Marine Biology

, 165:4 | Cite as

Large-scale movements in the oceanic environment identify important foraging areas for loggerheads in central Mediterranean Sea

  • Paolo Luschi
  • Resi Mencacci
  • Giulia Cerritelli
  • Luana Papetti
  • Sandra Hochscheid
Original paper
  • 261 Downloads

Abstract

Loggerhead sea turtles (Caretta caretta) are known to display a wide range of movement patterns during the different stages of their life cycle, but empirical information to document this extensive behavioural plasticity is still limited. This is especially true for large, adult-sized individuals, that are thought to mainly forage in neritic areas. In the present paper, eight adult-sized loggerhead turtles were tracked using satellite telemetry to identify the location of their foraging grounds in the seas along the western coast of the Italian peninsula. Tracked turtles mostly stayed in the region between the Italian peninsula and the islands of Sicily and Sardinia, that was reached following quick, directed movements by the turtles from a release site to the north. In this area, two turtles took up residence in spatially limited neritic sites along the coast, while the remaining six alternated circumscribed coastal stays with long-distance, circuitous movements in the oceanic environment. An utilization distribution analysis clearly identified an area, mostly comprising oceanic waters, that was continuously used by turtles in different seasons and years. The present results contribute to the still-limited knowledge of the spatial ecology of loggerheads frequenting the Western Mediterranean Sea and highlight the presence of a potentially important oceanic region in the Southern Tyrrhenian Sea where adult-sized turtles forage for extended periods. These findings increase our knowledge of complex life history traits of loggerhead turtles and provide important information to be considered for evidence-based conservation measures.

Notes

Acknowledgements

The authors are grateful to Mariapia Ciampa, Gianluca Treglia, Fulvio Maffucci and the staff of Punta Campanella Marine Protected Area, TartAmare and A.D. Club Subacqueo Grossetano (Grosseto) for their help in the recovery and releases of tracked turtles. Funds were obtained from SZN, University of Pisa (Progetti di Ricerca di Ateneo, Grant #PRA_2016_1) and Regione Toscana (Bando Go-Green Mare 2014). One satellite tag was purchased from a Grant to G. C. Hays from the Natural Environment Research Council of the U.K. (NERC, Grant NER/A/S/2003/00302).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Transmitter deployments were authorised by the Italian Ministry of Environment (Prot. nos. 002451/PNM, DPN-2010-0000872, 0042848/PNM 09 and DP-2009-0023740).

Supplementary material

227_2017_3255_MOESM1_ESM.pdf (612 kb)
Supplementary material 1 (PDF 612 kb)

References

  1. Arendt MD, Segars AL, Byrd JI, Boynton J, Whitaker JD, Parker L, Owens DW, Blanvillain G, Quattro JM, Roberts MA (2012a) Seasonal distribution patterns of juvenile loggerhead sea turtles (Caretta caretta) following capture from a shipping. Mar Biol 159:127–139CrossRefGoogle Scholar
  2. Arendt MD, Segars AL, Byrd JI, Boynton J, Schwenter JA, Whitaker JD, Parker L (2012b) Migration, distribution, and diving behavior of adult male loggerhead sea turtles (Caretta caretta) following dispersal from a major breeding aggregation in the Western North Atlantic. Mar Biol 159:113–125CrossRefGoogle Scholar
  3. Barcelo C, Domingo A, Miller P, Ortega L, Giffoni B, Sales G, McNaughton L, Marcovaldi MA, Heppell S, Swimmer Y (2013) High use areas, seasonal movements and dive patterns of juvenile loggerhead sea turtles in the Southwestern Atlantic Ocean. Mar Ecol Prog Ser 479:235–250CrossRefGoogle Scholar
  4. Bentivegna F (2002) Intra-Mediterranean migrations of loggerhead sea turtles (Caretta caretta) monitored by satellite telemetry. Mar Biol 141:795–800CrossRefGoogle Scholar
  5. Bolten AB (2003) Active swimmers—passive drifters: the oceanic juvenile stage of loggerheads in the Atlantic System. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution, Washington, pp 63–78Google Scholar
  6. Broderick AC, Coyne M, Fuller WJ, Glen F, Godley BJ (2007) Fidelity and over-wintering of sea turtles. Proc R Soc Lond B 274:1533–1538CrossRefGoogle Scholar
  7. Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519CrossRefGoogle Scholar
  8. Cardona L, Revelles M, Carreras C, San Felix 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 147:583–591CrossRefGoogle Scholar
  9. Cardona L, Revelles M, Parga M, Tomas J, Aguilar 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 156:2621–2630CrossRefGoogle Scholar
  10. Cardona L, Fernandez G, Revelles M, Aguilar A (2012) Readaptation to the wild of rehabilitated loggerhead sea turtles (Caretta caretta) assessed by satellite telemetry. Aquat Conserv 22:104–112CrossRefGoogle Scholar
  11. Casale P (2011) Sea turtle by-catch in the Mediterranean. Fish Fish 12(3):299–316CrossRefGoogle Scholar
  12. Casale P, Margaritoulis D (2010) Sea turtles in the Mediterranean: distribution, threats and conservation priorities. IUCN, GlandGoogle Scholar
  13. 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
  14. Casale P, Abbate G, Freggi D, Conte N, Oliverio M, Argano R (2008) Foraging ecology of loggerhead sea turtles Caretta caretta in the central Mediterranean Sea: evidence for a relaxed life history model. Mar Ecol Prog Ser 372:265–276CrossRefGoogle Scholar
  15. Casale P, Affronte M, Insacco G, Freggi D, Vallini C, D’Astore PP, Basso R, Paolillo G, Abbate G, Argano R (2010) Sea turtle strandings reveal high anthropogenic mortality in Italian waters. Aquat Conserv 20:611–620CrossRefGoogle Scholar
  16. Casale P, Mazaris AD, Freggi D (2011) Estimation of age at maturity of loggerhead sea turtles Caretta caretta in the Mediterranean using length-frequency data. Endang Species Res 13:123–129CrossRefGoogle Scholar
  17. Casale P, Affronte M, Scaravelli D, Lazar B, Vallini C, Luschi P (2012a) Foraging grounds, movement patterns and habitat connectivity of juvenile loggerhead turtles (Caretta caretta) tracked from the Adriatic Sea. Mar Biol 159:1527–1535CrossRefGoogle Scholar
  18. Casale P, Broderick AC, Freggi D, Mencacci R, Fuller WJ, Gadley BJ, Luschi P (2012b) Long-term residence of juvenile loggerhead turtles to foraging grounds: a potential conservation hotspot in the Mediterranean. Aquatic Conserv 22:144–154CrossRefGoogle Scholar
  19. Casale P, Freggi D, Cinà A, Rocco M (2013) Spatio-temporal distribution and migration of adult male loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea: further evidence of the importance of neritic habitats off North Africa. Mar Biol 160:703–718CrossRefGoogle Scholar
  20. Coll M, Piroddi C, Alboui C, Ben Rais Lasram F, Cheung WWL, Christensen V, Karpouzi VS, Guilhaumon F, Mouillo 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 21:465–480CrossRefGoogle Scholar
  21. Coyne MS, Godley BJ (2005) Satellite Tracking and Analysis Tool (STAT): an integrated system for archiving, analyzing and mapping animal tracking data. Mar Ecol Prog Ser 301:1–7CrossRefGoogle Scholar
  22. Dalleau M, Benhamou S, Sudre J, Ciccione S, Bourjea J (2014) The spatial ecology of juvenile loggerhead turtles (Caretta caretta) in the Indian Ocean sheds light on the “lost years” mystery. Mar Biol 161:1835–1849CrossRefGoogle Scholar
  23. Dujon AM, Schofield G, Lester RE, Esteban N, Hays GC (2017) Fastloc-GPS reveals the timing of departure and arrival during sea turtle migration and speed of travel patterns. Mar Biol.  https://doi.org/10.1007/s00227-017-3216-8 Google Scholar
  24. 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 18:290–308CrossRefGoogle Scholar
  25. Ehrhart LM, Ogren LH (1999) Studies in foraging habitats: capturing and handling 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 1–4Google Scholar
  26. Fiori C, Paolo C, Alessi J, Mandich A, Vassallo P (2016) Seamount attractiveness to top predators in the southern Tyrrhenian Sea (central Mediterranean). J Mar Biol Assoc UK 96:769–775Google Scholar
  27. Foley AM, Schroeder BA, Hardy R, MacPherson SL, Nicholas M, Coyne MS (2013) Postnesting migratory behavior of loggerhead sea turtles Caretta caretta from three Florida rookeries. Endang Species Res 21:129–142CrossRefGoogle Scholar
  28. Fossette S, Witt MJ, Miller P, Nalovic MA, Albareda D, Almeida AP, Broderick AC, Chacon-Chaverri D, Coyne MS, Domingo A, Eckert S, Evans D, Fallabrino A, Ferraroli S, Formia A, Giffoni B, Hays GC, Hughes G, Kelle L, Leslie A, Lopez-Mendilaharsu M, Luschi P, Prosdocimi L, Rodriguez-Heredia S, Turny A, Vehage S, Godley BJ (2014) Pan-Atlantic analysis of the overlap of a highly migratory species, the leatherback turtle, with pelagic longline fisheries. Proc R Soc Lond B 281:20133065CrossRefGoogle Scholar
  29. Godley BJ, Blumenthal JM, Broderick AC, Coyne M, Godfrey MH, Hawkes LA, Witt MJ (2008) Satellite tracking of sea turtles: where have we been and where do we go next? Endang Species Res 4:3–22CrossRefGoogle Scholar
  30. Hart KM, Sartain AR, Fujisaki I (2015) Bahamas connection: residence areas selected by breeding female loggerheads tagged in Dry Tortugas National Park, USA. Anim Biotelem 3:3CrossRefGoogle Scholar
  31. Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002) Size-related differences in feeding habitat use of adult female loggerheads Caretta caretta around Japan determined by stable isotope analyses and satellite telemetry. Mar Ecol Prog Ser 233:273–281CrossRefGoogle Scholar
  32. Hawkes LA, Broderick AC, Coyne M, Godfrey MH, Lopez-Jurado L-F, Lopez-Suarez P, Merino SE, Varo-Cruz N, Godley BJ (2006) Phenotipically linked dichotomy in sea turtle foraging requires multiple conservation approaches. Curr Biol 16:990–995CrossRefGoogle Scholar
  33. Hawkes LA, Witt MJ, Broderick AC, Coker JW, Coyne M, Dodd CK, Frick MG, Godfrey MH, Griffin DB, Murphy SR, Murphy TM, Williams KL, Godley BJ (2011) Home on the range: spatial ecology of loggerhead turtles in Atlantic waters of the USA. Divers Distrib 17:624–640CrossRefGoogle Scholar
  34. Hochscheid S, Bentivegna F, Bradai MN, Hays GC (2007) Overwintering behaviour in sea turtles: dormancy is optional. Mar Ecol Prog Ser 340:287–298CrossRefGoogle Scholar
  35. Hochscheid S, Bentivegna F, Hamza A, Hays GC (2010) When surfacers do not dive: multiple significance of extended surface times in marine turtles. J Exp Biol 213:1328–1337CrossRefGoogle Scholar
  36. Howell E, Dutton DL, Polovina JJ, Bailey H, Parker D, Balazs GH (2010) Oceanographic influences on the dive behavior of juvenile loggerhead turtles (Caretta caretta) in the North Pacific Ocean. Mar Biol 157:1011–1026CrossRefGoogle Scholar
  37. Kobayashi DR, Polovina JJ, Parker D, Kamezaki N, Cheng IJ, Uchida I, Dutton PH, Balazs GH (2008) Pelagic habitat characterization of loggerhead sea turtles, Caretta caretta, in the North Pacific Ocean (1997–2006): insight from satellite tag tracking and remotely sensed data. J Exp Mar Biol Ecol 356:96–114CrossRefGoogle Scholar
  38. Kobayashi DR, Cheng IJ, Parker DM, Polovina JJ, Kamezaki N, Balazs GH (2011) Loggerhead turtle (Caretta caretta) movement off the coast of Taiwan: characterization of a hotspot in the East China Sea and investigation of mesoscale eddies. ICES J Mar Sci 68:707–718CrossRefGoogle Scholar
  39. Lambardi P, Lutjeharms JRE, Mencacci R, Hays GC, Luschi P (2008) Influence of ocean currents on long-distance movement of leatherback sea turtles in the Southwest Indian Ocean. Mar Ecol Prog Ser 353:289–301CrossRefGoogle Scholar
  40. Lauriano G, Panigada S, Casale P, Pierantonio N, Donovan GP (2011) Aerial survey abundance estimates of the loggerhead sea turtle Caretta caretta in the Pelagos Sanctuary, northwestern Mediterranean Sea. Mar Ecol Prog Ser 437:291–302CrossRefGoogle Scholar
  41. Limpus CJ (1993) The green turtle, Chelonia mydas, in Queensland: breeding males in the southern Great Barrier Reef. Wildl Res 20:513–523CrossRefGoogle Scholar
  42. Luschi P, Casale P (2014) Movement patterns of marine turtles in the Mediterranean Sea: a review. Ital J Zool 81:478–495CrossRefGoogle Scholar
  43. Luschi P, Mencacci R, Vallini C, Ligas A, Lambardi P, Benvenuti S (2013) Long-term tracking of adult loggerhead turtles (Caretta caretta) in the Mediterranean Sea. J Herpetol 47:227–231CrossRefGoogle Scholar
  44. Marcovaldi MA, Lopez GG, Soares LS, Lima EHS, Thomé JCA, Almeida AP (2010) Satellite-tracking of female loggerhead turtles highlights fidelity behavior in northeastern Brazil. Endang Species Res 12:263–272CrossRefGoogle Scholar
  45. Margaritoulis D, Argano R, Baran I, Bentivegna F, Bradai MN, Caminas JA, Casale P, De Metrio G, Demetropoulos A, Gerosa G, Godley BJ, Haddoud DA, Houghton J, Laurent L, Lazar B (2003) Loggerhead turtles in Mediterranean Sea: present knowledge and conservation perspectives. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Books, Washington, pp 175–198Google Scholar
  46. Mazaris AD, Almpanidou V, Wallace B, Schofield G (2014) A global gap analysis of sea turtle protection coverage. Biol Conserv 173:17–23CrossRefGoogle Scholar
  47. McClellan CM, Read AJ (2007) Complexity and variation in loggerhead sea turtle life history. Biol Lett 3:592–594CrossRefGoogle Scholar
  48. Mencacci R, Ligas A, Meschini P, Luschi P (2011) Movements of three loggerhead sea turtles in Tuscany waters. Atti Soc Tosc Sci Nat Mem Serie B 118:117–120Google Scholar
  49. Mingozzi T, Mencacci R, Cerritelli G, Giunchi D, Luschi P (2016) Living between widely separated areas: long-term monitoring of Mediterranean loggerhead turtles sheds light on cryptic aspects of females spatial ecology. J Exp Mar Biol Ecol 485:8–17CrossRefGoogle Scholar
  50. Morato T, Hole SD, Allain V, Nicol S (2010) Seamounts are hotspots of pelagic biodiversity in the open ocean. Proc Natl Acad Sci USA 107:9707–9711CrossRefGoogle Scholar
  51. Musick JA, Limpus CJ (1997) Habitat utilization and migration in juvenile sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 137–164Google Scholar
  52. Pikesley SK, Broderick AC, Cejudo D, Coyne MS, Godfrey MH, Godley BJ, Lopez P, Lopez-Jurado L-F, Merino SE, Varo-Cruz N, Witt MJ, Hawkes LA (2015) Modelling the niche for a marine vertebrate: a case study incorporating behavioural plasticity, proximate threats and climate change. Ecography 38:803–812CrossRefGoogle Scholar
  53. Polovina JJ, Uchida I, Balazs G, Howell EA, Parker D, Dutton P (2006) The Kuroshio Extension Bifurcation Region: a pelagic hotspot for juvenile loggerhead sea turtles. Deep-Sea Res II 53:326–339CrossRefGoogle Scholar
  54. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, AustriaGoogle Scholar
  55. Rees AF, Hafez AA, Lloyd JR, Papathanasopoulou N, Godley BJ (2013) Green turtles, Chelonia mydas, in Kuwait: nesting and movements. Chelonian Conserv Biol 12:157–163CrossRefGoogle Scholar
  56. Revelles M, Isern-Fontanet J, Cardona L, San Felix M, Carreras C, Aguilar A (2007a) Mesoscale eddies, surface circulation and the scale of habitat selection by immature loggerhead sea turtles. J Exp Mar Biol Ecol 347:41–57CrossRefGoogle Scholar
  57. Revelles M, Cardona L, Aguilar A, San Felix M, Fernandez G (2007b) Habitat use by immature loggerhead sea turtles in the Algerian Basin (western Mediterranean): swimming behaviour, seasonality and dispersal pattern. Mar Biol 151:1501–1515CrossRefGoogle Scholar
  58. Robinson DP, Jabado RW, Rohner CA, Pierce SJ, Hyland KP, Baverstock WR (2017) Satellite tagging of rehabilitated green sea turtles Chelonia mydas from the United Arab Emirates, including the longest tracked journey for the species. PLoS One 12(9):e0184286CrossRefGoogle Scholar
  59. Rovere M, Bo M, Alessi J, Paoli C, Villani N, Vassallo P, Fiori C, Roccatagliata N (2015) Seamounts and seamount-like structures of the Tyrrhenian Sea. In: Würtz M, Rovere M (eds) Atlas of the Mediterranean Seamounts and seamount-like structures. IUCN, Gland, pp 111–186Google Scholar
  60. Schofield G, Bishop CM, Katselidis KA, Dimopoulos P, Pantis JD, Hays GC (2009) Microhabitat selection by sea turtles in a dynamic thermal marine environment. J Anim Ecol 78:14–21CrossRefGoogle Scholar
  61. Schofield G, Hobson VJ, Fossette S, Lilley MKS, Katselidis KA, Hays GC (2010) Fidelity to foraging sites, consistency of migration routes and habitat modulation of home range by sea turtles. Divers Distrib 16:840–853CrossRefGoogle Scholar
  62. Schofield G, Dimadi A, Fossette S, Katselidis KA, Koutsoubas D, Lilley MKS, Luckman A, Pantis JD, Karagouni AD, Hays GC (2013) Satellite tracking large numbers of individuals to infer population level dispersal and core areas for the protection of an endangered species. Divers Distrib 19:834–844CrossRefGoogle Scholar
  63. Seaman DE, Powell RA (1990) Identifying patterns and intensity of home range use. Int Conf Bear Res Manage 8:243–249Google Scholar
  64. van Dam RP, Diez CE, Balazs GH, Colon Colon LA, McMillan WO, Schroeder BA (2008) Sex-specific migration patterns of hawksbill turtles breeding at Mona Island, Puerto Rico. Endang Species Res 4:85–94CrossRefGoogle Scholar
  65. Varo-Cruz N, Bermejo JA, Calabuig P, Cejudo D, Godley BJ, Lopez-Jurado L-F, Pikesley SK, Witt MJ, Hawkes LA (2016) New findings about the spatial and temporal use of the Eastern Atlantic Ocean by large juvenile loggerhead turtles. Divers Distrib 22:481–492CrossRefGoogle Scholar
  66. Witt MJ, Åkesson S, Broderick AC, Coyne MS, Ellick J, Formia A, Hays GC, Luschi P, Stroud S, Godley BJ (2010) Assessing accuracy and utility of satellite-tracking data using Argos-linked Fastloc-GPS. Anim Behav 80:571–581CrossRefGoogle Scholar
  67. Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164–168CrossRefGoogle Scholar
  68. 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 153:899–906CrossRefGoogle Scholar
  69. Zbinden JA, Bearhop S, Bradshaw CJ, 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 421:291–302CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of BiologyUniversity of PisaPisaItaly
  2. 2.TartAmare-Centro di educazione ambientale e di didattica sul mareCentro per la conservazione delle tartarughe marineGrossetoItaly
  3. 3.Stazione Zoologica Anton DohrnNaplesItaly

Personalised recommendations