Marine Biology

, 163:122 | Cite as

Potential bycatch impact on distinct sea turtle populations is dependent on fishing ground rather than gear type in the Mediterranean Sea

  • Marcel Clusa
  • Carlos Carreras
  • Marta Pascual
  • Stephen J. Gaughran
  • Susanna Piovano
  • Diego Avolio
  • Gepi Ollano
  • Gloria Fernández
  • Jesús Tomás
  • Juan Antonio Raga
  • Alex Aguilar
  • Luis Cardona
Feature Article

Abstract

Bycatch is one of the main threats affecting marine megafauna worldwide, not only because of its prevalence, but also because the impact of high levels of bycatch in small oceanic regions may spread over whole oceans due to the complex dispersal patterns of bycaught species. Here, we use intrinsic and genetic markers to understand the impact of bycatch on the Atlantic and Mediterranean populations of the loggerhead turtle sharing the same foraging grounds in the western Mediterranean Sea. Turtles of Atlantic origin settle on the continental shelf later and at a larger size than turtles of Mediterranean origin and hence have been suggested to be more vulnerable to pelagic fishing gears, whereas those of Mediterranean origin would be more vulnerable to neritic ones. To assess whether this hypothesis holds true, we compared the genetic make-up of turtle bycatch from drifting longlines and bottom trawl/trammel nets in three different regions (eastern mainland Spain, southern Balearic Islands and southern Italy). A total of 176 incidentally caught turtles were considered, and size and habitat use, as revealed by stable isotopes, were incorporated to the analysis. No genetic, size or isotopic differences were found between turtles caught with drifting longlines and bottom trawl/trammel nets within any of the three regions. However, genetic, size and isotopic differences were detected among regions, regardless of the fishing gear. Thus, the population make-up of loggerhead bycatch depends on the area where the fishing operations are conducted, but not on the fishing gear used. Accordingly, the actual impact of loggerhead bycatch in the Mediterranean Sea will depend not only on the total number of turtles taken, but also on the geographic distribution of the fishing effort.

Supplementary material

227_2016_2875_MOESM1_ESM.pdf (217 kb)
Supplementary material 1 (PDF 217 kb)

References

  1. Abreu-Grobois A, Horrocks J, Formia A, Dutton P, 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 capacity of mixed stock analysis. In: Proceedings of the Annual Symposium on Sea Turtle Biology Conservation p 179Google Scholar
  2. 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 67:677–685CrossRefGoogle Scholar
  3. Álvarez de Quevedo I, San Félix M, Cardona L (2013) Mortality rates in by-caught loggerhead turtle Caretta caretta in the Mediterranean Sea and implications for the Atlantic populations. Mar Ecol Prog Ser 489:225–234CrossRefGoogle Scholar
  4. Álvarez de Quevedo I, San Félix M, Cardona L (2014) Temporal trends in the by-catch of loggerhead turtles Caretta caretta in the Mediterranean Sea: replay to Báez et al. Mar Ecol Prog Ser 504:303–304CrossRefGoogle Scholar
  5. Anderson JJ, Gurarie E, Bracis C, Burke BJ, Laidre KL (2013) Modeling climate change impacts on phenology and population dynamics of migratory marine species. Ecol Model 264:83–97CrossRefGoogle Scholar
  6. Arrington DA, Winemiller KO (2002) Preservation effects on stable isotope analysis of fish muscle. Trans Am Fish Soc 131:337–342CrossRefGoogle Scholar
  7. Bache SJ (2003) Bycatch mitigation tools: selecting fisheries, setting limits, and modifying gear. Ocean Coast Manag 46:103–125CrossRefGoogle Scholar
  8. Báez JC, García Barcelona S, Real R, Macías D et al (2014) Estimating by-catch of loggerhead turtles in the Mediterranean: comment on Álvarez de Quevedo et al. Mar Ecol Prog Ser 504:301–302CrossRefGoogle Scholar
  9. Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R (2015) RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol Ecol 24:3299–3315CrossRefGoogle Scholar
  10. Bentivegna F (2002) Intra-mediterranean migration of loggerhead sea turtles monitored by satellite telemetry. Mar Biol 141:795–800CrossRefGoogle Scholar
  11. 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 turtle. Smithsonian Books, Washington, pp 63–78Google Scholar
  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. Glob Biogeochem Cycles 18:1005CrossRefGoogle Scholar
  13. Bowen BW, Abreu-Grobois FA, Balazs GH, Kamezaki N, Limpus CJ, Ferl RJ (1995) Trans-Pacific migrations of the loggerhead turtle (Caretta caretta) demonstrated with mitochondrial DNA markers. PNAS 92:3731–3734CrossRefGoogle Scholar
  14. Bowen BW, Bass AL, Soares L, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol Ecol 14:2389–2402CrossRefGoogle Scholar
  15. Cardona L, Revelles M, Carreras C, San Félix 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
  16. 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 149:1269–1279CrossRefGoogle Scholar
  17. 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 8:761–775CrossRefGoogle Scholar
  18. 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 102:666–677CrossRefGoogle Scholar
  19. Casale P (2011) Sea turtle by-catch in the Mediterranean. Fish Fish 12:299–316CrossRefGoogle 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 119:287–295CrossRefGoogle Scholar
  21. Casale P, Abbate G, Freggi D, Conte N, Oliveiro 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
  22. Clusa M, Carreras C, Pascual M, Demetropoulos A, Margaritoulis D, Rees AF, Hamza AA, Khalil M, Aureggi M, Levy Y, Türkozan 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 439:15–24CrossRefGoogle Scholar
  23. Clusa M, Carreras C, Pascual M, Gaughran SJ, Piovano S, Giacoma C, Fernández G, Levy Y, Tomás J, Raga JA, Maffucci F, Hochscheid S, Aguilar A, Cardona L (2014) Fine-scale distribution of juvenile Atlantic and Mediterranean loggerhead turtles (Caretta caretta) in the Mediterranean Sea. Mar Biol 161:509–519CrossRefGoogle Scholar
  24. Deflorio M, Aprea A, Corriero A, Santamaria N, De Metrio G (2005) Incidental captures of sea turtles by swordfish and albacore longlines in the Ionian Sea. Fish Sci 71:1010–1018CrossRefGoogle Scholar
  25. Domènech F, Álvarez de Quevedo I, Merchán M, Revuelta O, Vélez-Rubio G, Bitón S, Cardona L, Tomás J (2014) Incidental catch of marine turtles by Spanish bottom trawlers in the western Mediterranean. Aquat Conserv. doi:10.1002/aqc.2463 Google Scholar
  26. Dutton PH, Roden SE, Stewart KR, LaCasella E, Tiwari M, Formia A, Thomé JC, Livingstone SR, Eckert S, Chacon-Chaverri D, Rivalan P, Allman P (2013) Population stock structure of leatherback turtles (Dermochelys coriacea) in the Atlantic revealed using mtDNA and microsatellite markers. Conserv Genet 14:625–636CrossRefGoogle Scholar
  27. Eder E, Ceballos A, Martins S, Pérez-García H, Marín I, Marco A, Cardona L (2012) Foraging dichotomy in loggerhead sea turtles Caretta caretta off northwestern Africa. Mar Ecol Prog Ser 470:113–122CrossRefGoogle Scholar
  28. Edwards SV, Silva MC, Friesen VL, Warheit KI (2001) Molecular genetic markers in the analysis of seabird bycatch populations. In: Melvin E, Parrish J (eds) Seabird bycatch: trends roadblocks and solutions. University of Alaska Sea Grant, Anchorage, pp 115–140CrossRefGoogle Scholar
  29. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567CrossRefGoogle Scholar
  30. FitzSimmons NN, Moritz C, Moore SS (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol Biol Evol 12:432–440Google Scholar
  31. FitzSimmons NN, Moritz C, Limpus CJ, Miller JD, Parmenter CJ, Prince RI (1996) Comparative genetic structure of green, loggerhead, and flatback population 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 Technical Memorandum NMFS-SEFSC-396, pp 25–32Google Scholar
  32. García-Párraga D, Crespo-Picazo JL, Bernaldo de Quirós Y, Cervera V, Martí-Bonmati L, Díaz-Delgado J, Arbelo M, Moore MJ, Jepson PD, Fernández A (2014) Decompression sickness (‘the bends’) in sea turtles. Dis Aquat Org 111:191–205CrossRefGoogle Scholar
  33. Garofalo L, Mastrogiacomo A, Casale P, Carlini R, Eleni C, Freggi D, Gelli D, Knittweis L, Mifsud C, Mingozzi T, Novarini N, Scaravelli D, Scillitani G, Oliveiro M, Novelleto A (2013) Genetic characterization of central Mediterranean stocks of the loggerhead turtle (Caretta caretta) using mitochondrial and nuclear markers, and conservation implications. Aquat Conserv 23:868–884CrossRefGoogle Scholar
  34. Gómez-Díaz E, González-Solís J (2007) Geographic assignment of seabirds to their origin: combining morphologic, genetic, and biogeochemical analyses. Ecol Appl 17:1484–1498CrossRefGoogle Scholar
  35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  36. Hamann M, Godfrey MH, Seminoff JA, Arthur K, Barata PCR, Bjorndal KA, Bolten A, Broderick AC, Campbell LM, Carreras C, Dutton PH, Epperly S, Fitzsimmons NN, Formia A, Girondot M, Hays GC, Jiunn CI, Kaska Y, Lewison R, Mortimer JA, Nichols WJ, Reina RD, Shanker K, Spotila JR, Tomás J, Wallace BP, Work TM, Zbinden JA, Godley BJ (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11:245–269CrossRefGoogle Scholar
  37. Heppell SS, Crowder LB, Menzel TR (1999) Life table analysis of long-lived marine species, with implications for conservation and management. In: Musick JA (ed) Life in the slow lane: ecology and conservation of long-lived marine animals. American Fisheries Society Symposium 23, Bethesda, pp 137–148Google Scholar
  38. Jribi I, Echwikhi Bradai MN, Bouain A (2008) Incidental capture of sea turtles by longlines in the Gulf of Gabès (South Tunisia): a comparative study between bottom and surface longlines. Sci Mar 72:337–342CrossRefGoogle Scholar
  39. 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, Hadjichristophorou M, Kornaraky L, Demirayak F, Gautier CH (1998) Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol Ecol 7:1529–1542CrossRefGoogle Scholar
  40. Lazar B, Tvrtkovic N (1995) Marine turtles in the eastern part of the Adriatic Sea: preliminary research. Natura Croat 4:59–74Google Scholar
  41. Lewison RL, Crowder LB (2007) Putting longline bycatch of sea turtles into perspective. Conserv Biol 21:79–86CrossRefGoogle Scholar
  42. Lewison RL, Crowder LB, Read AJ, Freeman SA (2004) Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol Evol 19:598–604CrossRefGoogle Scholar
  43. Logan JM, Lutcavage ME (2008) A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems. Rapid Commun Mass Spectrom 22:1081–1086CrossRefGoogle Scholar
  44. Maffucci F, Kooistra WHCF, Bentivegna F (2006) Natal origin of loggerhead turtles, Caretta caretta, in the neritic habitat off the Italian coasts, Central Mediterranean. Biol Conserv 127:183–189CrossRefGoogle Scholar
  45. Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142CrossRefGoogle Scholar
  46. Margaritoulis D, Argano R, Baran I, Bentivegna F, Bradai MN, Camiñas JA, Casale P, De Metrio G, Demetropoulos A, Gerosa G, Godley BJ, Haddoud DA, Houghton J, Laurent L, Lazar B (2003) Loggerhead turtles in the Mediterranean Sea: present knowledge and conservation perspectives. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtle. Smithsonian Books, Washington, pp 175–198Google Scholar
  47. Miller GA, Chapman JP (2001) Misunderstanding analysis of covariance. J Abnorm Psychol 110:40–48CrossRefGoogle Scholar
  48. Millot C (1999) Circulation in the Western Mediterranean Sea. J Mar Sys 20:423–442CrossRefGoogle Scholar
  49. Monzón-Argüello C, Muñoz J, Marco López-Jurado LF, Rico C (2008) Twelve new polymorphic microsatellite markers from the loggerhead sea turtle (Caretta caretta) and cross-species amplification on other marine turtle species. Conserv Genet 9:1045–1049CrossRefGoogle Scholar
  50. Moore MK, Ball RM Jr (2002) Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis. Mol Ecol 11:281–288CrossRefGoogle Scholar
  51. Naro-Maciel E, Reid BN, Alter E, Amato G, Bjorndal KA, Bolten AB, Martin M, Nairn CJ, Shamblin B, Pineda-Catalan O (2014) From refugia to rookeries: Phylogeography of Atlantic green turtles. J Exp Mar Biol Ecol 461:306–316CrossRefGoogle Scholar
  52. Navarro J, Coll M, Louzao M, Palomera I, Delgado A, Forero MG (2011) Comparison of ecosystem modelling and isotopic approach as ecological tools to investigate food webs in the NW Mediterranean Sea. J Exp Mar Biol Ecol 401:97–104CrossRefGoogle Scholar
  53. Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol Ecol 3:363–373CrossRefGoogle Scholar
  54. Oruç A (2001) Trawl fisheries in the eastern Mediterranean and their impact on marine turtles. Zool Middle East 24:119–125CrossRefGoogle Scholar
  55. Pantoja S, Repeta DJ, Sachs JP, Sigman DM (2002) Stable isotope constraints on the nitrogen cycle of the Mediterranean Sea water column. Deep Sea Res Part I 49:1609–1621CrossRefGoogle Scholar
  56. Pauly D, Watson R, Alder J (2005) Global trends in world fisheries: impacts on marine ecosystems and food security. Philos T Roy Soc B 360:5–12CrossRefGoogle Scholar
  57. Pinnegar JK, Polunin NVC (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122:399–409CrossRefGoogle Scholar
  58. Piovano S, Clusa M, Carreras C, Giacoma C, Pascual M, Cardona L (2011) Different growth rates between loggerhead sea turtles (Caretta caretta) of Mediterranean and Atlantic origin in the Mediterranean Sea. Mar Biol 158:2577–2587CrossRefGoogle Scholar
  59. Plotkin PT (2003) Adult migrations and habitat use. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles II. CRC Press, Boca Ratón, pp 225–241Google Scholar
  60. Pritchard JK, Stephens M, Donelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  61. Reich KJ, Bjorndal KA, Martínez del Rio C (2008) Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155:651–663CrossRefGoogle Scholar
  62. 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 (2007a) Evidence for an asymmetrical size exchange of loggerhead sea turtles between the Mediterranean and the Atlantic trough the Straits of Gibraltar. J Exp Mar Biol Ecol 349:261–271CrossRefGoogle Scholar
  63. Revelles M, Isern-Fontanet J, Cardona L, San Félix M, Carreras C, Aguilar A (2007b) Mesoscale eddies, surface circulation and the scale of habitat selection by immature loggerhead sea turtles. J Exp Mar Biol Ecol 347:41–57CrossRefGoogle Scholar
  64. Revelles M, Camiñas JA, Cardona L, Parga ML, Tomás J, Aguila A, Alegre F, Raga A, Bertolero A, Oliver G (2008) Tagging reveals limited exchange of immature loggerhead sea turtles (Caretta caretta) between regions in the western Mediterranean. Sci Mar 72:511–518CrossRefGoogle Scholar
  65. Robins CM, Goodspeed AM, Poiner I, Harch BD (2002) Monitoring the catch of turtles in the northern prawn fishery. Fisheries Research and Development Corporation Final Report. Department of Agriculture, Fisheries and Forestry, CanberraGoogle Scholar
  66. Saied A, Maffucci F, Hochscheid S, Dryag S, Swayeb B, Borra M, Oureghi A, Procaccini G, Bentivegna F (2012) Loggerhead turtles nesting in Libya: an important management unit for the Mediterranean stock. Mar Ecol Prog Ser 450:207–218CrossRefGoogle Scholar
  67. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33CrossRefGoogle Scholar
  68. Sequeira AMM, Mellin C, Meekan MG, Sims DW, Bradshaw CJA (2013) Inferred global connectivity of whale shark Rhincodon typus populations. J Fish Biol 82:367–389CrossRefGoogle Scholar
  69. Shamblin BM, Bolten AB, Abreu-Grobois FA, Bjorndal KA, Cardona L, Carreras C, Clusa M, Monzón-Argüello C, Nairn CJ, Nielsen JT, Nel R, Soares LS, Stewart KR, Vilaça ST, Türkozan O, Yilmaz C, Dutton PH (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:e85956CrossRefGoogle Scholar
  70. Turtle Expert Working Group (2009) An assessment of the loggerhead turtle population in the western north Atlantic Ocean. NOAA Tech Mem NMFS-SEFSC 575:1–131Google Scholar
  71. Valenzuela LO, Sironi M, Rowntree VJ, Seger J (2009) Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis). Mol Ecol 18:782–791CrossRefGoogle Scholar
  72. Wallace BP, Kot CY, DiMatteo AD, Lee T, Crowder LB, Lewison RL (2013) Impacts of fisheries bycatch on marine turtle populations worldwide: toward conservation and research priorities. Ecosphere 4: Article 40Google Scholar
  73. Watanabe KK, Hatase H, Kinoshita M, Omuta K, Bando T, Kamezaki N, Sato K, Matsuzawa Y, Goto K, Nakashima Y, Takeshita H, Aoyama J, Tsukamoto K (2011) Population structure of the loggerhead turtle Caretta caretta, a large marine carnivore that exhibits alternative foraging behaviors. Mar Ecol Prog Ser 424:273–283CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Marcel Clusa
    • 1
  • Carlos Carreras
    • 2
    • 3
  • Marta Pascual
    • 2
  • Stephen J. Gaughran
    • 4
    • 1
  • Susanna Piovano
    • 5
    • 6
  • Diego Avolio
    • 7
  • Gepi Ollano
    • 8
  • Gloria Fernández
    • 9
  • Jesús Tomás
    • 10
  • Juan Antonio Raga
    • 10
  • Alex Aguilar
    • 1
  • Luis Cardona
    • 1
  1. 1.Department of Animal Biology and IRBioUniversity of BarcelonaBarcelonaSpain
  2. 2.Department of Genetics and IRBioUniversity of BarcelonaBarcelonaSpain
  3. 3.Centre for Ecology and Conservation, Penryn CampusUniversity of ExeterPenrynUK
  4. 4.Sackler Institute for Comparative GenomicsAmerican Museum of Natural HistoryNew YorkUSA
  5. 5.Department of Life Sciences and Systems BiologyUniversity of TorinoTurinItaly
  6. 6.School of Biological and Chemical Sciences, Laucala CampusUniversity of the South PacificSuvaFiji
  7. 7.Sea Turtle Rescue Centre CTSBrancaleoneItaly
  8. 8.Cetaceans and Sea Turtles Rescue Centre Laguna di NoraNora, PulaItaly
  9. 9.Fundación Aspro NaturaCalviàSpain
  10. 10.Cavanilles Institute of Biodiversity and Evolutionary BiologyUniversity of ValenciaValenciaSpain

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