. 1998. Transatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis. Ecol. Appl. 8: 1-7. http://dx.doi.org/10.1890/1051-0761(1998)008[0001:TDMOLS]2.0.CO;2

Bowen B.W. 2003. What is a Loggerhead Turtle? The genetic perspective. In: Bolten A., Witherington B. (eds), Loggerhead Sea Turtles. Smithsonian Institution Press, Washington D.C. pp. 7-27.

Bowen B.W., Karl S.A. 2007. Population genetics and phylogeography of sea turtles. Mol. Ecol. 16: 4886-4907. http://dx.doi.org/10.1111/j.1365-294X.2007.03542.x PMid:17944856

Bowen B.W., Avise J.C., Richardson J.I., Meylan A., Margaritoulis D., Hopkins-Murphy S.R. 1993. Population structure of loggerhead turtles (Caretta caretta) in the Northwestern Atlantic Ocean and Mediterranean Sea. Conserv. Biol. 7: 834-844. http://dx.doi.org/10.1046/j.1523-1739.1993.740834.x

Bowen B.W., Abreu-Grobois A., Balazs G.H., Kamezaki N., Limpus C.J., Ferl R.J. 1995. Trans-Pacific migrations of the loggerhead turtle (Caretta caretta) demonstrated with mitochondrial DNA markers. Proc. Natl. Acad. Sci. USA 92: 3731-3734 http://dx.doi.org/10.1073/pnas.92.9.3731 PMid:7731974 PMCid:PMC42035

Bowen B.W., Bass A.L., Soares L., Toonen R.J. 2005. Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol. Ecol. 14: 2389-2402. http://dx.doi.org/10.1111/j.1365-294X.2005.02598.x PMid:15969722

Broderick A.C., Glen F., Godley B.J., Hays G.C. 2002. Estimating the number of green and loggerhead turtles nesting annually in the Mediterranean. Oryx 36: 227-235. http://dx.doi.org/10.1017/S0030605302000431

Cabin R.J., Mitchell R.J. 2000. To Bonferroni or not to bonferroni: when and how are the questions. Bull. Ecol. Soc. Am. 81: 246-248.

Cami-as J.A., Baez J.C., Valeiras X., Real R. 2006. Differential loggerhead by-catch and direct mortality due to surface longlines according to boat strata and gear type. Sci. Mar. 70: 661-665.

Carreras C., Cardona L., Aguilar A. 2004. Incidental catch of the loggerhead turtle Caretta caretta off the Balearic Islands (western Mediterranean). Biol. Conserv. 117: 321-329. http://dx.doi.org/10.1016/j.biocon.2003.12.010

Carreras C., Pont S., Maffucci F., Pascual M., Barcelo A., Bentivegna F., Cardona L., Alegre F., SanFelix M., Fernandez G., Aguilar A. 2006. Genetic structuring of immature loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea reflects water circulation patterns. Mar. Biol. 149: 1269-1279. http://dx.doi.org/10.1007/s00227-006-0282-8

Carreras C., Pascual M., Cardona L., Aguilar A., Margaritoulis D., Rees A.F., Turkozan O., Levy Y., Gasith A., Aureggi M., Khalil M. 2007. The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications. Conserv. Genet. 8: 761-775. http://dx.doi.org/10.1007/s10592-006-9224-8

Carreras C., Pascual M., Cardona L., Marco A., Bellido J.J., Castillo J.J., Tomás J., Raga J.A., Sanfelix M., Fernandez G., Aguilar A. 2011. Living Together but Remaining Apart: Atlantic and Mediterranean Loggerhead Sea Turtles (Caretta caretta) in Shared Feeding Grounds. J. Hered. 102: 666-677. http://dx.doi.org/10.1093/jhered/esr089 PMid:21934114

Casale P., Margaritoulis D. 2010. Sea turtles in the Mediterranean: distribution, threats and conservation priorities. IUCN/SSC Marine Turtle Specialist Group, Gland, Switzerland.

Casale P., Mazaris A.D., Freggi D., Basso R., Argano R. 2007. Survival probabilities of loggerhead sea turtles (Caretta caretta) estimated from capture-mark-recapture data in the Mediterranean Sea. Sci. Mar. 71: 365-372.

Casale P., Freggi D., Gratton P., Argano R., Oliverio M. 2008a. Mitochondrial DNA reveals regional and interregional importance of the central Mediterranean African shelf for loggerhead sea turtles (Caretta caretta). Sci. Mar. 72: 541-548. http://dx.doi.org/10.3989/scimar.2008.72n3541

Casale P., Freggi D., Rocco M. 2008b. Mortality induced by drifting longline hooks and branchlines in loggerhead sea turtles, estimated through observation in captivity. Aquatic Conservation-Marine and Freshwater Ecosystems 18: 945-954. http://dx.doi.org/10.1002/aqc.894

Casale P., Palilla G., Salemi A., Napoli A., Prinzi M., Genco L., Bonaviri D., Mastrogiacomo A., Oliverio M., Lo Valvo M. 2012. Exceptional sea turtle nest records in 2011 suggest an underestimated nesting potential in Sicily (Italy). Acta Herpetol. 7: 181-188.

Chaieb O., Ouaer A.E., Maffucci F., Bradai M.N., Bentivegna F., Said K., Chatti N. 2010. Genetic survey of loggerhead sea turtle Caretta caretta nesting population in Tunisia. Marine Biodiversity Records 3: 1-6. http://dx.doi.org/10.1017/S175526721000014X

Chaieb O., Elouaer A., Maffucci F., Karaa S., Bradai M.N., ElHili H., Bentivegna F., Said K., Chatti N. 2012. Population structure and dispersal patterns of loggerhead sea turtles Caretta caretta in Tunisian coastal waters, central Mediterranean. Endang. Species Res. 18: 35-45. http://dx.doi.org/10.3354/esr00428

Clusa M., Carreras C., Pascual M., Demetropoulos A., Margaritoulis D., Rees A.F., Hamza A.A., Khalil M., Aureggi M., Levy Y., Turkozan O., Marco A., Aguilar A., Cardona L. 2013. Mitochondrial DNA reveals Pleistocenic colonisation of the Mediterranean by loggerhead turtles (Caretta caretta). J. Exp. Mar. Biol. Ecol. 439: 15-24. http://dx.doi.org/10.1016/j.jembe.2012.10.011

Delaugerre M., Cesarini C. 2004. Confirmed nesting of the loggerhead turtle in Corsica. Marine Turtle Newsletter 104: 12.

Drummond A.J., Ashton B., Buxton S., Cheung M., Cooper A., Heled J., Moir R., Stones-Havas S., Sturrock S., Thierer T., Wilson A. 2011. Geneious v5.5 created by Biomatters. Available from http://www.geneious.com

Encalada S.E., Bjorndal K.A., Bolten A.B., Zurita J.C., Schroeder B., Possardt E., Sears C.J., Bowen B.W. 1998. Population structure of loggerhead turtle (Caretta caretta) nesting colonies in the Atlantic and Mediterranean as inferred from mitochondrial DNA control region sequences. Mar. Biol. 130: 567-575. http://dx.doi.org/10.1007/s002270050278

Excoffier L., Laval G., Schneider S. 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinform. 1: 47-50.

Fu Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925. PMid:9335623 PMCid:PMC1208208

Garofalo L., Mingozzi T., Mico A., Novelletto A. 2009. Loggerhead turtle (Caretta caretta) matrilines in the Mediterranean: further evidence of genetic diversity and connectivity. Mar. Biol. 156: 2085-2095. http://dx.doi.org/10.1007/s00227-009-1239-5

Giovannotti M., Franzellitti S., Cerioni P.N., Fabbri E., Guccione S., Vallini C., Tinti F., Caputo V. 2010. Genetic characterization of loggerhead turtle (Caretta caretta) individuals stranded and caught as bycatch from the North-Central Adriatic Sea. Amphibia-Reptilia 31: 127-133. http://dx.doi.org/10.1163/156853810790457902

Goudet J., Raymond M., de Meeu.s T. 1996. Testing differentiation in diploid populations. Genetics 144: 1931-1938.

Grant W.S., Milner G.B., Krasnowski P., Utter F.M. 1980. Use of biochemical genetic variants for identification of Sockeye salmon (Oncorhynchus nerca) stocks in Cook Inlet, Alaska. Can. J. Fish. Aquat. Sci. 37: 1236-1247. http://dx.doi.org/10.1139/f80-159

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.

Hamann M., Godfrey M.H., Seminoff J.A., Arthur K., Barata P.C.R., Bjorndal K.A., Bolten A., Broderick A.C., Campbell L.M., Carreras C., Dutton P.H., Epperly S., Fitzsimmons N.N., Formia A., Girondot M., Hays G.C., Jiunn C.I., Kaska Y., Lewison R., Mortimer J.A., Nichols W.J., Reina R.D., Shanker K., Spotila J.R., Tomás J., Wallace B.P., Work T.M., Zbinden J.A., Godley B.J. 2010. Global research priorities for sea turtles: informing management and conservation in the 21st century. Endang. Species Res. 11: 245-269. http://dx.doi.org/10.3354/esr00279

Larsson L.C., Charlier J., Laikre L., Ryman N. 2009. Statistical power for detecting genetic divergence-organelle versus nuclear markers. Conserv. Genet. 10: 1255-1264. http://dx.doi.org/10.1007/s10592-008-9693-z

Laurent L., Lescure J., Excoffier L., Bowen B.W., Domingo M., Hadjichristophorou M., Kornaraky L., Trabucht G. 1993. Genetic studies of relationships between Mediterranean and Atlantic populations of loggerhead turtle Caretta caretta with a mitochondrial marker. Comptes Rendus de l'Académie des Sciences de la Vie. Sciences de la Vie, Paris 316: 1233-1239.

Laurent L., Casale P., Bradai M.N., Godley B.J., Gerosa G., Broderick A.C., Schroth W., Schierwater B., Levy A.M., Freggi D., Abd El-Mawla E.M., Hadoud D.A., Gomati H.E., Domingo M., Hadjichristophorou M., Kornaraky L., Demirayak F., Gautier C. 1998. Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol. Ecol. 7: 1529-1542. http://dx.doi.org/10.1046/j.1365-294x.1998.00471.x PMid:9819906

Lee P.L.M. 2008. Molecular ecology of marine turtles: New approaches and future directions. J. Exp. Mar. Biol. Ecol. 356: 25-42. http://dx.doi.org/10.1016/j.jembe.2007.12.021

Maffucci F., Kooistra W., Bentiveyna F. 2006. Natal origin of loggerhead turtles, Caretta caretta, in the neritic habitat off the Italian coasts, Central Mediterranean. Biol. Conserv. 127: 183-189. http://dx.doi.org/10.1016/j.biocon.2005.08.009

Margaritoulis D. 1998. Interchange of nesting loggerheads among Greek beaches. In: Epperly S., Braun-McNeill J. (eds), Proceedings of the seventeenth annual sea turtle symposium. NOAA Technical Memorandum, National Marine Fisheries Service, Southeast Fisheries Science Center, Orlando, Florida, pp. 225-227.

Margaritoulis D., Argano R., Baran I., Bentivegna F., Bradai M.N., Cami-as J.A., Casale P., De Metrio G., Demetropoulos A., Gerosa G., Godley B.J., Hadoud D.A., Houghton J., Laurent L., Lazar B. 2003. Loggerhead Turtles in the Mediterranean Sea: Present Knowledge and Conservation Perspectives. In: Bolten A, Witherington BE (eds), Loggerhead Sea Turtles. Smithsonian Books, Washington D.C. pp. 175-198.

Meylan A.B., Bowen B.W., Avise J.C. 1990. A genetic test of the natal homing versus social facilitation models for green turtle migration. Science 248: 724-727. http://dx.doi.org/10.1126/science.2333522 PMid:2333522

Miller M. 1997. Tools for population genetic analyses (TFPGA) 1.3; a Windows program for the analysis of allozyme and molecular population genetic data. Documentation file. Available at: http://www.marksgeneticsoftware.net/tfpga.htm

Monzon-Arguello C., Rico C., Carreras C., Calabuig P., Marco A., Lopez-Jurado L.F. 2009. Variation in spatial distribution of juvenile loggerhead turtles in the eastern Atlantic and western Mediterranean Sea. J. Exp. Mar. Biol. Ecol. 373: 79-86. http://dx.doi.org/10.1016/j.jembe.2009.03.007

Monzon-Arguello C., Rico C., Naro-Maciel E., Varo-Cruz N., Lopez P., Marco A., Lopez-Jurado L.F. 2010. Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands. Conserv. Genet. 11: 1871-1884. http://dx.doi.org/10.1007/s10592-010-0079-7

Moran M.D. 2003. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100: 403-405. http://dx.doi.org/10.1034/j.1600-0706.2003.12010.x

Moritz C. 1994. Defining Evolutionarily Significant Units for Conservation. Trends Ecol. Evol. 9: 373-375. http://dx.doi.org/10.1016/0169-5347(94)90057-4

Narum S.R. 2006. Beyond Bonferroni: Less conservative analyses for conservation genetics. Conserv. Genet. 7: 783-787. http://dx.doi.org/10.1007/s10592-005-9056-y

Nei M. 1982. Evolution of Human Races at the Gene Level. In: Bonne-Tamir B., Cohen T., Goodman R.M. (eds), Human Genetics Part A: The Unfolding Genome. Alan R. Liss, New York, pp. 167-181. PMid:7163193

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. http://dx.doi.org/10.1111/j.1471-8286.2005.01155.x

Pella J., Masuda M. 2001. Bayesian methods for analysis of stock mixtures from genetic characters. Fish. Bull. 99: 151-167.

Pella J.J., Milner G.B. 1987. Use of genetic marks in stock composition analysis. In Ryman N., Utter F. (eds), Population Genetics and Fishery Management. Univ. Washington Press, Seattle and London, pp. 247-276.

Perneger T.V. 1998. What's wrong with Bonferroni adjustments. British Med. J. 316: 1236-1238. http://dx.doi.org/10.1136/bmj.316.7139.1236 PMid:9553006 PMCid:PMC1112991

Pritchard P.C.H. 1997. Evolution, phylogeny, and current status. In: Lutz P.L., Musick J.A. (eds), The biology of sea turtles. CRC Press, Boca Raton, FL, pp. 1-28. PMid:9025175

Revelles M., Carreras C., Cardona L., Marco A., Bentivegna F., Castillo J.J., De Martino G., Mons J.L., Smith M.B., Rico C., Pascual M., Aguilar A. 2007. Evidence for an asymmetrical size exchange of loggerhead sea turtles between the Mediterranean and the Atlantic through the Straits of Gibraltar. J. Exp. Mar. Biol. Ecol. 349: 261-271. http://dx.doi.org/10.1016/j.jembe.2007.05.018

Rolf D.A., Bentzen P. 1989. The statistical analysis of mitochondrial DNA polymorphisms: X2 and the problem of small samples. Mol. Biol. Evol. 6: 539-545.

Ryman N., Palm S. 2006. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol. Notes 6: 600-602. http://dx.doi.org/10.1111/j.1471-8286.2006.01378.x

Ryman N., Palm S., Andre C., Carvalho G.R., Dahlgren T.G., Jorde P.E., Laikre L., Larsson L.C., Palme A., Ruzzante D.E. 2006. Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol. Ecol. 15: 2031-2045. http://dx.doi.org/10.1111/j.1365-294X.2006.02839.x PMid:16780422

Saied A., Maffucci F., Hochscheid S., Dryag S., Swayeb B., Borra M., Ouerghi A., Procaccini G., Bentivegna F. 2012. Loggerhead turtles nesting in Libya: an important management unit for the Mediterranean stock. Mar. Ecol. Prog. Ser. 450: 207-224. http://dx.doi.org/10.3354/meps09548

Schroth W., Streit B., Schierwater B. 1996. Evolutionary handicap for turtles. Nature 384: 521-522. http://dx.doi.org/10.1038/384521a0

SEATURTLE.ORG Maptool 2002. http://www.seaturtle.org/maptool/. SEATURTLE.ORG, Inc.

Shamblin B.M., Bolten A.B., Bjorndal K.A., Dutton P.H., Nielsen J.T., Abreu-Grobois F.A., Reich K.J., Witherington B.E., Bagley D.A., Ehrhart L.M., Tucker A.D., Addison D.S., Arenas A., Johnson C., Carthy R.R., Lamont M.M., Dodd M.G., Gaines M.S., LaCasella E., Nairn C.J. 2012. Expanded mitochondrial control region sequences increase resolution of stock structure among North Atlantic loggerhead turtle rookeries. Mar. Ecol. Prog. Ser. 469: 145-160. http://dx.doi.org/10.3354/meps09980

Tomás J., Gazo M., Alvarez C., Gozalbes P., Perdiguero D., Raga J.A., Alegre F. 2008. Is the Spanish coast within the regular nesting range of the Mediterranean loggerhead sea turtle (Caretta caretta)? J. Mar. Biol. Ass. U. K. 88: 1509-1512. http://dx.doi.org/10.1017/S0025315408001768

Wallace B.P., DiMatteo A.D., Hurley B.J., Finkbeiner E.M., Bolten A.B., Chaloupka M.Y., Hutchinson B.J., Alberto Abreu-Grobois F., Amorocho D., Bjorndal K.A., Bourjea J., Bowen B.W., Briseno Duenas R., Casale P., Choudhury B.C., Costa A., Dutton P.H., Fallabrino A., Girard A., Girondot M., Godfrey M.H., Hamann M., Lopez-Mendilaharsu M., Marcovaldi M.A., Mortimer J.A., Musick J.A., Nel R., Pilcher N.J., Seminoff J.A., Troeng S., Witherington B., Mast R.B. 2010. Regional Management Units for Marine Turtles: A Novel Framework for Prioritizing Conservation and Research across Multiple Scales. PLoS One 5(12): e15465. http://dx.doi.org/10.1371/journal.pone.0015465 PMid:21253007 PMCid:PMC3003737

Wallace B.P., DiMatteo A.D., Bolten A.B., Chaloupka M.Y., Hutchinson B.J., Abreu-Grobois F.A., Mortimer J.A., Seminoff J.A., Amorocho D., Bjorndal K.A., Bourjea J., Bowen B.W., Duenas R.B., Casale P., Choudhury B.C., Costa A., Dutton P.H., Fallabrino A., Finkbeiner E.M., Girard A., Girondot M., Hamann M., Hurley B.J., Lopez-Mendilaharsu M., Marcovaldi M.A., Musick J.A., Nel R., Pilcher N.J., Troeng S., Witherington B., Mast R.B. 2011. Global Conservation Priorities for Marine Turtles. PLoS One 6(9): e24510. http://dx.doi.org/10.1371/journal.pone.0024510 PMid:21969858 PMCid:PMC3182175

Yilmaz C., Turkozan O., Bardakci F. 2011. Genetic structure of loggerhead turtle (Caretta caretta) populations in Turkey. Biochem. Syst. Ecol. 39: 266-276. http://dx.doi.org/10.1016/j.bse.2011.08.018

Yilmaz C., Turkozan O., Bardakci F., White M., Kararaj E. 2012. Loggerhead turtles (Caretta caretta) foraging at Drini Bay in Northern Albania: Genetic characterisation reveals new haplotypes. Acta Herpetol. 7: 155-162.




Copyright (c) 2014 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es