Abstract
For reptiles, the incubation environment experienced by embryos during development plays a major role in many biological processes. The unprecedented rate of climate change makes it critical to understand the effects that the incubation environment has on developing embryos, particularly in imperiled species such as chelonians. Consequently, a number of studies have focused on the effects of different environmental conditions on several developmental processes and hatchling phenotypic traits. In addition to the incubation environment, it is also essential to understand how parental contributions can influence hatchling quality. This is the first study that investigates the effects of parental origin and incubation conditions on sea turtle embryonic development and hatchling phenotype in nests incubating in the field (rather than under controlled laboratory conditions). Here, we used the loggerhead sea turtle (Caretta caretta) to investigate the effects of parental origin (clutch), incubation temperature, and the nest hydric environment on embryonic growth, incubation durations, hatching success, and hatchling phenotype. Our results show that nest moisture and temperature affect embryo mass towards the last third of development, with hatchling size positively correlated with nest moisture content, and maternal origin had a strong impact on hatching success and hatchling size regardless of the incubation conditions. The results from this experiment identify multiple factors that affect turtle embryonic development under field incubation conditions, a fundamental consideration when interpreting the potential impacts of climate change on reptilian development.
Similar content being viewed by others
References
Ackerman RA (1997) The nest environment and the embryonic development of sea turtles. Biol Sea Turt 1:83–106
Ackerman RA, Seagrave RC, Dmi’el R, Ar A (1985) Water and heat exchange between parchment-shelled reptile eggs and their surroundings. Copeia 1985:703. https://doi.org/10.2307/1444764
Bates DM, Maechler M, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105. https://doi.org/10.1093/icb/36.2.83
Bodensteiner BL, Mitchell TS, Strickland JT, Janzen FJ (2015) Hydric conditions during incubation influence phenotypes of neonatal reptiles in the field. Funct Ecol 29:710–717. https://doi.org/10.1111/1365-2435.12382
Booth D (2002) Incubation of rigid-shelled turtle eggs: do hydric conditions matter? J Comp Physiol B 172:627–633
Booth DT, Burgess E, McCosker J, Lanyon JM (2004) The influence of incubation temperature on post-hatching fitness characteristics of turtles. Int Congr Ser 1275:226–233. https://doi.org/10.1016/j.ics.2004.08.057
Booth DT, Feeney R, Shibata Y (2013) Nest and maternal origin can influence morphology and locomotor performance of hatchling green turtles (Chelonia mydas) incubated in field nests. Mar Biol 160:127–137. https://doi.org/10.1007/s00227-012-2070-y
Brooks RJ, Bobyn ML, Galbraith DA et al (1991) Maternal and environmental influences on growth and survival of embryonic and hatchling snapping turtles (Chelydra serpentina ). Can J Zool 69:2667–2676. https://doi.org/10.1139/z91-375
Delmas V, Bonnet X, Girondot M, Prévot-Julliard A (2008) Varying hydric conditions during incubation influence egg water exchange and hatchling phenotype in the red-eared slider turtle. Physiol Biochem Zool 81:345–355. https://doi.org/10.1086/529459
Dinno A (2015) Nonparametric pairwise multiple comparisons in independent groups using Dunn’s test. Stata J 15:292–300
Elphick MJ, Shine R (1998) Longterm effects of incubation temperatures on the morphology and locomotor performance of hatchling lizards (Bassiana duperreyi, Scincidae). Biol J Linn Soc 63:429–447. https://doi.org/10.1111/j.1095-8312.1998.tb01527.x
Erb V, Lolavar A, Wyneken J (2018) The role of sand moisture in shaping loggerhead sea turtle (Caretta Caretta) neonate growth in Southeast Florida. Chelonian Conserv Biol 17:245. https://doi.org/10.2744/CCB-1301.1
Georges A, Beggs K, Young JE, Doody JS (2005) Modelling development of reptile embryos under fluctuating temperature regimes. Physiol Biochem Zool 78:18–30. https://doi.org/10.1086/425200
Gilbert SF, Epel D (2015) Ecological developmental biology: the environmental regulation of development, health, and evolution. Sinauer Associates, Incorporated Publishers, Sunderland
Gillooly JF, Dodson SI (2000) The relationship of neonate mass and incubation temperature to embryonic development time in a range of animal taxa. J Zool 251:369–375. https://doi.org/10.1111/j.1469-7998.2000.tb01087.x
Gillooly JF, Charnov EL, West GB et al (2002) Effects of size and temperature on developmental time. Nature 417:70–73. https://doi.org/10.1038/417070a
Guirlet E, Das K, Thomé J-P, Girondot M (2010) Maternal transfer of chlorinated contaminants in the leatherback turtles, Dermochelys coriacea, nesting in French Guiana. Chemosphere 79:720–726. https://doi.org/10.1016/j.chemosphere.2010.02.047
Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2007) Investigating the potential impacts of climate change on a marine turtle population. Glob Change Biol 13:923–932. https://doi.org/10.1111/j.1365-2486.2007.01320.x
Hawkes L, Broderick A, Godfrey M, Godley B (2009) Climate change and marine turtles. Endanger Species Res 7:137–154. https://doi.org/10.3354/esr00198
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 Change Biol 9:642–646. https://doi.org/10.1046/j.1365-2486.2003.00606.x
Hewavisenthi S, Parmenter CJ (2002) Egg components and utilization of yolk lipids during development of the flatback turtle Natator depressus. J Herpetol 36:43–50. https://doi.org/10.1670/0022-1511(2002)036[0043:ECAUOY]2.0.CO;2
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Howard R, Bell I, Pike D (2014) Thermal tolerances of sea turtle embryos: current understanding and future directions. Endanger Species Res 26:75–86. https://doi.org/10.3354/esr00636
Janzen FJ (1993) An experimental analysis of natural selection on body size of hatchling turtles. Ecology 74:332–341. https://doi.org/10.2307/1939296
Janzen FJ, Ast JC, Paukstis GL (1995) Influence of the hydric environment and clutch on eggs and embryos of two sympatric map turtles. Funct Ecol 9:913. https://doi.org/10.2307/2389990
Janzen FJ, Tucker JK, Paukstis GL (2000) Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81:2290–2304. https://doi.org/10.1890/0012-9658(2000)081[2290:EAOAEL]2.0.CO;2
Kamel SJ, Mrosovsky N (2004) Nest site selection in leatherbacks, Dermochelys coriacea: individual patterns and their consequences. Anim Behav 68:357–366
Laloë J-O, Cozens J, Renom B et al (2017) Climate change and temperature-linked hatchling mortality at a globally important sea turtle nesting site. Glob Change Biol 23:4922–4931
Lasala JA, Hughes CR, Wyneken J (2018) Breeding sex ratio and population size of loggerhead turtles from Southwestern Florida. PLoS ONE 13:e0191615. https://doi.org/10.1371/journal.pone.0191615
Limpus CJ, Baker V, Miller JD (1979) Movement induced mortality of loggerhead eggs. Herpetologica 35:335–338
Lolavar A, Wyneken J (2015) Effect of rainfall on loggerhead turtle nest temperatures, sand temperatures and hatchling sex. Endanger Species Res 28:235–247. https://doi.org/10.3354/esr00684
Lolavar A, Wyneken J (2017) Experimental assessment of the effects of moisture on loggerhead sea turtle hatchling sex ratios. Zoology 123:64–70. https://doi.org/10.1016/j.zool.2017.06.007
Maloney JE, Darian-Smith C, Takahashi Y, Limpus CJ (1990) The environment for development of the embryonic loggerhead turtle (Caretta caretta) in Queensland. Copeia 1990:378. https://doi.org/10.2307/1446343
Miller JD (1997) Reproduction in sea turtles. Biol Sea Turt 1:51–82
Miller JD, Mortimer JA, Limpus CJ (2017) A field key to the developmental stages of marine turtles (Cheloniidae) with notes on the development of Dermochelys. Chelonian Conserv Biol 16:111–122. https://doi.org/10.2744/CCB-1261.1
Mitchell TS, Warner DA, Janzen FJ (2013) Phenotypic and fitness consequences of maternal nest-site choice across multiple early life stages. Ecology 94:336–345. https://doi.org/10.1890/12-0343.1
Mitchell TS, Maciel JA, Janzen FJ (2015) Maternal effects influence phenotypes and survival during early life stages in an aquatic turtle. Funct Ecol 29:268–276. https://doi.org/10.1111/1365-2435.12315
Monsinjon JR, Wyneken J, Rusenko K et al (2019) The climatic debt of loggerhead sea turtle populations in a warming world. Ecol Indic 107:105657
Morris KA, Packard GC, Boardman TJ et al (1983) Effect of the hydric environment on growth of embryonic snapping turtles (Chelydra serpentina). Herpetologica 39:272–285
Mrosovsky N, Yntema CL (1980) Temperature dependence of sexual differentiation in sea turtles: implications for conservation practices. Biol Conserv 18:271–280. https://doi.org/10.1016/0006-3207(80)90003-8
Packard GC, Packard MJ (2001) Environmentally induced variation in size, energy reserves and hydration of hatchling Painted Turtles, Chrysemys picta. Funct Ecol 15:481–489. https://doi.org/10.1046/j.0269-8463.2001.00543.x
Packard GC, Tracy CR, Roth JJ (1977) The physiological ecology of reptilian eggs and embryos. And the evolution of viviparity within the class Reptilia. Biol Rev 52:71–105. https://doi.org/10.1111/j.1469-185X.1977.tb01346.x
Packard GC, Packard MJ, Miller K, Boardman TJ (1987) Influence of moisture, temperature, and substrate on snapping turtle eggs and embryos. Ecology 68:983–993. https://doi.org/10.2307/1938369
Packard GC, Packard MJ, Birchard GF (1989) Sexual differentiation and hatching success by painted turtles incubating in different thermal and hydric environments. Herpetologica 45:385–392
Perrault J, Wyneken J, Thompson LJ et al (2011) Why are hatching and emergence success low? Mercury and selenium concentrations in nesting leatherback sea turtles (Dermochelys coriacea) and their young in Florida. Mar Pollut Bull 62:1671–1682. https://doi.org/10.1016/j.marpolbul.2011.06.009
Pieau C, Mrosovsky N (1991) Transitional range of temperature, pivotal temperatures and thermosensitive stages for sex determination in reptiles. Amphib Reptil 12:169–179. https://doi.org/10.1163/156853891X00149
Reneker JL, Kamel SJ (2016) The maternal legacy: female identity predicts offspring sex ratio in the loggerhead sea turtle. Sci Rep 6:1–8. https://doi.org/10.1038/srep29237
Rhodin AGJ, Stanford CB, Dijk PPV et al (2018) Global conservation status of turtles and tortoises (order Testudines). Chelonian Conserv Biol 17:135. https://doi.org/10.2744/CCB-1348.1
Salmon M, Scholl J (2014) Allometric growth in juvenile marine turtles: possible role as an antipredator adaptation. Zoology 117:131–138. https://doi.org/10.1016/j.zool.2013.11.004
Salmon M, Wyneken J, Hamann M, Whiting S (2016) Early growth and development of morphological defenses in post-hatchling flatbacks (Natator depressus) and green turtles (Chelonia mydas). Mar Freshw Behav Physiol 49:421–435. https://doi.org/10.1080/10236244.2016.1241460
Santos RG, Pinheiro HT, Martins AS et al (2016) The anti-predator role of within-nest emergence synchrony in sea turtle hatchlings. Proc R Soc B Biol Sci 283:20160697. https://doi.org/10.1098/rspb.2016.0697
Sheriff MJ, Krebs CJ, Boonstra R (2010) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–2994. https://doi.org/10.1890/09-1108.1
Sifuentes-Romero I, Tezak BM, Milton SL, Wyneken J (2018) Hydric environmental effects on turtle development and sex ratio. Zoology 126:89–97. https://doi.org/10.1016/j.zool.2017.11.009
Siviter H, Charles Deeming D, Rosenberger J et al (2017) The impact of egg incubation temperature on the personality of oviparous reptiles. Anim Cogn 20:109–116. https://doi.org/10.1007/s10071-016-1030-1
Steyermark AC, Spotila JR (2001) Effects of maternal identity and incubation temperature on hatching and hatchling morphology in snapping turtles, Chelydra serpentina. Copeia 2001:129–135. https://doi.org/10.1643/0045-8511(2001)001[0129:EOMIAI]2.0.CO;2
Team RC (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.r-proj.org
Tezak BM, Sifuentes-Romero I, Wyneken J (2018) A new approach for measuring temperature inside turtle eggs. J Exp Biol 221:jeb188698. https://doi.org/10.1242/jeb.188698
Tucker JK, Filoramo NI, Paukstis GL, Janzen FJ (1998) Response of red-eared slider, Trachemys scripta elegans, eggs to slightly differing water potentials. J Herpetol 32:124. https://doi.org/10.2307/1565492
van Buskirk J, Crowder LB (1994) Life-history variation in marine turtles. Copeia 1994:66. https://doi.org/10.2307/1446672
van de Merve J, Hodge M, Whittier J et al (2010) Persistent organic pollutants in the green sea turtle Chelonia mydas: nesting population variation, maternal transfer, and effects on development. Mar Ecol Prog Ser 403:269–278. https://doi.org/10.3354/meps08462
Wallace BP, Sotherland PR, Santidrian Tomillo P et al (2007) Maternal investment in reproduction and its consequences in leatherback turtles. Oecologia 152:37–47. https://doi.org/10.1007/s00442-006-0641-7
Weaver ICG, Cervoni N, Champagne FA et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854. https://doi.org/10.1038/nn1276
Wyneken J, Lolavar A (2015) Loggerhead sea turtle environmental sex determination: Implications of moisture and temperature for climate change based predictions for species survival: environmental sex determination in loggerhead turtles. J Exp Zoolog B Mol Dev Evol 324:295–314. https://doi.org/10.1002/jez.b.22620
Yntema CL (1978) Incubation times for eggs of the turtle Chelydra serpentina (Testudines: Chelydridae) at various temperatures. Herpetologica 34:274–277
Yntema CL, Mrosovsky N (1982) Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Can J Zool 60:1012–1016. https://doi.org/10.1139/z82-141
Zimm R, Bentley BP, Wyneken J, Moustakas-Verho JE (2017) Environmental causation of turtle scute anomalies in ovo and in silico. Integr Comp Biol 57:1303–1311. https://doi.org/10.1093/icb/icx066
Acknowledgements
We thank Dr. J. Wyneken for her guidance and constructive advice. This work would not be possible without the help from the staff of the Loggerhead Marinelife Center during the egg-collection process, particularly S. Hirsch and Dr. J. Perrault. The study was improved by FAU’s Marine Turtle Lab members who assisted and provided intellectual discussion. A special thanks to Morgan Baer and Motion Watersports for making our lives infinitely easier during the field data collection portion of this project. All work was done in accordance with animal care and use protocols approved by the Institutional Animal Care and Usage Committee at Florida Atlantic University (IACUC A13-04). Egg manipulations and sample collection were permitted through Florida Fish and Wildlife Conservation Commission (FWC Permits: MTP# 073A). The study was funded by grants awarded by the National Save the Sea Turtle Foundation, as well as funds from the Nelligan Sea Turtle Fund.
Author information
Authors and Affiliations
Contributions
BT and ISR conceived the idea for this project and came up with the experimental design. BT, ISR, MA, TS,and SM collected the data, BB led data analysis, BT and BB led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Additional information
Communicated by Mathew Samuel Crowther.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tezak, B., Bentley, B., Arena, M. et al. Incubation environment and parental identity affect sea turtle development and hatchling phenotype. Oecologia 192, 939–951 (2020). https://doi.org/10.1007/s00442-020-04643-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04643-7