Skip to main content

Advertisement

SpringerLink
Log in

Sequential scute growth layers reveal developmental histories of hawksbill sea turtles

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

Abstract

Understanding the basic life history patterns of highly migratory species is important for effective management. For sea turtles, evidence of developmental biogeography and discrete life stage residency provides key information for understanding resource use and population threats and defining conservation priorities. Resolving gaps in these knowledge areas is not straightforward, however. Inaccessible habitats, low survivorship, late maturity ages, and technology limitations all complicate monitoring individuals continuously throughout their life span. Here, we expand on previous studies and document a near-complete tissue record in the ultimate posterior marginal scutes of hawksbill sea turtle (Eretmochelys imbricata) carapace. Stable isotope analysis (SIA) of ventral scute surfaces reveals differences between three geographically isolated populations in the Pacific and Atlantic basins. Additionally, sequential sampling and SIA along growth line contours of sectioned scutes reveals developmental movements. Perhaps surprisingly, no clear or general patterns emerge. Bivariate isotope data (stable carbon, δ13C, and nitrogen δ15N) indicate that only one of six Central Pacific hawksbills showed a distinct ontogenetic shift. And while all three Western Pacific individuals showed evidence of ontogenetic shifts, these individuals had three unique patterns. We summarize regional stable isotope values for common hawksbill foraging items, discuss drivers of regional nitrogen structure, and make recommendations for future study.

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

Data Availability

Raw data are available in the Supplementary Information. High-resolution figures and data are also available at the third-party Open Science Framework repository: https://osf.io/2fh39/.

References

  • 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 Progr Ser 491:235–251

    Article  Google Scholar 

  • Avens L, Ramirez MD, Hall AG, Snover ML, Haas HL, Godfrey MH, Goshe LR, Cook M, Heppell SS (2020) Regional differences in Kemp’s ridley sea turtle growth trajectories and expected age at maturation. Mar Ecol Prog Ser 654:143–161

    Article  CAS  Google Scholar 

  • Balazs GH, Van Houtan KS, Hargrove SA, Brunson SM, Murakawa SK (2015) A review of the demographic features of Hawaiian green turtles (Chelonia mydas). Chelonian Conserv Biol 14:119–129

    Article  Google Scholar 

  • Becker B, Kromer B, Trimborn P (1991) A stable-isotope tree-ring timescale of the Late Glacial/Holocene boundary. Nature 353:647–649

    Article  Google Scholar 

  • Bjorndal KA, Bolten AB (2010) Hawksbill sea turtles in seagrass pastures: success in a peripheral habitat. Mar Biol 157:135–145. https://doi.org/10.1007/s00227-009-1304-0

    Article  Google Scholar 

  • Brunson S, Gaos AR, Kelly IK, Van Houtan KS, Swimmer Y, Hargrove S, Balazs GH, Work TM, Jones TT (2022) Three decades of stranding data reveal insights into endangered hawksbill sea turtles in Hawai ‘i. Endang Spec Res 47:109–118

    Article  Google Scholar 

  • Caine EA (1986) Carapace epibionts of nesting loggerhead sea turtles: Atlantic coast of USA. J Exper Mar Biol Ecol 95:15–26

    Article  Google Scholar 

  • Cardona L, Aguilar A, Pazos L (2009) Delayed ontogenic dietary shift and high levels of omnivory in green turtles (Chelonia mydas) from the NW coast of Africa. Mar Biol 156:1487–1495. https://doi.org/10.1007/s00227-009-1188-z

    Article  CAS  Google Scholar 

  • Clark ID, Fritz P (2013) Environmental isotopes in hydrogeology. CRC Press

    Book  Google Scholar 

  • Cleveland WS, Devlin SJ (1988) Locally Weighted Regression: An Approach to Regression Analysis by Local Fitting. J Am Stat Assoc 83:596–610

    Article  Google Scholar 

  • Clyde-Brockway CE, Heidemeyer M, Paladino FV, Flaherty EA (2022) Diet and foraging niche flexibility in green and hawksbill turtles. Mar Biol 169:108. https://doi.org/10.1007/s00227-022-04092-1

    Article  CAS  Google Scholar 

  • CocheretdelaMorinière EC, Pollux B, Nagelkerken I, Hemminga M, Huiskes A, van der Velde G (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Mar Ecol Prog Ser 246:279–289

    Article  Google Scholar 

  • Dailer ML, Knox RS, Smith JE, Napier M, Smith CM (2010) Using δ15 N values in algal tissue to map locations and potential sources of anthropogenic nutrient inputs on the island of Maui, Hawaii, USA. Mar Poll Bull 60:655–671

    Article  CAS  Google Scholar 

  • Deniro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • Donnelly M (2008) Trade routes for tortoiseshell. SWOT Report III:24–25

    Google Scholar 

  • Duarte CM, Delgado-Huertas A, Anton A, Carrillo-de-Albornoz P, López-Sandoval DC, Agustí S, Almahasheer H, Marbá N, Hendriks IE, Krause-Jensen D, Garcias-Bonet N (2018) Stable isotope (δ13C, δ15N, δ18O, δD) composition and nutrient concentration of red sea primary producers. Front Mari Sci. https://doi.org/10.3389/fmars.2018.00298

    Article  Google Scholar 

  • Eide M, Olsen A, Ninnemann US, Eldevik T (2017) A global estimate of the full oceanic 13C Suess effect since the preindustrial. Global Biogeochem Cycles 31:492–514

    Article  CAS  Google Scholar 

  • Espinoza EO, Baker BW, Berry CA (2007) The analysis of sea turtle and bovid keratin artefacts using drift spectroscopy and discriminant analysis. Archaeometry 49:685–698

    Article  CAS  Google Scholar 

  • Fiore CL, Baker DM, Lesser MP (2013) Nitrogen biogeochemistry in the caribbean sponge, xestospongia muta a source or sink of dissolved inorganic nitrogen? PLoS ONE 8:e72961. https://doi.org/10.1371/journal.pone.0072961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fireman AL (2021) On the Shell of the Turtle: Identifying the Isotopic Niche of Hawksbill Sea Turtles in Antigua, West Indies

  • Gagné TO, Hyrenbach KD, Hagemann ME, Bass OL, Pimm SL, MacDonald M, Peck B, Houtan KSV (2018a) Seabird trophic position across three ocean regions tracks ecosystem differences. Front Mari Sci 5:317

    Article  Google Scholar 

  • Gagné TO, Hyrenbach KD, Hagemann ME, Van Houtan KS (2018b) Trophic signatures of seabirds suggest shifts in oceanic ecosystems. Sci Adv 4:3946

    Article  Google Scholar 

  • Gaos AR, Lewison RL, Yañez IL, Wallace BP, Liles MJ, Nichols WJ, Baquero A, Hasbún CR, Vasquez M, Urteaga J (2012) Shifting the life-history paradigm: discovery of novel habitat use by hawksbill turtles. Biol Lett 8:54–56

    Article  PubMed  Google Scholar 

  • Gaos AR, LaCasella EL, Kurpita L, Balazs G, Hargrove S, King C, Bernard H, Jones TT, Dutton PH (2020) Hawaiian hawksbills: a distinct and isolated nesting colony in the central north pacific ocean revealed by mitochondrial DNA. Conserv Genet 21:771–783

    Article  Google Scholar 

  • Gaos AR, Kurpita L, Bernard H, Sundquist L, King CS, Browning JH, Naboa E, Kelly IK, Downs K, Eguchi T (2021) Hawksbill nesting in Hawai‘i: 30-year dataset reveals recent positive trend for a small, yet vital population. Front Mari Sci. 8:1719

    Google Scholar 

  • Graham SC (2009) Analysis of the foraging ecology of hawksbill turtles (Eretmochelys imbricata) on Hawai’i Island: An investigation utilizing satellite tracking and stable isotopes. University of Hawaii, Hilo, HI

    Google Scholar 

  • Grottoli AG, Eakin CM (2007) A review of modern coral δ18O and Δ14C proxy records. Earth-Sci Rev 81:67–91

    Article  Google Scholar 

  • Hawkes L, Tomás J, Revuelta O, León Y, Blumenthal J, Broderick A, Fish M, Raga J, Witt M, Godley B (2012) Migratory patterns in hawksbill turtles described by satellite tracking. Mar Ecol Progr Ser 461:223–232

    Article  Google Scholar 

  • Hobson KA, Wassenaar LI (2008) Tracking animal migration with stable isotopes. Academic Press

    Google Scholar 

  • Kelly EB (2012) Using stable isotope analysis to assess the foraging habits of palmyra atoll green turtles (Chelonia mydas). Columbia University, New York, NY

    Google Scholar 

  • Lemons G, Lewison R, Komoroske L, Gaos A, Lai C-T, Dutton P, Eguchi T, LeRoux R, Seminoff JA (2011) Trophic ecology of green sea turtles in a highly urbanized bay: insights from stable isotopes and mixing models. J Exper Mar Biol Ecol 405:25–32

    Article  Google Scholar 

  • Liles MJ, Peterson MJ, Seminoff JA, Altamirano E, Henríquez AV, Gaos AR, Gadea V, Urteaga J, Torres P, Wallace BP (2015) One size does not fit all: importance of adjusting conservation practices for endangered hawksbill turtles to address local nesting habitat needs in the eastern Pacific Ocean. Biol Conserv 184:405–413

    Article  Google Scholar 

  • Marcovaldi MÂ, Lopez GG, Soares LS, López-Mendilaharsu M (2012) Satellite tracking of hawksbill turtles Eretmochelys imbricata nesting in northern Bahia, Brazil: turtle movements and foraging destinations. Endang Spec Res 17:123–132

    Article  Google Scholar 

  • Méndez-Salgado E, Chacón-Chaverri D, Fonseca LG, Seminoff JA (2020) Trophic ecology of hawksbill turtles (Eretmochelys imbricata) in Golfo Dulce, Costa Rica: integrating esophageal lavage and stable isotope (δ13C, δ15N) analysis. Lat Am J Aquat Res 48:114–130

    Article  Google Scholar 

  • Miller EA, McClenachan L, Uni Y, Phocas G, Hagemann ME, Van Houtan KS (2019) The historical development of complex global trafficking networks for marine wildlife. Sci Adv 5:5948

    Article  Google Scholar 

  • Miller EA, Lisin SE, Smith CM, Van Houtan KS (2020) Herbaria macroalgae as a proxy for historical upwelling trends in Central California. Proc R Soc B 287:20200732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monzón-Argüello C, Rico C, Naro-Maciel E, Varo-Cruz N, López P, Marco A, López-Jurado LF (2010) Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands. Conserv Genet 11:1871–1884

    Article  Google Scholar 

  • Mortimer JA, Donnelly M (2008) Eretmochelys imbricata. IUCN Red List of Threatened Species 2011.1: www.iucnredlist.org

  • Palaniappan PM (2007) The carapacial scutes of hawksbill turtles (Eretmochelys imbricata): development, growth dynamics and utility as an age indicator. Charles Darwin University, Casuarina, NT, Australia

    Google Scholar 

  • Pannella G (1971) Fish otoliths: daily growth layers and periodical patterns. Science 173:1124–1127

    Article  Google Scholar 

  • Popp B, Graham B, Olson R, Hannides C, Lott M, López-Ibarra G, Galván-Magaña F, Fry B (2007) Stable isotopes as indicators of ecological change. Academic Press, New York

    Google Scholar 

  • Ramirez MD, Avens L, Seminoff JA, Goshe LR, Heppell SS (2015) Patterns of loggerhead turtle ontogenetic shifts revealed through isotopic analysis of annual skeletal growth increments. Ecosphere 6:1–17. https://doi.org/10.1890/ES15-00255.1

    Article  Google Scholar 

  • Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biol Lett 3:712–714

    Article  PubMed  PubMed Central  Google Scholar 

  • Schweingruber FH (2012) Tree rings: basics and applications of dendrochronology. Springer Science & Business Media, USA

    Google Scholar 

  • Seitz WA, Kagimoto KM, Luehrs B, Katahira L (2012) Twenty years of conservation and research findings of the Hawai‘i Island Hawksbill Turtle Recovery Project, 1989 to 2009. Pacific Cooperative Studies Unit Technical Report, University of Hawaii-Manoa, Department of Botany, Honolulu, HI

  • Seminoff JA, Jones TT, Eguchi T, Jones DR, Dutton PH (2006) Stable isotope discrimination (δ13C and δ15N) between soft tissues of the green sea turtle Chelonia mydas and its diet. Mar Ecol Progr Ser 308:271–278

    Article  CAS  Google Scholar 

  • Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dutton PH, Tapilatu RF, Popp BN (2012) Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids. PLoS ONE 7:e37403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seminoff JA, Allen CD, Balazs GH, Dutton PH, Eguchi T, Haas H, Hargrove SA, Jensen M, Klemm DL, Lauritsen AM, Mac Pherson SL, Opay P, Possardt EE, Pultz S, Van Houtan KS, Waples RS (2015) Status review of the green turtle (Chelonia mydas) under the Engangered Species Act. NOAA Tech Memo NOAA-TM-NMFS-SWFSC- 539:599

    Google Scholar 

  • Smith KJ, Trueman CN, France CAM, Sparks JP, Brownlow AC, Dähne M, Davison NJ, Guðmundsson G, Khidas K, Kitchener AC, Langeveld BW, Lesage V, Meijer HJM, Ososky JJ, Sabin RC, Timmons ZL, Víkingsson GA, Wenzel FW, Peterson MJ (2021) Stable isotope analysis of specimens of opportunity reveals ocean-scale site fidelity in an elusive whale species. Front Conservat Sci. https://doi.org/10.3389/fcosc.2021.653766

    Article  Google Scholar 

  • Snover ML (2002) Growth and ontogeny of sea turtles using skeletochronology: methods, validation and application to conservation. M.Sc. thesis: Duke University, Dureham, NC

  • Stock BC, Semmens BX (2016) Unifying error structures in commonly used biotracer mixing models. Ecology 97:2562–2569

    Article  PubMed  Google Scholar 

  • Stock BC, Jackson AL, Ward EJ, Parnell AC, Phillips DL, Semmens BX (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6:e5096

    Article  PubMed  PubMed Central  Google Scholar 

  • Trueman CN, MacKenzie K, Palmer M (2012) Identifying migrations in marine fishes through stable-isotope analysis. J Fish Biol 81:826–847

    Article  CAS  PubMed  Google Scholar 

  • Tucker AD, Broderick D, Kampe L (2001) Age estimation of Eretmochelys imbricata by sclerochronology of carapacial scutes. Chelonian Conserv Biol 4:219–222

    Google Scholar 

  • Tucker AD, MacDonald BD, Seminoff JA (2014) Foraging site fidelity and stable isotope values of loggerhead turtles tracked in the Gulf of Mexico and northwest Caribbean. Mar Ecol Prog Ser 502:267–279

    Article  CAS  Google Scholar 

  • Turner Tomaszewicz CN, Seminoff JA, Ramirez MD, Kurle CM (2015) Effects of demineralization on the stable isotope analysis of bone samples. Rapid Commun Mass Spectrom 29:1879–1888

    Article  CAS  Google Scholar 

  • Turner Tomaszewicz CN, Seminoff JA, Peckham SH, Avens L, Kurle CM (2017) Intrapopulation variability in the timing of ontogenetic habitat shifts in sea turtles revealed using δ15N values from bone growth rings. J Anim Ecol 86:694–704. https://doi.org/10.1111/1365-2656.12618

    Article  PubMed  PubMed Central  Google Scholar 

  • Turner Tomaszewicz C, Liles M, Avens L, Seminoff J (2022) Tracking movements and growth of post-hatchling to adult hawksbill sea turtles using skeleto+iso. Front Ecol Evol 10:983260

    Article  Google Scholar 

  • Van Houtan KS, Hargrove SK, Balazs GH (2010) Land use, macroalgae, and a tumor-forming disease in marine turtles. PLoS ONE 5:e12900

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Houtan KS, Hargrove SK, Balazs GH (2014a) Modeling sea turtle maturity age from partial life history records. Pac Sci 68:465–477

    Article  Google Scholar 

  • Van Houtan KS, Smith CM, Dailer ML, Kawachi M (2014b) Eutrophication and the dietary promotion of sea turtle tumors. Peer J. 2:602. https://doi.org/10.7717/peerj.602

    Article  Google Scholar 

  • Van Houtan KS, Andrews AH, Jones TT, Murakawa SKK, Hagemann ME (2016a) Time in tortoiseshell: a radiocarbon-validated chronology in sea turtle scutes. Proc R Soc B 283:1822

    Google Scholar 

  • Van Houtan KS, Francke D, Alessi S, Jones TT, Martin SL, Kurpita L, King C (2016b) The developmental biogeography of hawksbill sea turtles. Ecol Evol 6:2378–2389

    Article  PubMed  PubMed Central  Google Scholar 

  • Vander Zanden HB, Bjorndal KA, Mustin W, Ponciano JM, Bolten AB (2012) Inherent variation in stable isotope values and discrimination factors in two life stages of green turtles. Physiol Biochem Zool 85:431–441

    Article  CAS  PubMed  Google Scholar 

  • Vander Zanden HB, Bjorndal KA, Bolten AB (2013) Temporal consistency and individual specialization in resource use by green turtles in successive life stages. Oecologia 173:767–777. https://doi.org/10.1007/s00442-013-2655-2

    Article  PubMed  Google Scholar 

  • Walcott J, Eckert S, Horrocks J (2012) Tracking hawksbill sea turtles (Eretmochelys imbricata) during inter-nesting intervals around Barbados. Mar Biol 159:927–938

    Article  Google Scholar 

  • Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner EM, Bolten AB, Chaloupka MY, Hutchinson BJ, Abreu-Grobois FA, Amorocho D, Bjorndal KA (2010) Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS ONE 5:e15465

    Article  PubMed  PubMed Central  Google Scholar 

  • Wedemeyer-Strombel KR, Seminoff JA, Liles MJ, Sánchez RN, Chavarría S, Valle M, Altamirano E, Gadea V, Hernandez N, Peterson MJ (2021) Fishers’ ecological knowledge and stable isotope analysis reveal mangrove estuaries as key developmental habitats for critically endangered sea turtles. Front Conserv Sci. 2:115

    Article  Google Scholar 

  • Work TM (2000) Sea turtle necropsy manual for biologists in remote refuges. National Wildlife Health Center, Hawaii Field Station, USA

    Google Scholar 

  • Work TM, Balazs GH, Rameyer RA, Morris RA (2004) Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian Islands, 1993–2003. Dis Aquat Org 62:163–176

    Article  Google Scholar 

Download references

Acknowledgements

R. Humphreys provided access to laboratory space and equipment; J. Sampaga, E. Di Martini, A. Andrews, and B. Taylor advised on life history analysis methods. S. Murakawa, S. Brunson, D. Francke, A. Niccum, N. Sarto, and R. Dollar assisted with necropsies and specimen preparations. G. Balazs, A. Palermo, C. King, and W. Seitz provided specimens; B. Tibbats and C. Smith assisted with forage samples. A. Copenhaver and L. Kaneshiro provided program support. C. Turner Tomaszewicz and two anonymous reviewers provided helpful comments on earlier versions of this manuscript.

Funding

A Presidential Early Career Award in Science and Engineering to KV funded this study.

Author information

Authors and Affiliations

  1. Nicholas School of the Environment, Duke University, Durham, NC, 27708, USA

    Kyle S. Van Houtan

  2. NOAA Fisheries, Pacific Islands Fisheries Science Center, Honolulu, HI, 96818, USA

    T. Todd Jones & Alexander R. Gaos

  3. Vertebrate Zoology Collections, Bernice Pauahi Bishop Museum, Honolulu, HI, 96817, USA

    Molly E. Hagemann

  4. NOAA Fisheries, Southwest Fisheries Science Center, La Jolla, CA, 92037, USA

    Joel Schumacher & Jeffrey A. Seminoff

  5. Office of Law Enforcement, Regional Attaché to the US. Embassy (ret.), U.S. Fish and Wildlife Service, Bangkok, Thailand

    George Phocas

Authors
  1. Kyle S. Van Houtan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Todd Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Molly E. Hagemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joel Schumacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. George Phocas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexander R. Gaos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jeffrey A. Seminoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KV and JAS designed the study and wrote the manuscript. KV, TJ, MH, and GP provided and prepared specimens. JAS and JS performed the diagnostic analyses, while KV analyzed the data and generated the figures. All authors made contributions to and reviewed the manuscript.

Corresponding author

Correspondence to Kyle S. Van Houtan.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Ethical approval

All research followed the NOAA Institutional Animal Care and Use Committee criteria.

Additional information

Responsible Editor: P. Casale .

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 345 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Van Houtan, K.S., Jones, T.T., Hagemann, M.E. et al. Sequential scute growth layers reveal developmental histories of hawksbill sea turtles. Mar Biol 170, 79 (2023). https://doi.org/10.1007/s00227-023-04229-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-023-04229-w

Keywords

Search

Navigation