Patterns of trace element deposition in beluga whale teeth reflect early life history.

Determination of trace element concentrations in continuously growing biological structures such as otoliths, whiskers, and teeth can provide important insight into physiological and ontogenetic processes. We examined concentrations of 11 trace elements (Li, Mg, Mn, Cu, Zn, Se, Rb, Sr, Cs, Ba, Pb) in the annual dentine growth layer groups (GLGs) of teeth of 66 Eastern Canadian Arctic belugas (Delphinapterus leucas). Several of these trace elements displayed clear and consistent patterns in early life, though few longer term trends or signals were present in trace element data for either females or males. Large changes in Sr and Ba concentrations in fetal dentine reflected in utero shifts in element deposition in the teeth of developing belugas. Marked changes in these elements during the first years after birth were likely associated with the onset of nursing and subsequent weaning. Mg, Mn, and Zn also displayed clear and consistent patterns in early life that correlated strongly with dentine stable nitrogen isotope (δ15N) data, suggesting these elements merit further study as potential tools for studying nursing and weaning. Depositional patterns of Zn and Pb, which have been linked to sexual maturation in female Pacific walruses (Odobenus rosmarus divergens), were inconsistent in beluga teeth. Some individuals (including males) displayed patterns strongly resembling those observed in female walruses, whereas many animals did not, perhaps because they had not yet reached sexual maturity. The lack of clear patterns in trace element deposition after the first few years of life may have resulted from pooling samples from multiple populations/regions collected across more than two decades, but may also indicate that elemental concentrations are primarily driven by other, extrinsic processes later in life, and might be useful as biomonitors of environmental element concentrations or tools for delineating population structure.

Whiskers provide time-series of toxic and essential trace elements, Se:Hg molar ratios, and stable isotope values of an apex Antarctic predator, the leopard seal.

In an era of rapid environmental change and increasing human presence, researchers need efficient tools for tracking contaminants to monitor the health of Antarctic flora and fauna. Here, we examined the utility of leopard seal whiskers as a biomonitoring tool that reconstructs time-series of significant ecological and physiological biomarkers. Leopard seals (Hydrurga leptonyx) are a sentinel species in the Western Antarctic Peninsula due to their apex predator status and top-down effects on several Antarctic species. However, there are few data on their contaminant loads. We analyzed leopard seal whiskers (n = 18 individuals, n = 981 segments) collected during 2018-2019 field seasons to acquire longitudinal profiles of non-essential (Hg, Pb, and Cd) and essential (Se, Cu, and Zn) trace elements, stable isotope (ẟ15N and ẟ13C) values and to assess Hg risk with Se:Hg molar ratios. Whiskers provided between 46 and 286 cumulative days of growth with a mean ~ 125 days per whisker (n = 18). Adult whiskers showed variability in non-essential trace elements over time that could partly be explained by changes in diet. Whisker Hg levels were insufficient (<20 ppm) to consider most seals being at "high" risk for Hg toxicity. Nevertheless, maximum Hg concentrations observed in this study were greater than that of leopard seal hair measured two decades ago. However, variation in the Se:Hg molar ratios over time suggest that Se may detoxify Hg burden in leopard seals. Overall, we provide evidence that the analysis of leopard seal whiskers allows for the reconstruction of time-series ecological and physiological data and can be valuable for opportunistically monitoring the health of the leopard seal population and their Antarctic ecosystem during climate change.

Walrus teeth as biomonitors of trace elements in Arctic marine ecosystems.

Effective biomonitoring requires an understanding of the factors driving concentrations of the substances or compounds of interest in the tissues of studied organisms. Biomonitoring of trace elements, and heavy metals in particular, has been the focus of much research; however, the complex roles many trace elements play in animal and plant tissues can make it difficult to disentangle environmental signals from physiology. This study examined the concentrations of 15 trace elements in the teeth of 122 Pacific walruses (Odobenus rosmarus divergens) to investigate the potential for walrus teeth as biomonitors of trace elements in Arctic ecosystems. Elemental concentrations were measured across cementum growth layer groups (GLGs), thereby reconstructing a lifetime history of element concentrations for each walrus. The locations of GLGs were used to divide trace element time series into individual years, allowing each GLG to be associated with an animal age and a calendar year. The elements studied exhibited a great deal of complexity, reflecting the numerous factors responsible for generating tooth trace element concentrations. Generalized linear mixed models were used to investigate the importance of age and sex in explaining observed variation in trace element concentrations. Some elements exhibited clear physiological signals (particularly zinc, strontium, barium, and lead), and all elements except arsenic varied by age and/or sex. Pearson's correlations revealed that elements were more strongly correlated among calendar years than among individual walruses, and correlations of trace elements within individual walruses were generally inconsistent or weak. Plots of average elemental concentrations through time from 1945 to 2014 further supported the correlation analyses, with many elements exhibiting similar patterns across the ~70-year period. Together, these results indicate the importance of physiology in modulating tooth trace element concentrations in walrus tooth cementum, but suggest that many trace elements reflect a record of environmental exposure and dietary intake/uptake.

Evaluating tooth strontium and barium as indicators of weaning age in Pacific walruses.

Lactation length and weaning age provide important information about maternal investment, which can reflect the health and nutritional status of the mother, as well as broader reproductive strategies in mammals. Calcium-normalized strontium (Sr) and barium (Ba) concentrations in the growth layers of mammalian teeth differ for nursing animals and those consuming non-milk foods, thus can be used to estimate age-at-weaning. To date, this approach has been used only for terrestrial animals, and almost exclusively for primates.The goal of this study was to determine whether Sr and Ba concentrations in the cementum of Pacific walrus Odobenus rosmarus divergens teeth can be used to estimate weaning age. Teeth from 107 walruses were analysed using laser ablation inductively coupled plasma mass spectrometry, and calcium-normalized 88Sr and 137Ba concentrations were quantified.For most walruses, both Sr and Ba concentrations exhibited rapid changes in early life. Ba concentrations matched closely with expected patterns in the published literature, rapidly declining from high to low concentrations (typically from ~10 ppm to ~5 ppm). In contrast, Sr exhibited a pattern opposite to that presented in studies of terrestrial mammals, appearing nearly identical to Ba (typically declining from ~400 ppm to ~200 ppm). To explain these findings, we present conceptual models of the factors generating weaning signals in Sr and Ba for terrestrial mammals, as well as a new, hypothetical model for walruses. Both a visual and mathematical approach to weaning age estimation indicated a median weaning age of walruses at the end of the second year of life (in the second dark layer of the tooth cementum), with many walruses estimated to have weaned in their third year of life, and a smaller group weaning in their fourth or fifth year. This is later than expected, given a published estimate of walrus weaning at 18-24 months.These results do not conclusively support the use of tooth Sr and Ba for estimating weaning age in walruses, and further research is warranted to better understand the drivers of the observed patterns of Ba and Sr accumulation in walrus teeth.

Determining sex of adult Pacific walruses from mandible measurements.

Pacific walruses (Odobenus rosmarus divergens) play a vital role in Arctic marine ecosystems and the subsistence lifestyle of Alaska Native communities. Museum collections contain numerous archaeological and historic walrus specimens that have proven useful in a variety of studies; however, for many cases, the sex of these specimens is unknown. Sexes of adult (> 5 years determined by tooth aging) Atlantic walruses (Odobenus rosmarus rosmarus) have been accurately determined in previous studies using mandible measurements. We tested the validity of this approach for Pacific walruses, and used full fusion of the mandibular symphysis to define adults. Using high precision digital calipers (± 0.01 mm), four measurements were taken either on the left or right side of 91 walrus mandibles: 80 modern mandibles (70 known-sex specimens; 10 unknown-sex specimens) and 11 archaeological mandibles of unknown sex. We used linear discriminant function analysis (LDFA) to determine what measurements best distinguished Pacific walrus males from females. Minimum mandible thickness had the most predictive power, whereas mandible length, height, and depth, were less predictive. Posterior probabilities indicated that LDFA classified the known-sex Pacific walruses with 100% accuracy, and unknown sex with ≥ 90% probability. The ability to define the sex of unknown individuals accurately could greatly increase the sample size of future projects dealing with skeletal remains, and will improve future research efforts.

Ancient Beringian paleodiets revealed through multiproxy stable isotope analyses.

The earliest Native Americans have often been portrayed as either megafaunal specialists or generalist foragers, but this debate cannot be resolved by studying the faunal record alone. Stable isotope analysis directly reveals the foods consumed by individuals. We present multi-tissue isotope analyses of two Ancient Beringian infants from the Upward Sun River site (USR), Alaska (~11,500 years ago). Models of fetal bone turnover combined with seasonally-sensitive taxa show that the carbon and nitrogen isotope composition of USR infant bone collagen reflects maternal diets over the summer. Using comparative faunal isotope data, we demonstrate that although terrestrial sources dominated maternal diets, salmon was also important, supported by carbon isotope analysis of essential amino acids and bone bioapatite. Tooth enamel samples indicate increased salmon use between spring and summer. Our results do not support either strictly megafaunal specialists or generalized foragers but indicate that Ancient Beringian diets were complex and seasonally structured.

Zinc concentrations in teeth of female walruses reflect the onset of reproductive maturity.

Age at maturity is an important parameter in many demographic models and, for some species, can be difficult to obtain using traditional methods. Incremental growth structures act as biological archives, recording information throughout an organism's life and possibly allowing for the reconstruction of life history events. Concentrations of zinc (Zn) in animal tissues are known to be linked to life history, physiology and reproduction and may be retained in incremental growth structures. This study reconstructed lifetime Zn concentrations in teeth (n = 93) of female Pacific walruses (Odobenus rosmarus divergens) collected from 1932-2016. Zn displayed a characteristic pattern of accumulation, with a change point marking the beginning of a lifelong, linear increase in Zn concentrations. We hypothesized that this change point marks the onset of reproductive maturity. The age at which the change point occurred (agecp) was estimated by counting tooth cementum growth layers. These estimates closely matched literature values of timing of first ovulation in female walruses. Total number of ovulations (estimated from ovary corpora counts from paired tooth/ovary specimens) was closely related to reproductive lifespan (total lifespan - agecp; R2 = 0.70). Further, agecp tracked changes in Pacific walrus population size as a proportion of carrying capacity, decreasing when the population was depleted by commercial hunting and peaking when carrying capacity was exceeded. This novel approach will aid walrus management, and is likely applicable to other species, offering a potentially powerful tool for research, management and conservation of wildlife populations.

Author Correction: Lipid normalization and stable isotope discrimination in Pacific walrus tissues.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Corrigendum to: Heavy with child? Pregnancy status and stable isotope ratios as determined from biopsies of humpback whales.

[This corrects the article DOI: 10.1093/conphys/cow050.].

Lipid normalization and stable isotope discrimination in Pacific walrus tissues.

Analysis of stable carbon and nitrogen isotope values (δ13C and δ15N) of animal tissues can provide important information about diet, physiology, and movements. Interpretation of δ13C and δ15N values, however, is influenced by factors such as sample lipid content, tissue-specific isotope discrimination, and tissue turnover rates, which are typically species- and tissue-specific. In this study, we generated lipid normalization models for δ13C and investigated the effects of chemical lipid extractions on δ13C and δ15N in Pacific walrus (Odobenus rosmarus divergens) muscle, liver, and skin. We also evaluated tissue-specific isotope discrimination in walrus muscle, liver, skin, and bone collagen. Mean δ13Clipid-free of skin and bone collagen were similar, as were mean δ15N of muscle and liver. All other tissues differed significantly for both isotopes. Differences in δ13Clipid-free and δ15N among tissues agreed with published estimates of marine mammal tissue-specific isotope discrimination factors, with the exception of skin. The results of this work will allow researchers to gain a clearer understanding of walrus diet and the structure of Arctic food webs, while also making it possible to directly compare the results of contemporary walrus isotope research with those of historic and paleoecological studies.

Erratum: Heavy with child? Pregnancy status and stable isotope ratios as determined from biopsies of humpback whales.

[This corrects the article DOI: 10.1093/conphys/cow050.].

Heavy with child? Pregnancy status and stable isotope ratios as determined from biopsies of humpback whales.

Understanding reproductive rates of wild animal populations is crucially important for management and conservation. Assessing pregnancy status of free-ranging cetaceans has historically been difficult; however, recent advances in analytical techniques have allowed the diagnosis of pregnancy from small samples of blubber tissue. The primary objectives of this study were as follows: (i) to test the efficacy of blubber progesterone assays as a tool for diagnosing pregnancy in humpback whales (Megaptera novaeangliae); (ii) to estimate the pregnancy rate of humpback whales in Monterey Bay, California; and (iii) to investigate the relationship between stable isotopes and reproductive status of these whales. Progesterone concentrations of female whales fell into two distinct groups, allowing for diagnostic separation of pregnant and non-pregnant individuals. Pregnancy rate varied between years of the study (48.4%% in 2011 and 18.5% in 2012), but fell within the range of other estimates of reproductive success for this population. Stable carbon and nitrogen isotope ratios were examined to investigate the impacts of pregnancy on these values. Neither δ15N nor δ13C varied in a consistent way among animals of different sex or reproductive status. The relationship between δ15N and δ13C was strongly positive for male and non-pregnant female humpbacks; however, no relationship existed for pregnant whales. This difference may be indicative of the effects of pregnancy on δ15N, resulting from tissue synthesis and reduced excretion of nitrogenous waste, as well as on δ13C through increased mobilization of lipid stores to meet the energetic demands of pregnancy. Ultimately, our results support the use of blubber progesterone assays for diagnosing pregnancy in humpback whales and indicate that, when paired with other approaches (e.g. stable isotope analysis), pregnancy status can be an informative tool for addressing questions about animal physiology, ecology and population biology. This information will provide for more effective management and conservation efforts in a rapidly changing world.

Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current.

Large, migratory predators are often cited as sentinel species for ecosystem processes and climate-related changes, but their utility as indicators is dependent upon an understanding of their response to environmental variability. Documentation of the links between climate variability, ecosystem change and predator dynamics is absent for most top predators. Identifying species that may be useful indicators and elucidating these mechanistic links provides insight into current ecological dynamics and may inform predictions of future ecosystem responses to climatic change. We examine humpback whale response to environmental variability through stable isotope analysis of diet over a dynamic 20-year period (1993-2012) in the California Current System (CCS). Humpback whale diets captured two major shifts in oceanographic and ecological conditions in the CCS. Isotopic signatures reflect a diet dominated by krill during periods characterized by positive phases of the North Pacific Gyre Oscillation (NPGO), cool sea surface temperature (SST), strong upwelling and high krill biomass. In contrast, humpback whale diets are dominated by schooling fish when the NPGO is negative, SST is warmer, seasonal upwelling is delayed and anchovy and sardine populations display increased biomass and range expansion. These findings demonstrate that humpback whales trophically respond to ecosystem shifts, and as a result, their foraging behavior is a synoptic indicator of oceanographic and ecological conditions across the CCS. Multi-decadal examination of these sentinel species thus provides insight into biological consequences of interannual climate fluctuations, fundamental to advancing ecosystem predictions related to global climate change.