Conservation energetics of beluga whales: using resting and swimming metabolism to understand threats to an endangered population.

The balance between energetic costs and acquisition in free-ranging species is essential for survival, and provides important insights regarding the physiological impact of anthropogenic disturbances on wild animals. For marine mammals such as beluga whales (Delphinapterus leucas), the first step in modeling this bioenergetic balance requires an examination of resting and active metabolic demands. Here, we used open-flow respirometry to measure oxygen consumption during surface rest and submerged swimming by trained beluga whales, and compared these measurements with those of a commonly studied odontocete, the Atlantic bottlenose dolphin (Tursiops truncatus). Both resting metabolic rate (3012±126.0 kJ h-1) and total cost of transport (1.4±0.1 J kg-1 m-1) of beluga whales were consistent with predicted values for moderately sized marine mammals in temperate to cold-water environments, including dolphins measured in the present study. By coupling the rate of oxygen consumption during submerged swimming with locomotor metrics from animal-borne accelerometer tags, we developed predictive relationships for assessing energetic costs from swim speed, stroke rate and partial dynamic acceleration. Combining these energetic data with calculated aerobic dive limits for beluga whales (8.8 min), we found that high-speed responses to disturbance markedly reduce the whale's capacity for prolonged submergence, pushing the cetaceans to costly anaerobic performances that require prolonged recovery periods. Together, these species-specific energetic measurements for beluga whales provide two important metrics, gait-related locomotor costs and aerobic capacity limits, for identifying relative levels of physiological vulnerability to anthropogenic disturbances that have become increasingly pervasive in their Arctic habitats.

Racing extinction: Can science act fast enough to save large, endangered mammals?

How far can a polar bear swim? The answer to that one question could have altered the course of the global warming movement and tempered current public distrust in scienceand scientists. As is the case for many large, fierce mammals, many aspects of the basic biology that dictate what polar bears (Ursus maritimus) need to survive in a changing world remain a mystery. We don't know the limitations of the bear's thermoregulatory or swimming capabilities in Arctic waters. Nor do we know whether a terrestrial diet of berries and scavenging is able to sustain a mother bear throughout pregnancy and cub rearing should the continued deterioration of sea ice force them to remain on land. At a time when understanding animal capacities and resiliency in the face of human perturbation is crucial to species survival, science has been unable to keep pace with emerging environmental threats.

Mother Nature's playground: Sometimes in the wild it is all about fun.

From surfboard-stealing sea otters to sailboat-chomping killer whales, the summer of 2023 was a landmark year of wild animal antics. Why is wildlife suddenly interacting with humans and their toys in this way? Speculation and headlines have espoused theories about learned behaviors due to enticements with food, increased intrusion, and proximity of humans in wild habitats, as well as aberrant animal responses instigated by oceanic noise or disease-related neurological disorders. However, the most honest answer is, "We don't really know. Maybe the animals are just playing around."

Brain activity of diving seals reveals short sleep cycles at depth.

Sleep is a crucial part of the daily activity patterns of mammals. However, in marine species that spend months or entire lifetimes at sea, the location, timing, and duration of sleep may be constrained. To understand how marine mammals satisfy their daily sleep requirements while at sea, we monitored electroencephalographic activity in wild northern elephant seals (Mirounga angustirostris) diving in Monterey Bay, California. Brain-wave patterns showed that seals took short (less than 20 minutes) naps while diving (maximum depth 377 meters; 104 sleeping dives). Linking these patterns to accelerometry and the time-depth profiles of 334 free-ranging seals (514,406 sleeping dives) revealed a North Pacific sleepscape in which seals averaged only 2 hours of sleep per day for 7 months, rivaling the record for the least sleep among all mammals, which is currently held by the African elephant (about 2 hours per day).

Recasting the whale's wonderful net.

Modification of cerebral vasculature helps to cushion the brains of whales and dolphins against injury.

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals.

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

Racing Time: Physiological Rates and Metabolic Scaling in Marine Mammals.

Reinvasion of the oceans beginning 10-60 million years ago by ancient mammals instigated one of the most remarkable metabolic transitions across evolutionary time. A consequence of marine living, especially in colder waters, has been a 1.4 to 2.9-fold increase in resting metabolic rate (RMR) for otters, pinnipeds and cetaceans over predicted levels for terrestrial mammals of similar body mass. Notably, the greatest metabolic elevation occurred in the smallest marine mammals, suggesting an underlying thermal causative mechanism. Superimposed on these resting costs are the metabolic demands of locomotion. Collectively termed the field metabolic rate, such active costs consistently approach three times the resting rates of individuals regardless of locomotor style, species, foraging patterns, habitat or geographic location. In wild non-reproducing mammals, the FMR/RMR ratio averages 2.6-2.8 for both terrestrial and marine species, with the latter group maintaining larger absolute daily metabolic rates supported by comparatively higher food ingestion rates. Interestingly, the limit for habitual (multi-day), sustained maximal energy expenditure in human endurance athletes averages < 3.0 times resting metabolic levels, with a notable exception in Tour de France cyclists. Importantly, both athletes and wild mammals seem similarly constrained; that is, by the ability to process enough calories in a day to support exceptional metabolic performance.

Evidence of traumatic brain injury in headbutting bovids.

Traumatic brain injury (TBI) is a leading cause of neurologic impairment and death that remains poorly understood. Rodent models have yet to produce clinical therapies, and the exploration of larger and more diverse models remains relatively scarce. We investigated the potential for brain injury after headbutting in two combative bovid species by assessing neuromorphology and neuropathology through immunohistochemistry and stereological quantification. Postmortem brains of muskoxen (Ovibos moschatus, n = 3) and bighorn sheep (Ovis canadensis, n = 4) were analyzed by high-resolution MRI and processed histologically for evidence of TBI. Exploratory histological protocols investigated potential abnormalities in neurons, microglia, and astrocytes in the prefrontal and parietal cortex. Phosphorylated tau protein, a TBI biomarker found in the cerebrospinal fluid and in neurodegenerative lesions, was used to detect possible cellular consequences of chronic or acute TBI. MRI revealed no abnormal neuropathological changes; however, high amounts of tau-immunoreactive neuritic thread clusters, neurites, and neurons were concentrated in the superficial layers of the neocortex, preferentially at the bottom of the sulci in the muskoxen and occasionally around blood vessels. Tau-immunoreactive lesions were rare in the bighorn sheep. Additionally, microglia and astrocytes showed no grouping around tau-immunoreactive cells in either species. Our preliminary findings indicate that muskoxen and possibly other headbutting bovids suffer from chronic or acute brain trauma and that the males' thicker skulls may protect them to a certain extent.

Temporal scale of habitat selection for large carnivores: Balancing energetics, risk and finding prey.

When navigating heterogeneous landscapes, large carnivores must balance trade-offs between multiple goals, including minimizing energetic expenditure, maintaining access to hunting opportunities and avoiding potential risk from humans. The relative importance of these goals in driving carnivore movement likely changes across temporal scales, but our understanding of these dynamics remains limited. Here we quantified how drivers of movement and habitat selection changed with temporal grain for two large carnivore species living in human-dominated landscapes, providing insights into commonalities in carnivore movement strategies across regions. We used high-resolution GPS collar data and integrated step selection analyses to model movement and habitat selection for African lions Panthera leo in Laikipia, Kenya and pumas Puma concolor in the Santa Cruz Mountains of California across eight temporal grains, ranging from 5 min to 12 hr. Analyses considered landscape covariates that are related to energetics, resource acquisition and anthropogenic risk. For both species, topographic slope, which strongly influences energetic expenditure, drove habitat selection and movement patterns over fine temporal grains but was less important at longer temporal grains. In contrast, avoiding anthropogenic risk during the day, when risk was highest, was consistently important across grains, but the degree to which carnivores relaxed this avoidance at night was strongest for longer term movements. Lions and pumas modified their movement behaviour differently in response to anthropogenic features: lions sped up while near humans at fine temporal grains, while pumas slowed down in more developed areas at coarse temporal grains. Finally, pumas experienced a trade-off between energetically efficient movement and avoiding anthropogenic risk. Temporal grain is an important methodological consideration in habitat selection analyses, as drivers of both movement and habitat selection changed across temporal grain. Additionally, grain-dependent patterns can reflect meaningful behavioural processes, including how fitness-relevant goals influence behaviour over different periods of time. In applying multi-scale analysis to fine-resolution data, we showed that two large carnivore species in very different human-dominated landscapes balanced competing energetic and safety demands in largely similar ways. These commonalities suggest general strategies of landscape use across large carnivore species.

Metabolic trade-offs in tropical and subtropical marine mammals: unique maintenance and locomotion costs in West Indian manatees and Hawaiian monk seals.

Unlike the majority of marine mammal species, Hawaiian monk seals (Neomonachus schauinslandi) and West Indian manatees (Trichechus manatus latirostris) reside exclusively in tropical or subtropical waters. Although potentially providing an energetic benefit through reduced maintenance and thermal costs, little is known about the cascading effects that may alter energy expenditure during activity, dive responses and overall energy budgets for these warm-water species. To examine this, we used open-flow respirometry to measure the energy expended during resting and swimming in both species. We found that the average resting metabolic rates (RMRs) for both the adult monk seal (753.8±26.1 kJ h-1, mean±s.e.m.) and manatees (887.7±19.5 kJ h-1) were lower than predicted for cold-water marine mammal species of similar body mass. Despite these relatively low RMRs, both total cost per stroke and total cost of transport (COTTOT) during submerged swimming were similar to predictions for comparably sized marine mammals (adult monk seal: cost per stroke=5.0±0.2 J kg-1 stroke-1, COTTOT=1.7±0.1 J kg-1 m-1; manatees: cost per stroke=2.0±0.4 J kg-1 stroke-1, COTTOT=0.87±0.17 J kg-1 m-1). These lower maintenance costs result in less variability in adjustable metabolic costs that occur during submergence for warm-water species. However, these reduced maintenance costs do not appear to confer an advantage in overall energetic costs during activity, potentially limiting the capacity of warm-water species to respond to anthropogenic or environmental threats that require increased energy expenditure.

Unconventional animal models for traumatic brain injury and chronic traumatic encephalopathy.

Traumatic brain injury (TBI) is one of the main causes of death worldwide. It is a complex injury that influences cellular physiology, causes neuronal cell death, and affects molecular pathways in the brain. This in turn can result in sensory, motor, and behavioral alterations that deeply impact the quality of life. Repetitive mild TBI can progress into chronic traumatic encephalopathy (CTE), a neurodegenerative condition linked to severe behavioral changes. While current animal models of TBI and CTE such as rodents, are useful to explore affected pathways, clinical findings therein have rarely translated into clinical applications, possibly because of the many morphofunctional differences between the model animals and humans. It is therefore important to complement these studies with alternative animal models that may better replicate the individuality of human TBI. Comparative studies in animals with naturally evolved brain protection such as bighorn sheep, woodpeckers, and whales, may provide preventive applications in humans. The advantages of an in-depth study of these unconventional animals are threefold. First, to increase knowledge of the often-understudied species in question; second, to improve common animal models based on the study of their extreme counterparts; and finally, to tap into a source of biological inspiration for comparative studies and translational applications in humans.

Physiological consequences of Arctic sea ice loss on large marine carnivores: unique responses by polar bears and narwhals.

Rapid environmental changes in the Arctic are threatening the survival of marine species that rely on the predictable presence of the sea ice. Two Arctic marine mammal specialists, the polar bear (Ursus maritimus) and narwhal (Monodon monoceros), appear especially vulnerable to the speed and capriciousness of sea ice deterioration as a consequence of their unique hunting behaviors and diet, as well as their physiological adaptations for slow-aerobic exercise. These intrinsic characteristics limit the ability of these species to respond to extrinsic threats associated with environmental change and increased industrial activity in a warming Arctic. In assessing how sea ice loss may differentially affect polar bears that hunt on the ice surface and narwhals that hunt at extreme depths below, we found that major ice loss translated into elevated locomotor costs that range from 3- to 4-fold greater than expected for both species. For polar bears this instigates an energy imbalance from the combined effects of reduced caloric intake and increased energy expenditure. For narwhals, high locomotor costs during diving increase the risk of ice entrapment due to the unreliability of breathing holes. These species-specific physiological constraints and extreme reliance on the polar sea ice conspire to make these two marine mammal specialists sentinels of climate change within the Arctic marine ecosystem that may foreshadow rapid changes to the marine ecosystem.

Physiological resiliency in diving mammals: Insights on hypoxia protection using the Krogh principle to understand COVID-19 symptoms.

Sequential diving by wild marine mammals results in a lifetime of rapid physiological transitions between lung collapse-reinflation, bradycardia-tachycardia, vasoconstriction-vasodilation, and oxygen store depletion-restoration. The result is a cycle of normoxia and hypoxia in which blood oxygen partial pressures can decline to <20-30 mmHg during a dive, a level considered injurious to oxygen-dependent human tissues (i.e., brain, heart). Safeguards in the form of enhanced on-board oxygen stores, selective oxygen transport, and unique tissue buffering capacities enable marine-adapted mammals to maintain physiological homeostasis and energy metabolism even when breathing and pulmonary gas exchange cease. This stands in stark contrast to the vulnerability of oxygen-sensitive tissues in humans that may undergo irreversible damage within minutes of ischemia and tissue hypoxia. Recently, these differences in protection against hypoxic injury have become evident in the systemic, multi-organ physiological failure during COVID-19 infection in humans. Prolonged recoveries in some patients have led to delays in the return to normal exercise levels and cognitive function even months later. Rather than a single solution to this problem, we find that marine mammals rely on a unique, integrative assemblage of protections to avoid the deleterious impacts of hypoxia on tissues. Built across evolutionary time, these solutions provide a natural template for identifying the potential for tissue damage when oxygen is lacking, and for guiding management decisions to support oxygen-deprived tissues in other mammalian species, including humans, challenged by hypoxia.

Changes in Northern Elephant Seal Skeletal Muscle Following Thirty Days of Fasting and Reduced Activity.

Northern elephant seals (NES, Mirounga angustirostris) undergo an annual molt during which they spend ∼40 days fasting on land with reduced activity and lose approximately one-quarter of their body mass. Reduced activity and muscle load in stereotypic terrestrial mammalian models results in decreased muscle mass and capacity for force production and aerobic metabolism. However, the majority of lost mass in fasting female NES is from fat while muscle mass is largely preserved. Although muscle mass is preserved, potential changes to the metabolic and contractile capacity are unknown. To assess potential changes in NES skeletal muscle during molt, we collected muscle biopsies from 6 adult female NES before the molt and after ∼30 days at the end of the molt. Skeletal muscle was assessed for respiratory capacity using high resolution respirometry, and RNA was extracted to assess changes in gene expression. Despite a month of reduced activity, fasting, and weight loss, skeletal muscle respiratory capacity was preserved with no change in OXPHOS respiratory capacity. Molt was associated with 162 upregulated genes including those favoring lipid metabolism. We identified 172 downregulated genes including those coding for ribosomal proteins and genes associated with skeletal muscle force transduction and glucose metabolism. Following ∼30 days of molt, NES skeletal muscle metabolic capacity is preserved although mechanotransduction may be compromised. In the absence of exercise stimulus, fasting-induced shifts in muscle metabolism may stimulate pathways associated with preserving the mass and metabolic capacity of slow oxidative muscle.

Some like it cold: Temperature-dependent habitat selection by narwhals.

The narwhal (Monodon monoceros) is a high-Arctic species inhabiting areas that are experiencing increases in sea temperatures, which together with reduction in sea ice are expected to modify the niches of several Arctic marine apex predators. The Scoresby Sound fjord complex in East Greenland is the summer residence for an isolated population of narwhals. The movements of 12 whales instrumented with Fastloc-GPS transmitters were studied during summer in Scoresby Sound and at their offshore winter ground in 2017-2019. An additional four narwhals provided detailed hydrographic profiles on both summer and winter grounds. Data on diving of the whales were obtained from 20 satellite-linked time-depth recorders and 16 Acousonde™ recorders that also provided information on the temperature and depth of buzzes. In summer, the foraging whales targeted depths between 300 and 850 m where the preferred areas visited by the whales had temperatures ranging between 0.6 and 1.5°C (mean = 1.1°C, SD = 0.22). The highest probability of buzzing activity during summer was at a temperature of 0.7°C and at depths > 300 m. The whales targeted similar depths at their offshore winter ground where the temperature was slightly higher (range: 0.7-1.7°C, mean = 1.3°C, SD = 0.29). Both the probability of buzzing events and the spatial distribution of the whales in both seasons demonstrated a preferential selection of cold water. This was particularly pronounced in winter where cold coastal water was selected and warm Atlantic water farther offshore was avoided. It is unknown if the small temperature niche of whales while feeding is because prey is concentrated at these temperature gradients and is easier to capture at low temperatures, or because there are limitations in the thermoregulation of the whales. In any case, the small niche requirements together with their strong site fidelity emphasize the sensitivity of narwhals to changes in the thermal characteristics of their habitats.

Surviving in steep terrain: a lab-to-field assessment of locomotor costs for wild mountain lions (Puma concolor).

BACKGROUND: Under current scenarios of climate change and habitat loss, many wild animals, especially large predators, are moving into novel energetically challenging environments. Consequently, changes in terrain associated with such moves may heighten energetic costs and effect the decline of populations in new localities. METHODS: To examine locomotor costs of a large carnivorous mammal moving in mountainous habitats, the oxygen consumption of captive pumas (Puma concolor) was measured during treadmill locomotion on level and incline (6.8°) surfaces. These data were used to predict energetic costs of locomotor behaviours of free-ranging pumas equipped with GPS/accelerometer collars in California's Santa Cruz Mountains. RESULTS: Incline walking resulted in a 42.0% ± 7.2 SEM increase in the costs of transport compared to level performance. Pumas negotiated steep terrain by traversing across hillsides (mean hill incline 17.2° ± 0.3 SEM; mean path incline 7.3° ± 0.1 SEM). Pumas also walked more slowly up steeper paths, thereby minimizing the energetic impact of vertical terrains. Estimated daily energy expenditure (DEE) based on GPS-derived speeds of free-ranging pumas was 18.3 MJ day- 1 ± 0.2 SEM. Calculations show that a 20 degree increase in mean steepness of the terrain would increase puma DEE by less than 1% as they only spend a small proportion (10%) of their day travelling. They also avoided elevated costs by utilizing slower speeds and shallower path angles. CONCLUSIONS: While many factors influence survival in novel habitats, we illustrate the importance of behaviours which reduce locomotor costs when traversing new, energetically challenging environments, and demonstrate that these behaviours are utilised by pumas in the wild.

The seasonal energetic landscape of an apex marine carnivore, the polar bear.

Divergent movement strategies have enabled wildlife populations to adapt to environmental change. In recent decades, the Southern Beaufort Sea subpopulation of polar bears (Ursus maritimus) has developed a divergent movement strategy in response to diminishing sea ice where the majority of the subpopulation (73-85%) stays on the sea ice in summer and the remaining bears move to land. Although declines in sea ice are generally considered a challenge to energy balance in polar bears residing in some regions of the Arctic, little quantitative data exists concerning the seasonal energy expenditures of this apex marine carnivore. We used GPS satellite collars with tri-axial accelerometers and conductivity sensors to measure the location, behavior, and energy expenditure of five adult female polar bears in the southern Beaufort Sea across seasons of sea ice breakup and minimum extent. Using a Bayesian mixed-effects model, we found that energy expenditure was influenced by month, ocean depth, and habitat type (sea ice or land). Total energy expenditure from May through September ranged from 37.7 to 47.2 mJ/kg for individual bears. Bears that moved to land expended 7% more energy on average from May through September than bears that remained on the receding sea ice. In August, when bears were moving from the sea ice to land or moving north with the receding pack ice, bears that moved to land spent 7% more time swimming and expended 22% more energy. This means the immediate cost of moving to land exceeded the cost of remaining on the receding summer pack ice. These findings suggest a physiological reason why the majority of the Southern Beaufort Sea subpopulation continues to inhabit a diminishing summer ice platform. However, bears that moved to land spent 29% more time in preferred hunting habitats over the continental shelf than bears that remained on the sea ice. Bears on land also had access to subsistence-harvested bowhead whale carcasses. Hence, our findings indicate there may be a greater overall energetic benefit to move to land in this region, which suggests that the use of the diminishing summer sea ice may be functioning as an ecological trap.

How smooth is a dolphin? The ridged skin of odontocetes.

Dolphin skin has long been an inspiration for research on drag reduction mechanisms due to the presence of skin ridges that could reduce fluid resistance. We gathered in vivo three-dimensional surface data on the skin from five species of odontocetes to quantitatively examine skin texture, including the presence and size of ridges. We used these data to calculate k+ values, which relate surface geometry to changes in boundary layer flow. Our results showed that while ridge size differs among species, odontocete skin was surprisingly smooth compared to the skin of other swimmers (average roughness = 5.3 µm). In addition, the presence of ridges was variable among individuals of the same species. We predict that odontocete skin ridges do not alter boundary layer flows at cruising swimming speeds. By combining k+ values and morphological data, our work provides evidence that skin ridges are unlikely to be an adaptation for drag reduction and that odontocete skin is exceptionally smooth compared to other pelagic swimmers.

Estimating the energy expenditure of free-ranging polar bears using tri-axial accelerometers: A validation with doubly labeled water.

Measures of energy expenditure can be used to inform animal conservation and management, but methods for measuring the energy expenditure of free-ranging animals have a variety of limitations. Advancements in biologging technologies have enabled the use of dynamic body acceleration derived from accelerometers as a proxy for energy expenditure. Although dynamic body acceleration has been shown to strongly correlate with oxygen consumption in captive animals, it has been validated in only a few studies on free-ranging animals. Here, we use relationships between oxygen consumption and overall dynamic body acceleration in resting and walking polar bears Ursus maritimus and published values for the costs of swimming in polar bears to estimate the total energy expenditure of 6 free-ranging polar bears that were primarily using the sea ice of the Beaufort Sea. Energetic models based on accelerometry were compared to models of energy expenditure on the same individuals derived from doubly labeled water methods. Accelerometer-based estimates of energy expenditure on average predicted total energy expenditure to be 30% less than estimates derived from doubly labeled water. Nevertheless, accelerometer-based measures of energy expenditure strongly correlated (r 2 = 0.70) with measures derived from doubly labeled water. Our findings highlight the strengths and limitations in dynamic body acceleration as a measure of total energy expenditure while also further supporting its use as a proxy for instantaneous, detailed energy expenditure in free-ranging animals.