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.

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.

Context Matters: Hawaiian Monk Seals Switch Between Feeding Strategies Depending on Ecological Context.

The ability to expand the behavioral repertoire past seemingly rigid morphological features enables animals to succeed in a variety of ecological contexts. The integration of morphology, performance, and behavior produces diverse animal feeding strategies. These different strategies reflect trade-offs between specialization, prey choice, and energetic expenditure, which have important consequences for understanding individual and population-level flexibility in response to environmental change. Here we examined the feeding strategies used by the Hawaiian monk seal (Neomonachus schauinslandi), an endangered marine predator. We tested how Hawaiian monk seal feeding strategies change in response to ecological context, specifically prey size and prey location at different depths. Seven captive Hawaiian monk seals were fed five prey types across a continuum of sizes, and prey were presented at three depths to represent surface, pelagic, and benthic feeding. Hawaiian monk seals used suction feeding and biting strategies, and these strategies were associated with significant differences in behavior and kinematic performance. Hawaiian monk seals used suction feeding most frequently when targeting small to medium prey (0-79% of the seal's head length) but switched to biting when consuming large prey (>80% of the seal's head length). These results demonstrate that prey size drives the transition between suction feeding and biting strategies. Seals also switched strategies based on prey position in the water column, primarily using suction feeding when prey were benthic and pelagic, and biting when prey were at the water's surface. Overall, suction feeding was three to five times faster than biting, required a smaller gape, and used fewer jaw movements, allowing seals to quickly consume numerous small to medium sized prey. In contrast, biting was slower but resulted in the ability to target larger, potentially more energy rich prey. Our results show that Hawaiian monk seals exhibit flexibility in their use of different feeding strategies, which likely facilitates increased foraging success when feeding in spatially and temporally dynamic marine environments.

Hawaiian monk seals exhibit behavioral flexibility when targeting prey of different size and shape.

Animals use diverse feeding strategies to capture and consume prey, with many species switching between strategies to accommodate different prey. Many marine animals exhibit behavioral flexibility when feeding to deal with spatial and temporal heterogeneity in prey resources. However, little is known about flexibility in the feeding behavior of many large marine predators. Here, we documented the feeding behavior and kinematics of the endangered Hawaiian monk seal (Neomonachus schauinslandi, n=7) through controlled feeding trials. Seals were fed multiple prey types (e.g. night smelt, capelin, squid and herring) that varied in size and shape to examine behavioral flexibility in feeding. Hawaiian monk seals primarily used suction feeding (91% of all feeding trials) across all prey types, but biting, specifically pierce feeding, was also observed (9% of all feeding trials). Suction feeding was characterized by shorter temporal events, a smaller maximum gape and gape angle, and a fewer number of jaw motions than pierce feeding; suction feeding kinematic performance was also more variable compared with pierce feeding. Seals showed behavioral flexibility in their use of the two strategies. Suction feeding was used most frequently when targeting small to medium sized prey and biting was used with increasing frequency on larger prey. The feeding kinematics differed between feeding strategies and prey types, showing that Hawaiian monk seals adjusted their behaviors to particular feeding contexts. Hawaiian monk seals are opportunistic marine predators and their ability to adapt their feeding strategy and behavior to specific foraging scenarios allows them to target diverse prey resources.

Swimming and diving energetics in dolphins: a stroke-by-stroke analysis for predicting the cost of flight responses in wild odontocetes.

Exponential increases in hydrodynamic drag and physical exertion occur when swimmers move quickly through water, and underlie the preference for relatively slow routine speeds by marine mammals regardless of body size. Because of this and the need to balance limited oxygen stores when submerged, flight (escape) responses may be especially challenging for this group. To examine this, we used open-flow respirometry to measure the energetic cost of producing a swimming stroke during different levels of exercise in bottlenose dolphins (Tursiops truncatus). These data were then used to model the energetic cost of high-speed escape responses by other odontocetes ranging in mass from 42 to 2738 kg. The total cost per stroke during routine swimming by dolphins, 3.31±0.20 J kg-1 stroke-1, was doubled during maximal aerobic performance. A comparative analysis of locomotor costs (LC; in J kg-1 stroke-1), representing the cost of moving the flukes, revealed that LC during routine swimming increased with body mass (M) for odontocetes according to LC=1.46±0.0005M; a separate relationship described LC during high-speed stroking. Using these relationships, we found that continuous stroking coupled with reduced glide time in response to oceanic noise resulted in a 30.5% increase in metabolic rate in the beaked whale, a deep-diving odontocete considered especially sensitive to disturbance. By integrating energetics with swimming behavior and dive characteristics, this study demonstrates the physiological consequences of oceanic noise on diving mammals, and provides a powerful tool for predicting the biological significance of escape responses by cetaceans facing anthropogenic disturbances.

The high cost of reproduction in sea otters necessitates unique physiological adaptations.

Superimposed on inherently high basal metabolic demands, the additional energetic requirements of reproduction can push female sea otters beyond physiological limits. Indeed, the resulting energy imbalance contributes to disproportionately high rates of mortality at the end of lactation in this species. To examine and quantify metabolic changes associated with reproduction, we measured the resting metabolic rate (RMR) of a female sea otter across gestation, lactation and non-reproductive periods. Concurrently, measurements were made on a non-breeding control female. Our results suggest that RMR declines during gestation. Conversely, RMR increases during lactation, reaches a peak at 3-4 months postpartum, and remains elevated until weaning. Combining these direct measurements with published data, we found the cost of pup rearing to be significantly higher than previously estimated. High baseline energy demands and limited energy reserves, combined with significant lactation and pup rearing costs, appear to necessitate metabolic and thermal lability during key reproductive stages.

Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals.

Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper accelerations of bottlenose dolphins (Tursiops truncatus) and Weddell seals (Leptonychotes weddellii) diving from the surface to >200 m. Here we report that both exercise and depth alter the bradycardia associated with the dive response, with the greatest impacts at depths inducing lung collapse. Unexpectedly, cardiac arrhythmias occurred in >73% of deep, aerobic dives, which we attribute to the interplay between sympathetic and parasympathetic drivers for exercise and diving, respectively. Such marked cardiac variability alters the common view of a stereotypic 'dive reflex' in diving mammals. It also suggests the persistence of ancestral terrestrial traits in cardiac function that may help explain the unique sensitivity of some deep-diving marine mammals to anthropogenic disturbances.

Mammalian energetics. Instantaneous energetics of puma kills reveal advantage of felid sneak attacks.

Pumas (Puma concolor) live in diverse, often rugged, complex habitats. The energy they expend for hunting must account for this complexity but is difficult to measure for this and other large, cryptic carnivores. We developed and deployed a physiological SMART (species movement, acceleration, and radio tracking) collar that used accelerometry to continuously monitor energetics, movements, and behavior of free-ranging pumas. This felid species displayed marked individuality in predatory activities, ranging from low-cost sit-and-wait behaviors to constant movements with energetic costs averaging 2.3 times those predicted for running mammals. Pumas reduce these costs by remaining cryptic and precisely matching maximum pouncing force (overall dynamic body acceleration = 5.3 to 16.1g) to prey size. Such instantaneous energetics help to explain why most felids stalk and pounce, and their analysis represents a powerful approach for accurately forecasting resource demands required for survival by large, mobile predators.

The dive response redefined: underwater behavior influences cardiac variability in freely diving dolphins.

A hallmark of the dive response, bradycardia, promotes the conservation of onboard oxygen stores and enables marine mammals to submerge for prolonged periods. A paradox exists when marine mammals are foraging underwater because activity should promote an elevation in heart rate (f(H)) to support increased metabolic demands. To assess the effect of the interaction between the diving response and underwater activity on f(H), we integrated interbeat f(H) with behavioral observations of adult bottlenose dolphins diving and swimming along the coast of the Bahamas. As expected for the dive response, f(H) while resting during submergence (40±6 beats min(-1)) was significantly lower than f(H) while resting at the water surface (105±8 beats min(-1)). The maximum recorded f(H) (f(H,max)) was 128±7 beats min(-1), and occurred during post-dive surface intervals. During submergence, the level of bradycardia was modified by activity. Behaviors such as simple head bobbing at depth increased f(H) by 40% from submerged resting levels. Higher heart rates were observed for horizontal swimming at depth. Indeed, the dolphins operated at 37-58% of their f(H,max) while active at depth and approached 57-79% of their f(H,max) during anticipatory tachycardia as the animals glided to the surface. f(H) was significantly correlated with stroke frequency (range=0-2.5 strokes s(-1), r=0.88, N=25 dives) and calculated swim speed (range=0-5.4 m s(-1), r=0.88, N=25 dives). We find that rather than a static reflex, the dive response is modulated by behavior and exercise in a predictable manner.