Different growth rates between loggerhead sea turtles (Caretta caretta) of Mediterranean and Atlantic origin in the Mediterranean Sea

Marine Biology

Volumn 158, Issue 11, 2011, Pages 2577-2587

  Piovano, Susanna ^a   Clusa, Marcel ^b   Carreras, Carlos ^b   Giacoma, Cristina ^a   Pascual, Marta ^b   Cardona, Luis ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CONSPECIFIC; FEEDING GROUND; GENETIC ANALYSIS; GROWTH MODELING; GROWTH RATE; NESTING; TURTLE;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHWEST); MEDITERRANEAN SEA;

CARETTA; CARETTA CARETTA; TESTUDINES;

EID: 80255134495     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-011-1759-7     Document Type: Article

References (86)

1. Abreu-Grobois A, Horrocks J, Formia A, Dutton P, LeRoux R, Velez-Zuazo X, Soares L, Meylan P (2006) New mtDNA dloop primers which work for a variety of marine turtle species may increase the resolution capacity of mixed stock analysis. In: Frick M, Panagopoulou A, Rees AF, Williams K (eds) Book of abstracts 26th annual symposium on sea turtle biology and conservation. International Sea Turtle Society, Athens, Greece, p 179.
2. Avens L, Goshe LR (2007) Comparative skeletochronological analysis of Kemp's ridley (Lepidochelys kempii) and loggerhead (Caretta caretta) humeri and scleral ossicles. Mar Biol 152: 1309-1317. doi: 10. 1007/s00227-007-0779-9.
3. Avens L, Taylor C, Goshe L, Jones TT, Hastings M (2009) Use of skeletochronological analysis to estimate the age of leatherback sea turtles Dermochelys coriacea in the western North Atlantic. Endang Species Res 8: 165-177. doi: 10. 3354/esr00202.
4. Bjorndal KA, Zug G (1995) Growth and age of sea turtle. In: Bjorndal KA (ed) Biology and conservation of sea turtles, rev edn. Smithsonian Institution Press, Washington and London, pp 599-600.
5. Bjorndal KA, Bolten AB, Bennett RA, Jacobson ER, Wronski TJ, Valeski JJ, Eliazar PJ (1998) Age and growth in sea turtles: limitations of skeletochronology for demographic studies. Copeia 1: 23-30.
6. Bjorndal KA, Bolten A, Martins HR (2000) Somatic growth model of juvenile loggerhead sea turtles Caretta caretta: duration of pelagic stage. Mar Ecol Prog Ser 202: 265-272.
7. Bjorndal KA, Bolten AB, Koike B, Schroeder BA, Shaver DJ, Teas WG, Witzell WN (2001) Somatic growth function for immature loggerhead sea turtles, Caretta caretta, in southeastern US waters. Fish Bull 99: 240-246.
8. Bjorndal KA, Bolten AB, Dellinger T, Delgado C, Martins HR (2003) Compensatory growth in oceanic loggerhead sea turtles: response to a stochastic environment. Ecology 84: 1237-1249.
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 4, pp 110-114.
10. Bolten AB, Balazs GH (1995) Biology of the early pelagic stage-the "lost year". In: Bjorndal KA (ed) Biology and conservation of sea turtles, rev edn. Smithsonian Institution Press, Washington and London, pp 579-581.
11. Bolten AB, Bjorndal K, Martins HR, Dellinger T, Boscoito MJ, Encalada SE, Bowen BW (1998) Transatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis. Ecol Appl 8: 1-7. doi: 10. 1890/1051-0761(1998)008[0001: TDMOLS]2. 0. CO; 2.
12. Bosc E, Bricaud A, Antoine D (2004) Seasonal and interannual variability in algal biomass and primary production in the Mediterranean Sea, as derived from 4 years of SeaWiFS observations. Global Biogeochem Cycles 18: GB1006. doi: 10. 1029/2003GB002034.
13. Braun-McNeill J, Epperly SP, Avens L, Snover ML, Taylor JC (2008) Growth rates of loggerhead sea turtles (Caretta caretta) from the western north Atlantic. Herpetol Conserv Biol 3: 273-281.
14. Cardona L, Revelles M, Carreras C, Sanfélix M, Gazo M, Aguilar A (2005) Western Mediterranean immature loggerhead turtles: habitat use in spring and summer assessed through satellite tracking and aerial surveys. Mar Biol 147: 583-591. doi: 10. 1007/s00227-005-1578-9.
15. Cardona L, Revelles M, Parga ML, Tomás J, Aquilar A, Alegre F, Raga A, Ferrer X (2009) Habitat use by loggerhead sea turtles Caretta caretta off the coast of eastern Spain results in a high vulnerability to neritic fishing gear. Mar Biol 156: 2621-2630. doi: 10. 1007/s00227-009-1288-9.
16. Carr A (1987) New perspective on the pelagic stage of sea turtle development. Conserv Biol 1: 103-121.
17. Carreras C, Pont S, Maffucci F, Pascual M, Barceló A, Bentivegna F, Cardona L, Alegre F, Sanfélix M, Fernández 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. doi: 10. 1007/s00227-006-0282-8.
18. Carreras C, Pascual M, Cardona L, Aguilar A, Margaritoulis D, Rees A, 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. doi: 10. 1007/s10592-006-9224-8.
19. Carreras C, Pascual M, Cardona L, Marco A, Bellido JJ, Castillo JJ, Tomás J, Raga JA, Sanfélix M, Fernández G, Aguilar A (in press) Living together apart: Atlantic and Mediterranean loggerhead sea turtles (Caretta caretta) in shared feeding grounds. J Hered.
20. Casale P, Abbate G, Freggi D, Conte N, Oliverio M, Argano R (2008a) Foraging ecology of loggerhead sea turtles Caretta caretta in the central Mediterranean Sea: evidence for a relaxed life history model. Mar Ecol Prog Ser 372: 265-276. doi: 10. 3354/meps07702.
21. Casale P, Freggi D, Gratton P, Argano R, Oliverio M (2008b) Mitochondrial DNA reveals regional and interregional importance of the central Mediterranean African shelf for loggerhead sea turtles (Caretta caretta). Sci Mar 72: 541-548.
22. Casale P, d'Astore PP, Argano R (2009a) Age at size and growth rates of early juvenile loggerhead sea turtles (Caretta caretta) in the Mediterranean based on length frequency analysis. Herpetol J 19: 29-33.
23. Casale P, Mazaris AD, Freggi D, Vallini C, Argano R (2009b) Growth rates and age at adult size of loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea, estimated through capture-mark-recapture records. Sci Mar 73: 589-595. doi: 10. 3989/scimar. 2009. 73n3589.
24. Casale P, Conte N, Freggi D, Cioni C, Argano R (2011a) Age and growth determination by skeletochronology in loggerhead sea turtles (Caretta caretta) from the Mediterranean Sea. Sci Mar 75: 197-203. doi: 10. 3989/scimar. 2011. 75n1197.
25. Casale P, Mazaris AD, Freggi D (2011b) Estimation of age at maturity of loggerhead sea turtles Caretta caretta in the Mediterranean using length-frequency data. Endang Species Res 13: 123-129. doi: 10. 3354/esr00319.
26. Castanet J (1985) La squelettochronologie chez les Reptiles. I. Résultats expérimentaux sur la signification des marques de croissance squelettiques chez les Lézards et les Tortues. Ann Sci Nat Zool (Paris) 7: 23-40.
27. Castanet J, Smirina E (1990) Introduction to the skeletochronological method in amphibians and reptiles. Ann Sci Nat Zool (Paris) 11: 191-196.
28. Coles WC, Musick JA, Williamson LA (2001) Skeletochronology validation from an adult loggerhead (Caretta caretta). Copeia 1: 240-242.
29. Crouse DT, Crowder LB, Caswell H (1987) A stage-based population model for loggerhead sea turtles and implications for conservation. Ecology 68: 1412-1423.
30. Crowder LB, Crouse DT, Heppell SS, Martin TM (1994) Predicting the impact of turtle excluder devices on loggerhead sea turtle populations. Ecol Appl 4: 437-445.
31. Curtin AJ, Zug GR, Medica PA, Spotila JR (2008) Assessing age in the desert tortoise Gopherus agassizii: testing skeletochronology with individuals of known age. Endang Species Res 5: 21-27. doi: 10. 3354/esr00108.
32. Curtin AJ, Zug GR, Spotila JR (2009) Longevity and growth strategies of the desert tortoise (Gopherus agassizii) in two American deserts. J Arid Env 73: 463-471. doi: 10. 1016/j. jaridenv. 2008. 11. 011.
33. Dodd Jr CK (1988) Synopsis of the biological data on the loggerhead sea turtle. US Fish Wildl Serv Biol Rep 88: 1-110.
34. Eckert SA, Moore JE, Dunn DC, Sagarminaga van Buiten R, Eckert KL, Halpin PN (2008) Modeling loggerhead turtle movement in the Mediterranean: importance of body size and oceanography. Ecol Appl 18: 290-308.
35. Ehret DJ (2007) Skeletochronology, a method for determining the individual age and growth of modern and fossil tortoises (Reptilia Testudines). Bull Florida Museum Nat Hist 47: 49-72.
36. Ehrhart LM, Yoder RG (1978) Marine turtles of Merritt Island National Wildlife Refuge, Kennedy Space Center, Florida. Fla Mar Res Publ 33: 25-30.
37. Encalada SE, Bjorndal KA, Bolten AB, Zurita JC, Schroeder B, Possardt E, Sears CJ, Bowen BW (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.
38. Enlow DH (1969) The bone of reptiles. In: Gans C, d'A Bellairs A, Parsons TS (eds) Biology of the Reptilia: morphology A. Academic Press, London and New York, pp 45-80.
39. Fabens AJ (1965) Properties and fitting of the von Bertalanffy growth curve. Growth 29: 265-289.
40. Fitzsimmons NN, Moritz C, Moore SS (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol Biol Evol 12: 432-440.
41. FitzSimmons NN, Moritz C, Limpus CJ, Miller JD, Parmenter CJ, Prince R (1996) Comparative genetic structure of green, loggerhead, and flatback populations in Australia based on variable mtDNA and nDNA regions. In: Bowen BW, Witzell WN (eds) Proceedings of the international symposium on sea turtle conservation genetics. NOAA Tech Mem NMFS-SEFSC, vol 396, pp 25-32.
42. Francis R (1990) Back-calculation of fish length: a critical review. J Fish Biol 36: 883-902.
43. Frazer NB, Ehrhart LM (1985) Preliminary growth models for green, Chelonia mydas, and loggerhead, Caretta caretta, turtles in the wild. Copeia 1: 73-79.
44. Garofalo L, Mingozzi T, Micò A, Novelletto A (2009) Loggerhead turtle (Caretta caretta) matrilines in the Mediterranean: further evidence of genetic diversity and connectivity. Mar Biol 156: 2085-2095. doi: 10. 1007/s00227-009-1239-5.
45. Goshe LR, Avens L, Bybee J, Hohn AA (2009) An evaluation of histological techniques used in skeletochronological age estimation of sea turtles. Chelon Conserv Biol 8: 217-222.
46. Goshe LR, Avens L, Scharf FS, Southwood AL (2010) Estimation of age at maturation and growth of Atlantic green turtles (Chelonia mydas) using skeletochronology. Mar Biol 157: 1725-1740. doi: 10. 1007/s00227-010-1446-0.
47. Guarino FM, Angelini F, Cammarota M (1995) A skeletochronological analysis in three syntopic species of southern Italy. Amphibia-Reptilia 16: 297-302.
48. Guarino FM, Di Maio A, Caputo V (2004) Age estimation by phalangeal skeletochronology of Caretta caretta from the Mediterranean Sea. Ital J Zool 2(Suppl): 175-179. doi: 10. 1080/11250000409356630.
49. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41: 95-98.
50. Heppell SS, Crowder LB, Crouse DT, Epperly SP, Frazer NB (2003) Population models for Atlantic loggerheads: past, present, and future. In: Bolten AB, Witherington B (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, pp 255-273.
51. IUCN (2010) Red list of threatened species. Version 2010. 4. http://www. iucnredlist. org. Accessed 10 Mar 2011.
52. Klinger RC, Musick JA (1992) Annular growth layers in juvenile loggerhead turtles (Caretta caretta). Bull Mar Sci 51: 224-230.
53. Klinger RC, Musick JA (1995) Age and growth of loggerhead turtles (Caretta caretta) from Chesapeake Bay. Copeia 1: 204-209.
54. Kolarov T, Ljubisavljević K, Polović L, Džukić G, Kalezić ML (2010) The body size, age structure and growth pattern of the endemic Balkan Mosor rock lizard (Dinarolacerta mosorensis kolombatović, 1886). Acta zool hung 56: 55-71.
55. Laurent L, Casale P, Bradai MN, Godley BJ, Gerosa G, Broderick AC, Schroth W, Schierwater B, Levy AM, Freggi D, Abd El-Mawla EM, Hadoud DA, Gomati HE, Domingo M, Hadjichristophorous M, Kornaraki 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.
56. Leclair Jr R, Castanet J (1987) A skeletochronological assessment of age and growth in the frog Rana pipiens Schreber (Amphibia, Anura) from Southwestern Quebec. Copeia 2: 361-369.
57. Lewison RL, Freeman SA, Crowder LB (2004) Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles. Ecol Lett 7: 221-231. doi: 10. 1111/j. 1461-0248. 2004. 00573. x.
58. Longhurst A (1998) Ecological geography of the sea. Academic Press, San Diego.
59. Margaritoulis D, Argano R, Baran I, Bentivegna F, Bradai MN, Caminas JA, Casale P, De Metrio G, Demetropoulos A, Gerosa G, Godley B, Houghton J, Laurent L, Lazar B (2003) Loggerhead turtles in the Mediterranean Sea: present knowledge and conservation perspectives. In: Bolten AB, Witherington B (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, pp 175-198.
60. Mendonca MT (1981) Comparative growth rates of wild immature Chelonia mydas and Caretta caretta in Florida. J Herpetol 15: 447-451.
61. Mingozzi T, Masciari G, Paolillo G, Pisani B, Russo M, Massolo A (2007) Discovery of a regular nesting area of loggerhead turtle Caretta caretta in southern Italy: a new perspective for national conservation. Biodivers Conserv 16: 3519-3541. doi: 10. 1007/s10531-006-9098-6.
62. Monzón-Argüello C, Rico C, Naro-Maciel E, Varo-Cruz N, López P, Marco A, López-Jurado LF (2010) Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands. Conserv Genet 11: 1871-1884. doi: 10. 1007/s10592-010-0079-7.
63. Moore MK, Ball RM (2002) Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis. Mol Ecol 11: 281-288.
64. Parham JF, Zug GR (1997) Age and growth of loggerhead sea turtles (Caretta caretta) of coastal Georgia: an assessment of skeletochronological age-estimates. Bull Mar Sci 61: 287-304.
65. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
66. Ramsey FL, Schafer DW (2002) The statistical sleuth: a course in methods of data analysis, 2nd edn. Duxbury, Pacific Grove.
67. R-Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www. R-project. org. Downloaded 21 Jan 2011.
68. Revelles M, Cardona L, Aguilar A, Sanfélix M, Fernández G (2007a) Habitat use by immature loggerhead sea turtles in the Algerian Basin (western Mediterranean): swimming behaviour, seasonality and dispersal pattern. Mar Biol 151: 1501-1515. doi: 10. 1007/s00227-006-0602-z.
69. Revelles M, Carreras C, Cardona L, Marco A, Bentivegna F, Castillo JJ, de Martino G, Mons JL, Smith MB, Rico C, Pascual M, Aquilar A (2007b) 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. doi: 10. 1016/j. jembe. 2007. 05. 018.
70. Seglie D, Roy D, Giacoma C (2010) Sexual dimorphism and age structure in a population of Tylototriton verrucosus (Amphibia: Salamandridae) from the Himalayan Region. Copeia 4: 600-608.
71. Shaver DJ (1994) Relative abundance, temporal patterns, and growth of sea turtles at the Mansfield Channel, Texas. J Herpetol 28: 491-497.
72. Snover ML (2002) Growth and ontogeny of sea turtles using skeletochronology: methods, validation, and application to conservation. PhD Dissertation, Duke University, USA.
73. Snover ML, Hohn AA (2004) Validation and interpretation of annual skeletal marks in loggerhead (Caretta caretta) and Kemp's ridley (Lepidochelys kempii) sea turtles. Fish Bull 102: 682-692.
74. Snover ML, Avens L, Hohn AA (2007a) Back-calculating length from skeletal growth marks in loggerhead sea turtles Caretta caretta. Endanger Species Res 3: 95-104.
75. Snover ML, Hohn AA, Crowder LB, Heppell SS (2007b) Age and growth in Kemp's ridley sea turtles. In: Plotkin PT (ed) Biology and conservation of ridley sea turtles. The John Hopkins University Press, Baltimore, pp 89-105.
76. Snover ML, Hohn AA, Crowder LB, Macko SA (2010) Combining stable isotopes and skeletal growth marks to detect habitat shifts in juvenile loggerhead sea turtles Caretta caretta. Endang Species Res 13: 25-31. doi: 10. 3354/esr00311.
77. Tiwari M, Bjorndal KA (2000) Variation in morphology and reproduction in loggerheads, Caretta caretta, nesting in the United States, Brazil, and Greece. Herpetologica 56: 343-356.
78. Turtle Expert Working Group (2009) An assessment of the loggerhead turtle population in the western north Atlantic Ocean. NOAA Tech Mem NMFS-SEFSC 575: 1-131.
79. Wallace BP, Heppell SS, Lewison RL, Kelez S, Crowder LB (2008) Impacts of fisheries bycatch on loggerhead turtles worldwide inferred from reproductive value analyses. J Appl Ecol 45: 1076-1085. doi: 10. 1111/j. 1365-2664. 2008. 01507. x.
80. Zug GR, Glor RE (1998) Estimates of age and growth in a population of green sea turtles (Chelonia mydas) from the Indian River lagoon system, Florida: a skeletochronological analysis. Can J Zool 76: 1497-1506.
81. Zug GR, Parham JF (1996) Age and growth in leatherback turtles, Dermochelys coriacea (Testudines: Dermochelydae): a skeletochronological analysis. Chelonian Conserv Biol 2: 244-249.
82. Zug GR, Wynn AH, Ruckdeschel C (1986) Age determination of loggerhead sea turtles, Caretta caretta, by incremental growth marks in the skeleton. Smithsonian Inst Contrib Zool 427: 1-34.
83. Zug GR, Balazs GH, Wetherall JA (1995) Growth in juvenile loggerhead sea turtles (Caretta caretta) in the north Pacific pelagic habitat. Copeia 2: 484-487.
84. Zug GR, Kalb HJ, Luzar SJ (1997) Age and growth in wild Kemp's ridley sea turtles Lepidochelys kempii from skeletochronological data. Biol Conserv 80: 261-268.
85. Zug GR, Balazs GH, Wetherall JA, Parker DM, Murakawa SKK (2002) Age and growth of Hawaiian green sea turtles (Chelonia mydas): an analysis based on skeletochronology. Fish Bull 100: 117-127.
86. Zug GR, Chaloupka M, Balazs GH (2006) Age and growth in olive ridley sea turtles (Lepidochelys olivacea) from the North-central Pacific: a skeletochronological analysis. Mar Ecol 27: 263-270. doi: 10. 1111/j. 1439-0485. 2006. 00109. x.