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1.
Glob Chang Biol ; 30(6): e17366, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38847450

ABSTRACT

Changes in body size have been documented across taxa in response to human activities and climate change. Body size influences many aspects of an individual's physiology, behavior, and ecology, ultimately affecting life history performance and resilience to stressors. In this study, we developed an analytical approach to model individual growth patterns using aerial imagery collected via drones, which can be used to investigate shifts in body size in a population and the associated drivers. We applied the method to a large morphological dataset of gray whales (Eschrichtius robustus) using a distinct foraging ground along the NE Pacific coast, and found that the asymptotic length of these whales has declined since around the year 2000 at an average rate of 0.05-0.12 m/y. The decline has been stronger in females, which are estimated to be now comparable in size to males, minimizing sexual dimorphism. We show that the decline in asymptotic length is correlated with two oceanographic metrics acting as proxies of habitat quality at different scales: the mean Pacific Decadal Oscillation index, and the mean ratio between upwelling intensity in a season and the number of relaxation events. These results suggest that the decline in gray whale body size may represent a plastic response to changing environmental conditions. Decreasing body size could have cascading effects on the population's demography, ability to adjust to environmental changes, and ecological influence on the structure of their community. This finding adds to the mounting evidence that body size is shrinking in several marine populations in association with climate change and other anthropogenic stressors. Our modeling approach is broadly applicable across multiple systems where morphological data on megafauna are collected using drones.


Subject(s)
Body Size , Climate Change , Whales , Animals , Female , Male , Whales/physiology , Ecosystem , Models, Biological , Pacific Ocean
2.
Gen Comp Endocrinol ; 352: 114492, 2024 06 01.
Article in English | MEDLINE | ID: mdl-38479678

ABSTRACT

Individual-level assessments of wild animal health, vital rates, and foraging ecology are critical for understanding population-wide impacts of exposure to stressors. Large whales face multiple stressors, including, but not limited to, ocean noise, pollution, and ship strikes. Because baleen is a continuously growing keratinized structure, serial extraction, and quantification of hormones and stable isotopes along the length of baleen provide a historical record of whale physiology and foraging ecology. Furthermore, baleen analysis enables the investigation of dead specimens, even decades later, allowing comparisons between historic and modern populations. Here, we examined baleen of five sub-adult gray whales and observed distinct patterns of oscillations in δ15N values along the length of their baleen plates which enabled estimation of baleen growth rates and differentiation of isotopic niche widths of the whales during wintering and summer foraging. In contrast, no regular patterns were apparent in δ13C values. Prolonged elevation of cortisol in four individuals before death indicates that chronic stress may have impacted their health and survival. Triiodothyronine (T3) increased over months in the whales with unknown causes of death, simultaneous with elevations in cortisol, but both hormones remained stable in the one case of acute death attributed to killer whale predation. This parallel elevation of cortisol and T3 challenges the classic understanding of their interaction and might relate to increased energetic demands during exposure to stressors. Reproductive hormone profiles in subadults did not show cyclical trends, suggesting they had not yet reached sexual maturity. This study highlights the potential of baleen analysis to retrospectively assess gray whales' physiological status, exposure to stressors, reproductive status, and foraging ecology in the months or years leading up to their death, which can be a useful tool for conservation diagnostics to mitigate unusual mortality events.


Subject(s)
Endocrinology , Whales , Animals , Hydrocortisone , Longitudinal Studies , Retrospective Studies
3.
Conserv Physiol ; 11(1): coad082, 2023.
Article in English | MEDLINE | ID: mdl-38026800

ABSTRACT

Understanding how individual animals respond to stressors behaviourally and physiologically is a critical step towards quantifying long-term population consequences and informing management efforts. Glucocorticoid (GC) metabolite accumulation in various matrices provides an integrated measure of adrenal activation in baleen whales and could thus be used to investigate physiological changes following exposure to stressors. In this study, we measured GC concentrations in faecal samples of Pacific Coast Feeding Group (PCFG) gray whales (Eschrichtius robustus) collected over seven consecutive years to assess the association between GC content and metrics of exposure to sound levels and vessel traffic at different temporal scales, while controlling for contextual variables such as sex, reproductive status, age, body condition, year, time of year and location. We develop a Bayesian Generalized Additive Modelling approach that accommodates the many complexities of these data, including non-linear variation in hormone concentrations, missing covariate values, repeated samples, sampling variability and some hormone concentrations below the limit of detection. Estimated relationships showed large variability, but emerging patterns indicate a strong context-dependency of physiological variation, depending on sex, body condition and proximity to a port. Our results highlight the need to control for baseline hormone variation related to context, which otherwise can obscure the functional relationship between faecal GCs and stressor exposure. Therefore, extensive data collection to determine sources of baseline variation in well-studied populations, such as PCFG gray whales, could shed light on cetacean stress physiology and be used to extend applicability to less-well-studied taxa. GC analyses may offer greatest utility when employed as part of a suite of markers that, in aggregate, provide a multivariate measure of physiological status, better informing estimates of individuals' health and ultimately the consequences of anthropogenic stressors on populations.

4.
Integr Org Biol ; 4(1): obac014, 2022.
Article in English | MEDLINE | ID: mdl-35617113

ABSTRACT

Male mammals of seasonally reproducing species typically have annual testosterone (T) cycles, with T usually peaking during the breeding season, but occurrence of such cycles in male mysticete whales has been difficult to confirm. Baleen, a keratinized filter-feeding apparatus of mysticetes, incorporates hormones as it grows, such that a single baleen plate can record years of endocrine history with sufficient temporal resolution to discern seasonal patterns. We analyzed patterns of T every 2 cm across the full length of baleen plates from nine male bowhead whales (Balaena mysticetus) to investigate occurrence and regularity of T cycles and potential inferences about timing of breeding season, sexual maturation, and reproductive senescence. Baleen specimens ranged from 181-330 cm in length, representing an estimated 11 years (smallest whale) to 22 years (largest whale) of continuous baleen growth, as indicated by annual cycles in stable isotopes. All baleen specimens contained regularly spaced areas of high T content (T peaks) confirmed by time series analysis to be cyclic, with periods matching annual stable isotope cycles of the same individuals. In 8 of the 9 whales, T peaks preceded putative summer isotope peaks by a mean of 2.8 months, suggesting a mating season in late winter / early spring. The only exception to this pattern was the smallest and youngest male, which had T peaks synchronous with isotope peaks. This smallest, youngest whale also did not have T peaks in the first half of the plate, suggesting initiation of T cycling during the period of baleen growth. Linear mixed effect models suggest that whale age influences T concentrations, with the two largest and oldest males exhibiting a dramatic decline in T peak concentration across the period of baleen growth. Overall, these patterns are consistent with onset of sexual maturity in younger males and possible reproductive senescence in older males. We conclude that adult male bowheads undergo annual T cycles, and that analyses of T in baleen may enable investigation of reproductive seasonality, timing of the breeding season, and life history of male whales.

5.
Gen Comp Endocrinol ; 315: 113828, 2022 01 01.
Article in English | MEDLINE | ID: mdl-34058189

ABSTRACT

Obtaining endocrine data from alternative sample types such as baleen and other keratinized tissues has proven a valuable tool to investigate reproductive and stress physiology via steroid hormone quantification, and metabolic stress via thyroid hormone quantification in whales and other vertebrates. These alternative sample types provide an integrated measure of plasma levels over the period that the structure was growing, thus capturing months or even years of an individual's endocrine history. Additionally, their robust and stable keratin matrix allows such samples to be stored for years to decades, enabling the analysis and comparison of endocrine patterns from past and modern populations. However, the extraction and analysis of hormones from baleen and other keratinized tissues remains novel and requires both biological and analytical validations to ensure the method fulfills the requirements for its intended use. We utilized baleen recovered at necropsy from southern right whales (Eubalaena australis) that died at Península Valdés, Argentina, using a commercially available progesterone enzyme immunoassay (EIA) to address two methodological questions: 1) what is the minimum sample mass required to reliably quantify hormone content of baleen samples analyzed with commercially available EIAs, and 2) what is the optimal ratio of solvent volume to sample mass, i.e., the ratio that yields the maximum amount of hormone with high accuracy and low variability between replicates. We concluded that masses of at least 20 mg should be used whenever possible, and extraction is best performed using an 80:1 ratio of solvent to sample (volume of solvent to sample mass; µl:mg). These results can help researchers to make informed methodological decisions when using a destructive extraction method with rare or unique specimens.


Subject(s)
Hormones , Whales , Animals , Endocrine System , Gastrointestinal Tract , Hormones/metabolism , Solvents/metabolism , Whales/metabolism
6.
Oecologia ; 198(1): 21-34, 2022 Jan.
Article in English | MEDLINE | ID: mdl-34800166

ABSTRACT

In waters off Península Valdés (PV), Argentina, southern right whales (SRW, Eubalaena australis) are occasionally exposed to domoic acid (DA), a neurotoxin produced by diatoms of the genus Pseudo-nitzschia. Domoic acid toxicity in marine mammals can cause gastrointestinal and neurological clinical signs, alterations in hematologic and endocrine variables, and can be fatal in extreme cases. In this study, we validated an enzyme immunoassay to quantify fecal glucocorticoid metabolites (fGCm) in 16 SRW fecal samples from live and dead stranded whales in PV from 2013 to 2018 and assessed fGCm levels associated with DA exposure. Overall, fGCm levels were significantly lower in SRWs with detectable fecal DA (n = 3) as compared to SRWs with undetectable fecal DA levels (n = 13). The highest fecal DA was observed in a live lactating female, which had low fGCm compared to the other lactating females studied. The highest fGCm was observed in a lactating female with undetectable DA; interestingly, at the time of sample collection, this female was sighted with two calves, an extremely unusual occurrence in this species. Though the sample size of these exceptionally rare breeding-season fecal samples was unavoidably small, our study provides evidence of potential adrenal alterations in whales exposed to an environmental neurotoxin such as DA.


Subject(s)
Lactation , Whales , Animals , Female , Kainic Acid/analogs & derivatives , Seasons
7.
Gen Comp Endocrinol ; 309: 113795, 2021 08 01.
Article in English | MEDLINE | ID: mdl-33891932

ABSTRACT

Monitoring the physiology of wild populations presents many technical challenges. Blood samples, long the gold standard of wildlife endocrinology studies, cannot always be obtained. The validation and use of non-plasma samples to obtain hormone data have greatly improved access to more integrated information about an organism's physiological state. Keratinous tissues like skin, hair, nails, feathers, or baleen store steroid hormones in physiologically relevant concentrations, are stable across decades, and can be used to retrospectively infer physiological state at prior points in time. Most protocols for steroid extraction employ physical pulverization or cutting of the sample, followed by mixing with a solvent. Such methods do produce repeatable and useful data, but low hormone yield and detectability issues can complicate research on small or rare samples. We investigated the use of keratinase, an enzyme that breaks down keratin, to improve the extraction and yield of corticosterone from vertebrate keratin tissues. Corticosterone content of keratinase-digested extracts were compared to non-keratinase extracts for baleen from three species of whale (blue, Balaenoptera musculus; bowhead, Balaena mysticetus; southern right, SRW; Eubalaena australis), shed skin from two reptiles (tegu lizard, Salvator merianae; narrow-headed garter snake, Thamnophis rufipunctatus), hair from arctic ground squirrel (AGS; Urocitellus parryii), feathers from Purple Martins (PUMA; Progne subis), and spines from the short-beaked echidna (Tachyglossus aculeatus). We tested four starting masses (10, 25, 50, 100 mg) for each sample; digestion was most complete in the 10 and 25 mg samples. A corticosterone enzyme immunoassay (EIA) was validated for all keratinase-digested extracts. In all sample types except shed skin from reptiles, keratinase digestion improved hormone yield, with PUMA feathers and blue whale baleen having the greatest increase in apparent corticosterone content (100% and 66% more hormone, respectively). The reptilian shed skin samples did not benefit from keratinase digestion, actually yielding less hormone than controls. With further optimization and refinement, keratinase digestion could greatly improve yield of steroid hormones from various wildlife epidermal tissue types, allowing more efficient use of samples and ultimately improving understanding of the endocrine physiology of wild populations.


Subject(s)
Balaenoptera , Keratins , Animals , Corticosterone , Digestion , Peptide Hydrolases , Retrospective Studies , Steroids
8.
Gen Comp Endocrinol ; 296: 113536, 2020 09 15.
Article in English | MEDLINE | ID: mdl-32540491

ABSTRACT

Physiological measurements are informative in assessing the relative importance of stressors that potentially impact the health of wildlife. Kelp Gulls, Larus dominicanus (KG), resident to the region of Península Valdés, Argentina, have developed a unique behavior of landing on the backs of southern right whale adults and calves, Eubalaena australis (SRW), where they feed on their skin and blubber. This parasitic behavior results in large open wounds on the dorsal surface of the whale. Coincidently, the SRW population off the coast of Península Valdés has experienced elevated calf mortality. We quantified levels of glucocorticoids and thyroid hormone extracted from baleen of dead calves to evaluate, retrospectively, the endocrine response of whale calves to gull wounding and harassment. Baleen accumulates hormones as it grows, allowing evaluation of long-term trends in physiological condition. While glucocorticoids (GCs) are known to increase in response to stressors such as disturbance, the metabolic hormone triiodothyronine (T3) has been shown to decrease under sustained food deprivation but is largely unaffected by disturbance stress. We quantified lifetime patterns of GCs and T3 in baleen recovered at necropsy from 36 southern right whale calves with varying severity of wounding from KGs. GC levels in baleen correlated positively with the degree of wounding, while T3 levels remained stable irrespective of the severity of the wounding. Our results suggest no evidence of malnutrition in low vs. severely wounded whales. However, the positive correlation of GCs with wound severity indicates that heavily wounded calves are suffering high levels of physiological stress before they die. This suggests that KG wounding may have contributed to the high southern right whale calf mortality observed in the Península Valdés region of Argentina.


Subject(s)
Charadriiformes/physiology , Endocrine System/metabolism , Hormones/metabolism , Whales/metabolism , Wounds and Injuries/pathology , Animals , Area Under Curve , Argentina , Corticosterone/metabolism , Female , Glucocorticoids/metabolism , Hydrocortisone/metabolism , Immunoenzyme Techniques , Linear Models , Male , Steroids/metabolism , Triiodothyronine/metabolism
9.
Conserv Physiol ; 6(1): coy049, 2018.
Article in English | MEDLINE | ID: mdl-30254748

ABSTRACT

Male baleen whales have long been suspected to have annual cycles in testosterone, but due to difficulty in collecting endocrine samples, little direct evidence exists to confirm this hypothesis. Potential influences of stress or adrenal stress hormones (cortisol, corticosterone) on male reproduction have also been difficult to study. Baleen has recently been shown to accumulate steroid hormones during growth, such that a single baleen plate contains a continuous, multi-year retrospective record of the whale's endocrine history. As a preliminary investigation into potential testosterone cyclicity in male whales and influences of stress, we determined patterns in immunoreactive testosterone, two glucocorticoids (cortisol and corticosterone), and stable-isotope (SI) ratios, across the full length of baleen plates from a bowhead whale (Balaena mysticetus), a North Atlantic right whale (Eubalaena glacialis) and a blue whale (Balaenoptera musculus), all adult males. Baleen was subsampled at 2 cm (bowhead, right) or 1 cm (blue) intervals and hormones were extracted from baleen powder with methanol, followed by quantification of all three hormones using enzyme immunoassays validated for baleen extract of these species. Baleen of all three males contained regularly spaced peaks in testosterone content, with number and spacing of testosterone peaks corresponding well to SI data and to species-specific estimates of annual baleen growth rate. Cortisol and corticosterone exhibited some peaks that co-occurred with testosterone peaks, while other glucocorticoid peaks occurred independent of testosterone peaks. The right whale had unusually high glucocorticoids during a period with a known entanglement in fishing gear and a possible disease episode; in the subsequent year, testosterone was unusually low. Further study of baleen testosterone patterns in male whales could help clarify conservation- and management-related questions such as age of sexual maturity, location and season of breeding, and the potential effect of anthropogenic and natural stressors on male testosterone cycles.

10.
Conserv Physiol ; 6(1): coy045, 2018.
Article in English | MEDLINE | ID: mdl-30151197

ABSTRACT

Baleen tissue accumulates stress hormones (glucocorticoids, GC) as it grows, along with other adrenal, gonadal and thyroid hormones. The hormones are deposited in a linear fashion such that a single plate of baleen allows retrospective assessment and evaluation of long-term trends in the whales' physiological condition. In whale calves, a single piece of baleen contains hormones deposited across the lifespan of the animal, with the tip of the baleen representing prenatally grown baleen. This suggests that baleen recovered from stranded carcasses of whale calves could be used to examine lifetime patterns of stress physiology. Here we report lifetime profiles of cortisol and corticosterone in baleen of a North Atlantic right whale ('NARW'-Eubalaena glacialis) calf that died from a vessel strike, as well as four southern right whale ('SRW'-Eubalaena australis) calves that were found dead with varying severity of chronic wounding from Kelp Gull (Larus dominicanus) attacks. In all five calves, prenatally grown baleen exhibited a distinctive profile of elevated glucocorticoids that declined shortly before birth, similar to GC profiles reported from baleen of pregnant females. After birth, GC profiles in calf baleen corresponded with the degree of wounding. The NARW calf and two SRW calves with no or few gull wounds had relatively low and constant GC content throughout life, while two SRW calves with high numbers of gull wounds had pronounced elevations in baleen GC content in postnatal baleen followed by a precipitous decline shortly before death, a profile suggestive of prolonged chronic stress. Baleen samples may present a promising and valuable tool for defining the baseline physiology of whale calves and may prove useful for addressing conservation-relevant questions such as distinguishing acute from chronic stress and, potentially, determining cause of death.

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