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Body size constrains maternal investment in a small sea turtle species

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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.

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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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Barneche DR, Robertson DR, White CR, Marshall DJ (2018) Fish reproductive-energy output increases disproportionately with body size. Science 360:642–645

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Booth D (2017) The influence of incubation temperature on sea turtle hatchling quality. Integr Zool 12:352–360

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Broderick AC, Glen F, Godley BJ, Hays GC (2003) Variation in reproductive output of marine turtles. J Exp Mar Biol Ecol 288:95–109

    Google Scholar 

  • Caldwell DK, Carr A, Ogren L (1959) Nesting and migration of the Atlantic loggerhead turtle. Bull Florida State Mus 4:295–308

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Christiansen JS, Fevolden SE, Karamushko OV, Karamushko LI (1998) Maternal output in polar fish reproduction fishes of Antarctica. Springer, Berlin, pp 41–52

    Google Scholar 

  • 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

    Google Scholar 

  • Congdon JD (1989) Proximate and evolutionary constraints on energy relations of reptiles. Physiol Zool 62:356–373

    Google Scholar 

  • Congdon JD, Gibbons JW (1987) Morphological constraint on egg size: a challenge to optimal egg size theory? Proc Natl Acad Sci 84:4145–4147

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Frazier J (1983) Analisis estadistico de la tortuga golfina Lepidochelys olivacea (Eschscholtz) de Oaxaca, Mexico. Cienc Pesq 4:49–75

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Georges J-Y, Fossette S (2006) Estimating body mass in leatherback turtles Dermochelys coriacea. Mar Ecol Prog Ser 318:255–262

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gyuris E (1994) The rate of predation by fishes on hatchlings of the green turtle (Chelonia mydas). Coral Reefs 13:137–144

    Google Scholar 

  • 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

    Google Scholar 

  • Hatase H, Omuta K, Tsukamoto K (2013) A mechanism that maintains alternative life histories in a loggerhead sea turtle population. Ecology 94:2583–2594

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Janzen FJ (1993) An experimental analysis of natural selection on body size of hatchling turtles. Ecology 74:332–341

    Google Scholar 

  • 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

    Google Scholar 

  • Lack D (1947) The significance of clutch-size. Ibis 89:302–352

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Moran A, Emlet R (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology 82:1597–1612

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Paladino FV, O’Connor MP, Spotila JR (1990) Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344:858–860

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Pike DA, Roznik EA, Bell I (2015) Nest inundation from sea-level rise threatens sea turtle population viability. R Soc Open Sci 2:150127

    PubMed  PubMed Central  Google Scholar 

  • Plotkin P (2003) Adult migrations and habitat use. Biol Sea Turt 2:225–241

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Roff D (1993) Evolution of life histories: theory and analysis. Springer, Berlin

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Shine R, Harlow PS (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77:1808–1817

    Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Zbinden JA, Margaritoulis D, Arlettaz R (2006) Metabolic heating in Mediterranean loggerhead sea turtle clutches. J Exp Mar Biol Ecol 334:151–157

    Google Scholar 

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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.

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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.

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All authors conceived and designed the experiments, contributed to the data collection, and participated in writing the manuscript. CG conducted the data analyses.

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Correspondence to Christopher R. Gatto.

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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.

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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

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