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The efficiency of phenological shifts as an adaptive response against climate change: a case study of loggerhead sea turtles (Caretta caretta) in the Mediterranean

Mitigation and Adaptation Strategies for Global Change volume 23, pages 1143–1158 (2018)Cite this article

Abstract

Phenological shifts are widely reported for different species as a response to climate change. Still, the efficiency of this mechanism is questioned because of the accelerated rate of change and the different change patterns of various climate parameters that may cause mismatches. Here, using loggerhead sea turtles (Caretta caretta) as model species, we examined whether phenological shifts could be an effective adaptive strategy over the critical period that determines reproductive output in the Mediterranean region. We compared the rate of temperature and precipitation change over the recent past (1971–2015) and future periods (2016–2060) along the 45 main nesting sites of the Mediterranean population, during the incubation period. Next, utilizing predictions of an earlier nesting season, we evaluated whether the timing of incubation will impact offspring survival on the Mediterranean population. To further assess species vulnerability, we investigated any potential relationship between hatching success and climate parameters at the largest Mediterranean nesting rookery (Zakynthos, Greece). We found that phenological changes would allow species to capture a thermal window similar to one they experience nowadays during the incubation period. Still, phenological shifts might be less adequate to follow precipitation changes, which however, were found to have a limited impact upon hatching success. Global adaptation management strategies should be directed towards (a) acquisition of long-term high-resolution temperature and precipitation series at nesting sites, (b) developing early warning systems to prevent negative impacts upon reproductive outputs, and (c) directly applying cooling of the nests when first altered climate signs are detected.

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References

  • Ackerman RA, Lutz P, Musick J (1997) The nest environment and the embryonic development of sea turtles. Biol Sea Turt 1:83–106

    Google Scholar 

  • Alberto FJ, Aitken SN, Alía R, González-Martínez SC, Hänninen H, Kremer A, Lefèvre F, Lenormand T, Yeaman S, Whetten R, Savolainen O (2013) Potential for evolutionary responses to climate change—evidence from tree populations. Glob Chang Biol 19(6):1645–1661. https://doi.org/10.1111/gcb.12181

    Article  Google Scholar 

  • Almpanidou V, Schofield G, Kallimanis AS, Türkozan O, Hays GC, Mazaris AD (2016) Using climatic suitability thresholds to identify past, present and future population viability. Ecol Indic 71:551–556. https://doi.org/10.1016/j.ecolind.2016.07.038

    Article  Google Scholar 

  • Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc R Soc B 279(1743):3843-52

  • ARCHELON, the Sea Turtle Protection Society of Greece (2012) Sea turtle monitoring and conservation in Laganas Bay, Zakynthos, Greece, during 2012 Short report submitted to the European Commission, and the Bern Convention (Council of Europe) Prepared by S. Touliatou and D. Margaritoulis

  • Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15(4):365–377. https://doi.org/10.1111/j.1461-0248.2011.01736.x

    Article  Google Scholar 

  • Both C, Artemyev AV, Blaauw B, Cowie RJ, Dekhuijzen AJ, Eeva T, Enemar A, Gustafsson L, Ivankina EV, Jarvinen A, Metcalfe NB, Nyholm NEI, Potti J, Ravussin PA, Sanz JJ, Silverin B, Slater FM, Sokolov LV, Torok J, Winkel W, Wright J, Zang H, Visser ME (2004) Large–scale geographical variation confirms that climate change causes birds to lay earlier. Proc R Soc B 271(1549):1657–1662. https://doi.org/10.1098/rspb.2004.2770

    Article  Google Scholar 

  • Casale P, Margaritoulis D (2010) Sea turtles in the Mediterranean: distribution, threats and conservation priorities. IUCN, Gland

    Google Scholar 

  • 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. Endanger Species Res 13(2):123–129. https://doi.org/10.3354/esr00319

    Article  Google Scholar 

  • Cleveland WS, Devlin SJ (1988) Locally weighted regression: an approach to regression analysis by local fitting. J Am Stat Assoc 83(403):596–610. https://doi.org/10.1080/01621459.1988.10478639

    Article  Google Scholar 

  • Davidson AD, Boyer AG, Kim H, Pompa-Mansilla S, Hamilton MJ, Costa DP, Ceballos G, Brown JH (2012) Drivers and hotspots of extinction risk in marine mammals. Proc Natl Acad Sci U S A 109(9):3395–3400. https://doi.org/10.1073/pnas.1121469109

    Article  Google Scholar 

  • Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332(6025):53–58. https://doi.org/10.1126/science.1200303

    Article  Google Scholar 

  • Duputié A, Rutschmann A, Ronce O, Chuine I (2015) Phenological plasticity will not help all species adapt to climate change. Glob Chang Biol 21(8):3062–3073. https://doi.org/10.1111/gcb.12914

    Article  Google Scholar 

  • Foden WB, Butchart SH, Stuart SN et al (2013) Identifying the world's most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS One 8(6):e65427. https://doi.org/10.1371/journal.pone.0065427

    Article  Google Scholar 

  • Fuentes MMPB, Maynard JA, Guinea M, Bell IP, Werdell PJ, Hamann M (2009) Proxy indicators of sand temperature help project impacts of global warming on sea turtles in northern Australia. Endanger Species Res 9:33–40. https://doi.org/10.3354/esr00224

    Article  Google Scholar 

  • Fuentes MMPB, Limpus CJ, Hamann M (2011) Vulnerability of sea turtle nesting grounds to climate change. Glob Chang Biol 17(1):140–153. https://doi.org/10.1111/j.1365-2486.2010.02192.x

    Article  Google Scholar 

  • Fuentes MMPB, Fish MR, Maynard JA (2012) Management strategies to mitigate the impacts of climate change on sea turtle’s terrestrial reproductive phase. Mitig Adapt Strateg Glob Chang 17(1):51–63. https://doi.org/10.1007/s11027-011-9308-8

    Article  Google Scholar 

  • Gibbs JP, Breisch AR (2001) Climate warming and calling phenology of frogs near Ithaca, New York, 1900–1999. Conserv Biol 15(4):1175–1178. https://doi.org/10.1046/j.1523-1739.2001.0150041175.x

    Article  Google Scholar 

  • Giorgi F, Gutowski WJ Jr (2015) Regional dynamical downscaling and the CORDEX initiative. Annu Rev Environ Resour 40(1):467–490. https://doi.org/10.1146/annurev-environ-102014-021217

    Article  Google Scholar 

  • Godfrey MH, Mrosovsky N, Barreto R (1996) Estimating past and present sex ratios of sea turtles in Suriname. Can J Zool 74(2):267–277. https://doi.org/10.1139/z96-033

    Article  Google Scholar 

  • Godley B, Broderick AC, Downie JR et al (2001) Thermal conditions in nests of loggerhead turtles: further evidence suggesting female skewed sex ratios of hatchling production in the Mediterranean. J Exp Mar Biol Ecol 263(1):45–63. https://doi.org/10.1016/S0022-0981(01)00269-6

    Article  Google Scholar 

  • Hays GC, Broderick AC, Glen F, Godley BJ (2003) Climate change and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Glob Chang Biol 9(4):642–646. https://doi.org/10.1046/j.1365-2486.2003.00606.x

    Article  Google Scholar 

  • Hays GC, Mazaris AD, Schofield G (2014) Different male vs. female breeding periodicity helps mitigate offspring sex ratio skews in sea turtles. Front Mar Sci 1:43

    Article  Google Scholar 

  • Hays GC, Mazaris AD, Schofield G, Laloë J-O (2017) Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination. Proc R Soc B 284(1848):20162576. https://doi.org/10.1098/rspb.2016.2576

    Article  Google Scholar 

  • Hempel S, Frieler K, Warszawski L, Schewe J, Piontek F (2013) A trend-preserving bias correction–the ISI-MIP approach. Earth Syst Dynam 4(2):219–236. https://doi.org/10.5194/esd-4-219-2013

    Article  Google Scholar 

  • Houghton J, Myers A, Lloyd C, King R, Isaacs C, Hays G (2007) Protracted rainfall decreases temperature within leatherback turtle (Dermochelys coriacea) clutches in Grenada, West Indies: ecological implications for a species displaying temperature dependent sex determination. J Exp Mar Biol Ecol 345(1):71–77. https://doi.org/10.1016/j.jembe.2007.02.001

    Article  Google Scholar 

  • Howard R, Bell I, Pike DA (2014) Thermal tolerances of sea turtle embryos: current understanding and future directions. Endanger Species Res 26(1):75–86. https://doi.org/10.3354/esr00636

    Article  Google Scholar 

  • James MC, Andrea Ottensmeyer C, Myers RA (2005) Identification of high-use habitat and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecol Lett 8(2):195–201. https://doi.org/10.1111/j.1461-0248.2004.00710.x

    Article  Google Scholar 

  • Jourdan J, Fuentes MMPB (2015) Effectiveness of strategies at reducing sand temperature to mitigate potential impacts from changes in environmental temperature on sea turtle reproductive output. Mitig Adapt Strateg Glob Chang 20(1):121–133. https://doi.org/10.1007/s11027-013-9482-y

    Article  Google Scholar 

  • Katselidis KA, Schofield G, Dimopoulos P, Stamou GN, Pantis JD (2012) Females first? Past, present and future variability in offspring sex-ratio at a temperate sea turtle breeding area. Anim Conserv 15(5):508–518. https://doi.org/10.1111/j.1469-1795.2012.00543.x

    Article  Google Scholar 

  • Katselidis KA, Schofield G, Dimopoulos P, Stamou GN, Pantis JD (2013a) Employing sea-level rise scenarios to strategically select sea turtle nesting habitat important for long-term management. J Exp Mar Biol Ecol 450:47–54

    Article  Google Scholar 

  • Katselidis KA, Schofield G, Dimopoulos P, Stamou GN, Pantis JD (2013b) Evidence based management to regulate the impact of tourism at a key sea turtle rookery. Oryx 47(04):584–594. https://doi.org/10.1017/S0030605312000385

    Article  Google Scholar 

  • Lawson AM, Weir JT (2014) Latitudinal gradients in climatic-niche evolution accelerate trait evolution at high latitudes. Ecol Lett 17(11):1427–1436. https://doi.org/10.1111/ele.12346

    Article  Google Scholar 

  • Lolavar A, Wyneken J (2015) Effect of rainfall on loggerhead turtle nest temperatures, sand temperatures and hatchling sex. Endanger Species Res 28(3):235–247. https://doi.org/10.3354/esr00684

    Article  Google Scholar 

  • Margaritoulis D (2005) Nesting activity and reproductive output of loggerhead sea turtles, Caretta caretta, over 19 seasons (1984–2002) at Laganas Bay, Zakynthos, Greece: the largest rookery in the Mediterranean. Chelonian Conserv Biol 4:916–929

    Google Scholar 

  • Margaritoulis D, Rees AF, Dean CJ, Riggall T (2011) Reproductive data of loggerhead turtles in Laganas Bay, Zakynthos Island, Greece, 2003 – 2009. Mar Turt Newsl 131:2–6

    Google Scholar 

  • Mazaris AD, Kallimanis AS, Sgardelis SP, Pantis JD (2008) Do long-term changes in sea surface temperature at the breeding areas affect the breeding dates and reproduction performance of Mediterranean loggerhead turtles? Implications for climate change. J Exp Mar Biol Ecol 367(2):219–226. https://doi.org/10.1016/j.jembe.2008.09.025

    Article  Google Scholar 

  • Mazaris AD, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2009a) Sea surface temperature variations in core foraging grounds drive nesting trends and phenology of loggerhead turtles in the Mediterranean Sea. J Exp Mar Biol Ecol 379(1-2):23–27. https://doi.org/10.1016/j.jembe.2009.07.026

    Article  Google Scholar 

  • Mazaris AD, Matsinos G, Pantis JD (2009b) Evaluating the impacts of coastal squeeze on sea turtle nesting. Ocean Coast Manag 52(2):139–145. https://doi.org/10.1016/j.ocecoaman.2008.10.005

    Article  Google Scholar 

  • Mazaris AD, Kallimanis AS, Pantis JD, Hays GC (2013) Phenological response of sea turtles to environmental variation across a species’ northern range. Proc R Soc B 280:20122397

    Article  Google Scholar 

  • McGehee MA (1990) Effects of moisture on eggs and hatchlings of loggerhead sea turtles (Caretta caretta). Herpetologica 46:251–258

  • Miller JD (1982) Embryology of marine turtles, PhD dissertation, University of New England, Armidale, New South Wales, Australia

  • Miller JD (1997) Reproduction in sea turtles. In: Lutz P, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 51–80

    Google Scholar 

  • Moran EV, Alexander JM (2014) Evolutionary responses to global change: lessons from invasive species. Ecol Lett 17(5):637–649. https://doi.org/10.1111/ele.12262

    Article  Google Scholar 

  • Mortimer JA (1990) The influence of beach sand characteristics on the nesting behavior and clutch survival of green turtles (Chelonia mydas). Copeia (3):802–817

  • Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, van Vuuren DP, Carter TR, Emori S, Kainuma M, Kram T, Meehl GA, Mitchell JFB, Nakicenovic N, Riahi K, Smith SJ, Stouffer RJ, Thomson AM, Weyant JP, Wilbanks TJ (2010) The next generation of scenarios for climate change research and assessment. Nature 463(7282):747–756. https://doi.org/10.1038/nature08823

    Article  Google Scholar 

  • Nenzén HK, Araújo M (2011) Choice of threshold alters projections of species range shifts under climate change. Ecol Model 222(18):3346–3354. https://doi.org/10.1016/j.ecolmodel.2011.07.011

    Article  Google Scholar 

  • Otero J, L'Abée-Lund JH, Castro-Santos T, Leonardsson K, Storvik GO, Jonsson B, Dempson B, Russell IC, Jensen AJ, Baglinière JL, Dionne M, Armstrong JD, Romakkaniemi A, Letcher BH, Kocik JF, Erkinaro J, Poole R, Rogan G, Lundqvist H, MacLean JC, Jokikokko E, Arnekleiv JV, Kennedy RJ, Niemelä E, Caballero P, Music PA, Antonsson T, Gudjonsson S, Veselov AE, Lamberg A, Groom S, Taylor BH, Taberner M, Dillane M, Arnason F, Horton G, Hvidsten NA, Jonsson IR, Jonsson N, McKelvey S, Naesje TF, Skaala Ø, Smith GW, Saegrov H, Stenseth NC, Vøllestad LA (2014) Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar). Glob Chang Biol 20(1):61–75. https://doi.org/10.1111/gcb.12363

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37(1):637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100

    Article  Google Scholar 

  • Patel SH, Morreale SJ, Saba VS, Panagopoulou A, Margaritoulis D, Spotila JR (2016) Climate impacts on sea turtle breeding phenology in Greece and associated foraging habitats in the wider Mediterranean region. PLoS One 11(6):e0157170. https://doi.org/10.1371/journal.pone.0157170

    Article  Google Scholar 

  • Patino-Martinez J, Marco A, Quiñones L, Hawkes L (2012) A potential tool to mitigate the impacts of climate change to the Caribbean leatherback sea turtle. Glob Chang Biol 18(2):401–411. https://doi.org/10.1111/j.1365-2486.2011.02532.x

    Article  Google Scholar 

  • Pike DA (2014) Forecasting the viability of sea turtle eggs in a warming world. Glob Chang Biol 20(1):7–15. https://doi.org/10.1111/gcb.12397

    Article  Google Scholar 

  • Pike DA, Antworth RL, Stiner JC (2006) Earlier nesting contributes to shorter nesting seasons for the loggerhead seaturtle, Caretta caretta. J Herpetol 40(1):91–94. https://doi.org/10.1670/100-05N.1

    Article  Google Scholar 

  • Poloczanska ES, Limpus CJ, Hays GC (2009) Vulnerability of marine turtles to climate change. Adv Mar Biol 56:151–211. https://doi.org/10.1016/S0065-2881(09)56002-6

    Article  Google Scholar 

  • Rees AF, Alfaro-Shigueto J, Barata PCR, Bjorndal KA, Bolten AB, Bourjea J, Broderick AC, Campbell LM, Cardona L, Carreras C, Casale P, Ceriani SA, Dutton PH, Eguchi T, Formia A, Fuentes MMPB, Fuller WJ, Girondot M, Godfrey MH, Hamann M, Hart KM, Hays GC, Hochscheid S, Kaska Y, Jensen MP, Mangel JC, Mortimer JA, Naro-Maciel E, Ng CKY, Nichols WJ, Phillott AD, Reina RD, Revuelta O, Schofield G, Seminoff JA, Shanker K, Tomás J, van de Merwe JP, van Houtan KS, Vander Zanden HB, Wallace BP, Wedemeyer-Strombel KR, Work TM, Godley BJ (2016) Are we working towards global research priorities for management and conservation of sea turtles? Endanger Species Res 31:337–382. https://doi.org/10.3354/esr00801

    Article  Google Scholar 

  • Robinson NJ, Valentine SE, Santidrián-Tomillo P, Saba VS, Spotila JR, Paladino FV (2014) Multidecadal trends in the nesting phenology of Pacific and Atlantic leatherback turtles are associated with population demography. Endanger Species Res 24(3):197–206. https://doi.org/10.3354/esr00604

    Article  Google Scholar 

  • Santidrián-Tomillo P, Saba VS, Lombard CD et al (2015) Global analysis of the effect of local climate on the hatchling output of leatherback turtles. Sci Rep 5(1):16789. https://doi.org/10.1038/srep16789

    Article  Google Scholar 

  • Schofield G, Hobson VJ, Fossette S, Lilley MK, Katselidis KA, Hays GC (2010) Biodiversity research: fidelity to foraging sites, consistency of migration routes and habitat modulation of home range by sea turtles. Divers Distrib 16(5):840–853. https://doi.org/10.1111/j.1472-4642.2010.00694.x

    Article  Google Scholar 

  • Schofield G, Dimadi A, Fossette S, Katselidis KA, Koutsoubas D, Lilley MKS, Luckman A, Pantis JD, Karagouni AD, Hays GC (2013a) Satellite tracking large numbers of individuals to infer population level dispersal and core areas for the protection of an endangered species. Divers Distrib 19(7):834–844. https://doi.org/10.1111/ddi.12077

    Article  Google Scholar 

  • Schofield G, Scott R, Dimadi A, Fossette S, Katselidis KA, Koutsoubas D, Lilley MKS, Pantis JD, Karagouni AD, Hays GC (2013b) Evidence-based marine protected area planning for a highly mobile endangered marine vertebrate. Biol Conserv 161:101–109. https://doi.org/10.1016/j.biocon.2013.03.004

    Article  Google Scholar 

  • Spotila JR (2004) Sea turtles: a complete guide to their biology, behavior, and conservation. JHU Press, Baltimore

    Google Scholar 

  • Spotila JR, Standora EA, Morreale SJ, Ruiz GJ (1987) Temperature-dependent sex determination in the green turtle Chelonia mydas: effects on the sex ratio on a natural beach. Herpetologica 43:74–81

    Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B 275(1635):649–659. https://doi.org/10.1098/rspb.2007.0997

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272(1581):2561–2569. https://doi.org/10.1098/rspb.2005.3356

    Article  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879):389–395. https://doi.org/10.1038/416389a

    Article  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3–an R package for estimation and inference about allometric lines. Methods Ecol Evol 3(2):257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x

    Article  Google Scholar 

  • Weishampel JF, Bagley DA, Ehrhart LM (2004) Earlier nesting by loggerhead sea turtles following sea surface warming. Glob Chang Biol 10(8):1424–1427. https://doi.org/10.1111/j.1529-8817.2003.00817.x

    Article  Google Scholar 

  • Weishampel JF, Bagley DA, Ehrhart LM, Weishampel AC (2010) Nesting phenologies of two sympatric sea turtle species related to sea surface temperatures. Endanger Species Res 12(1):41–47. https://doi.org/10.3354/esr00290

    Article  Google Scholar 

  • Wyneken J, Lolavar A (2015) Loggerhead sea turtle environmental sex determination: implications of moisture and temperature for climate change based predictions for species survival. J Exp Zool B Mol Dev Evol 324(3):295–314. https://doi.org/10.1002/jez.b.22620

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Ecology, School of Biology, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

    Vasiliki Almpanidou & Antonios D. Mazaris

  2. Department of Meteorology and Climatology, School of Geology, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

    Eleni Katragkou

Authors
  1. Vasiliki Almpanidou
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  2. Eleni Katragkou
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  3. Antonios D. Mazaris
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Contributions

ADM and VA conceived the study. VA and EK collected the data. VA conducted the analyses. VA led writing with contributions for all authors.

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Correspondence to Vasiliki Almpanidou.

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Almpanidou, V., Katragkou, E. & Mazaris, A.D. The efficiency of phenological shifts as an adaptive response against climate change: a case study of loggerhead sea turtles (Caretta caretta) in the Mediterranean. Mitig Adapt Strateg Glob Change 23, 1143–1158 (2018). https://doi.org/10.1007/s11027-017-9777-5

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Keywords

  • Adaptation
  • Climatic niche
  • Impact
  • Marine turtles
  • Resilience
  • Species persistence