Abstract
To maximise reproductive fitness, species make trade-offs among reproductive traits, e.g., offspring quantity vs. offspring size, within energetic, anatomical, and physiological constraints. Sea turtles are a model taxon to study reproductive trade-offs, because they lack parental care and because there are strong selective pressures on hatchlings due to high predation rates. Natural selection therefore typically favours optimising offspring size over offspring quantity. Nevertheless, the balance between these traits varies between both sea turtle populations and species. Here, we quantified individual variation in reproductive traits of olive ridley turtles (Lepidochelys olivacea) in northwest Costa Rica. Olive ridley females displayed considerable inter-female variation in reproductive traits with larger females producing larger clutches. These larger females also produced longer and heavier hatchlings than smaller females despite producing similar sized eggs. Females did not exhibit a trade-off between clutch size and egg mass, although variation in clutch size (coefficient of variation = 16.8%) was greater than that of egg mass (10.1%). Producing more eggs per clutch had 1.8 times the effect of producing heavier eggs at increasing clutch mass. The effect of clutch frequency was 2.5 times that of clutch size on seasonal egg production and 2.4 times that of clutch size on seasonal hatchling production. In conclusion, olive ridley turtles exhibit considerable variation in reproductive traits, but their small body size constrains clutch size and has implications for their overall reproductive output.
Similar content being viewed by others
Availability of data and material
The datasets generated during and/or analysed during the current study are available from the corresponding authors on reasonable request and with permission of The Leatherback Trust.
References
Allen RM, Marshall D (2014) Egg size effects across multiple life-history stages in the marine annelid Hydroides diramphus. PLoS ONE 9:e102253
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
Barneche DR, Robertson DR, White CR, Marshall DJ (2018) Fish reproductive-energy output increases disproportionately with body size. Science 360:642–645
Barrientos-Muñoz KG, Ramírez-Gallego C, Páez V (2014) Nesting ecology of the olive ridley sea turtle (Lepidochelys olivacea) (Cheloniidae) at El Valle Beach, Northern Pacific, Colombia. Acta Biológica Colombiana 19:437–445
Bell BA, Spotila JR, Paladino FV, Reina RD (2004) Low reproductive success of leatherback turtles, Dermochelys coriacea, is due to high embryonic mortality. Biol Conserv 115:131–138
Bézy VS, Valverde RA, Plante CJ (2015) Olive ridley sea turtle hatching success as a function of the microbial abundance in nest sand at Ostional, Costa Rica. PLoS ONE 10:e0118579
Binckley CA, Spotila JR, Wilson KS, Paladino FV (1998) Sex determination and sex ratios of Pacific leatherback turtles, Dermochelys coriacea. Copeia 1998(2):291–300
Bjorndal KA, Carr A (1989) Variation in clutch size and egg size in the green turtle nesting population at Tortuguero, Costa Rica. Herpetologica 45:181–189
Bjorndal KA, Carr A, Meylan AB, Mortimer JA (1985) Reproductive biology of the hawksbill Eretmochelys imbricata at Tortuguero, Costa Rica, with notes on the ecology of the species in the Caribbean. Biol Conserv 34:353–368
Booth D (2017) The influence of incubation temperature on sea turtle hatchling quality. Integr Zool 12:352–360
Booth D, Astill K (2001) Temperature variation within and between nests of the green sea turtle, Chelonia mydas (Chelonia: Cheloniidae) on Heron Island, Great Barrier Reef. Aust J Zool 49:71–84
Bowden R, Harms H, Paitz R, Janzen F (2004) Does optimal egg size vary with demographic stage because of a physiological constraint? Funct Ecol 18:522–529
Broderick AC, Godley BJ, Hays GC (2001) Trophic status drives interannual variability in nesting numbers of marine turtles. Proc R Soc Lond B 268:1481–1487
Broderick AC, Glen F, Godley BJ, Hays GC (2003) Variation in reproductive output of marine turtles. J Exp Mar Biol Ecol 288:95–109
Caldwell DK, Carr A, Ogren L (1959) Nesting and migration of the Atlantic loggerhead turtle. Bull Florida State Mus 4:295–308
Cavallo C, Dempster T, Kearney MR, Kelly E, Booth D, Hadden KM, Jessop TS (2015) Predicting climate warming effects on green turtle hatchling viability and dispersal performance. Funct Ecol 29:768–778
Chen C-L, Wang C-C, Cheng I-J (2010) Effects of biotic and abiotic factors on the oxygen content of green sea turtle nests during embryogenesis. J Comp Physiol B 180:1045–1055
Christiansen JS, Fevolden SE, Karamushko OV, Karamushko LI (1998) Maternal output in polar fish reproduction fishes of Antarctica. Springer, Berlin, pp 41–52
Colman LP, Sampaio CLS, Weber MI, de Castilhos JC (2014) Diet of olive Ridley sea turtles, Lepidochelys olivacea, in the waters of Sergipe, Brazil. Chelonian Conserv Biol 13:266–271
Congdon JD (1989) Proximate and evolutionary constraints on energy relations of reptiles. Physiol Zool 62:356–373
Congdon JD, Gibbons JW (1987) Morphological constraint on egg size: a challenge to optimal egg size theory? Proc Natl Acad Sci 84:4145–4147
Dapp D, Arauz R, Spotila JR, O’Connor MP (2013) Impact of Costa Rican longline fishery on its bycatch of sharks, stingrays, bony fish and olive ridley turtles (Lepidochelys olivacea). J Exp Mar Biol Ecol 448:228–239
Dornfeld TC, Robinson NJ, Tomillo PS, Paladino FV (2015) Ecology of solitary nesting olive ridley sea turtles at Playa Grande, Costa Rica. Mar Biol 162:123–139
Doyle TK, Houghton JD, McDevitt R, Davenport J, Hays GC (2007) The energy density of jellyfish: estimates from bomb-calorimetry and proximate-composition. J Exp Mar Biol Ecol 343:239–252
Ekanayake E, Kapurusinghe T, Saman M, Rathnakumara D, Samaraweera P, Rajakaruna R (2016) Reproductive output and morphometrics of green turtle, Chelonia mydas nesting at the Kosgoda rookery in Sri Lanka. Ceylon J Sci 45:103–116
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 17:245–251
Foley AM, Peck SA, Harman GR (2006) Effects of sand characteristics and inundation on the hatching success of loggerhead sea turtle (Caretta caretta) clutches on low-relief mangrove islands in southwest Florida. Chelonian Conserv Biol 5:32–41
Frazer NB, Richardson JI (1986) The relationship of clutch size and frequency to body size in loggerhead turtles, Caretta caretta. J Herpetol 20:81–84
Frazier J (1983) Analisis estadistico de la tortuga golfina Lepidochelys olivacea (Eschscholtz) de Oaxaca, Mexico. Cienc Pesq 4:49–75
Garrett K, Wallace BP, Garner J, Paladino FV (2010) Variations in leatherback turtle nest environments: consequences for hatching success. Endanger Species Res 11:147–155
Gatto CR, Reina RD (2020) Sea turtle hatchling locomotor performance: incubation moisture effect, ontogeny and species-specific patterns. J Comp Physiol B 190(6):779–793
Georges J-Y, Fossette S (2006) Estimating body mass in leatherback turtles Dermochelys coriacea. Mar Ecol Prog Ser 318:255–262
Glen F, Broderick A, Godley B, Hays G (2003) Incubation environment affects phenotype of naturally incubated green turtle hatchlings. J Mar Biol Assoc U K 83:1183–1186
Guisande C, Sanchez J, Maneiro I, Miranda A (1996) Trade-off between offspring number and offspring size in the marine copepod Euterpina acutifrons at different food concentrations. Mar Ecol Prog Ser 143:37–44
Gyuris E (1994) The rate of predation by fishes on hatchlings of the green turtle (Chelonia mydas). Coral Reefs 13:137–144
Gyuris E (2000) The relationship between body size and predation rates on hatchlings of the green turtle (Chelonia mydas): is bigger better. Academic Press, New York
Hatase H, Omuta K, Tsukamoto K (2013) A mechanism that maintains alternative life histories in a loggerhead sea turtle population. Ecology 94:2583–2594
Hatase H, Omuta K, Komatsu T (2014) Do loggerhead turtle (Caretta caretta) eggs vary with alternative foraging tactics? J Exp Mar Biol Ecol 455:56–61
Hatase H, Omuta K, Komatsu T (2015) Loggerhead turtle (Caretta caretta) offspring size does not vary with maternal alternative foraging behaviors: support for their phenotypic plasticity. Mar Biol 162:1567–1578
Hatase H, Omuta K, Itou K, Komatsu T (2018) Effect of maternal foraging habitat on offspring quality in the loggerhead sea turtle (Caretta caretta). Ecol Evol 8:3543–3555
Hays GC, Speakman JR (1991) Reproductive investment and optimum clutch size of loggerhead sea turtles (Caretta caretta). J Anim Ecol 60(2):455–462
Hirth HF (1980) Some aspects of the nesting behavior and reproductive biology of sea turtles. Am Zool 20:507–523
Hughes GR (1973) The sea turtles of South East Africa. Department of Animal Biology
Hussey NE, Wintner SP, Dudley SF, Cliff G, Cocks DT, MacNeil MA (2010) Maternal investment and size-specific reproductive output in carcharhinid sharks. J Anim Ecol 79:184–193
Ito K (1997) Egg-size and-number variations related to maternal size and age, and the relationship between egg size and larval characteristics in an annual marine gastropod, Haloa japonica (Opisthobranchia; Cephalaspidea). Mar Ecol Prog Ser 152:187–195
Janzen FJ (1993) An experimental analysis of natural selection on body size of hatchling turtles. Ecology 74:332–341
Janzen F, Tucker J, Paukstis G (2000) Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. J Evol Biol 13:947–954
Lack D (1947) The significance of clutch-size. Ibis 89:302–352
Le Gouvello DZ, Nel R, Cloete AE (2020) The influence of individual size on clutch size and hatchling fitness traits in sea turtles. J Exp Mar Biol Ecol 527:151372
LeBlanc AM, Rostal DC, Drake KK, Williams KL, Frick MG, Robinette J, Barnard-Keinath DE (2014) The influence of maternal size on the eggs and hatchlings of loggerhead sea turtles. Southeast Nat 13:587–600
Llodra ER (2002) Fecundity and life-history strategies in marine invertebrates. Adv Mar Biol 43:87–170
Marshall DJ, Keough MJ (2008) The relationship between offspring size and performance in the sea. Am Nat 171:214–224
Matsuzawa Y, Sato K, Sakamoto W, Bjorndal K (2002) Seasonal fluctuations in sand temperature: effects on the incubation period and mortality of loggerhead sea turtle (Caretta caretta) pre-emergent hatchlings in Minabe, Japan. Mar Biol 140:639–646
Maulany RI, Booth D, Baxter G (2012) The effect of incubation temperature on hatchling quality in the olive ridley turtle, Lepidochelys olivacea, from Alas Purwo National Park, East Java, Indonesia: implications for hatchery management. Mar Biol 159:2651–2661
Miller JD (1997) Reproduction in sea turtles. In: Lutz PL, Musick J (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 51–81
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
Moran A, Emlet R (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology 82:1597–1612
Mueller MS, Ruiz-García NA, García-Gasca A, Abreu-Grobois FA (2019) Best swimmers hatch from intermediate temperatures: effect of incubation temperature on swimming performance of olive ridley sea turtle hatchlings. J Exp Mar Biol Ecol 519:151186
Olsson M, Shine R (1997) The limits to reproductive output: offspring size versus number in the sand lizard (Lacerta agilis). Am Nat 149:179–188
Önder BF, Candan O (2016) The feminizing effect of metabolic heating in Green Turtle (Chelonia mydas) clutches in the eastern Mediterranean. Zool Middle East 62:239–246
Paladino FV, O’Connor MP, Spotila JR (1990) Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344:858–860
Patel SH, Panagopoulou A, Morreale SJ, Kilham SS, Karakassis I, Riggall T, Margaritoulis D, Spotila JR (2015) Differences in size and reproductive output of loggerhead turtles Caretta caretta nesting in the eastern Mediterranean Sea are linked to foraging site. Mar Ecol Prog Ser 535:231–241
Peavey LE, Popp BN, Pitman RL, Gaines SD, Arthur KE, Kelez S, Seminoff JA (2017) Opportunism on the high seas: foraging ecology of olive ridley turtles in the eastern Pacific Ocean. Front Mar Sci 4:348
Pike DA, Roznik EA, Bell I (2015) Nest inundation from sea-level rise threatens sea turtle population viability. R Soc Open Sci 2:150127
Plotkin P (2003) Adult migrations and habitat use. Biol Sea Turt 2:225–241
Plotkin PT (2010) Nomadic behaviour of the highly migratory olive ridley sea turtle Lepidochelys olivacea in the eastern tropical Pacific Ocean. Endanger Species Res 13:33–40
Price ER, Wallace BP, Reina RD, Spotila JR, Paladino FV, Piedra R, Vélez E (2004) Size, growth, and reproductive output of adult female leatherback turtles Dermochelys coriacea. Endanger Species Res 5:1–8
Ralph CR, Reina RD, Wallace BP, Sotherland PR, Spotila JR, Paladino FV (2005) Effect of egg location and respiratory gas concentrations on developmental success in nests of the leatherback turtle, Dermochelys coriacea. Aust J Zool 53:289–294
Reina RD, Mayor PA, Spotila JR, Piedra R, Paladino FV (2002) Nesting ecology of the leatherback turtle, Dermochelys coriacea, at Parque Nacional Marino las Baulas, Costa Rica: 1988–1989 to 1999–2000. Copeia 2002:653–664
Rings CC, Rafferty AR, Guinea ML, Reina RD (2014) The impact of extended preovipositional arrest on embryonic development and hatchling fitness in the flatback sea turtle. Physiol Biochem Zool 88:116–127
Robinson NJ, Valentine SE, Tomillo PS, 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 24:197–206
Roff D (1993) Evolution of life histories: theory and analysis. Springer, Berlin
Rusli MU, Booth DT, Joseph J (2016) Synchronous activity lowers the energetic cost of nest escape for sea turtle hatchlings. J Exp Biol 219:1505–1513
Saba VS, Santidrián-Tomillo P, Reina RD, Spotila JR, Musick JA, Evans DA, Paladino FV (2007) The effect of the El Niño Southern Oscillation on the reproductive frequency of eastern Pacific leatherback turtles. J Appl Ecol 44:395–404
Saba VS, Stock CA, Spotila JR, Paladino FV, Tomillo PS (2012) Projected response of an endangered marine turtle population to climate change. Nat Climate Change 2:814–820
Santidrián Tomillo P, Vélez E, Reina RD, Piedra R, Paladino FV, Spotila JR (2007) Reassessment of the leatherback turtle (Dermochelys coriacea) nesting population at Parque Nacional Marino Las Baulas, Costa Rica: effects of conservation efforts. Chelonian Conserv Biol 6:54–62
Santidrián Tomillo P, Suss JS, Wallace BP, Magrini KD, Blanco G, Paladino FV, Spotila JR (2009) Influence of emergence success on the annual reproductive output of leatherback turtles. Mar Biol 156:2021–2031
Santidrián Tomillo P, Paladino FV, Suss JS, Spotila JR (2010) Predation of leatherback turtle hatchlings during the crawl to the water. Chelonian Conserv Biol 9:18–25
Santidrián Tomillo P, Saba VS, Blanco GS, Stock CA, Paladino FV, Spotila JR (2012) Climate driven egg and hatchling mortality threatens survival of Eastern Pacific leatherback turtles. PLoS ONE 7:e37602
Santidrián Tomillo P, Oro D, Paladino FV, Piedra R, Sieg AE, Spotila JR (2014) High beach temperatures increased female-biased primary sex ratios but reduced output of female hatchlings in the leatherback turtle. Biol Conserv 176:71–79
Santidrián Tomillo P, Fonseca L, Ward M, Tankersley N, Robinson N, Orrego C, Paladino F, Saba V (2020) The impacts of extreme El Niño events on sea turtle nesting populations. Clim Change 159:163–176
Shine R, Harlow PS (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77:1808–1817
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Tiwari M, Bjorndal KA (2000) Variation in morphology and reproduction in loggerheads, Caretta caretta, nesting in the United States, Brazil, and Greece. Herpetologica 56:343–356
Tucker AD, Frazer NB (1991) Reproductive variation in leatherback turtles, Dermochelys coriacea, at Culebra National Wildlife Refuge, Puerto Rico. Herpetologica 47(1):115–124
Van De Merwe J, Ibrahim K, Whittier J (2006) Effects of nest depth, shading, and metabolic heating on nest temperatures in sea turtle hatcheries. Chelonian Conserv Biol 5:210–215
Wallace BP, Sotherland PR, Spotila JR, Reina RD, Franks BF, Paladino FV (2004) Biotic and abiotic factors affect the nest environment of embryonic leatherback turtles, Dermochelys coriacea. Physiol Biochem Zool 77:423–432
Wallace BP, Kilham SS, Paladino FV, Spotila JR (2006a) Energy budget calculations indicate resource limitation in Eastern Pacific leatherback turtles. Mar Ecol Prog Ser 318:263–270
Wallace BP, Sotherland PR, Tomillo PS, Bouchard SS, Reina RD, Spotila JR, Paladino FV (2006b) Egg components, egg size, and hatchling size in leatherback turtles. Comp Biochem Physiol A: Mol Integr Physiol 145:524–532
Wallace BP, Sotherland PR, Tomillo PS, Reina RD, Spotila JR, Paladino FV (2007) Maternal investment in reproduction and its consequences in leatherback turtles. Oecologia 152:37–47
Zbinden JA, Margaritoulis D, Arlettaz R (2006) Metabolic heating in Mediterranean loggerhead sea turtle clutches. J Exp Mar Biol Ecol 334:151–157
Acknowledgements
Thank you to all of the field assistants and volunteers who helped collect the data used in this study. Thank you to the Ministry of Environment and Energy of Costa Rica (MINAE) for grating the research permits. Thank you to three anonymous reviewers for their useful comments on this manuscript. This work was supported by The Leatherback Trust, Purdue University Schrey Professorship, the Betz Chair of Environmental Science at Drexel University, and the Earthwatch Institute. This research was conducted under Purdue University Animal Care approval #131000989.
Funding
This work was supported by The Leatherback Trust, Purdue University Schrey Professorship, the Betz Chair of Environmental Science at Drexel University, and the Earthwatch Institute.
Author information
Authors and Affiliations
Contributions
All authors conceived and designed the experiments, contributed to the data collection, and participated in writing the manuscript. CG conducted the data analyses.
Corresponding author
Ethics declarations
Conflict of interest
The authors do not have any conflicts of interest to declare.
Ethical approval
All applicable international, national, and/or institutional guidelines for sampling, care, and experimental use of organisms for the study have been followed, and all necessary approvals have been obtained. This research was conducted under Purdue University Animal Care approval #131000989.
Additional information
Responsible Editor: L. Avens.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by J. Miller, S. Patel and an undisclosed expert.
Rights and permissions
About this article
Cite this article
Gatto, C.R., Robinson, N.J., Spotila, J.R. et al. Body size constrains maternal investment in a small sea turtle species. Mar Biol 167, 182 (2020). https://doi.org/10.1007/s00227-020-03795-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-020-03795-7