Intrapopulation variability in the timing of ontogenetic habitat shifts in sea turtles revealed using δ¹⁵N values from bone growth rings

Abstract

Summary Determining location and timing of ontogenetic shifts in the habitat use of highly migratory species, along with possible intrapopulation variation in these shifts, is essential for understanding mechanisms driving alternate life histories and assessing overall population trends. Measuring variations in multi-year habitat use patterns is especially difficult for remote oceanic species.To investigate the potential for differential habitat use among migratory marine vertebrates, we measured the naturally occurring stable nitrogen isotope (δ15N) patterns that differentiate distinct ocean regions to create a “regional isotope characterization”, analyzed the δ15N values from annual bone growth layer rings from dead-stranded animals, then combined the bone and regional isotope data to track individual animal movement patterns over multiple years.We used humeri from juvenile North Pacific loggerhead turtles (Caretta caretta), animals that undergo long migrations across the North Pacific Ocean (NPO), using multiple discrete regions as they develop to adulthood. Typical of many migratory marine species, ontogenetic changes in habitat use throughout their decades-long juvenile stage is poorly understood, but each potential habitat has unique foraging opportunities and spatially explicit natural and anthropogenic threats that could affect key life history parameters.We found a bimodal size/age distribution in the timing that juveniles underwent an ontogenetic habitat shift from the oceanic central North Pacific (CNP) to the neritic east Pacific region near the Baja California Peninsula (BCP) (42.7±7.2 vs. 68.3±3.4 cm carapace length, 7.5±2.7 vs. 15.6±1.7 years). Important to the survival of this population, these disparate habitats differ considerably in their food availability, energy requirements, and threats, and these differences can influence life history parameters such as growth, survival, and future fecundity. This is the first evidence of alternative ontogenetic shifts and habitat use patterns for juveniles foraging in the eastern NPO.We combine two techniques, skeletochronology and stable isotope analysis, to reconstruct multi-year habitat use patterns of a remote migratory species, linked to estimated ages and body sizes of individuals, to reveal variable ontogeny during the juvenile life stage that could drive alternate life histories and that has the potential to illuminate the migration patterns for other species with accretionary tissues.

Stable isotope discrimination factors and between‐tissue isotope comparisons for bone and skin from captive and wild green sea turtles (Chelonia mydas)

“…The ratios of stable isotopes (SI) such as carbon ( 12 C/ 13 C; δ 13 C value) and nitrogen ( 14 N/ 15 N; δ 15 N value) in consumer tissues can provide valuable insights into the trophic relationships and foraging ecology of populations and communities in a variety of ecosystems (e.g. ). Stable carbon and nitrogen isotopes fractionate during biological processing (e.g.…”

“…Because δ 15 N values are especially useful for informing consumer trophic levels, diet studies utilizing SI ratios of modern animal bones use primarily bone collagen. Practitioners of SI studies using sea turtle bones typically analyze the cortical portion because that is where the growth layers are retained, the carbonate content is low, and the composition is almost entirely of collagen . To our knowledge, no study has yet assessed the cortical bone‐diet discrimination factors of any reptile, including sea turtles.…”

Multi‐decadal and ontogenetic trophic shifts inferred from stable isotope ratios of pinniped teeth

“…Retrospective studies of stable isotope variation are possible for many body tissues that remain metabolically inert after formation, including teeth (Koch et al , Hanson et al ), baleen (Schell ), bone (Christensen and Richardson , Turner Tomaszewicz et al ), calcified cartilage (Carlisle et al ), and fish scales or otoliths (MacKenzie et al , Hanson et al ). These structures have the advantage of recording both individual life history and long‐term chemical signals.…”

Ancient DNA Analysis and Stable Isotope Ecology of Sea Turtles (Cheloniidae) from the Gold Rush-era (1850s) Eastern Pacific Ocean

“…The addition of bone collagen and apatite analyses also provides insights into the latter processes, specifically foraging ecology, and for the purposes of this study, helps provide a dataset to compare modern and archaeological samples. Pioneering work on sea turtle bone stable isotopes has demonstrated their value in understanding sea turtle and ocean water physiological processes, species-specific identifications (Biasatti 2002(Biasatti , 2004, isotopic assimilation and paleoclimatic relationships (Coulson et al 2008), and the effects of bone preparation protocols, ontogenetic shifts, migration, residency duration and tissue-specific isotopic discrimination (Turner Tomaszewicz et al 2015, 2016, 2018. We include bone apatite d 13 C ap and d…”

“…In addition, bone collagen comparisons occur in two forms. First, a direct bone-to-bone d (Figure 2; Lemons et al 2011;Lewis 2009;Rodríguez-Barón 2010;Turner Tomaszewicz et al 2015, 2016, 2018.…”