Abstract
In migratory marine species, demographic estimates are often generated from capture-mark-recapture (CMR) studies conducted at terrestrial breeding sites. However, when logistical difficulties limit the geographic area of these surveys, demographic estimates are vulnerable to biases. We compared demographic rates generated from CMR data of nesting loggerhead turtles (Caretta caretta) collected between 2010 and 2017 at one focal site (Wassaw Island, Georgia, USA; 31.89° N, 80.97° W) with estimates generated from the same group of turtles but including all other nesting events from adjacent sites in Georgia, South Carolina, and North Carolina. We found that estimates of annual recruitment at the focal site were overestimated: each year, 29–45% putative first-time nesters at the focal beach had, in fact, nested on a different beach in a previous season. Estimates of clutch frequency and breeding frequency generated at the focal site were biased low and skewed towards values of one, while estimates for remigration interval were not significantly over- or underestimated. Additionally, estimates of annual and total population productivity in terms of clutches, eggs, and hatchlings were underestimated by more than half at the focal site. Our results show how weak fidelity to a focal nesting/tagging site can affect demographic estimates in marine turtle populations and highlight the need to reconsider estimates from other populations that might be vulnerable to similar biases.
Similar content being viewed by others
References
Alvarado-Díaz J, Arias-Coyotl E, Delgado-Trejo C (2003) Clutch frequency of the Michoacan green seaturtle. J Herpetol 37:183–185
Avens L, Goshe LR, Coggins L, Snover ML, Pajuelo M, Bjorndal KA, Bolten AB (2015) Age and size at maturation- and adult-stage duration for loggerhead sea turtles in the western North Atlantic. Mar Biol 162:1749–1767. https://doi.org/10.1007/s00227-015-2705-x
Balazs GH, Chaloupka M (2004) Thirty-year recovery trend in the once depleted Hawaiian green sea turtle stock. Biol Conserv 117(5):491–498. https://doi.org/10.1016/j.biocon.2003.08.008
Bjorndal KA, Schroeder BA, Foley AM, Witherington BE, Bresette M, Clark D et al (2013) Temporal, spatial, and body size effects on growth rates of loggerhead sea turtles (Caretta caretta) in the Northwest Atlantic. Mar Biol 160:2711–2721. https://doi.org/10.1007/s00227-013-2264-y
Bjorndal KA, Bolten AB, Chaloupka M, Saba VS, Bellini C, Marcovaldi MA, Santos AJ, Bortolon LF, Meylan AB, Meylan PA, Gray J et al (2017) Ecological regime shift drives declining growth rates of sea turtles throughout the West Atlantic. Global Change Biol 23(11):4556–4568. https://doi.org/10.1111/gcb.13712
Bjorndal KA, Meylan AB, Turner BJ (1983) Sea turtles nesting at Melbourne Beach, Florida, I. Size, growth and reproductive biology. Biol Conserv 26(1):65–77. https://doi.org/10.1016/0006-3207(83)90049-6
Bolten AB (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol II. CRC Press, Boca Raton, pp 243–257
Bolten AB, Crowder LB, Dodd MG, Lauritsen AM, Musick JA, Schroeder BA, Witherington BE (2019) Assessment of Progress Toward Recovery for the NW Atlantic Population of the Loggerhead Sea Turtle (Caretta caretta). Report from the NW Atlantic Loggerhead Recovery Team
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400. https://doi.org/10.3929/ethz-b-000240890
Burgman MA, Ferson S, Akçakaya HR (1993) Risk assessment in conservation biology. Chapman and Hall, New York
Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. https://doi.org/10.1007/s00265-010-1029-6
Casale P, Ceriani SA (2020) Sea turtle populations are overestimated worldwide from remigration intervals: correction for bias. Endanger Species Res 41:141–151. https://doi.org/10.3354/esr01019
Ceriani SA, Casale P, Brost M, Leone EH, Witherington BE (2019) Conservation implications of sea turtle nesting trends: elusive recovery of a globally important loggerhead population. Ecosphere 10(11):e02936. https://doi.org/10.1002/ecs2.2936
Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M (1999) Research and management techniques for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4
Ekanayake EM, Kapurusinghe T, Saman MM, Rathnakumara DS, Samaraweera P, Rajakaruna RS (2016) Reproductive output and morphometrics of green turtle, Chelonia mydas nesting at the Kosgoda rookery in Sri Lanka. Ceylon J Sci 45(3):103–116. https://doi.org/10.4038/cjs.v45i3.7406
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. https://doi.org/10.1098/rspb.2016.2581
Frazer NB (1983) Survivorship of adult female loggerhead sea turtles, Caretta caretta, nesting on Little Cumberland Island, Georgia, USA. Herpetologica 39:436–447
Frazer NB, Richardson JI (1985) Annual variation in clutch size and frequency for loggerhead turtles, Caretta caretta, nesting at Little Cumberland Island, Georgia, USA. Herpetologica 41:246–251
Frey A, Dutton PH, Shaver DJ, Walker JS, Rubio C (2014) Kemp’s ridley Lepidochelys kempii nesting abundance in Texas, USA: a novel approach using genetics to improve population census. Endanger Species Res 23(1):63–71. https://doi.org/10.3354/esr00565
Hamann M, Godfrey MH, Seminoff JA, Arthur K, Barata PCR, Bjorndal KA et al (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11:245–269. https://doi.org/10.3354/esr00279
Hamilton RJ, Bird T, Gereniu C, Pita J, Ramohia PC, Walter R, Goerlich C, Limpus C (2015) Solomon Islands largest hawksbill turtle rookery shows signs of recovery after 150 years of excessive exploitation. PLoS ONE 10(4):e0121435. https://doi.org/10.1371/journal.pone.0121435
Hardin JW, Hilbe JM (2007) Generalized linear models and extensions. Stata Press, College Station
Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2005) Status of nesting loggerhead turtles Caretta caretta at Bald Head Island (North Carolina, USA) after 24 years of intensive monitoring and conservation. Oryx 39(1):65–72. https://doi.org/10.1017/S0030605305000116
Hays GC (2000) The implications of variable remigration intervals for the assessment of population size in marine turtles. J Theor Biol 206:221–227. https://doi.org/10.1006/jtbi.2000.2116
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, Bethesda, pp 137–148
Heppell SS, Snover ML, Crowder LB (2003) Sea turtle population ecology. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol II. CRC Press, Boca Raton, pp 259–306
Jerde CL, Kraskura K, Eliason EJ, Csik SR, Stier AC, Taper ML (2019) Strong evidence for an intraspecific metabolic scaling coefficient near 0.89 in fish. Front Physiol 10:1–17. https://doi.org/10.3389/fphys.2019.01166
Joe H, Zhu R (2005) Generalized Poisson distribution: the property of mixture of Poisson and comparison with negative binomial distribution. Biom J 47:219–229. https://doi.org/10.1002/bimj.200410102
Kalinowski ST, Taper ML, Marshall TC (2010) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 19:1512–1512. https://doi.org/10.1111/j.1365-294X.2010.04544.x
Kendall WL, Bjorkland R (2001) Using open robust design models to estimate temporary emigration from capture-recapture data. Biometrics 57:1113–1122. https://doi.org/10.1111/j.1365-294X.2007.03089.x
Kendall WL, Nichols JD, Hines JE (1997) Estimating temporary emigration using capture-recapture data with Pollock’s robust design. Ecology 78:563–578. https://doi.org/10.1890/0012-9658(1997)078[0563:ETEUCR]2.0.CO;2
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. https://doi.org/10.1007/s00227-014-2537-0
Lenth RV (2021) emmeans: estimated marginal means, aka least-squares means. R package version 1.7.0. https://CRAN.R-project.org/package=emmeans
Limpus CJ, Nicholls N (1988) The southern oscillation regulates the annual numbers of green turtles (Chelonia mydas) breeding around northern Australia. Wildlife Res 15(2):157–161. https://doi.org/10.1071/WR9880157
SEATURTLE.ORG Maptool (2002) SEATURTLE.ORG, Inc. http://www.seaturtle.org/maptool/. Accessed 11 Oct 2017
Meylan A (1982) Estimation of population size in sea turtles. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution, Washington, DC, pp 135–138
Miller JD (1997) Reproduction in sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 51–81
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. https://doi.org/10.1007/s10144-010-0205-x
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 137–163
Musick JA (1999) Ecology and conservation of long-lived marine animals. In: Musick JA (ed) Life in the slow lane: ecology and conservation of long-lived marine animals. American Fisheries Society Symposium 23, Bethesda, pp 1–10
NMFS and USFWS (National Marine Fisheries Service, US Fish and Wildlife Service) (2008) Recovery plan for the Northwest Atlantic population of the loggerhead sea turtle (Caretta caretta), 2nd rev. NMFS, Silver Spring. www.nmfs.noaa.gov/pr/pdfs/recovery/turtle_loggerhead_atlantic.pdf
NRC (National Research Council) (2010) Assessment of sea-turtle status and trends: integrating demography and abundance. National Academies Press, Washington, DC
Ondich BL, Andrews KM (2013) A history of sea turtle tagging and monitoring on Jekyll Island, Georgia, USA. Mar Turt Newsl 138:11–15
Pfaller JB, Bjorndal KA, Chaloupka M, Williams KL, Frick MG, Bolton AB (2013) Accounting for imperfect detection is critical for inferring marine turtle nesting population trends. PLoS ONE 8:e62326. https://doi.org/10.1371/journal.pone.0062326
Pfaller JB, Chaloupka M, Bolten AB, Bjorndal KA (2018) Phylogeny, biogeography and methodology: a meta-analytic perspective on heterogeneity in adult marine turtle survival rates. Sci Rep 8:5852. https://doi.org/10.1038/s41598-018-24262-w
Pfaller JB, Williams KL, Frick MG, Shamblin BM, Nairn CJ, Girondot M (2019) Genetic determination of tag loss dynamics in nesting loggerhead turtles: a new chapter in “the tag loss problem.” Mar Biol 166(7):97. https://doi.org/10.1007/s00227-019-3545-x
Phillips K, Mansfield KL, Die DJ, Addison DS (2014) Survival and remigration probabilities for loggerhead turtles (Caretta caretta) nesting in the Eastern Gulf of Mexico. Mar Biol 161:863–870. https://doi.org/10.1007/s00227-013-2386-2
Richards PM, Epperly SP, Heppell SS, King RT, Sasso CR, Moncada F, Nodarse G, Shaver DJ, Medina Y, Zurita J (2011) Sea turtle population estimates incorporating uncertainty: a new approach applied to western North Atlantic loggerheads Caretta caretta. Endanger Species Res 15(2):151–158. https://doi.org/10.1643/0045-8511(2002)002[0653:NEOTLT]2.0.CO;2
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
Rivalan P, Pradel R, Choquet R, Girondot M, Prévot-Julliard AC (2006) Estimating clutch frequency in the sea turtle Dermochelys coriacea using stopover duration. Mar Ecol Prog Ser 317:285–295. https://doi.org/10.3354/meps317285
Schroeder BA, Foley AM, Bagley DA (2003) Nesting patterns, reproductive migrations, and adult foraging areas of loggerhead turtles. In: Witherington BE, Bolten AB (eds) Loggerhead sea turtles. Smithsonian Institution, Washington, DC, pp 114–124
Schwarz CJ, Stobo WT (1997) Estimating temporary migration using the robust design. Biometrics 53:178–194. https://doi.org/10.2307/2533106
Scott R, Marsh R, Hays G (2012) Life in the really slow lane: loggerhead sea turtles mature late relative to other reptiles. Funct Ecol 26:227–235. https://doi.org/10.1111/j.1365-2435.2011.01915.x
Scott JA (2006) Use of satellite telemetry to determine ecology and management of loggerhead turtle (Caretta caretta) during the nesting season in Georgia. Master’s Thesis, University of Georgia
Shamblin BM, Faircloth BC, Dodd M, Wood-Jones A, Castleberry SB, Carroll JP et al (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Mol Ecol Notes 7:784–787. https://doi.org/10.1111/j.1471-8286.2007.01701.x
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. https://doi.org/10.1007/s10592-008-9573-6
Shamblin BM, Dodd MG, Bagley DA, Ehrhart LM, Tucker AD, Johnson C et al (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(3):571–587. https://doi.org/10.1007/s00227-010-1582-6
Shamblin BM, Dodd MG, Williams KL, Frick MG, Bell R, Nairn CJ (2011b) Loggerhead turtle egg shells as a source of maternal nuclear genomic DNA for population genetic studies. Mol Ecol Res 11:110–115. https://doi.org/10.1111/j.1755-0998.2010.02910.x
Shamblin BM, Dodd MG, Griffin DBB, Pate SM, Godfrey MH, Coyne MS et al (2017) Improved female abundance and reproductive parameter estimates through subpopulation-scale genetic capture-recapture of loggerhead turtles. Mar Biol 164:138. https://doi.org/10.1007/s00227-017-3166-1
Shamblin BM, Dodd MG, Pate SM, Godfrey MH, Pfaller JB, Williams KL et al (2021) In search of the “missing majority” of nesting loggerhead turtles: improved inter-seasonal recapture rates through subpopulation-scale genetic tagging. Mar Biol 168:16. https://doi.org/10.1007/s00227-020-03820-9
Solow AR, Bjorndal KA, Bolten AB (2002) Annual variation in nesting numbers of marine turtles: the effect of sea surface temperature on re-migration intervals. Ecol Lett 5:742–746. https://doi.org/10.1046/j.1461-0248.2002.00374.x
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
Stearns S (1992) The Evolution of Life Histories. Oxford University Press, Oxford, UK
Stokes KL, Fuller WJ, Glen F, Godley BJ, Hodgson DJ, Rhodes KA et al (2014) Detecting green shoots of recovery: the importance of long-term individual based monitoring of marine turtles. Anim Conserv 17:593–602. https://doi.org/10.1111/acv.12128
Tucker AD (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 Biol Ecol 383:48–55. https://doi.org/10.1016/j.jembe.2009.11.009
Vander Zanden HB, Pfaller JB, Reich KJ, Pajuelo M, Bolten AB, Williams KL et al (2014) Foraging areas differentially affect reproductive output and interpretation of trends in abundance of loggerhead turtles. Mar Biol 161:585–598. https://doi.org/10.1007/s00227-013-2361-y
Williams KL, Frick MG (2008) Tag returns from loggerhead turtles from Wassaw Island, GA. Southeast Nat 7:165–172. https://doi.org/10.1656/1528-7092(2008)7[165:TRFLTF]2.0.CO;2
Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations: modeling, estimation, and decision making. Academic Press, San Diego
Williams KL, Frick MG (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, pp 1–32
Acknowledgements
We thank the volunteers and supporters of the Caretta Research Project and the many beach monitoring programs and surveyors on the coast of Georgia, North Carolina, and South Carolina, as well as those responsible for DNA analysis and genotyping at the University of Georgia. Without these valuable contributions this work would not be possible.
Funding
This work was funded through National Oceanographic and Atmospheric Administration-National Marine Fisheries Service Sect. 6 Grant award NA13NMF4720040 to the Georgia Department of Natural Resources and the South Carolina Department of Natural Resources.
Author information
Authors and Affiliations
Contributions
JBP and BMS conceived the study. KLW and CJN provided logistical support and funding. MGD, MHG, DBG, and SMP coordinated sample collection and provided nest metadata from their respective state monitoring programs. JBP and KLW collected samples and provided nest metadata for Wassaw Island. JBP, SMW, and CGG collated nesting data, conducted analyses, and composed the manuscript with input from all other authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethics approval
All applicable national and institutional guidelines for the care and use of animals were followed (University of Georgia 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).
Availability of data and material
All data generated or analyzed during this study are provided in Online Resource 1.
Code availability
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Responsible Editor: L. Avens.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pfaller, J.B., Weaver, S.M., Williams, K.L. et al. One beach amongst many: how weak fidelity to a focal nesting site can bias demographic rates in marine turtles. Mar Biol 169, 8 (2022). https://doi.org/10.1007/s00227-021-03991-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03991-z