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In search of the “missing majority” of nesting loggerhead turtles: improved inter-seasonal recapture rates through subpopulation-scale genetic tagging

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Abstract

Capture–mark–recapture (CMR) studies on marine turtle nesting beaches provide data on reproductive periodicity that inform population trends and models. Annual survival is estimated from observations of remigration, the return of females in subsequent nesting seasons. However, a significant proportion of tagged females are never encountered remigrating in many studies, presumably due to weak nest site fidelity (NSF). We employed a genetic CMR approach based on subpopulation-scale clutch sampling to conduct a 5-year evaluation of inter-seasonal recapture rates and NSF for Northern Recovery Unit loggerhead turtles (Caretta caretta). Of 1770 females genetically tagged from Georgia through Maryland in 2010, 1156 (65%) remigrated between 2011 and 2015. Inter-seasonal NSF, measured as shifts in median latitude nesting locations between years, was highly variable among individuals but strong overall (mean: 15.08 (± 44.61) km, median: 1.84 km). Among three focal beaches with nocturnal tagging projects, 69 of 173 females (40%) remigrated onsite whereas 115 (66%) were detected overall. Regional genetic sampling therefore yielded significantly higher inter-seasonal recapture rates, which may improve precision in future survival analyses. However, despite sampling ~ 1000 km with high annual detection probabilities (p* ≥ 0.94), 35% of 2010-females were not detected remigrating. Several non-exclusive hypotheses to explain these remaining “missing” remigrants should be considered: longer remigration intervals, imperfect detection within the study area, emigration to Florida, anthropogenic mortality, and natural mortality or senescence. This genetic tagging approach can be applied over large spatial scales where nesting densities permit, better characterizing inter-seasonal dispersal.

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References

  • Avens L, Goshe L, Coggins L, Snover ML, Pajuelo M, Bjorndal KA, Bolten AB (2015) Age and size at maturation- and adult-stage duration in loggerhead sea turtles in the western North Atlantic. Mar Biol 162:1749–1767

    Article  CAS  Google Scholar 

  • Baldwin WP, Jr, Lofton JM, Jr (1940) The loggerheads of Cape Romain. U.S. Biological Survey Report, McClellanville, SC. pp. 69

  • Baretto J, Thomé JC, Baptistotte C, Rieth D, Marcovaldi MÂ, Marcovaldi GGD, Bellini C, Scalfoni JT, Filgueiras H, Vila-Verde L, Cabral L, Marcondes AC, Almeida AP (2019) Reproductive longevity of the loggerhead sea turtle, Caretta caretta, in Espírito Santo, Brazil. Mar Turt Newsl 157:10–12

    Google Scholar 

  • Bjorndal KA, Meylan AB, Turner BJ (1983) Sea turtles nesting at Melbourne Beach, Florida, I. Size, growth and reproductive biology. Biol Conserv 26:65–77

    Article  Google Scholar 

  • Bolten AB, Crowder LB, Dodd MG, Lauritsen AM, Musick JA, Schroeder BA, Witherington BE (2019) Recovery plan for the Northwest Atlantic Population of the Loggerhead Sea Turtle (Caretta caretta) Second Revision (2008): Assessment of Progress Toward Recovery. http://fws.gov/northflorida/seaturtles/Docs/FINAL_NW_Atl_CC_Loggerhead-_Recovery_Team_Progress_Report_12-19-19.pdf. Accessed 27 Jul 2020

  • Bowen BW, Bass AL, Soares LS, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol Ecol 14:2389–2402

    Article  CAS  PubMed  Google Scholar 

  • Caldwell DK (1962) Comments on the nesting behavior of Atlantic loggerhead sea turtles, based primarily on tagging returns. Quart J Fla Acad Sci 25:287–302

    Google Scholar 

  • Carr AF (1980) Some problems of sea turtle ecology. Am Zool 20:489–498

    Article  Google Scholar 

  • Carr AF, Ogren LH (1960) The ecology and migrations of sea turtles 4. The green turtle in the Caribbean Sea. Bull AMNH 121:1

    Google Scholar 

  • Casale P, Ceriani SA (2020) Sea turtle populations are overestimated worldwide from remigration intervals: correction for bias. Endang Species Res 41:141–151

    Article  Google Scholar 

  • Ceriani SA, Roth JD, Evan DR, Weishampel JF, Ehrhart LM (2012) Inferring foraging areas of nesting loggerhead turtles using satellite telemetry and stable isotopes. PLoS ONE 7:e45335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceriani SA, Casale P, Brost M, Leone EH, Witherington BE (2019) Conservation implications of sea turtle nesting trends: elusive recovery of a globally important population. Ecosphere 10:e02936

    Article  Google Scholar 

  • Ehrhart LM (1980) A continuation of the baseline studies for environmentally monitoring space transportation systems (STS) at John F. Kennedy Space Center. Vol. 4. Threatened and endangered species of the Kennedy Space Center. Part 1: Marine turtle studies. Final report 197

  • Ehrhart L, Redfoot W, Bagley D, Mansfield K (2014) Long-term trends in loggerhead (Caretta caretta) nesting and reproductive success at an important Western Atlantic rookery. Chelonian Conserv Biol 13:173–181

    Article  Google Scholar 

  • Epperly SP, Braun McNeill J, Chester AJ, Cross FA, Merriner JV, Tester PA, Churchill JH (1996) Beach strandings as an indicator of at-sea mortality of sea turtles. Bull Mar Sci 59:289–297

    Google Scholar 

  • Esteban N, Mortimer JA, Hays GC (2017) How numbers of nesting sea turtles can be overestimated by nearly a factor of two. Proc R Soc B 284:20162581

    Article  PubMed  Google Scholar 

  • Finkbeiner EM, Wallace BP, Moore JE, Lewison RL, Crowder LB, Read AJ (2011) Cumulative estimates of sea turtle bycatch and mortality in USA fisheries between 1990 and 2007. Biol Conserv 144:2719–2727

    Article  Google Scholar 

  • Foley A, Stacy BA, Hardy RF, Shea C, Minch K, Schroeder BA (2019) Characterizing watercraft-related mortality of sea turtles in Florida. J Wildl Manage 83:1057–1072

    Article  Google Scholar 

  • Griffin DB, Murphy SR, Frick MG, Broderick AC, Coker JW, Coyne MS, Dodd MG, Godfrey MH, Godley BJ, Hawkes LA, Murphy TM, Williams KL, Witt MJ (2013) Foraging habitats and migration corridors utilized by a recovering subpopulation of adult female loggerhead sea turtles: implications for conservation. Mar Biol 160:3071–3086

    Article  Google Scholar 

  • Hatase H, Matsuzawa Y, Sato K, Bando T, Goto K (2004) Remigration and growth of loggerhead turtles (Caretta caretta) nesting on Senri Beach in Minabe, Japan: life-history polymorphism in a sea turtle population. Mar Biol 144:807–811

    Article  Google Scholar 

  • Hays GC, Sutherland JM (1991) Remigration and beach fidelity of loggerhead turtles on the island of Cephalonia, Greece. J Herpetol 25:232–233

    Article  Google Scholar 

  • Hendrickson JR (1958) The green sea turtle, Chelonia mydas (Linn.) in Malaya and Sarawak. Proc Zool Soc Lond 130:455–535

    Article  Google Scholar 

  • Hines JE, Kendall WL, Nichols JD (2003) On the use of the robust design model with transient capture–recapture models. Auk 120:1151–1158

    Article  Google Scholar 

  • Hughes GR (1974) The sea turtles of southeast Africa II. Investigational report 36. South African Association of Marine Biological Research, Durban, South Africa

  • Hughes GR (1982) Nesting cycles in sea turtles-typical or atypical? In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington, D.C., USA, pp 81–89

    Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kendall WL, Bjorkland R (2001) Using open robust design models to estimate temporary emigration from capture–recapture data. Biometrics 57:1113–1122

    Article  CAS  PubMed  Google Scholar 

  • Lamont MM, Fujisaki I, Carthy RR (2014) Estimates of vital rates for a declining loggerhead turtle (Caretta caretta) subpopulation: implications for management. Mar Biol 161:2659–2668

    Article  Google Scholar 

  • Monk MH, Berkson J, Rivalan P (2011) Estimating demographic parameters for loggerhead sea turtles using mark-recapture data and a multistate model. Popul Ecol 53:165–174

    Article  Google Scholar 

  • Nel R, Punt AE, Hughes GR (2013) Are coastal areas always effective in achieving population recovery for nesting sea turtles? PLoS ONE 8:e63525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • NMFS and U.S. FWS (2008) Recovery Plan for the Northwest Atlantic Population of the Loggerhead Sea Turtle (Caretta caretta), Second Revision. National Marine Fisheries Service, Silver Spring, MD

  • Ondich BL, Andrews KM (2013) A history of sea turtle tagging and monitoring on Jekyll Island, Georgia, USA. Mar Turt Newsl 138:11–15

    Google Scholar 

  • Pfaller JB, Bjorndal KA, Chaloupka M, Williams KL, Frick MG, Bolten AB (2013) Accounting for imperfect detection is critical for inferring marine turtle nesting population trends. PLoS ONE 8:e62326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaller JB, Chaloupka M, Bjorndal KA, Bolten AB (2018) Phylogeny, biogeography and methodology: a meta-analytic perspective on heterogeneity in adult marine turtle survival estimates. Sci Rep 8:5852

    Article  PubMed  PubMed Central  Google Scholar 

  • Phillips KF, Mansfield KL, Die DJ, Addison DS (2014) Survival and remigration probabilitis for loggerhead turtles (Caretta caretta) nesting in the eastern Gulf of Mexico. Mar Biol 161:863–870

    Article  Google Scholar 

  • Piovanno S, Kaska Y, Prazzi E, Nannarelli S, Giacoma C (2011) Low incidence of twinning in the loggerhead sea turtle. J Vertebr Biol 60:159–166

    Google Scholar 

  • Pradel R, Hines JE, Lebreton J-D, Nichole JD (1997) Capture–recapture survival models taking account of transients. Biometrics 53:60–72

    Article  Google Scholar 

  • Ramirez A, Kot C, Piatkowski D (2017) Review of sea turtle entrainment risk by trailing suction hopper dredges in the US Atlantic and Gulf of Mexico and the development of the ASTER decision support tool. US Department of the Interior, Bureau of Ocean Energy Management. OCS Study BOEM 2017-084. Sterling, Virginia, pp. 275

  • Richardson JI (1982) A population model for adult female loggerhead sea turtles (Caretta caretta) nesting in Georgia. Doctoral dissertation, University of Georgia, Athens, Georgia

  • Richardson TH, Richardson JI, Ruckdeschel C, Dix MW (1978) Remigration patterns of loggerhead sea turtles (Caretta caretta) nesting on Little Cumberland and Cumberland Islands, Georgia. Fla Mar Res Publ 33:39–44

    Google Scholar 

  • Rivalan P, Prévot-Julliard A-C, Choquet R, Pradel R, Jacquemin B, Girondot M (2005) Trade-offs between current reproductive effort and delay to nest reproduction in the leatherback sea turtle. Oecol 145:564–574

    Article  Google Scholar 

  • Schroeder BA, Foley AM, Bagley DA (2003) Nesting patterns, reproductive migrations, and adult foraging areas of loggerhead turtles. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, D.C., USA, pp 114–124

    Google Scholar 

  • Scott JA (2006) Use of satellite telemetry to determine ecology and management of loggerhead turtle (Caretta caretta) during the nesting season in Georgia. Masters thesis, University of Georgia, Athens, Georgia, USA

  • Scott JA, Dodd MG, Castleberry SB (2013) Assessment of management scenarios to reduce loggerhead turtle interactions with shrimp trawlers. Mar Coast Fish 5:281–290

    Article  Google Scholar 

  • Shamblin BM, Faircloth BC, Dodd M, Wood-Jones A, Castleberry SB, Carroll JP, Nairn CJ (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Mol Ecol Notes 7:784–787

    Article  CAS  Google Scholar 

  • Shamblin BM, Faircloth BC, Dodd MG, Bagley DA, Ehrhart LM, Dutton PH, Frey A, Nairn CJ (2009) Tetranucleotide markers from the loggerhead sea turtle (Caretta caretta) and their cross-amplification in other marine turtle species. Conserv Genet 10:577–580

    Article  CAS  Google Scholar 

  • Shamblin BM, Dodd MG, Bagley DA, Ehrhart LM, Tucker AD, Johnson C, Carthy RR, Scarpino RA, McMichael E, Addison DS, Williams KL, Frick MG, Ouellette S, Meylan AB, Godfrey MH, Murphy SR, Nairn CJ (2011a) Genetic structure of the Southeastern United States loggerhead turtle nesting aggregation: evidence of additional structure within the peninsular Florida recovery unit. Mar Biol 158:1–17

    Article  Google Scholar 

  • Shamblin BM, Dodd MG, Williams KL, Frick MG, Bell R, Nairn CJ (2011b) Loggerhead turtle eggshells as a source of maternal nuclear genomic DNA for population genetic studies. Mol Ecol Resour 11:110–115

    Article  PubMed  Google Scholar 

  • Shamblin BM, Bolten AB, Bjorndal KA, Dutton PH, Nielsen JT, Abreu-Grobois FA, Reich KJ, Witherington BE, Bagley DA, Ehrhart LM, Tucker AD, Addison DS, Arenas A, Johnson C, Carthy RR, Lamont MM, Dodd MG, Gaines MS, LaCasella E, Nairn CJ (2012) Expanded mitochondrial control region sequences increase resolution of stock structure among North Atlantic loggerhead turtle rookeries. Mar Ecol Prog Ser 469:145–160

    Article  Google Scholar 

  • Shamblin BM, Dodd MG, Griffin DB, Pate SM, Godfrey MH, Coyne MS, Williams KL, Pfaller JB, Ondich BL, Andrews KM, Boettcher R, Nairn CJ (2017) Improved female abundance and reproductive parameter estimates through subpopulation-scale genetic capture–recapture of loggerhead turtles. Mar Biol 158:1–17

    Google Scholar 

  • Stoneburner DL (1981) Summary of the loggerhead sea turtle research project conducted at Canaveral National Seashore, Cumberland Island National Seashore, Cape Lookout National Seashore: A final report. National Park Service, Southeast Regional Office, Atlanta, Georgia, USA. pp. 31

  • Stoneburner DL, Ehrhart LM (1981) Observations of Caretta c. caretta: a record internesting migration in the Atlantic. Herpetol Rev 12:66

    Google Scholar 

  • Talbert OR Jr, Stancyk SE, Dean JM, Will JM (1980) Nesting activity of the loggerhead turtle (Caretta caretta) in South Carolina I: a rookery in transition. Copeia 1980(4):709–718

    Article  Google Scholar 

  • Thorson JT, Punt AE, Nel R (2012) Evaluating population recovery for sea turtles under nesting beach protection while accounting for nesting behaviours and changes in availability. J App Ecol 49:601–610

    Google Scholar 

  • Tucker A (2010) Nest site fidelity and clutch frequency of loggerhead turtles are better elucidated by satellite telemetry than by nocturnal tagging efforts: implications for stock estimation. J Exp Mar Bio Ecol 383:48–55

    Article  Google Scholar 

  • Weber N, Weber SB, Godley BJ, Ellick J, Witt MJ, Broderick AC (2013) Telemetry as a tool for improving estimates of marine turtle abundance. Biol Conserv 167:90–96

    Article  Google Scholar 

  • Williams K, Frick M (2001) Results from the long-term monitoring of nesting loggerhead sea turtles (Caretta caretta) on Wassaw Island, Georgia: 1973–2000. NOAA Technical Memorandum NMFS-SEFSC-446. Miami, Florida

  • Williams KL, Frick MG (2008) Tag returns from loggerhead turtles from Wassaw Island, GA. Southeast Nat 7:165–172

    Article  Google Scholar 

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Acknowledgements

This work would not have been possible without the enthusiastic support of the many beach monitoring projects along the Atlantic coast of the United States north of Florida. We gratefully acknowledge the personnel representing the authors’ institutions and agencies as well as hundreds of surveyors representing the NRU beach monitoring projects who have collected samples for this study over the years, including the Americorps members and Caretta Research Project volunteers who participated in tagging and collection of genetic samples. We also acknowledge dozens of undergraduate student workers who performed DNA extractions. We thank the reviewers for greatly improving the quality of this manuscript.

Funding

This work was funded through National Oceanographic and Atmospheric Administration-National Marine Fisheries Service Section 6 Grant award NA13NMF4720040 to the Georgia Department of Natural Resources and South Carolina Department of Natural Resources.

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Authors and Affiliations

  1. Daniel B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA, 30602, USA

    Brian M. Shamblin & Campbell J. Nairn

  2. Georgia Department of Natural Resources, One Conservation Way, Brunswick, GA, 31520, USA

    Mark G. Dodd

  3. South Carolina Department of Natural Resources, P.O. Box 12559, Charleston, SC, 29412, USA

    S. Michelle Pate

  4. North Carolina Wildlife Resources Commission, 1507 Ann Street, Beaufort, NC, 28516, USA

    Matthew H. Godfrey

  5. Caretta Research Project, P.O. Box 9841, Savannah, GA, 31412, USA

    Joseph B. Pfaller & Kristina L. Williams

  6. Archie Carr Center for Sea Turtle Research and Department of Biology, University of Florida, P.O. Box 118525, Gainesville, FL, 32611, USA

    Joseph B. Pfaller

  7. Georgia Sea Turtle Center, 214 Stable Road, Jekyll Island, GA, 31527, USA

    Breanna L. Ondich & David A. Steen

  8. Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, 1105 SW Williston Street, Gainesville, FL, 32601, USA

    David A. Steen

  9. Bald Head Island Conservancy, 700 Federal Road, Bald Head Island, NC, 28461, USA

    Elizabeth S. Darrow & Paul Hillbrand

  10. Virginia Department of Wildlife Resources, 12610 Jacobus Creek Road, Machipongo, VA, 23405, USA

    Ruth Boettcher

  11. Seaturtle.Org, 1 Southampton Place, Durham, NC, 27705, USA

    Michael S. Coyne

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  1. Brian M. Shamblin
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  2. Mark G. Dodd
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  3. S. Michelle Pate
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  13. Campbell J. Nairn
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Contributions

BMS and CJN conceived the study. MGD, SMP, MHG and RMB coordinated sample collection and provided nest metadata from their respective state monitoring programs. JBP, KLW, BLO, DAS, ESD and PH collected and provided individual female and nest metadata from their respective tagging projects. MSC built and maintained the nesting and genetics databases and assisted with spatial analyses. BMS led the analyses and writing with input from all authors.

Corresponding author

Correspondence to Brian M. Shamblin.

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Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable national and institutional guidelines for the care and use of animals were followed (UGA Animal Care and Use Permits A2009 3-050 and A2015 01-011-Y1-A0 and permitted by the individual state sea turtle management agencies under the authority of the United States Fish and Wildlife Service).

Data availability

Spatial and remigration data for individual females are provided in Online Resource 1.

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Shamblin, B.M., Dodd, M.G., Pate, S.M. et al. In search of the “missing majority” of nesting loggerhead turtles: improved inter-seasonal recapture rates through subpopulation-scale genetic tagging. Mar Biol 168, 16 (2021). https://doi.org/10.1007/s00227-020-03820-9

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