Tracing gestation and lactation in free ranging gray whales using the stable isotopic composition of epidermis layers

Abstract

The isotopic composition of baleen whales’ epidermis structural layers can give information about dietary change over time. This study investigated if epidermis layers integrated isotopic values that record physiological changes from gestation to lactation. Epidermis tissues (n = 43) were collected from free ranging lactating female gray whale and calves during the beginning of three breeding seasons. Modelling of δ 13 C and δ 15 N values show intra- and inter-individual differences based on epidermal layers, age class and year of sampling. The isotopic composition of mother-calf pairs is correlated, and the estimates of the maximum mother-to-calf isotopic difference was ~1.4‰ for δ 13 C and between 1 and 1.5‰ for δ 15 N values. Change in δ 15 N values among epidermal layers in calves was associated with the transition from fetus to consumption of maternal milk. It is here proposed when lactation influences calf epidermis, δ 15 N values decrease consistently from the outermost to the innermost layer. However, if a calf was born only few days before collection, epidermis integrates more variable δ 15 N patterns because gestation still affects the isotopic composition of the layers. The possibility of calculating mother-to-calf nitrogen isotope fractionation, and the regularity of changes between calf layer δ 15 N values, allowed results of an isotopic clock model to predict the age of each calf when sampled with its mother. This model has the potential to be a straightforward method to estimate the beginning of lactation, therefore calf birth date when direct observations are not feasible. The non-lethal remote collection of epidermis appears to be an effective tool for the study of the physiology of reproduction of baleen whales. The parallel study of the three epidermal structural layers highlighted the importance of considering the unique mother-calf pair physiological status at the time of sampling time when stable isotope results are interpreted.

Isotopic composition of the eastern gray whale epidermis indicates contribution of prey outside Arctic feeding grounds

“…Samples were collected as described in Gelippi et al. 31 . In brief, focal sampling methodologies 47 and photoidentification techniques 48 , 49 were applied to all specimens except those collected in 2011.…”

“…Recently, temporal changes in feeding preferences and seasonal and regional movements of different species of baleen whales were reflected in epidermal inter-layer δ 13 C and δ 15 N variability in blue 28 , 29 , humpback, sperm and fin whale 30 . Differences among epidermal layer isotope values are reported for the gray whale 31 . Specifically, variations in inter-layer isotope values appear to exist in lactating mothers and calves, possibly due to the effect of physiological/dietary transition from gestation (placental blood) to lactation (maternal milk).…”

“…Direct observation of events that can influence life-history events, such as pregnancy and lactation, of marine highly mobile animals is challenging 27 . The carbon (δ 13 C) and nitrogen (δ 15 N) stable isotope analysis of whales’ epidermal structural layers is a promising tool that can be used to indirectly investigate diet during cryptic life stages 28 – 31 . Carbon and nitrogen isotope composition of marine primary producers differ among environments in predictable ways related to water temperature and nutrient sources that vary along latitudinal gradients 32 .…”

“…Epidermis is different from metabolically active tissues (as plasma and muscles) in that it grows continuously and provides an ~ 70 day archive of isotopic compositions in its three layers, the innermost “stratum basale”(SB), the intermediate “stratum spinosum” (SS) and the outermost “stratum corneum” (SC) 40 , 41 . Therefore δ 13 C and δ 15 N values in each epidermal layer can reflect those of diet integrated over specific periods of tissue growth 28 – 31 . When new cells are formed in the SB, their δ 13 C and δ 15 N values reflect that of blood stream components 42 .…”

Trophic ecology and foraging areas of cetaceans sampled in the coastal waters of south-eastern Brazil assessed through skin δ13C and δ15N

“…An increase in δ 13 C may be observed in the tissues of lactating females due to the production of lipid-rich 13 C-depleted maternal milk (e.g. Borrell et al, 2016;Gellippi et al, 2020). Additionally, the protein synthesis during lactation reduces the δ 15 N values in the maternal body protein (Kurle, 2002).…”