Skip to main content
SpringerLink
Log in

Loggerhead turtle (Caretta caretta) offspring size does not vary with maternal alternative foraging behaviors: support for their phenotypic plasticity

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Revealing the causes and consequences of differential habitat use among previously untrackable species will help advance our understanding of how organisms have survived and adapted during their evolutionary histories. Among loggerhead sea turtles (Caretta caretta) nesting on one Japanese beach, small females tend to forage on planktonic prey in oceanic waters (depth >200 m) as the juveniles do, while large females tend to forage on benthic prey in neritic waters (depth <200 m). These alternative foraging behaviors are presumably maintained by a strategy depending on growth conditions during oceanic early life, and each tactic would be consistently used throughout the adult stage. To verify whether the morphology of emerged hatchlings varies with maternal alternative foraging behaviors, the clutches of similar egg characteristics derived from oceanic and neritic foragers were incubated in a common beach area (30°24′N, 130°26′E), Yakushima Island, Japan, 2014. There were no significant differences in straight carapace length and width and body mass of emerged hatchlings between the two foraging groups, which were classified based on stable isotope ratios, suggesting that the development process of hatchling tissue from yolk and albumen is genetically similar between the two groups. Egg size and mass significantly increased with female body size only in neritic foragers that laid larger clutches than oceanic foragers, whereas hatchling size and mass significantly increased with egg mass in both groups. This suggested that larger females produced larger hatchlings within neritic foragers, and indeed, there was a significant positive correlation in body size between females and hatchlings only within neritic foragers. However, significant negative correlations between the number of eggs reburied per nest and emergence success that might explain the above phenomenon were not found in either oceanic or neritic foragers. Effects of a seasonal rise in ambient temperature on embryonic development and hatchling morphology were also similar between the two foraging groups, implying their genetic similarity in thermal response, consistent with their phenotypic plasticity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ackerman RA (1997) The nest environment and the embryonic development of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles, vol I. CRC Press, Boca Raton, pp 83–106

    Google Scholar 

  • Avens L, Goshe LR, Pajuelo M, Bjorndal KA, MacDonald BD, Lemons GE, Bolten AB, Seminoff JA (2013) Complementary skeletochronology and stable isotope analyses offer new insight into juvenile loggerhead sea turtle oceanic stage duration and growth dynamics. Mar Ecol Prog Ser 491:235–251

    Article  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 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bowen BW, Abreu-Grobois FA, Balazs GH, Kamezaki N, Limpus CJ, Ferl RJ (1995) Trans-Pacific migrations of the loggerhead turtle (Caretta caretta) demonstrated with mitochondrial DNA markers. Proc Natl Acad Sci USA 92:3731–3734

    Article  CAS  Google Scholar 

  • Cardona L, Clusa M, Eder E, Demetropoulos A, Margaritoulis D, Rees AF, Hamza AA, Khalil M, Levy Y, Türkozan O, Marín I, Aguilar A (2014) Distribution patterns and foraging ground productivity determine clutch size in Mediterranean loggerhead turtles. Mar Ecol Prog Ser 497:229–241

    Article  Google Scholar 

  • Ceriani SA, Roth JD, Sasso CR, McClellan CM, James MC, Haas HL, Smolowitz RJ, Evans DR, Addison DS, Bagley DA, Ehrhart LM, Weishampel JF (2014) Modeling and mapping isotopic patterns in the Northwest Atlantic derived from loggerhead sea turtles. Ecosphere 5(9):122

    Article  Google Scholar 

  • Cheng I-J, Lin C-H, Tseng C-T (2015) Factors influencing variations of oxygen content in nests of green sea turtles during egg incubation with a comparison of two nesting environments. J Exp Mar Biol Ecol 471:104–111

    Article  Google Scholar 

  • Christians JK (2002) Avian egg size: variation within species and infexibility within individuals. Biol Rev 77:1–26

    Article  Google Scholar 

  • da Costa Araújo J, e Rosa PV, das Dores Correia Palha M, Rodrigues PB, de Freitas RTF, do Socorro Lima da Silva A (2013) Effect of three feeding management systems on some reproductive parameters of Scorpion mud turtles (Kinosternon scorpioides) in Brazil. Trop Anim Health Prod 45:729–735

  • Danzmann RG, Ferguson MM, Skúlason S, Snorrason SS, Noakes DLG (1991) Mitochondrial DNA diversity among four sympatric morphs of Arctic charr, Salvelinus alpinus L., from Thingvallavatn, Iceland. J Fish Biol 39:649–659

    Article  CAS  Google Scholar 

  • Denoël M, Joly P, Whiteman HH (2005) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev 80:663–671

    Article  Google Scholar 

  • Eder E, Ceballos A, Martins S, Pérez-García H, Marín I, Marco A, Cardona L (2012) Foraging dichotomy in loggerhead sea turtles Caretta caretta off northwestern Africa. Mar Ecol Prog Ser 470:113–122

    Article  Google Scholar 

  • Gíslason D, Ferguson MM, Skúlason S, Snorasson SS (1999) Rapid and coupled phenotypic and genetic divergence in Icelandic Arctic char (Salvelinus alpinus). Can J Fish Aquat Sci 56:2229–2234

    Article  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    Article  CAS  Google Scholar 

  • Harrison RG (1980) Dispersal polymorphisms in insects. Ann Rev Ecol Syst 11:95–118

    Article  Google Scholar 

  • Hatase H, Matsuzawa Y, Sakamoto W, Baba N, Miyawaki I (2002a) Pelagic habitat use of an adult Japanese male loggerhead turtle Caretta caretta examined by the Argos satellite system. Fish Sci 68:945–947

    Article  CAS  Google Scholar 

  • Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002b) Size-related differences in feeding habitat use of adult female loggerhead turtles Caretta caretta around Japan determined by stable isotope analyses and satellite telemetry. Mar Ecol Prog Ser 233:273–281

    Article  Google Scholar 

  • Hatase H, Matsuzawa Y, Sato K, Bando T, Goto K (2004) Remigration and growth of loggerhead turtles (Caretta caretta) nesting on Senri Beach in Minabe, Japan: life-history polymorphism in a sea turtle population. Mar Biol 144:807–811

    Article  Google Scholar 

  • Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 149:52–64

    Article  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

    Article  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

    Article  Google Scholar 

  • Hawkes LA, Broderick AC, Coyne MS, Godfrey MH, Lopez-Jurado L-F, Lopez-Suarez P, Merino SE, Varo-Cruz N, Godley BJ (2006) Phenotypically linked dichotomy in sea turtle foraging requires multiple conservation approaches. Curr Biol 16:990–995

    Article  CAS  Google Scholar 

  • Hays GC, Speakman JR (1993) Nest placement by loggerhead turtles, Caretta caretta. Anim Behav 45:47–53

    Article  Google Scholar 

  • Hays GC, Adams CR, Speakman JR (1993) Reproductive investment by green turtles nesting on Ascension Island. Can J Zool 71:1098–1103

    Article  Google Scholar 

  • Hays GC, Fossette S, Katselidis KA, Mariani P, Schofield G (2010) Ontogenetic development of migration: Lagrangian drift trajectories suggest a new paradigm for sea turtles. J R Soc Interface 7:1319–1327

    Article  Google Scholar 

  • Iguchi K (2012) Egg size plasticity corresponding to maternal food conditions in an annual fish, Ayu Plecoglossus altivelis. Ichthyol Res 59:14–19

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jones TT, Seminoff JA (2013) Feeding biology: advances from field-based observations, physiological studies, and molecular techniques. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol III. CRC Press, Boca Raton, pp 211–247

    Chapter  Google Scholar 

  • Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fish 3:348–365

    Article  Google Scholar 

  • Jonsson N, Jonsson B, Fleming IA (1996) Does early growth cause a phenotypically plastic response in egg production of Atlantic Salmon? Funct Ecol 10:89–96

    Article  Google Scholar 

  • Kamel SJ, Mrosovsky N (2005) Repeatability of nesting preferences in the hawksbill sea turtle, Eretmochelys imbricata, and their fitness consequences. Anim Behav 70:819–828

    Article  Google Scholar 

  • Kaplan RH (1987) Developmental plasticity and maternal effects of reproductive characteristics in the frog, Bombina orientalis. Oecologia 71:273–279

    Article  CAS  Google Scholar 

  • Lowther AD, Harcourt RG, Hamer DJ, Goldsworthy SD (2011) Creatures of habit: foraging habitat fidelity of adult female Australian sea lions. Mar Ecol Prog Ser 443:249–263

    Article  Google Scholar 

  • Lundberg P (1988) The evolution of partial migration in birds. Trends Ecol Evol 3:172–175

    Article  CAS  Google Scholar 

  • Mansfield KL, Wyneken J, Porter WP, Luo J (2014) First satellite tracks of neonate sea turtles redefine the ‘lost years’ oceanic niche. Proc R Soc B 281:20133039

    Article  Google Scholar 

  • Matsuzawa Y, Sato K, Sakamoto W, Bjorndal KA (2002) Seasonal fluctuations in sand temperature: effects on the incubation period and mortality of loggerhead turtle (Caretta caretta) pre-emergent hatchlings in Minabe, Japan. Mar Biol 140:639–646

    Article  Google Scholar 

  • McGinley MA (1989) The influence of a positive correlation between clutch size and offspring fitness on the optimal offspring size. Evol Ecol 3:150–156

    Article  Google Scholar 

  • Morita K, Takashima Y (1998) Effect of female size on fecundity and egg size in white-spotted charr: comparison between sea-run and resident forms. J Fish Biol 53:1140–1142

    Article  Google Scholar 

  • Özdemir A, Ilgaz Ç, Kumlutaş Y, Durmuş SH, Kaska Y, Türkozan O (2007) An assessment of initial body size in loggerhead sea turtle (Caretta caretta) hatchlings in Turkey. Zool Sci 24:376–380

    Article  Google Scholar 

  • Pajuelo M, Bjorndal KA, Reich KJ, Arendt MD, Bolten AB (2012) Distribution of foraging habitats of male loggerhead turtles (Caretta caretta) as revealed by stable isotopes and satellite telemetry. Mar Biol 159:1255–1267

    Article  Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592

    Article  Google Scholar 

  • Pinckney J (1990) Correlation analysis of adult female, egg and hatchling sizes in the loggerhead turtle, Caretta caretta (L.), nesting at Kiawah Island, South Carolina, USA. Bull Mar Sci 47:670–679

    Google Scholar 

  • Read T, Booth DT, Limpus CJ (2012) Effect of nest temperature on hatchling phenotype of loggerhead turtles (Caretta caretta) from two South Pacific rookeries, Mon Repos and La Roche Percée. Aust J Zool 60:402–411

    Article  Google Scholar 

  • Reznick D, Yang AP (1993) The influence of fluctuating resources on life history: patterns of allocation and plasticity in female guppies. Ecology 74:2011–2019

    Article  Google Scholar 

  • Skúlason S, Snorrason SS, Noakes DLG, Ferguson MM (1996) Genetic basis of life history variations among sympatric morphs of Arctic char, Salvelinus alpinus. Can J Fish Aquat Sci 53:1807–1813

    Article  Google Scholar 

  • Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

    Article  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 

  • Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714

    Article  Google Scholar 

  • Vander Zanden HB, Pfaller JB, Reich KJ, Pajuelo M, Bolten AB, Williams KL, Frick MG, Shamblin BM, Nairn CJ, Bjorndal KA (2014) Foraging areas differentially affect reproductive output and interpretation of trends in abundance of loggerhead turtles. Mar Biol 161:585–598

    Article  Google Scholar 

  • Varo-Cruz N, Hawkes LA, Cejudo D, López P, Coyne MS, Godley BJ, López-Jurado LF (2013) Satellite tracking derived insights into migration and foraging strategies of male loggerhead turtles in the eastern Atlantic. J Exp Mar Biol Ecol 443:134–140

    Article  Google Scholar 

  • Vieira S, Martins S, Hawkes LA, Marco A, Teodósio MA (2014) Biochemical indices and life traits of loggerhead turtles (Caretta caretta) from Cape Verde Islands. PLoS ONE 9:e112181

    Article  Google Scholar 

  • Volpe JP, Ferguson MM (1996) Molecular genetic examination of the polymorphic Arctic charr Salvelintis alpinus of Thingvallavatn, Iceland. Mol Ecol 5:763–772

    Article  CAS  Google Scholar 

  • Wallace BP, Saba VS (2009) Environmental and anthropogenic impacts on intra-specific variation in leatherback turtles: opportunities for targeted research and conservation. Endanger Species Res 7:11–21

    Article  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

    Article  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 152:32–47

    Article  Google Scholar 

  • Warner DA, Lovern MB (2014) The maternal environment affects offspring viability via an indirect effect of yolk investment on offspring size. Physiol Biochem Zool 87:276–287

    Article  Google Scholar 

  • Warner DA, Lovern MB, Shine R (2007) Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination. Proc R Soc B 274:883–890

    Article  CAS  Google Scholar 

  • Watanabe KK, Hatase H, Kinoshita M, Omuta K, Bando T, Kamezaki N, Sato K, Matsuzawa Y, Goto K, Nakashima Y, Takeshita H, Aoyama J, Tsukamoto K (2011) Population structure of the loggerhead turtle Caretta caretta, a large marine carnivore that exhibits alternative foraging behaviors. Mar Ecol Prog Ser 424:273–283

    Article  Google Scholar 

  • Weber SB, Broderick AC, Groothuis TGG, Ellick J, Godley BJ, Blount JD (2012) Fine-scale thermal adaptation in a green turtle nesting population. Proc R Soc B 279:1077–1084

    Article  Google Scholar 

  • Yakushima Sea Turtle Research Group (2011) Report on the ecology of sea turtles at Yakushima Island during 1985–2009. Yakushima Sea Turtle Research Group, Kagoshima (in Japanese)

    Google Scholar 

Download references

Acknowledgments

We thank T. Hidaka, the staff (M. Ono, N. Omuta, T. Araishi, S. Koide, and M. Uchida) and volunteers (R. Shimizu, N. Sugio, R. Kawasaki, K. Nakajima, K. Yamada, and others) of the Yakushima Sea Turtle Research Group for field assistance and logistical support. The Associate Editor, G.C. Hays, and one anonymous reviewer provided constructive criticism. Field sampling was conducted under licenses issued by the municipalities of Kagoshima Prefecture (Nos. 11-2 and 11-3) and Yakushima Town (No. 981) and in accordance with the Animal Care Authorization (No. P14-1) of The University of Tokyo. This work was supported by JSPS KAKENHI Grant Number 25870141 to H.H.

Author information

Authors and Affiliations

  1. Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan

    Hideo Hatase & Teruhisa Komatsu

  2. Yakushima Sea Turtle Research Group, 489-8 Nagata, Yakushima, Kagoshima, 891-4201, Japan

    Kazuyoshi Omuta

Authors
  1. Hideo Hatase
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuyoshi Omuta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Teruhisa Komatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hideo Hatase.

Ethics declarations

Funding

This study was funded by JSPS KAKENHI (Grant Number 25870141) to the first author, Hideo Hatase.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

All procedures performed in this study involving animals were in accordance with the Animal Care Authorization (No. P14-1) of The University of Tokyo.

Additional information

Communicated by B. Wallace.

Reviewed by G.C. Hays and an undisclosed expert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 61 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hatase, H., Omuta, K. & Komatsu, T. Loggerhead turtle (Caretta caretta) offspring size does not vary with maternal alternative foraging behaviors: support for their phenotypic plasticity. Mar Biol 162, 1567–1578 (2015). https://doi.org/10.1007/s00227-015-2693-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2693-x

Keywords

Search

Navigation