Abstract
Satellite telemetry was used to track inter-nesting, post-nesting, and foraging movements of six green turtles that nested on Bioko Island, Equatorial Guinea at the end of the 2019 nesting season, as well as foraging movements of five green turtles after the 2018 nesting season (n = 11 across two seasons), from the same nesting population. These tracks were fit with a switching state-space model to characterize movements and then analyzed in relation to environmental and anthropogenic factors. Inter-nesting movements of two turtles included separate oceanic loops, in which turtles traveled > 40 km away from nesting beaches. Four complete migrations were observed to two distinct foraging grounds, with two turtles migrating west for an average of 1064 km to the coastal waters of Ghana, and two migrating south for an average of 1563 km to a newly discovered foraging ground in the coastal waters of Angola. All migrations included intermittent foraging at stopover sites, including one period of possible oceanic foraging. Turtles at both foraging grounds maintained distinct core use areas in shallow, near-shore (< 20 km from coast) waters. Spatial and depth data reveal critical habitats for this population throughout inter-nesting, post-nesting, and foraging behaviors. Tracks spanned nine countries, highlighting the need for multi-national cooperation in the development of marine conservation management plans in the area. The long distances covered by these turtles suggests that fisheries bycatch and direct harvest throughout the East Atlantic may impact this population. Additionally, spatial and dive depth data can inform zonal fishing regulations and provide the information needed to modify fishing practices and gear in ways likely to reduce sea turtle bycatch.
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References
Agostinho D, Fielding P, Sowman M, Bergh M (2005) Overview and analysis of socio-economic and fisheries information to promote the management of artisanal fisheries in the BCLME region–Angola. Fisheries, Angola
Amante C, Eakins BW (2009) ETOPO1 1 arc-minute global relief model: procedures, data sources and analysis. US Department of Commerce, National Oceanic and Atmospheric Administration, National Environmental Satellite, Data, and Information Service, National Geophysical Data Center. Marine Geology and Geophysics Division. https//doi.org/10.7289/V5C8276M
Amiteye BT (2002) Distribution and ecology of nesting sea turtles in Ghana. Doctoral dissertation, University of Ghana
Baudouin M, de Thoisy B, Chambault P, Berzins R, Entraygues M, Kelle L, Turny A, Le Maho Y, Chevallier D (2015) Identification of key marine areas for conservation based on satellite tracking of post-nesting migrating green turtles (Chelonia mydas). Biol Conserv 184:36–41
Balazs GH (1996) Procedures to attach a satellite transmitter to the carapace of an adult green turtle, Chelonia mydas. In: Proceedings of the 15th annual symposium on sea turtle biology and conservation, 1996
Bass AL, Epperly SP, Braun-Mcneill J (2006) Green turtle (Chelonia mydas) foraging and nesting aggregations in the Caribbean and Atlantic: impact of currents and behavior on dispersal. J Hered 97:346–354
Belhabib D, Hellebrandt Da Silva D, Allison EH, Zeller D, Pauly D (2016) Filling a blank on the map: 60 years of fisheries in Equatorial Guinea. Fish Manag Ecol 23:119–132. https://doi.org/10.1111/fme.12161
Blumenthal JM, Solomon JL, Bell CD, Austin TJ, Ebanks-Petrie G, Coyne MS, Broderick AC, Godley BJ (2006) Satellite tracking highlights the need for international cooperation in marine turtle management. Endanger Species Res. https://doi.org/10.3354/esr002051
Booth J, Peters JA (1972) Behavioural studies on the green turtle (Chelonia mydas) in the sea. Anim Behav 20(4):808–812
Bowen BW, Meylan AB, Ross JP, Limpus CJ, Balazs GH, Avise JC (1992) Global population structure and natural history of the green turtle (Chelonia mydas) in terms of matriarchal phylogeny. Evolution 46:865–881
Broderick AC, Coyne MS, Fuller WJ, Glen F, Godley BJ (2007) Fidelity and over-wintering of sea turtles. Proc R Soc Lond B Biol Sci 274:1533–1539
Brownfield ME, Charpentier RR, Schenk CJ, Klett TR, Cook TA, and Pollastro RM (2016) Assessment of undiscovered oil and gas resources of the West African Coastal Province, West Africa. Geologic Assessment of Undiscovered Hydrocarbon Resources of Sub-Saharan Africa. In: Digital data series, vol 69. https://doi.org/10.3133/fs20113034
Carr A (1980) Meylan AB (1980) Evidence of passive migration of green turtle hatchlings in Sargassum. Copeia 2:366–368
Carranza A, Domingo A, Estrades A (2006) Pelagic longlines: a threat to sea turtles in the Equatorial Eastern Atlantic. Biol Conserv 131:52–57. https://doi.org/10.1016/j.biocon.2006.02.003
Casale P, Abitsi G, Aboro MP, Agamboue PD, Agbode L, Allela NL, Angueko D, Nguema JN, Boussamba F, Cardiec F, Chartrain E (2017) A first estimate of sea turtle bycatch in the industrial trawling fishery of Gabon. Biodivers Conserv 26:2421–2433
Cheng I-J (2000) Post-nesting migrations of green turtles (Chelonia mydas) at Wan-An Island, Penghu Archipelago, Taiwan. Mar Biol 137:747–754. https://doi.org/10.1007/s002270000375
Cheng I-J (2009) Changes in diving behaviour during the internesting period by green turtles. J Exp Mar Biol Ecol 381:18–24. https://doi.org/10.1016/j.jembe.2009.08.021
Christiansen F, Esteban N, Mortimer JA, Dujon AM, Hays GC (2017) Diel and seasonal patterns in activity and home range size of green turtles on their foraging grounds revealed by extended Fastloc-GPS tracking. Mar Biol 164:10. https://doi.org/10.1007/s00227-016-3048-y
Cynthia L, Fianko JR, Akiti TT, Osei J, Brimah AK, Osae S, Bam EK (2011) Determination of trace elements in the Sakumo wetland sediments. Res J Environ Earth Sci 3:417–421
Dossa JS, Sinsin BA, Mensah GA (2007) Conflicts and social dilemmas associated with the incidental capture of marine turtles by artisanal fishers in Benin. Mar Turtle Newsl 116:10–12
Eisentraut M (1964). Meeresschildkroten an der kuste von Fernando Poo. Cited in Seminoff JA (Southwest Fisheries Science Center, U.S.) (2004) Chelonia mydas. The IUCN red list of threatened species 2004: e.T4615A11037468
Entsua-Mensah M (2002) The contribution of coastal lagoons to the continental shelf ecosystem of Ghana. In: Large marine ecosystems. Elsevier, London, pp 161–169. https://doi.org/10.1016/s1570-0461(02)80035-0
FAO fishery statistical collections 2011. https://www.fao.org/fishery/statistics/globalcapture-production/4/en
FAO (2016-2019) Fishery and aquaculture country profiles. Ghana (2016) country profile fact sheets. In: FAO Fisheries and Aquaculture Department (online), Rome. Updated 2016. https://www.fao.org/fishery/. Accessed 30 Mar 2019
Fitzgerald DB, Ordway E, Honarvar S, Hearn GW (2011) Challenges confronting sea turtle conservation on Bioko Island, Equatorial Guinea. Chelonian Conserv Biol 10:177–180. https://doi.org/10.2744/CCAB-0889.1
Flanders Marine Institute (2014). Union of the ESRI country shapefile and the exclusive economic zones (version 2). https://www.marineregions.org/. Accessed 21 Mar 2019
Formia A, Tiwari M, Fretey J, Billes A (2003) Sea turtle conservation along the Atlantic coast of Africa. Mar Turt Newsl 100:33–37
Formia A, Fallabrinio A, Obama C, Mba Mba J, Villarubia A (2008) The sea turtles of Corisco Bay (Equatorial Guinea, Gabon); threats and conservation potential. In: Rees AF, Fick M, Panagopoulou A, Williams K (comps) Proceedings of the 27th annual symposium on sea turtle biology and conservation. NOAA technical memorandum, NMFSSEFSC-569, p 171
Fretey J (2001) Biogeography and conservation of marine turtles of the Atlantic coast of Africa. United Nations Premises in Bonn
Fretey J (1998) Marine turtles of the Atlantic Coast of Africa. In: Bonn CMS, Gawler M, Agardy T 1994. Developing WWF priorities for marine conservation in Africa & Madagascar Region. WWF Africa & Madagascar Subcommittee and WWF Marine Advisory Group
García-Rodríguez FJ, García-Rodríguez JL, Castilla-Gutiérrez C, Major SA (2013) Corporate social responsibility of oil companies in developing countries: from altruism to business strategy: environmental responsibility of oil companies in developing countries. Corp Soc Respons Environ Manag 20:371–384. https://doi.org/10.1002/csr.1320
Godley BJ, Richardson S, Broderick AC, Coyne MS, Glen F, Hays GC (2002) Long-term satellite telemetry of the movements and habitat utilisation by green turtles in the Mediterranean. Ecography 25:352–362. https://doi.org/10.1034/j.1600-0587.2002.250312.x
Godley BJ, Almeida A, Barbosa C, Broderick AC, Catry PX, Hays GC et al (2003) Using satellite telemetry to determine post-nesting migratory corridors and foraging grounds of green turtles nesting at Poilão, Guinea Bissau. Methodology 5
Hart K, Fujisaki I (2010) Satellite tracking reveals habitat use by juvenile green sea turtles Chelonia mydas in the Everglades, Florida, USA. Endang Species Res 11:221–232. https://doi.org/10.3354/esr00284
Hart KM, Zawada DG, Fujisaki I, Lidz BH (2013) Habitat use of breeding green turtles Chelonia mydas tagged in Dry Tortugas National Park: Making use of local and regional MPAs. Biol Conserv 161:142–154. https://doi.org/10.1016/j.biocon.2013.03.019
Hart KM, Iverson AR, Benscoter AM, Fujisaki I et al (2017) Resident areas and migrations of female green turtles nesting at Buck Island Reef National Monument, St. Croix. US Virgin Islands Endang Species Res 32:89–101. https://doi.org/10.3354/esr00793
Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 149:52–64. https://doi.org/10.1007/s00442-006-0431-2
Hays GC, Adams CR, Broderick AC, Godley BJ, Lucas DJ, Metcalfe JD, Prior AA (2000) The diving behaviour of green turtles at Ascension Island. Anim Behav 59:577–586. https://doi.org/10.1006/anbe.1999.1326
Hays GC, Broderick AC, Godley BJ, Lovell P, Martin C, McConnell BJ, Richardson S (2002a) Biphasal long-distance migration in green turtles. Anim Behav 64:895–898. https://doi.org/10.1006/anbe.2002.1975
Hays GC, Glen F, Broderick AC, Godley BJ, Metcalfe JD (2002b) Behavioural plasticity in a large marine herbivore: contrasting patterns of depth utilisation between two green turtle (Chelonia mydas) populations. Mar Biol 141(5):985–990
Hays GC, Mortimer JA, Ierodiaconou D, Esteban N (2014) Use of long-distance migration patterns of an endangered species to inform conservation planning for the world's largest marine protected area. Conserv Biol 28(6):1636–1644
Heithaus MR, Frid A (2003) Optimal diving under the risk of predation. J Theor Biol 223:79–92. https://doi.org/10.1016/S0022-5193(03)00073-0
Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder L (2007) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844. https://doi.org/10.1111/j.1365-2656.2007.01260.x
Honarvar S, Fitzgerald DB, Weitzman CL, Sinclair EM, Echube JME, O’Connor M, Hearn GW (2016) Assessment of important marine turtle nesting populations on the southern coast of Bioko Island, Equatorial Guinea. Chelonian Conserv Biol 15:79–89. https://doi.org/10.2744/CCB-1194.1
IUCN and UNEP-WCMC (2014) The World database on protected areas (WDPA) (online). UNEP-WCMC, Cambridge. https://www.protectedplanet.net
Jonsen I, Myers R, James M (2007) Identifying leatherback turtle foraging behaviour from satellite telemetry using a switching state-space model. Mar Ecol Prog Ser 337:255–264. https://doi.org/10.3354/meps337255
Jonsen I, Bestley S, Wotherspoon S, Sumner M, Flemming JM (2017) bsam: Bayesian state-space models for animal movement. R Package Vers 1(1):2
Komoroske LM, Lewison RL, Seminoff JA, Deheyn DD, Dutton PH (2011) Pollutants and the health of green sea turtles resident to an urbanized estuary in San Diego, CA. Chemosphere 84:544–552. https://doi.org/10.1016/j.chemosphere.2011.04.023
Levy Y, Keren T, Leader N, Weil G, Tchernov D, Rilov G (2017) Spatiotemporal hotspots of habitat use by loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtles in the Levant basin as tools for conservation. Mar Ecol Prog Ser 575:165–179. https://doi.org/10.3354/meps12146
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(3):221–231
Luschi P, Hays GC, Del Seppia C, Marsh R, Papi F (1998) The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry. Proc R Soc Lond B 265:2279–2284. https://doi.org/10.1098/rspb.1998.0571
Luschi P, Åkesson S, Broderick A, Glen F, Godley B, Papi F, Hays G (2001) Testing the navigational abilities of ocean migrants: displacement experiments on green sea turtles (Chelonia mydas). Behav Ecol Sociobiol 50:528–534. https://doi.org/10.1007/s002650100396
Lutcavage ME, Plotkin P, Witherington B, and Lutz PL (2017) Human impacts on sea turtle survival. In: The biology of sea turtles, vol 1, p 45
Mahu E, Nyarko E, Hulme S, Coale KH (2015) Distribution and enrichment of trace metals in marine sediments from the Eastern Equatorial Atlantic, off the Coast of Ghana in the Gulf of Guinea. Mar Pollut Bull 98:301–307
Maxwell SM, Breed GA, Nickel BA, Makanga-Bahouna J, Pemo-Makaya E, Parnell RJ, Formia A, Ngouessono S, Godley BJ, Costa DP, Witt MJ, Coyne MS (2011) Using satellite tracking to optimize protection of long-lived marine species: olive ridley sea turtle conservation in Central Africa. PLoS ONE 6:e19905. https://doi.org/10.1371/journal.pone.0019905
Mettler E, Clyde-Brockway CE, Honarvar S, Paladino FV (2019) Migratory corridor linking Atlantic green turtle, Chelonia mydas, nesting site on Bioko Island, Equatorial Guinea to Ghanaian foraging grounds. PLoS ONE 14:e0213231. https://doi.org/10.1371/journal.pone.0213231
Meylan A (1995) Behavioral ecology of the west Caribbean green turtle (Chelonia mydas) in the internesting habitat. Biology and conservation of sea turtles revised edition. Smithsonian Institution, Washington DC, pp 67–80
Minamikawa S, Naito YA, Sato KA, Matsuzawa YO, Bando TA, Sakamoto W (2000) Maintenance of neutral buoyancy by depth selection in the loggerhead turtle Caretta caretta. J Exp Biol 203(19):2967–2975
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 85:8–17
Moore JE, Cox TM, Lewison RL, Read AJ, Bjorkland R, McDonald SL, Crowder LB, Aruna E, Ayissi I, Espeut P, Joynson-Hicks C (2010) An interview-based approach to assess marine mammal and sea turtle captures in artisanal fisheries. Biol Cons 143(3):795–805
Papi F, Liew HC, Luschi P, Chan EH (1995) Long-range migratory travel of a green turtle tracked by satellite: evidence for navigational ability in the open sea. Mar Biol 122:171–175
Parker DM, Dutton PH, Balazs GH (2011) Oceanic diet and distribution of haplotypes for the green turtle, Chelonia mydas, in the Central North Pacific. Pac Sci 65:419–431. https://doi.org/10.2984/65.4.419
Pendoley K (2018) Angola LNG olive ridley tracking project. Data originated from satellite tracking and analysis tool (STAT). https://www.seaturtle.org/tracking/index.shtml?project_id=263
Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biol Lett 3(6):712–714
Rice MR, Balazs GH (2008) Diving behavior of the Hawaiian green turtle (Chelonia mydas) during oceanic migrations. J Exp Mar Biol Ecol 356:121–127. https://doi.org/10.1016/j.jembe.2007.12.010
Richardson PB, Broderick AC, Coyne MS, Ekanayake L, Kapurusinghe T, Premakumara C, Ranger S, Saman MM, Witt MJ, Godley BJ (2013) Satellite telemetry reveals behavioural plasticity in a green turtle population nesting in Sri Lanka. Mar Biol 160:1415–1426. https://doi.org/10.1007/s00227-013-2194-8
Riskas KA, Tiwari M (2013) An overview of fisheries and sea turtle bycatch along the Atlantic coast of Africa. Munibe Monogr Nat Ser 1:71–82. https://doi.org/10.21630/mmns.2013.1.10
Scheren PA, Ibe AC, Janssen FJ, Lemmens AM (2002) Environmental pollution in the Gulf of Guinea—a regional approach. Mar Pollut Bull 44:633–641. https://doi.org/10.1016/S0025-326X(01)00305-8
Seminoff JA (Southwest Fisheries Science Center, U.S.) (2004) Chelonia mydas. The IUCN red list of threatened species 2004: e.T4615A11037468. https://doi.org/10.2305/IUCN.UK.2004.RLTS.T4615A11037468.en. Downloaded on 30 December 2017
Seminoff J, Zárate P, Coyne M, Foley D, Parker D, Lyon B, Dutton P (2008) Post-nesting migrations of Galápagos green turtles Chelonia mydas in relation to oceanographic conditions: integrating satellite telemetry with remotely sensed ocean data. Endang Species Res 4:57–72. https://doi.org/10.3354/esr00066
Shamblin BM, Witherington BE, Hirama S, Hardy RF, Nairn CJ (2018) Mixed stock analyses indicate population-scale connectivity effects of active dispersal by surface-pelagic green turtles. Mar Ecol-Prog Ser 601:215–226. https://doi.org/10.3354/meps12693
Shimada T, Limpus C, Jones R, Hazel J, Groom R, Hamann M (2016) Sea turtles return home after intentional displacement from coastal foraging areas. Mar Biol 163(8):1–14. https://doi.org/10.1007/s00227-015-2771-0
Spotila JR, Reina RD, Steyermark AC, Plotkin PT, Paladino FV (2000) Pacific leatherback turtles face extinction. Nature 405:529–530. https://doi.org/10.1038/35014729
Stokes KL, Broderick AC, Canbolat AF, Candan O, Fuller WJ, Glen F, Levy Y, Rees AF, Rilov G, Snape RT, Stott I, Tchernov D, Godley BJ (2015) Migratory corridors and foraging hotspots: critical habitats identified for Mediterranean green turtles. Divers Distrib 21:665–674. https://doi.org/10.1111/ddi.12317
Tanner C (2014) Sea turtle bycatch off the western region of the Ghanaian Coast. Mar Turt Newsl 140:8–11
Tomás J, Castroviejo J, Raga JA (1999) Sea turtles in the south of Bioko Island (Equatorial Guinea). Mar Turt Newsl 84:4–6
Tomás J, Formia A, Castroviejo J, Raga JA (2001) Post-nesting movements of the green turtle, Chelonia mydas, nesting in the south of Bioko Island, Equatorial Guinea, West Africa. Mar Turt Newsl 94:3–6
Tomás J, Godley BJ, Castroviejo J, Raga JA (2010) Bioko: critically important nesting habitat for sea turtles of West Africa. Biodivers Conserv 19(9):2699–2714
Troëng S, Evans DR, Harrison E, Lagueux CJ (2005) Migration of green turtles Chelonia mydas from Tortuguero, Costa Rica. Mar Biol 148(2):435–447. https://doi.org/10.1007/s00227-005-0076-4
UNEP-WCMC, Short FT (2018) Global distribution of seagrasses (version 6.0). Sixth update to the data layer used in Green and Short (2003). UN Environment World Conservation Monitoring Centre, Cambridge. https://data.unep-wcmc.org/datasets/7
Verhage B, Moundjim EB, Livingstone SR (2006) Four years of marine turtle monitoring in the Gamba complex of protected areas-Gabon. World Wildlife Fund, Bangui, Central African Republic, Central Africa
Wallace BP, Lewison RL, McDonald SL, McDonald RK, Kot CY, Kelez S, Bjorkland RK, Finkbeiner EM, Helmbrecht S, Crowder LB (2010) Global patterns of marine turtle bycatch. Conserv Lett 3:131–142. https://doi.org/10.1111/j.1755-263X.2010.00105.x
Weir CR, Ron T, Morais M, Duarte AD (2007) Nesting and at-sea distribution of marine turtles in Angola, West Africa, 2000–2006: occurrence, threats and conservation implications. Oryx 41(2):224–231
Witherington B, Pendoley K, Hearn GW, Honarvar S (2009) Ancient mariners, ancient fuels: how sea turtles cope with our modern fossil fuel dependency. SWOT Rep 4
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 80:571–581. https://doi.org/10.1016/j.anbehav.2010.05.022
Zug GR, Balazs GH, Wetherall JA, Parker DM, Murakawa SK (2002) Age and growth of Hawaiian seaturtles (Chelonia mydas): an analysis based on skeletochronology. Fish Bull 100(1):117–127
Acknowledgements
Sadly, the first author on this paper Emily Mettler passed away unexpectedly shortly after submitting the final revisions. We would like to acknowledge Emily for her hard work and dedication to conservation and we offer our deepest condolences to her family, friends and colleagues. The authors thank research assistants with Purdue University Fort Wayne and the Bioko Marine Turtle Program, Brian Dennis, Amanda Rohr, Abby Khraling, Sam Riley, Brad Leuenhagen, Parker Levinson, Rachel Schleicher, and Eley Meeth for help with transmitter attachment. We also thank the National University of Equatorial Guinea (UNGE) and Instituto Nacional de Desarrollo Forestal y Gestión del Sistema de Áreas Protegidas (INDEFOR-AP) for their support.
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This study was funded by the Kosmos Trident Energy grant, Grant # F.900001149.02.005, and Funds from the Schrey Distinguished Professorship, Grant # F.900001149.03.001.
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Mettler, E.K., Clyde-Brockway, C.E., Sinclair, E.M. et al. Determining critical inter-nesting, migratory, and foraging habitats for the conservation of East Atlantic green turtles (Chelonia mydas). Mar Biol 167, 106 (2020). https://doi.org/10.1007/s00227-020-03724-8
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DOI: https://doi.org/10.1007/s00227-020-03724-8