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Marine Biology

, 166:64 | Cite as

Stable isotope analyses of cold-stunned Kemp’s ridley (Lepidochelys kempii) sea turtles at the northern extent of their coastal range

  • Sarah B. Bean
  • John M. LoganEmail author
Original Paper

Abstract

Kemp’s ridley (Lepidochelys kempii) sea turtles strand on Cape Cod, USA (41.894757°N, − 70.289372°W) as water temperatures drop in November, but little is known about their pre-stranding ecology. Carbon and nitrogen stable isotope values of soft tissues (liver and muscle) and scutes (anterior edge and interior) from cold-stunned individuals (n = 26) sampled from 2006 to 2008 were used to assess general patterns of local and early life-history habitat use. After adjusting for trophic discrimination, anterior scute carbon and nitrogen isotope values (n = 11) representative of recent feeding were lower and higher, respectively, than potential offshore prey but similar to many local neritic prey and sea turtle-derived isoscapes for New England waters. These results combined with a significant increase in δ15N values for scute edge relative to scute interior samples representative of early life history suggest local foraging prior to stranding. Interior scute δ13C and δ15N values mirrored Gulf of Mexico isoscapes, consistent with early life-history foraging near nesting habitat. Liver (rapid) and muscle (slow turnover) isotope offsets differed among individuals (n = 15), suggesting that the cold-stunned population does not have a homogenous migratory and/or trophic history. Liver tissue showed evidence of starvation-induced δ15N alteration, which could bias interpretation of isotope data from rapid turnover tissues. Further stable isotope analyses including complementary tracers and techniques will improve our knowledge of this poorly understood assemblage at the northern extent of the species’ coastal range. Such data will aid managers in preserving foraging habitat and prey resources in New England waters that may become increasingly important if Kemp’s ridley distribution shifts polewards with climate change.

Notes

Acknowledgements

We thank Andrew Ouimette and the staff of the University of New Hampshire Stable Isotope Laboratory for performing elemental composition and stable isotope analyses. Keith Matassa provided assets, both financial and material, for the completion of this project. Heather Haas, Samir Patel, Lindsey Peavey Reeves, and one anonymous reviewer provided insightful edits to previous versions of this manuscript. David Taylor, Maureen Conte, Emily DeFelippis, Ruth Carmichael, Eric Morgan, and Rainer Lohmann generously provided raw stable isotope and elemental composition data to allow for comparison with our dataset. We thank Robert Prescott and all of the staff and volunteers of Mass Audubon’s Wellfleet Bay Wildlife Sanctuary who tirelessly walk the cold beaches of Cape Cod searching for live and dead cold-stunned sea turtles. Finally, we want to recognize the numerous staff and volunteers of the New England Aquarium who care for the stranded turtles, as well as those of the secondary care facilities who continue the rehabilitation prior to release.

Compliance with ethical standards

Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2019_3516_MOESM1_ESM.tiff (3.3 mb)
Figure S1. Serial sampling information for a single Kemps ridley based on eleven sub-samples collected from the anterior to posterior and inner to outer sections of the third costal scute. Sub-sample locations are depicted in A) and also at the isotope value locations overlaid on heat maps for B) carbon and C) nitrogen stable isotope values for different scute sampling locations from a single Kemp’s ridley. The boxes in B) and C) represent the margins of the scute, while color interpolation is constrained to the scute region that we sub-sampled (TIFF 3424 kb)
227_2019_3516_MOESM2_ESM.pdf (251 kb)
Figure S2. Image of third costal scute showing sampling locations for recent feeding history collected from the anterior edge (A) and early life-history feeding from the posterior (P) section. The scute in this figure was also serially sampled in relation to the posterior sample both towards the outer edge and from the far posterior to anterior edge margins. Shell image provided by H. Haas (PDF 251 kb)

References

  1. Alibardi L (2005) Proliferation in the epidermis of chelonians and growth of the horny scutes. J Morphol 265:52–69CrossRefGoogle Scholar
  2. Bleakney JS (1965) Reports of marine turtles from New England and eastern Canada. Can Field Nat 79:120–128Google Scholar
  3. Bolten AB (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol II. CRC Press, Boca Raton, pp 243–257Google Scholar
  4. Burke VJ, Standora EA, Morreale SJ (1993) Diet of juvenile Kemp’s ridley and loggerhead sea turtles from Long Island, New York. Copeia 4:1176–1180CrossRefGoogle Scholar
  5. Burke VJ, Morreale SJ, Standora EA (1994) Diet of the Kemp’s ridley sea-turtle, Lepidochelys kempi, in New York waters. Fish Bull 92:26–32Google Scholar
  6. Carmichael RH, Rutecki D, Annett B, Gaines E, Valiela I (2004) Position of horseshoe crabs in estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition. J Exp Mar Biol Ecol 299:231–253CrossRefGoogle Scholar
  7. Carr A (1967) So excellent a fishe: a natural history of sea turtles. Scribner, New YorkGoogle Scholar
  8. 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 5:122CrossRefGoogle Scholar
  9. Cherel Y, Hobson KA, Hassani S (2005) Isotopic discrimination between food and blood and feathers of captive penguins: Implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115CrossRefGoogle Scholar
  10. Dalerum F, Angerbjӧrn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658CrossRefGoogle Scholar
  11. Davenport J (1997) Temperature and the life-history strategies of sea turtles. J Therm Biol 22:479–488CrossRefGoogle Scholar
  12. DeFelippis E, Conte M, Weber JC (2017) Lipids and stable isotope profiles in cold stunned juvenile sea turtles of Cape Cod. Unpublished Report. Semester in Environmental Science. Ecosytem Center of the Marine Biological Laboratory. http://www.mbl.edu/ses/files/2018/02/DeFelippis_Final-Paper.pdf. Accessed 7 Dec 2018
  13. Dodge KL, Logan JM, Lutcavage ME (2011) Foraging ecology of leatherback sea turtles in the Western North Atlantic determined through multi-tissue stable isotope analyses. Mar Biol 158:2813–2824CrossRefGoogle Scholar
  14. Doucett RR, Booth RK, Power G, McKinley RS (1999) Effects of the spawning migration on the nutritional status of anadromous Atlantic salmon (Salmo salar): insights from stable-isotope analysis. Can J Fish Aquat Sci 56:2172–2180CrossRefGoogle Scholar
  15. Epperly SP, Heppell SS, Richards RM, Castro Martínez MA, Zapata Najera BM, Sarti Martínez AL, Peña LJ, Shaver DJ (2013) Mortality rates of Kemp’s ridley sea turtles in the neritic waters of the United States. In: Tucker T, Belskis L, Panagopoulou A, Rees A, Frick M, Williams K, LeRoux R, Stewart K (eds) Proceedings of the thirty-third annual symposium of sea turtle biology and conservation. NOAA Technical Memorandum NMFS-SEFSC 645, p 219Google Scholar
  16. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  17. Fry B (2006) Stable isotope ecology. Springer, New YorkCrossRefGoogle Scholar
  18. Fry B, Baltz DM, Benfield MC, Fleeger JW, Gace A, Haas HL, Quiñones-Rivera ZJ (2003) Stable isotope indicators of movement and residency for brown shrimp (Farfantepenaeus aztecus) in coastal Louisiana marshscapes. Estuaries 26:82–97CrossRefGoogle Scholar
  19. Gannes LZ, O’Brien DM, Martínez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276CrossRefGoogle Scholar
  20. Graham BS, Koch P, Newsome S, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern and processes on Earth through isotope mapping. Springer, New YorkGoogle Scholar
  21. Griffin LP, Griffin CR, Finn JT, Prescott RL, Faherty M, Still BM, Danylchuk AJ (2019) Warming seas increase cold-stunning events for Kemp’s ridley sea turtles in the northwest Atlantic. PLoS One 14:e0211503.  https://doi.org/10.1371/journal.pone.0211503 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Guelinckx J, Maes J, Van Den Driessche P, Geysen B, Dehairs F, Ollevier F (2007) Changes in δ13C and δ15N in different tissues of juvenile sand goby Pomatoschistus minutus: a laboratory diet-switch experiment. Mar Ecol Prog Ser 341:205–215CrossRefGoogle Scholar
  23. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefGoogle Scholar
  24. Hobson KA, Alisaiskas RT, Clark RG (1993) Stable nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analysis of diet. Condor 95:388–394CrossRefGoogle Scholar
  25. Jardine T, Cunjak R (2005) Analytical error in stable isotope ecology. Oecologia 144:528–533CrossRefGoogle Scholar
  26. 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 211–247CrossRefGoogle Scholar
  27. Kenney RD, Vigness-Raposa KJ (2010) Chapter 10. Marine mammals and sea turtles of Narragansett Bay, Block Island Sound, Rhode Island Sound, and nearby waters: an analysis of existing data for the Rhode Island Ocean Special Area Management Plan. In: RICRMC (Rhode Island Coastal Resources Management Council) Ocean Special Area Management Plan (SAMP), vol 2Google Scholar
  28. Kraus SD, Leiter S, Stone K, Wikgren B, Mayo C, Hughes P, Kenney RD, Clark CW, Rice AN, Estabrook B, Tielens J (2016) Northeast large pelagic survey collaborative aerial and acoustic surveys for large whales and sea turtles. U.S. Department of the Interior, Bureau of Ocean Energy Management, Sterling, Virginia. OCS Study BOEM 2016-054Google Scholar
  29. Lazell JD Jr (1980) New England waters: critical habitat for marine turtles. Copeia 2:290–295CrossRefGoogle Scholar
  30. Liu X, Manning J, Prescott R, Zou H, Faherty M (2018) On simulating cold stunned turtle strandings on Cape Cod. bioRxiv.  https://doi.org/10.1101/418335
  31. Logan JM, Lutcavage ME (2013) Assessment of trophic dynamics of cephalopods and large pelagic fishes in the central North Atlantic Ocean using stable isotope analysis. Deep Sea Res Part II 95:63–73CrossRefGoogle Scholar
  32. Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77:838–846CrossRefGoogle Scholar
  33. Magozzi S, Yool A, Vander Zanden HB, Wunder MB, Trueman CN (2017) Using ocean models to predict spatial and temporal variation in marine carbon isoscapes. Ecosphere 8:e01763CrossRefGoogle Scholar
  34. Mansfield KL, Wyneken J, Rittschof D, Walsh M, Lim CW, Richards PM (2012) Satellite tag attachment methods for tracking neonate sea turtles. Mar Ecol Prog Ser 457:181–192CrossRefGoogle Scholar
  35. McClellan CM, Braun-McNeill J, Avens L, Wallace BP, Read AJ (2010) Stable isotopes confirm a foraging dichotomy in juvenile loggerhead sea turtles. J Exp Mar Biol Ecol 387:44–51CrossRefGoogle Scholar
  36. McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390CrossRefGoogle Scholar
  37. McMahon KW, McCarthy MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere 7:e01511CrossRefGoogle Scholar
  38. McMahon KW, Newsome SD (2019) Amino acid isotope analysis: a new frontier in studies of animal migration and foraging ecology. In: Hobson KA, Wassenaar LI (eds) Tracking animal migrations with stable isotopes, 2nd edn. Academic Press, San Diego, pp 173–190CrossRefGoogle Scholar
  39. Morgan EJ, Lohmann R (2010) Dietary uptake from historically contaminated sediments as a source of PCBs to migratory fish and invertebrates in an urban estuary. Environ Sci Technol 44:5444–5449CrossRefGoogle Scholar
  40. Morreale SJ, Standora EA (2005) Western North Atlantic waters: crucial developmental habitat for Kemp’s ridley and loggerhead sea turtles. Chelonian Conserv Biol 4:872–882Google Scholar
  41. Newell RIE (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (North and Mid-Atlantic)–blue mussel. United States Fish and Wildlife Service, Biological Report 82(11.102). U.S. Army Corps of Engineers, TR E1-82-4, pp 25Google Scholar
  42. Ogren LH (1989) Distribution of juvenile and subadult Kemp’s ridley sea turtles: preliminary results from 1984-1987 surveys. In: Caillouet Jr CW, Landry Jr AM (eds) Proceedings of the first international symposium on Kemp’s ridley sea turtle biology, conservation, and management, pp 116–123Google Scholar
  43. Pearson RM, van de Merwe JP, Limpus CJ, Connolly RM (2017) Realignment of sea turtle isotope studies needed to match conservation priorities. Mar Ecol Prog Ser 583:259–271CrossRefGoogle Scholar
  44. 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.  https://doi.org/10.3389/fmars.2017.00348 CrossRefGoogle Scholar
  45. Pershing AJ, Alexander MA, Hernandez CM, Kerr LA, Le Bris A, Mills KE, Nye JA, Record NR, Scannell HA, Scott JD, Sherwood GD, Thomas AC (2015) Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery. Science 350:809–812CrossRefGoogle Scholar
  46. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  47. Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231CrossRefGoogle Scholar
  48. Piraino MN, Taylor DL (2009) Bioaccumulation and trophic transfer of mercury in striped bass (Morone saxatilis) and tautog (Tautoga onitis) from the Narragansett Bay (Rhode Island, USA). Mar Environ Res 67:117–128CrossRefGoogle Scholar
  49. Plotkin P (2003) Adult migrations and habitat use. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol II. CRC Press, Boca Raton, pp 225–241Google Scholar
  50. Poloczanska ES, Limpus CJ, Hays GC (2009) Vulnerability of marine turtles to climate change. In: Sims DW (ed) Advances in marine biology, vol 56. Academic Press, Burlington, pp 151–211Google Scholar
  51. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  52. Putman NF, Mansfield KL, He R, Shaver DJ, Verley P (2013) Predicting the distribution of oceanic-stage Kemp’s ridley sea turtles. Biol Lett 9:20130345CrossRefGoogle Scholar
  53. Reich KJ, Bjorndal KA, Bolten AB (2007) The “lost years” of green turtles: using stable isotopes to study cryptic lifestages. Biol Lett 3:712–714CrossRefGoogle Scholar
  54. Reich KJ, Bjorndal KA, Martínez del Rio C (2008) Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155:651–663CrossRefGoogle Scholar
  55. Reich KJ, López-Castro MC, Shaver DJ, Iseton C, Hart KM, Hooper MJ, Schmitt CJ (2017) δ13C and δ15N in the endangered Kemp’s ridley sea turtle Lepidochelys kempii after the Deepwater Horizon oil spill. Endanger Species Res 33:281–289CrossRefGoogle Scholar
  56. 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 Prog Ser 308:271–278CrossRefGoogle Scholar
  57. Seminoff JA, Bjorndal KA, Bolten AB (2007) Stable carbon and nitrogen isotope discrimination and turnover in pond sliders Trachemys scripta: insights for trophic study of freshwater turtles. Copeia 3:534–542CrossRefGoogle Scholar
  58. 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(5):e37403.  https://doi.org/10.1371/journal.pone.0037403 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Somes CJ, Schmittner A, Galbraith ED, Lehmann MF, Altabet MA, Montoya JP, Letelier RM, Mix AC, Bourbonnais A, Eby M (2010) Simulating the global distribution of nitrogen isotopes in the ocean. Glob Biogeochem Cycles 24:4019CrossRefGoogle Scholar
  60. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  61. Thomas SM, Crowther TW (2015) Predicting rates of isotopic turnover across the animal kingdom: a synthesis of existing data. J Anim Ecol 84:861–870CrossRefGoogle Scholar
  62. 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 6:711–714CrossRefGoogle Scholar
  63. Vander Zanden HB, Arthur KE, Bolten AB, Popp BN, Lagueux CJ, Harrison E, Campbell CL, Bjorndal KA (2013) Trophic ecology of a green turtle breeding population. Mar Ecol Prog Ser 476:237–249CrossRefGoogle Scholar
  64. Vander Zanden HB, Tucker AD, Bolten AB, Reich KJ, Bjorndal KA (2014) Stable isotopic comparison between loggerhead sea turtle tissues. Rapid Commun Mass Spectrom 28:2059–2064CrossRefGoogle Scholar
  65. Vander Zanden HB, Tucker AD, Hart KM, Lamont MM, Fujisaki I, Addison DS, Mansfield KL, Phillips KF, Wunder MB, Bowen GJ, Pajuelo M, Bolten AB, Bjorndal KA (2015a) Determining origin in a migratory marine vertebrate: a novel method to integrate stable isotopes and satellite tracking. Ecol Appl 25:320–335CrossRefGoogle Scholar
  66. Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015b) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS One 10:e0116182.  https://doi.org/10.1371/journal.pone.0116182 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182CrossRefGoogle Scholar
  68. Varela JL, Ortega A, de la Gándara F, Medina A (2015) Effects of starvation on δ15N and δ13C in Atlantic bonito, Sarda sarda (Block, 1793). Aquac Res 46:2043–2047.  https://doi.org/10.1111/are.12351:1-5 CrossRefGoogle Scholar
  69. West JB, Bowen GJ, Dawson TE, Tu KP (2010) Isoscapes: understanding movement, pattern, and processing on Earth through isotope mapping. Springer, New YorkCrossRefGoogle Scholar
  70. Witherington B, Hirama S, Hardy R (2012) Young sea turtles of the pelagic Sargassum-dominated drift community: habitat use, population density, and threats. Mar Ecol Prog Ser 463:1–22CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.University of New EnglandBiddefordUSA
  2. 2.Massachusetts Division of Marine FisheriesNew BedfordUSA

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