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Behavioral Ecology of Cetaceans: The Relationship of Body Condition with Behavior and Reproductive Status
Dr. Patrick Miller | University of Saint Andrews
This study focused on the ‘Behavioral Ecology of Cetaceans’. The risk of harm to cetaceans from underwater noise is an important environmental and regulatory issue faced by the Department of Defense (DoD). Long-term consequences of disturbance are particularly difficult to quantify. Noise may reduce foraging rates and thereby health of individual animals which could then negatively impact survival and reproduction ultimately affecting vital rates of populations. Lipid-store body condition, defined here as the quantity of lipid store carried by an animal, is a measure of individual health which has been shown to be a good predictor of offspring survival and reproductive success in seals. Body condition is thought to influence how animals broadly trade-off foraging and anti-predator behaviors, and modulates responses to natural and anthropogenic disturbance. Unfortunately, for free-ranging cetaceans that cannot be captured for study, it is not possible to use the ‘gold-standard’ method to measure lipid store in mammals (isotope dilution), though indicators of body condition have been developed using visual observation, measurement of body shape from photogrammetry, and analysis of remotely collected biopsy samples of blubber.
In this study, the research team developed and cross-validated a novel, state-of-the-art non-invasive method to measure total body lipid-stores of free-ranging cetaceans based upon their tissue body density. Tissue body density measures from individual animals were compared to two independent indicators of body condition: body shape and lipid and steroid hormonal markers in blubber. The research team describes how these three measures of body condition vary with reproductive status, location, and timing in relation to feeding and fasting cycles. Finally, the research team explored how body condition of individuals relates to behavioral time budgets, focusing on foraging effort versus resting and/or anti-predator behaviors.
Fieldwork efforts were conducted with two key species: the beaked whale Hyperodoon ampullatus (northern bottlenose whale) and mysticete whale Megaptera novaeangliae (humpback whale), after the research team demonstrated that it was possible to calculate body tissue density from those species. A beaked whale was selected based upon their sensitivity to naval sonar signals, and a mysticete whale based upon their known cycling of lipid fat stores across annual fasting and feeding seasons. Measurement of body density was conducted via analysis of gliding performance from data collected by an external tag attached to the body using non-invasive suction cups. Body density determines the overall buoyancy of cetaceans in seawater, which affects speed changes during glides in the ascent and descent phases of cetacean dives. State-of-the-art Bayesian statistical techniques simultaneously account for the effects of diving air volume and body drag on gliding performance, providing a rich set of physiological measurements. The same animal-attached tag records high-resolution behavioral data used for classification of functional feeding and antipredator behaviors, enabling exploration of how body condition relates to foraging time budgets.
In addition to concurrent attachment of suction cup tags, fieldwork efforts focused on collection of measurements of body shape and remote biopsy sample collection including external blubber layers. Following evaluation of an approach to measure body shape using a three-dimensional two scanning sonar, the research team systematically used digital photography from Unmanned Aerial Vehicles (UAV) to collect body shape images of humpback whales. Analysis of photogrammetry images entailed calculation of body width versus length, which the research team quantified using a length-standardized surface area index (LSSAI). Collection of biopsy samples from tagged animals enables both estimation of female reproductive status and estimation of lipid-store body condition based upon blubber lipid content or hormone concentrations. Hormonal and potential proteomic approaches to quantify body condition were tested and refined based upon analysis of tissue samples obtained from stranded or by-caught cetacean carcasses. Blubber cortisol concentration was found to correlate with body condition based upon morphometric condition indices of stranded cetaceans, so was used as the primary hormonal indicator of body condition in this study. Proteins in blubber using a ‘shotgun’ proteomic approach were also explored in relation to body condition.
The project team successfully conducted multiple field efforts with three excursions to study northern bottlenose whales off Jan Mayen, Norway (June 2014-2016) and seven excursions early and later in the feeding season for humpback whales in the Gulf of St Lawrence, Canada (three during June-September 2016-2017) and northern Norway (four during May-January 2014, 2016-2018). Additional tag data for these species were obtained during Limited Scope fieldwork in the Gully and Gulf of St Lawrence funded by SERDP prior to commencement of this full project, and from collaborating partners. Calculation of tissue body density was successfully accomplished for the two target species, and another deep-diving delphinidae Globicephala melas, the long-finned pilot whale. In all species studied, tissue body density modulated swimming patterns during ascent and descent phases of dives, with more gliding in the direction aided by buoyancy. Northern bottlenose whales were found to have individual differences in tissue body density, but the range of observed densities (1028.4 to 1033.9 kg m−3) over 21 tag deployments in the Gully and Jan Mayen was narrow compared to what was measured for humpback whales (1027.8 to 1050.8 kg m-3.) over 59 tag deployments in Canada and Norway, indicating that unlike humpback whales that cycle lipid fat stores seasonally, free-ranging bottlenose whales maintain an allostatic body condition, probably by continuous feeding. Interestingly, bottlenose whales tagged off Jan Mayen had a consistently lower tissue body density, indicating larger lipid stores, than whales tagged off Nova Scotia, Canada. Greater deviations away from neutral buoyancy observed in the Gully animals may entail higher dive transit swimming costs, indicating greater metabolic requirements than occur for bottlenose whales off Jan Mayen.
As predicted for humpback whales, tissue body density was higher (indicating smaller lipid stores) early in the feeding season and lower (indicating greater lipid stores) later in the feeding season. Statistical analysis indicated that across both Norway and Canada, tissue body density of whales decreased by 0.03 kg m-3 per day, or 2.7 kg m-3 over 90 days of the feeding period. A similar seasonal trend was found for the body shape measure LSSAI of 55 humpback whales for which photogrammetry images were taken using a drone UAV, indicating whales were wider per unit length later in the feeding season. Reproductive status also influenced tissue body shape with lactating females being thinner per unit length than other adult females, as expected. The project team found a strong statistical correlation between LSSAI and tissue body density with wider adult humpback whales having a lower body density, as predicted (N = 18). In contrast, cortisol concentrations of 73 blubber samples of humpback whales did not vary with season and did not correlate with tissue body density or LSSAI across the 33 tagged animals for which biopsy samples were also collected. However, the project team found a strong trend between body density and cortisol across nine pregnant females, those with lower tissue density (hence greater lipid stores) had higher cortisol concentrations. Whilst blubber cortisol concentrations per se were not a useful quantitative indicator of condition, the validation studies (and recently additional published studies in cetaceans) indicate they provide information on the metabolic state of the tissue at the time of sampling, where high concentrations are seen in animals mobilizing fat and lower concentrations are seen when fat is being deposited. Thus, overall, the strongest and statistically significant correlation was found between tissue body density and LSSAI for adult humpback whales (R2 =29.9%, N=18).
As expected for whales tagged during the feeding season, production of echolocation click buzzes by northern bottlenose whales and performance of underwater lunges by humpback whales indicated active feeding by animals tagged in the study. Humpback whales spent a relatively large amount of time foraging in both the early (68 ± 19%, range, 17-92%, n = 17 whales) and middle season (61 ± 38%, range, 7-93%, n = 4 whales) in Canada. Tagged whales in Norway spent relatively little time foraging in the late season (18 ± 24%, range, 0-62%, n = 10 whales) compared with the early season (42 ± 31%, range, 17-92%, n = 14 whales). Indeed, time spent feeding substantially decreased with decreasing tissue body density. The result suggests lipid store body condition affects feeding behavior and that relatively fat humpback whales might be less motivated to feed, as predicted by starvation-predation tradeoff theory. Intriguingly, the opposite trend was observed across the 15 northern bottlenose whales tagged off Jan Mayen. Contrary to predictions of starvation-predation tradeoff theory, lower tissue body density (indicating a greater lipid store) was found to predict more foraging time and less anti-predator behavior, indicating that lipid-store body condition may be the consequence, rather than the driver, of foraging effort over the narrow ranges of body condition observed for northern bottlenose whales.
This study has made several fundamental advances in methods to estimate body condition of freeranging cetaceans, and the understanding of the factors that can influence it. The method of analyzing gliding performance to estimate tissue body density has now been applied to several cetacean species, including a DoD priority beaked whale and a relatively shallower-diving baleen whale. This confirms that the tissue body density method can be a widely-applicable tool, enabling routine measurement of body condition of free-ranging cetaceans. As a tag-based method, it has the potential to enable longitudinal measurement of body condition changes in the same individual animal. Long-term monitoring of the body condition of individuals can be a powerful tool to measure health changes that might arise from disturbance associated with DoD activities. Transition of this technology and its incorporation into a longer-duration tag, with on board calculation of body density and satellite telemetry of the results, has been started under the Office of Naval Research funding.
The study has also confirmed that the camera-mounted UAV approach to measure body condition via photogrammetry is effective and correlates well with the body density approach to estimate full body lipid stores in humpback whales. As a low-cost method that is even less invasive than suction-cup tagging, the project team expects that UAV approaches to measure body shape will also become more widely used to study body condition of free-ranging cetaceans. The study also showed that use of remotely collected biopsy samples to estimate body condition requires care as simple measures like lipid content are not reliable. Hormones such as the glucocorticoids that are upregulated in response to local tissue metabolic state and particularly when measured in combination with other regulatory proteins and peptides, have the potential to add valuable information on the energetic status of the animals at the time of sampling.
These approaches have advanced the ability to measure body condition of this group of animals. By quantifying how natural factors of season and reproductive status affect body condition, this study enables fuller evaluation of the possible biologically-significant effects of disturbance on cetaceans, including by DoD activities.