Validation of back-calculated body lengths and timing of growth mark deposition in Hawaiian green sea turtles

Abstract

Somatic growth rate data for wild sea turtles can provide insight into life-stage durations, time to maturation, and total lifespan. When appropriately validated, the technique of skeletochronology allows prior growth rates of sea turtles to be calculated with considerably less time and labor than required by mark-–recapture studies. We applied skeletochronology to 10 dead, stranded green turtles Chelonia mydas that had previously been measured, tagged, and injected with OTC (oxytetracycline) during mark–recapture studies in Hawaii for validating skeletochronological analysis. We tested the validity of back-calculating carapace lengths (CLs) from diameters of LAGs (lines of arrested growth), which mark the outer boundaries of individual skeletal growth increments. This validation was achieved by comparing CLs estimated from measurements of the LAG proposed to have been deposited closest to the time of tagging to actual CLs measured at the time of tagging. Measureable OTC-mark diameters in five turtles also allowed us to investigate the time of year when LAGs are deposited. We found no significant difference between CLs measured at tagging and those estimated through skeletochronology, which supports calculation of somatic growth rates by taking the difference between CLs estimated from successive LAG diameters in humerus bones for this species. Back-calculated CLs associated with the OTC mark and growth mark deposited closest to tagging indicated that annual LAGs are deposited in the spring. The results of this validation study increase confidence in utilization of skeletochronology to rapidly obtain accurate age and growth data for green turtles.

References Avens, L., and M. L. Snover. 2013. Age and age estimation in sea turtles. Pp. 97–134 in J. Wyneken, K. J. Lohmann and J. A. Musick, eds. The biology of sea turtles, volume III. CRC Press, Boca Raton, FL. Avens, L., L. R. Goshe, C. A. Harms, E. T. Anderson, A. G. Hall, W. M. Cluse, et al. 2012. Population characteristics, age structure, and growth dynamics of neritic juvenile green turtles (Chelonia mydas) in the northeastern Gulf of Mexico. Mar. Ecol. Prog. Ser. 458:213–229. Avens, L., L. R. Goshe, M. Pajuelo, K. A. Bjorndal, B. D. MacDonald, G. E. Lemons, et al. 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. Avens, L., L. R. Goshe, L. Coggins, M. L. Snover, M. Pajuelo, K. A. Bjorndal, et al. 2015. Age and size at maturation and adult-stage duration for loggerhead sea turtles in the western North Atlantic. Mar. Biol. 162:1749–1767. Balazs, G. H. (1999) Factors to consider in the tagging of sea turtles. Pp. 101–109 in K. L. Eckert, K. A. Bjorndal, F. A. Abreu-Grobois, and M. Donnelly, eds. Research and management techniques for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4, Washington, DC. Balazs, G. H., and M. Chaloupka. 2004. Spatial and temporal variability in somatic growth of green sea turtles (Chelonia mydas) resident in the Hawaiian archipelago. Mar. Biol. 145:1043–1059. Balazs, G. H., K. S. Van Houtan, S. A. Hargrove, S. M. Brunson, and S. K. K. Murakawa. 2015. A review of the demographic features of Hawaiian green turtles (Chelonia mydas). Chelonian Conserv. Biol. 14:119–129. Bjorndal, K. A., B. A. Schroeder, A. M. Foley, B. E. Witherington, D. C. Bresette, R. M. Herren, et al. 2013. Temporal, spatial, and body size effects on growth rates of loggerhead sea turtles (Caretta caretta) in the Northwest Atlantic. Mar. Biol. 160:2711–2721. Braun-McNeill, J., S. P. Epperly, L. Avens, M. L. Snover, and J. C. Taylor. 2008. Growth rates of loggerhead sea turtles (Caretta caretta) from the western North Atlantic. Herpetol. Conserv. Biol. 3:273–281. Casale, P., A. D. Mazaris, D. Freggi, C. Vallini, and R. Argano. 2009. Growth rates and age at adult size of loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea, estimated through capture-mark-recapture records. Sci. Mar. 73:589–595. Casale, P., A. D. Mazaris, and D. Freggi. 2011a. Estimation of age at maturity of loggerhead sea turtles Caretta caretta in the Mediterranean using length-frequency data. Endanger. Species Res. 13:123–129. Casale, P., N. Conte, D. Freggi, C. Cioni, and R. Argano. 2011b. Age and growth determination by skeletochronology in loggerhead sea turtles (Caretta caretta) from the Mediterranean Sea. Sci. Mar. 75:197–203. Castanet, J., H. Francillon-Viellot, F. J. Meunier, and A. DeRicqles. 1993. Bone and individual aging. Pp. 245–283 in B. K. Hall, ed. Bone, bone growth – B, volume 7. CRC Press, Boca Raton, FL. Castanet, J., S. Croci, F. Aujard, M. Perret, J. Cubo, and E. de Margerie. 2004. Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J. Zool. 263:31–39. Chaloupka, M., and G. Balazs. 2005. Modelling the effect of fibropapilloma disease on the somatic growth dynamics of Hawaiian green sea turtles. Mar. Biol. 147:1251–1260. Chaloupka, M. Y., and J. A. Musick. 1997. Age, growth, and population dynamics. Pp. 233–276 in P. L. Lutz and J. A. Musick, eds. The biology of sea turtles. CRC Press, Boca Raton, FL. Coles, W. C., J. A. Musick, and L. A. Williamson. 2001. Skeletochronology validation from an adult loggerhead (Caretta caretta). Copeia 2001:240–242. Field, K. J., C. R. Tracy, P. A. Medica, R. W. Marlow, and P. S. Corn. 2007. Return to the wild: translocation as a tool in conservation of the Desert Tortoise (Gopherus agassizii). Biol. Conserv. 136:232–245. Francis, R. I. C. C. 1990. Back-calculation of fish length: a critical review. J. Fish Biol. 36:883–902. Goshe, L. R., L. Avens, F. S. Scharf, and A. L. Southwood. 2010. Estimation of age at maturation and growth of Atlantic green turtles (Chelonia mydas) using skeletochronology. Mar. Biol. 157:1725–1740. Heppell, S. S., M. L. Snover, and L. B. Crowder. 2002. Sea turtle population ecology. Pp. 275–306 in P. Lutz, J. A. Musick and J. Wyneken, eds. The biology of sea turtles, volume II. CRC Press, Boca Raton, FL. Heppell, S. S., L. B. Crowder, D. T. Crouse, S. P. Epperly, and N. B. Frazer. 2003. Population models for Atlantic loggerheads: past, present and future. Pp. 255–273 in A. B. Bolton and B. E. Witherington, eds. Loggerhead sea turtles. Smithsonian Books, Washington, DC. Herbst, L. H. 1994. Fibropapillomatosis in marine turtles. Annu. Rev. Fish Dis. 4:389–425. Klevezal, G. A.. 1996. Recording structures of mammals: determination of age and reconstruction of life history. A. A. Balkema, Brookfield, VT. Klinger, R. C., and J. A. Musick. 1992. Annular growth layers in juvenile loggerhead turtles (Caretta caretta). Bull. Mar. Sci. 51:224–230. Loehr, V. J. T., M. D. Hofmeyr, and B. T. Henen. 2007. Growing and shrinking in the smallest tortoise, Homopus signatus signatus: the importance of rain. Oecologia 153:479–488. Milch, R. A., D. P. Rall, and J. E. Tobie. 1958. Fluorescence of tetra-cycline antibiotics in bone. J. Bone Joint Surg. Am. 40:897–910. Murakawa, S. K. K. 2012. Determination of growth spurts in Hawaiian green sea turtles using skeletochronology and histological analysis of gonads. [Master thesis], University of Hawai'i at Manoa, Honolulu. Musick, J. A., and C. J. Limpus. 1997. Habitat utilization and migration in juvenile sea turtles. Pp. 137–164 in P. L. Lutz and J. A. Musick, eds. The biology of sea turtles. CRC Press, Boca Raton, FL. National Research Council (NRC). 2010. Assessment of sea-turtle status and trends: integrating demography and abundance. National Academies Press, Washington, DC. Petitet, R., E. R. Secchi, L. Avens, and P. G. Kinas. 2012. Age and growth of loggerhead sea turtles in southern Brazil. Mar. Ecol. Prog. Ser. 456:255–268. Petitet, R., L. Avens, J. C. Castilhos, P. G. Kinas, and L. Bugoni. 2015. Age and growth of olive ridley sea turtles Lepidochelys olivacea in the main Brazilian nesting ground. Mar. Ecol. Prog. Ser. 541:205–218. Piovano, S., M. Clusa, C. Carreras, C. Giacoma, M. Pascual, and L. Cardona. 2011. Different growth rates between loggerhead sea turtles (Caretta caretta) of Mediterranean and Atlantic origin in the Mediterranean Sea. Mar. Biol. 158:2577–2587. Snover, M. L., and A. A. Hohn. 2004. Validation and interpretation of annual skeletal marks in loggerhead (Caretta caretta) and Kemp's ridley (Lepidochelys kempii) sea turtles. Fish. Bull. 102:682–692. Snover, M. L., L. Avens, and A. A. Hohn. 2007a. Back-calculating length from skeletal growth marks in loggerhead sea turtles Caretta caretta. Endanger. Species Res. 3:95–104. Snover, M. L., A. A. Hohn, L. B. Crowder, and S. S. Heppell. 2007b. Age and growth in Kemp's ridley sea turtles: evidence from mark-recapture and skeletochronology. Pp. 89–105 in P. T. Plotkin, ed. Biology and conservation of ridley sea turtles. Johns Hopkins Univ. Press, Baltimore, MD. Snover, M. L., A. A. Hohn, L. R. Goshe, and G. H. Balazs. 2011. Validation of annual skeletal marks in green sea turtles Chelonia mydas using tetracycline labeling. Aquat. Biol. 12:197–204. Snover, M. L., G. H. Balazs, S. K. K. Murakawa, S. K. Hargrove, M. R. Rice, and W. A. Seitz. 2013. Age and growth rates of Hawaiian hawksbill turtles (Eretmochelys imbricata) using skeletochronology. Mar. Biol. 160:37–46. Van Houtan, K. S., S. K. Hargrove, and G. H. Balazs. 2014. Modeling sea turtle maturity age from partial life history records. Pac. Sci. 68:465–477. Wikelski, M., and C. Thom. 2000. Marine iguanas shrink to survive El Niño. Nature 403:37–38. Wyneken, J. 2001. The anatomy of sea turtles. NOAA Technical Memorandum NMFS-SEFSC-470. Available at http://www.sefsc.noaa.gov/turtles/TM_470_Wyneken.pdf. (accessed 18 November 2015) Zar, J. H. 2010. Biostatistical analysis, 5th ed. Prentice-Hall, Upper Saddle River, New Jersey. Zug, G. R., and R. E. Glor. 1998. Estimates of age and growth in a population of green sea turtles (Chelonia mydas) from the Indian River lagoon system, Florida: a skeletochronological analysis. Can. J. Zool. 76:1497–1506. Zug, G. R., A. H. Wynn, and C. Ruckdeschel. 1986. Age determination of loggerhead sea turtles, Caretta caretta, by incremental growth marks in the skeleton. Smithsonian Contrib. Zool. 427:1–34. Zug, G. R., M. Chaloupka, and G. H. Balazs. 2006. Age and growth in olive ridley seaturtles (Lepidochelys olivacea) from the North-central Pacific: a skeletochronological analysis. Mar. Ecol. 27:263–270.