Marine Biology

, 165:68 | Cite as

A comprehensive mitochondrial DNA mixed-stock analysis clarifies the composition of loggerhead turtle aggregates in the Adriatic Sea

  • Livia Tolve
  • Paolo Casale
  • Angela Formia
  • Luisa Garofalo
  • Bojan Lazar
  • Chiara Natali
  • Andrea Novelletto
  • Carola Vallini
  • Elena Bužan
  • Guido Chelazzi
  • Stefania Gaspari
  • Caterina Fortuna
  • Ivna Kocijan
  • Erica Marchiori
  • Nicola Novarini
  • Lisa Poppi
  • Pasquale Salvemini
  • Claudio Ciofi
Original paper

Abstract

Migration is one of several marine vertebrate traits increasingly affected by human encroachment. The Adriatic Sea is an important foraging and wintering site for loggerhead turtles (Caretta caretta), and one of the Mediterranean regions where they are most heavily impacted, particularly by fisheries bycatch. Conservation measures concern foraging and wintering areas and nesting grounds, and must, therefore, be informed by the natal origin of individuals in these mixed aggregates. Genetic diversity was investigated among 488 loggerheads found stranded or incidentally captured in fishing gear across the Adriatic and the origin of individuals was assessed through mixed-stock analysis based on comparison of 755 bp of mitochondrial DNA control region sequence. In addition, we highlight the importance of the Gulf of Manfredonia (Apulia, Italy), and of the northeastern Adriatic—a previously genetically undescribed foraging ground. No significant genetic divergence was recorded among sampling areas, between turtles sampled in cold and warm months or between adults and juveniles. The distribution of turtles across the Adriatic Sea appeared not to depend on individual origin. Rookeries in western Greece and Crete provided the most important contributions to the Adriatic mixed stock. In particular, the Greek populations were the most abundant locally in the Gulf of Manfredonia, so they are likely to experience an even greater impact than previously thought because of the severe fishery bycatch levels in this area. This study also provides an example of how substantial increases in sample sizes permit a relatively comprehensive testing of genetic structure across groupings in foraging aggregations.

Notes

Acknowledgements

This study was funded by the University of Florence, the Italian Department of Fishery and Aquaculture (BYCATCH Project—Ministry of Agriculture, Food and Forestry), the Italian National Institute for Environmental Protection and Research, the European Union NETCET project (IPA Inter-Adriatic), and the Slovenian Research Agency under Grant P1-0386. We thank Fondazione Cetacea ONLUS, the Veneto stranding network (Coordinamento Tartarughe marine del Litorale Veneto), WWF (Area Marina Protetta di Miramare, Trieste), and F. Zuppa and M. Tempesta from APS DelTa for support and for providing samples from the northwestern Adriatic. We are also grateful to V. Angelini, E. Filidei jr, L. Mizzan, G. Palmisano, P. Perlasca, S. Pari, and E. Zanetti for their help with sample collection and to P. Blasi and L. Testa for the assistance during lab work. All collaborating fishermen are particularly acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care of animals were followed. This work was conducted under all necessary permits. Live bycaught sea turtles were released after sample collection according to the IUCN/SSC Marine Turtle Specialist Group guidelines (Eckert et al. 1999). None of the procedures used in the study met the criteria which would define them as “experiments” according to article 2 of the Council of European Communities Directive 86/609/EEC on the protection of animals used for experimental and other scientific purposes. Approval by the institutional ethics committee (Commissione per l’Etica della Ricerca di Ateneo, University of Florence) was not required.

Supplementary material

227_2018_3325_MOESM1_ESM.pdf (790 kb)
Supplementary material 1 (PDF 790 kb)

References

  1. Abreu-Grobois FA, Horrocks J, Formia A, Dutton PH, LeRoux R, Vélez-Zuazo X, Soares L, Meylan P (2006) New mtDNA Dloop primers which work for a variety of marine turtle species may increase the resolution of mixed stock analyses. In: Frick M, Panagopoulou A, Rees AF, Williams K (eds) Book of Abstracts. Twenty Sixth Annual Symposium on Sea Turtle Biology and Conservation, 2006. International Sea Turtle Society, Athens, GreeceGoogle Scholar
  2. Agostini VN, Bakun A (2002) `Ocean triads’ in the Mediterranean Sea: physical mechanisms potentially structuring reproductive habitat suitability (with example application to European anchovy, Engraulis encrasicolus). Fish Oceanogr 11:129–142.  https://doi.org/10.1046/j.1365-2419.2002.00201.x CrossRefGoogle Scholar
  3. Artegiani A, Bregant D, Paschini E, Pinardi N, Raicich F, Russo A (1997) The Adriatic Sea general circulation. Part I: air-sea interactions and water mass structure. J Phys Oceanogr 27:1492–1514CrossRefGoogle Scholar
  4. Avens L, Braun-McNeill J, Epperly S, Lohmann KJ (2003) Site fidelity and homing behavior in juvenile loggerhead sea turtles (Caretta caretta). Mar Biol 143:211–220.  https://doi.org/10.1007/s00227-003-1085-9 CrossRefGoogle Scholar
  5. Bass AL, Epperly SP, Braun-McNeill J (2004) Multi-year analysis of stock composition of a loggerhead turtle (Caretta caretta) foraging habitat using maximum likelihood and Bayesian methods. Conserv Genet 5:783–796.  https://doi.org/10.1007/s10592-004-1979-1 CrossRefGoogle Scholar
  6. Bjorndal KA, Bolten AB (2008) Annual variation in source contributions to a mixed stock: implications for quantifying connectivity. Mol Ecol 17:2185–2193.  https://doi.org/10.1111/j.1365-294X.2008.03752.x CrossRefPubMedGoogle Scholar
  7. Bolker B, Okuyama T (2014) Mixed stock analysis in R: getting started with the mixstock package. https://r-forge.r-project.org/R/?group_id=189
  8. Bolker B, Okuyama T, Bjorndal K, Bolten A (2003) Sea turtle stock estimation using genetic markers: accounting for sampling error of rare genotypes. Ecol Appl 13:763–775.  https://doi.org/10.1890/1051-0761(2003)013[0763:Stseug]2.0.Co;2 CrossRefGoogle Scholar
  9. Bolten AB (1999) Techniques for measuring sea turtles. In: Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M (eds) Research and management techniques for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4, Consolidated Graphic Communications, Blanchard, PA, pp 110–114Google Scholar
  10. Bowen BW, Bass AL, Chow S, Bostrom M, Bjorndal KA, Bolten AB, Okuyama T, Bolker BM, Epperly S, Lacasella E (2004) Natal homing in juvenile loggerhead turtles (Caretta caretta). Mol Ecol 13:3797–3808.  https://doi.org/10.1111/j.1365-294X.2004.02356.x CrossRefPubMedGoogle Scholar
  11. Bowen BW, Bass AL, Soares L, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol Ecol 14:2389–2402.  https://doi.org/10.1111/j.1365-294X.2005.02598.x CrossRefPubMedGoogle Scholar
  12. Bowen BW, Grant WS, Hillis-Starr Z, Shaver DJ, Bjorndal KA, Bolten AB, Bass AL (2007) Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol Ecol 16:49–60.  https://doi.org/10.1111/j.1365-294X.2006.03096.x CrossRefPubMedGoogle Scholar
  13. Carreras C, Pascual M, Cardona L, Aguilar A, Margaritoulis D, Rees A, Turkozan O, Levy Y, Gasith A, Aureggi 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.  https://doi.org/10.1007/s10592-006-9224-8 CrossRefGoogle Scholar
  14. Carreras C, Pascual M, Cardona L, Marco A, Bellido JJ, Castillo JJ, Tomás J, Raga JA, Sanfélix M, Fernández 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.  https://doi.org/10.1093/Jhered/Esr089 CrossRefPubMedGoogle Scholar
  15. Carreras C, Rees AF, Broderick AC, Godley BJ, Margaritoulis D (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. Sci Mar 78:115–124.  https://doi.org/10.3989/scimar.03865.27b CrossRefGoogle Scholar
  16. Casale P (2011) Sea turtle by-catch in the Mediterranean. Fish Fish 12:299–316.  https://doi.org/10.1111/j.1467-2979.2010.00394.x CrossRefGoogle Scholar
  17. Casale P, Margaritoulis D (eds) (2010) Sea turtles in the Mediterranean: distribution, threats and conservation priorities. IUCN, GlandGoogle Scholar
  18. Casale P, Mariani P (2014) The first ‘lost year’of Mediterranean sea turtles: dispersal patterns indicate subregional management units for conservation. Mar Ecol Prog Ser 498:263–274.  https://doi.org/10.3354/meps10640 CrossRefGoogle Scholar
  19. Casale P, Simone G (2017) Seasonal residency of loggerhead turtles Caretta caretta tracked from the Gulf of Manfredonia, south Adriatic. Mediterr Mar Sci 18:4–10.  https://doi.org/10.12681/mms.1663 CrossRefGoogle Scholar
  20. Casale P, Laurent L, De Metrio G (2004) Incidental capture of marine turtles by the Italian trawl fishery in the north Adriatic Sea. Biol Conserv 119:287–295.  https://doi.org/10.1002/aqc.841 CrossRefGoogle Scholar
  21. Casale P, Freggi D, Basso R, Argano R (2005) Size at male maturity, sexing methods and adult sex ratio in loggerhead turtles (Caretta caretta) from Italian waters investigated through tail measurements. Herpetol J 15:145–148Google Scholar
  22. Casale P, Freggi D, Basso R, Vallini C, Argano R (2007) A model of area fidelity, nomadism, and distribution patterns of loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea. Mar Biol 152:1039–1049.  https://doi.org/10.1007/s00227-007-0752-7 CrossRefGoogle Scholar
  23. Casale P, Affronte M, Insacco G, Freggi D, Vallini C, Pino d’Astore P, Basso R, Paolillo G, Abbate G, Argano R (2010) Sea turtle strandings reveal high anthropogenic mortality in Italian waters. Aquat Conserv 20:611–620.  https://doi.org/10.1002/aqc.1133 CrossRefGoogle Scholar
  24. Casale P, Simone G, Conoscitore C, Conoscitore M, Salvemini P (2012) The Gulf of Manfredonia: a new neritic foraging area for loggerhead sea turtles in the Adriatic Sea. Acta Herpetol 7:1–12.  https://doi.org/10.13128/Acta_Herpetol-9897 Google Scholar
  25. Casale P, Freggi D, Furii G, Vallini C, Salvemini P, Deflorio M, Totaro G, Raimondi S, Fortuna C, Godley BJ (2015) Annual survival probabilities of juvenile loggerhead sea turtles indicate high anthropogenic impact on Mediterranean populations. Aquat Conserv 25:690–700.  https://doi.org/10.1002/aqc.2467 CrossRefGoogle Scholar
  26. Casale P, Freggi D, Rigoli A, Ciccocioppo A, Luschi P (2017) Geometric morphometrics, scute patterns and biometrics of loggerhead turtles (Caretta caretta) in the central Mediterranean. Amphibia-Reptilia 38:145–156.  https://doi.org/10.1163/15685381-00003096 CrossRefGoogle Scholar
  27. Chaieb O, El Ouaer A, Maffucci F, Bradai MN, Bentivegna F, Said K, Chatti N (2010) Genetic survey of loggerhead turtle Caretta caretta nesting population in Tunisia. Mar Biodivers Rec 3:e20.  https://doi.org/10.1017/S175526721000014X CrossRefGoogle Scholar
  28. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659.  https://doi.org/10.1046/j.1365-294x.2000.01020.x CrossRefPubMedGoogle Scholar
  29. Clusa M, Carreras C, Pascual M, Demetropoulos A, Margaritoulis D, Rees AF, Hamza AA, Khalil M, Aureggi M, Levy Y (2013) Mitochondrial DNA reveals Pleistocenic colonisation of the Mediterranean by loggerhead turtles (Caretta caretta). J Exp Mar Biol Ecol 439:15–24.  https://doi.org/10.1016/j.jembe.2012.10.011 CrossRefGoogle Scholar
  30. Clusa M, Carreras C, Pascual M, Gaughran SJ, Piovano S, Giacoma C, Fernández G, Levy Y, Tomás J, Raga JA (2014) Fine-scale distribution of juvenile Atlantic and Mediterranean loggerhead turtles (Caretta caretta) in the Mediterranean Sea. Mar Biol 161:509–519.  https://doi.org/10.1007/s00227-013-2353-y CrossRefGoogle Scholar
  31. Coll M, Piroddi C, Albouy C, Ben Rais Lasram F, Cheung WWL, Christensen V, Karpouzi VS, Guilhaumon F, Mouillot D, Paleczny M, Palomares ML, Steenbeek J, Trujillo P, Watson R, Pauly D (2012) The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Global Ecol Biogeogr 21:465–480.  https://doi.org/10.1111/j.1466-8238.2011.00697.x CrossRefGoogle Scholar
  32. Cushman-Roisin B, Gačić M, Poulain P-M, Artegiani A (eds) (2001) Physical oceanography of the Adriatic Sea. Past, present and future. Kluwer Academic Publishers, DordrechtGoogle Scholar
  33. Drosopoulou E, Tsiamis G, Mavropoulou M, Vittas S, Katselidis KA, Schofield G, Palaiologou D, Sartsidis T, Bourtzis K, Pantis J, Scouras ZG (2012) The complete mitochondrial genome of the loggerhead turtle Caretta caretta (Testudines: Cheloniidae): Genome description and phylogenetic considerations. Mitochondr DNA 23:1–12.  https://doi.org/10.3109/19401736.2011.637109 CrossRefGoogle Scholar
  34. Duchene S, Frey A, Alfaro-Nunez A, Dutton PH, Gilbert MTP, Morin PA (2012) Marine turtle mitogenome phylogenetics and evolution. Mol Phylogenet Evol 65:241–250.  https://doi.org/10.1016/j.ympev.2012.06.010 CrossRefPubMedGoogle Scholar
  35. Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M (eds) (1999) Research and management techniques for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4, Consolidated Graphic Communications, BlanchardGoogle Scholar
  36. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567.  https://doi.org/10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  37. 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 131:479–494PubMedPubMedCentralGoogle Scholar
  38. Formia A, Godley BJ, Dontaine JF, Bruford MW (2006) Mitochondrial DNA diversity and phylogeography of endangered green turtle (Chelonia mydas) populations in Africa. Conserv Genet 7:353–369.  https://doi.org/10.1007/s10592-005-9047-z CrossRefGoogle Scholar
  39. Fortuna CM, Vallini C, Filidei E Jr, Ruffino M, Consalvo I, Di Muccio S, Gion C, Scacco U, Tarulli E, Giovanardi O, Mazzola A (2010) By-catch of cetaceans and other species of conservation concern during pair trawl fishing operations in the Adriatic Sea (Italy). Chem Ecol 26:65–76.  https://doi.org/10.1080/02757541003627662 CrossRefGoogle Scholar
  40. Franzellitti S, Locatelli C, Gerosa G, Vallini C, Fabbri E (2004) Heavy metals in tissues of loggerhead turtles (Caretta caretta) from the northwestern Adriatic Sea. Comp Biochem Phis C 138:187–194.  https://doi.org/10.1016/j.cca.2004.07.008 CrossRefGoogle Scholar
  41. Garofalo L, Mastrogiacomo A, Casale P, Carlini R, Eleni C, Freggi D, Gelli D, Knittweis L, Mifsud C, Mingozzi T (2013) Genetic characterization of central Mediterranean stocks of the loggerhead turtle (Caretta caretta) using mitochondrial and nuclear markers, and conservation implications. Aquat Conserv 23:868–884.  https://doi.org/10.1002/aqc.2338 CrossRefGoogle Scholar
  42. Garofalo L, Marsili L, Terracciano G, Baini M, Senese M, Mancusi C, Lorenzini R (2016a) Welcome to the North! Genetic makeup of loggerhead Caretta caretta females from the northernmost Italian nesting site. In: Menegon M, Rodriguez-Prieto A, Deflorian MC (eds) Atti XI Congresso Nazionale Societas Herpetologica Italica. Ianieri Edizioni, Trento, Italy.  https://doi.org/10.13140/rg.2.2.14077.15849
  43. Garofalo L, Insacco G, Scaravelli D, Lorenzini R (2016b) On the connectivity between nesting colonies of the loggerhead turtle Caretta caretta in the Ionian Region. In: Menegon M, Rodriguez-Prieto A, Deflorian MC (eds) Atti XI Congresso Nazionale Societas Herpetologica Italica. Ianieri Edizioni, Trento, Italy, pp 135–136.  https://doi.org/10.13140/rg.2.2.34209.81766
  44. Garoia F, Guarniero I, Piccinetti C, Tinti F (2004) First microsatellite loci of red mullet (Mullus barbatus) and their application to genetic structure analysis of Adriatic shared stock. Mar Biotechnol 6:446–452.  https://doi.org/10.1007/s10126-004-3045-x CrossRefPubMedGoogle Scholar
  45. Gaspari S, Holcer D, Mackelworth P, Fortuna C, Frantzis A, Genov T, Vighi M, Natali C, Rako N, Banchi E, Chelazzi G, Ciofi C (2015) Population genetic structure of common bottlenose dolphins (Tursiops truncatus) in the Adriatic Sea and contiguous regions: implications for international conservation. Aquat Conserv 25:212–222.  https://doi.org/10.1002/aqc.2415 CrossRefGoogle Scholar
  46. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–472CrossRefGoogle Scholar
  47. Halpern BS, Selkoe KA, Micheli F, Kappel CV (2007) Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conserv Biol 21:1301–1315CrossRefPubMedGoogle Scholar
  48. Hamann M, Godfrey MH, Seminoff JA, Arthur K, Barata PCR, Bjorndal KA, Bolten AB, Broderick AC, Campbell LM, Carreras C (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11:245–269.  https://doi.org/10.3354/esr00279 CrossRefGoogle Scholar
  49. Hamza AA (2010) Libya. In: Casale P, Margaritoulis D (eds) Sea turtles in the Mediterranean: distribution, threats and conservation priorities. IUCN, Gland, pp 157–170Google Scholar
  50. Hawkes L, Broderick AC, Coyne MS, Godfrey MH, Godley BJ (2007) Only some like it hot—quantifying the environmental niche of the loggerhead sea turtle. Divers Distrib 13:447–457.  https://doi.org/10.1111/j.1472-4642.2007.00354.x CrossRefGoogle Scholar
  51. Hays GC, Fossette S, Katselidis KA, Mariani P, Schofield G (2010) Ontogenetic development of migration: lagrangian drift trajectories suggest a new paradigm for sea turtles. J R Soc Interface 7:1319–1327.  https://doi.org/10.1098/rsif.2010.0009 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Laurent L, Casale P, Bradai MN, Godley BJ, Broderick GG, Schroth W, Schierwater B, Levy AM, Freggi D, Abd El-Mawla EM (1998) Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol Ecol 7:1529–1542.  https://doi.org/10.1046/j.1365-294x.1998.00471.x CrossRefPubMedGoogle Scholar
  53. Lazar B, Gračan R (2011) Ingestion of marine debris by loggerhead sea turtles, Caretta caretta, in the Adriatic Sea. Marine Poll Bull 62:43–47.  https://doi.org/10.1016/j.marpolbul.2010.09.013 CrossRefGoogle Scholar
  54. Lazar B, Borboroglu PG, Tvrtković N, Žiža V (2002) Temporal and spatial distribution of the loggerhead sea turtle, Caretta caretta, in the eastern Adriatic Sea: a seasonal migration pathway? In: Seminoff JA (compiler) Proceedings of the twenty-second annual symposium on sea turtle biology and conservation. NOAA Technical Memorandum NMFS-SEFSC-503, Miami, pp 283–284Google Scholar
  55. Lazar B, Margaritoulis D, Tvrtković N (2004) Tag recoveries of the loggerhead sea turtle Caretta caretta in the eastern Adriatic Sea: implications for conservation. J Mar Biol Assoc UK 84:475–480.  https://doi.org/10.1017/S0025315404009488h CrossRefGoogle Scholar
  56. Lazar B, Gračan R, Katić J, Zavodnik D, Jaklin A, Tvrtković N (2011) Loggerhead sea turtles (Caretta caretta) as bioturbators in neritic habitats: an insight through the analysis of benthic molluscs in the diet. Mar Ecol 32:65–74.  https://doi.org/10.1111/j.1439-0485.2010.00402.x CrossRefGoogle Scholar
  57. Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116.  https://doi.org/10.1111/2041-210X.12410 CrossRefGoogle Scholar
  58. Luschi P, Casale P (2014) Movement patterns of marine turtles in the Mediterranean Sea: a review. Ital J Zool 81:478–495.  https://doi.org/10.1080/11250003.2014.963714 CrossRefGoogle Scholar
  59. Maffucci F, Corrado R, Palatella L, Borra M, Marullo S, Hochscheid S, Lacorata G, Iudicone D (2016) Seasonal heterogeneity of ocean warming: a mortality sink for ectotherm colonizers. Sci Rep UK 6:Article no. 23983  https://doi.org/10.1038/srep23983
  60. Margaritoulis D, Argano R, Baran I, Bentivegna F, Bradai MN, Camiñas JA, Casale P, De Metrio G, Demetropoulos A, Gerosa G (2003) Loggerhead turtles in the Mediterranean: present knowledge and conservation perspectives. In: Bolten AB, Wutherington BE (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington DC, pp 175–198Google Scholar
  61. Millot C, Taupier-Letage I (2005) Circulation in the Mediterranean sea. In: Saliot A (ed) The Mediterranean Sea. Springer, Berlin, pp 323–334  https://doi.org/10.1007/b107143
  62. Monzón-Argüello C, Rico C, Carreras C, Calabuig P, Marco A, López-Jurado LF (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.  https://doi.org/10.1016/j.jembe.2009.03.007 CrossRefGoogle Scholar
  63. Naro-Maciel E, Gaughran SJ, Putman NF, Amato G, Arengo F, Dutton PH, McFadden KW, Vintinner EC, Sterling EJ (2014) Predicting connectivity of green turtles at Palmyra Atoll, central Pacific: a focus on mtDNA and dispersal modelling. J R Soc Interface 11:20130888.  https://doi.org/10.1098/rsif.2013.0888 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol Ecol 3:363–373.  https://doi.org/10.1111/j.1365-294X.1994.tb00076.x CrossRefPubMedGoogle Scholar
  65. Novelletto A, Testa L, Iacovelli F, Blasi P, Garofalo L, Mingozzi T, Falconi M (2016) Polymorphism in mitochondrial coding regions of Mediterranean loggerhead turtles: evolutionary relevance and structural effects. Physiol Biochem Zool 89:473–486.  https://doi.org/10.1086/688679 CrossRefPubMedGoogle Scholar
  66. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 282:537–2539Google Scholar
  67. Pella J, Masuda M (2001) Bayesian methods for analysis of stock mixtures from genetic characters. Fish B-NOAA 99:151Google Scholar
  68. Poulain P-M (2001) Adriatic Sea surface circulation as derived from drifter data between 1990 and 1999. J Mar Syst 29:3–32CrossRefGoogle Scholar
  69. Rees AF, Carreras C, Broderick AC, Margaritoulis D, Stringell TB, Godley BJ (2017) Linking loggerhead locations: using multiple methods to determine the origin of sea turtles in feeding grounds. Mar Biol 164:30.  https://doi.org/10.1007/s00227-016-3055-z CrossRefPubMedPubMedCentralGoogle Scholar
  70. Revelles M, Carreras C, Cardona L, Marco A, Bentivegna F, Castillo JJ, de Martino G, Mons JL, Smith MB, Rico C, Pascual M, Aguilar A (2007) Evidence for an asymmetrical size exchange of loggerhead sea turtles between theMediterranean and the Atlantic through the Straits of Gibraltar. J Exp Mar Biol Ecol 349:261–271.  https://doi.org/10.1016/j.jembe.2007.05.018 CrossRefGoogle Scholar
  71. Ruggeri P, Splendiani A, Occhipinti G, Fioravanti T, Santojanni A, Leonori I, De Felice A, Arneri E, Procaccini G, Catanese G, Tičina V, Bonanno A, Nisi Cerioni P, Giovannotti M, Grant WS, Caputo Barucchi V (2016) Biocomplexity in populations of European anchovy in the Adriatic Sea. PLoS One 11:e0153061.  https://doi.org/10.1371/journal.pone.0153061 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sambrook JF, Russel DW (eds) (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  73. Schofield G, Bishop CM, Katselidis KA, Dimopoulos P, Pantis JD, Hay GC (2009) Microhabitat selection by sea turtles in a dynamic thermal marine environment. J Anim Ecol 78:14–21.  https://doi.org/10.1111/j.1365-2656.2008.01454.x CrossRefPubMedGoogle Scholar
  74. Shamblin BM, Bolten AB, Bjorndal KA, Dutton PH, Nielsen JT, Abreu-Grobois FA, Reich KJ, Witherington BE, Bagley DA, Ehrhart LM (2012) Expanded mitochondrial control region sequences increase resolution of stock structure among North Atlantic loggerhead turtle rookeries. Mar Ecol Prog Ser 469:145–160.  https://doi.org/10.3354/meps09980 CrossRefGoogle Scholar
  75. Shamblin BM, Bolten AB, Abreu-Grobois FA, Bjorndal KA, Cardona L, Carreras C, Clusa M, Monzón-Argüello C, Nairn CJ, Nielsen JT (2014) Geographic patterns of genetic variation in a broadly distributed marine vertebrate: new insights into loggerhead turtle stock structure from expanded mitochondrial DNA sequences. PLoS One 9:e85956.  https://doi.org/10.1371/journal.pone.0085956 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genet Mol Biol 132:619–633Google Scholar
  77. Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner EM, Bolten AB, Chaloupka MY, Hutchinson BJ, Abreu-Grobois FA, Amorocho D, Bjorndal KA (2010) Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS One 5:e15465.  https://doi.org/10.1371/journal.pone.0015465 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Yilmaz C, Turkozan O, Bardakcı 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.  https://doi.org/10.13128/Acta_Herpetol-10286 Google Scholar
  79. Zbinden JA, Aebischer A, Margaritoulis D, Arlettaz R (2008) Important areas at sea for adult loggerhead sea turtles in the Mediterranean Sea: satellite tracking corroborates findings from potentially biased sources. Mar Biol 153:899–906.  https://doi.org/10.1007/s00227-007-0862-2 CrossRefGoogle Scholar
  80. Zbinden JA, Bearhop S, Bradshaw P, Gill B, Margaritoulis D, Newton J, Godley BJ (2011) Migratory dichotomy and associated phenotypic variation in marine turtles revealed by satellite tracking and stable isotope analysis. Mar Ecol Prog Ser 421:291–302.  https://doi.org/10.3354/meps08871 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Livia Tolve
    • 1
  • Paolo Casale
    • 2
  • Angela Formia
    • 1
    • 3
  • Luisa Garofalo
    • 4
  • Bojan Lazar
    • 5
    • 6
  • Chiara Natali
    • 1
  • Andrea Novelletto
    • 7
  • Carola Vallini
    • 8
  • Elena Bužan
    • 5
  • Guido Chelazzi
    • 1
  • Stefania Gaspari
    • 9
  • Caterina Fortuna
    • 10
  • Ivna Kocijan
    • 11
    • 12
  • Erica Marchiori
    • 13
  • Nicola Novarini
    • 14
  • Lisa Poppi
    • 13
  • Pasquale Salvemini
    • 15
  • Claudio Ciofi
    • 1
  1. 1.Department of BiologyUniversity of FlorenceSesto FiorentinoItaly
  2. 2.Department of BiologyUniversity of PisaPisaItaly
  3. 3.Global Conservation ProgramWildlife Conservation SocietyBronxUSA
  4. 4.Istituto Zooprofilattico Sperimentale delle Regioni Lazio e ToscanaCentro di Referenza Nazionale per la Medicina Forense VeterinariaRietiItaly
  5. 5.Department of Biodiversity, Faculty of Mathematics, Natural Sciences and Information TechnologiesUniversity of PrimorskaKoperSlovenia
  6. 6.Marine Sciences ProgramJuraj Dobrila University of PulaPulaCroatia
  7. 7.Department of BiologyUniversity of Rome “Tor Vergata”RomeItaly
  8. 8.A.R.C.H.È. OnlusFerraraItaly
  9. 9.Institute of Marine Sciences (ISMAR)National Research Council (CNR)AnconaItaly
  10. 10.Italian National Institute for Environmental Protection and Research (ISPRA)RomeItaly
  11. 11.Department of Anatomy and PhysiologyUniversity of Applied Health SciencesZagrebCroatia
  12. 12.Department of BiologyUniversity of Applied Health SciencesZagrebCroatia
  13. 13.Department of Comparative Biomedicine and Food ScienceUniversity of PaduaLegnaroItaly
  14. 14.Museum of Natural History of VeniceVeniceItaly
  15. 15.Panda Molfetta OnlusMolfettaItaly

Personalised recommendations