Annual variability in dentin δ¹⁵N and δ¹³C reveal sex differences in weaning age and feeding habits in Risso's dolphins (Grampus griseus)

Abstract

Teeth of odontocetes accumulate annual dentinal growth layer groups (GLGs) that record isotope ratios, which reflect the time of their synthesis. Collectively, they provide lifetime records of individual feeding patterns from which life history traits can be inferred. We subsampled the prenatal dentin and postnatal GLGs in Risso's dolphins (Grampus griseus) (n = 65) that stranded or were collected as bycatch in Taiwan (1994–2014) and analyzed them for δ15N and δ13C. Age‐specific δ15N and δ13C values were corrected for effects of calendar year, stranding site, C/N, and sex. δ15N values were higher in prenatal layers (14.94‰ ± 0.74‰) than in adult female GLGs (12.58‰ ± 0.20‰), suggesting fetal enrichment during gestation. Decreasing δ15N values in early GLGs suggested changes in dietary protein sources during transition to complete weaning. Weaning age was earlier in males (1.09 yr) than in females (1.81 yr). Significant differences in δ15N values between weaned males and females suggest potential sexual segregation in feeding habits. δ13C values increased from the prenatal to the 4th GLG by ~1.0‰, indicative of a diet shift from 13C‐depleted milk to prey items. Our results provide novel insights into the sex‐specific ontogenetic changes in feeding patterns and some life history traits of Risso's dolphins.

Prolonged maternal investment in northern bottlenose whales alters our understanding of beaked whale reproductive life history

“…Although the trend for carbon is consistent with our inferences of prolonged nursing and a gradual transition from milk to solid food, gradual enrichment in 13 C has not always been observed in other studies of odontocetes (e.g. D. leucas, [16]; Grampus griseus, [17]). As juvenile H. ampullatus whales learn to forage deeper, the increase in δ 13 C may reflect increasing consumption of bentho-pelagic species, which would be expected to have higher δ 13 C values [46].…”

“…Interestingly, our finding that δ 15 N in fetal dentine was almost 1 ‰ lower than GLG 1 differs from the pattern of steady decline in δ 15 N from a peak in fetal dentine observed in other species of cetaceans (Grampus griseus, [17]; Monodon Monoceros, Zhao et al unpublished data; Delphinapterus leucas, Matthews & Zhao, unpublished data). Our explanations for the inconsistencies between enrichment patterns in fetal dentine across cetacean species consider two possibilities: (1) if tissues measured in other studies are actually neonatal rather than fetal dentine, δ 15 N for other species would reflect an ongoing decline in post-partum nursing [51]; or (2) differences are due to species-specific reproductive biology, such as physiological differences between capital and income breeders or growth dependent trophic enrichment factors.…”

“…The weaning period, which includes the introduction to solid food accompanied by nursing, can vary in length depending on whether maternal weaning strategies are abrupt or gradual. Using the timing associated with the cessation of a general declining trend in δ 15 N, changepoint analysis or model fit against a number of theoretical curves, a number of authors PLOS ONE [14,16,17] have proposed that unlike baleen whales, weaning in odontocetes is a relatively gradual process. While the introduction of solid food may occur within the first year, this is often accompanied by prolonged nursing across a number of odontocete species [4], suggesting stomach contents are unlikely to provide good evidence of the age when weaning is complete.…”

“…However weaning related relationships with δ 13 C are less clear and across studies there is no consistent trend or pattern reported for isotopic carbon found in marine mammal tissues during the dietary transition from milk to prey (e.g. [16][17][18]).…”

“…Across studies, behavioural observations typically reported the oldest average age at weaning (27 months), in contrast with stomach content analyses, which found average weaning age occurred much younger (16 months, S1 Table). Temporal analysis of nitrogen stable isotopes (δ 15 N) in accretionary tissues, such as sequential growth layer groups (GLGs) in dentine, have also been used to estimate weaning age and other ontogenetic shifts in individual foraging and trophic level based on nutritional physiology [13][14][15][16][17]. As δ 15 N decreases during the transition from juveniles feeding exclusively on milk to independent foraging, differences in δ 15 N between GLGs in tooth dentine can be used to estimate nursing duration and weaning completion e.g.…”