Tracking of marine predators to protect Southern Ocean ecosystems.

Southern Ocean ecosystems are under pressure from resource exploitation and climate change1,2. Mitigation requires the identification and protection of Areas of Ecological Significance (AESs), which have so far not been determined at the ocean-basin scale. Here, using assemblage-level tracking of marine predators, we identify AESs for this globally important region and assess current threats and protection levels. Integration of more than 4,000 tracks from 17 bird and mammal species reveals AESs around sub-Antarctic islands in the Atlantic and Indian Oceans and over the Antarctic continental shelf. Fishing pressure is disproportionately concentrated inside AESs, and climate change over the next century is predicted to impose pressure on these areas, particularly around the Antarctic continent. At present, 7.1% of the ocean south of 40°S is under formal protection, including 29% of the total AESs. The establishment and regular revision of networks of protection that encompass AESs are needed to provide long-term mitigation of growing pressures on Southern Ocean ecosystems.

Whiskers as hydrodynamic prey sensors in foraging seals.

The darkness of the deep ocean limits the vision of diving predators, except when prey emit bioluminescence. It is hypothesized that deep-diving seals rely on highly developed whiskers to locate their prey. However, if and how seals use their whiskers while foraging in natural conditions remains unknown. We used animal-borne tags to show that free-ranging elephant seals use their whiskers for hydrodynamic prey sensing. Small, cheek-mounted video loggers documented seals actively protracting their whiskers in front of their mouths with rhythmic whisker movement, like terrestrial mammals exploring their environment. Seals focused their sensing effort at deep foraging depths, performing prolonged whisker protraction to detect, pursue, and capture prey. Feeding-event recorders with light sensors demonstrated that bioluminescence contributed to only about 20% of overall foraging success, confirming that whiskers play the primary role in sensing prey. Accordingly, visual prey detection complemented and enhanced prey capture. The whiskers' role highlights an evolutionary alternative to echolocation for adapting to the extreme dark of the deep ocean environment, revealing how sensory abilities shape foraging niche segregation in deep-diving mammals. Mammals typically have mobile facial whiskers, and our study reveals the significant function of whiskers in the natural foraging behavior of a marine predator. We demonstrate the importance of field-based sensory studies incorporating multimodality to better understand how multiple sensory systems are complementary in shaping the foraging success of predators.

Individual variation in life-history timing: synchronous presence, asynchronous events and phenological compensation in a wild mammal.

Many animals and plants have species-typical annual cycles, but individuals vary in their timing of life-history events. Individual variation in fur replacement (moult) timing is poorly understood in mammals due to the challenge of repeated observations and longitudinal sampling. We examined factors that influence variation in moult duration and timing among elephant seals (Mirounga angustirostris). We quantified the onset and progression of fur loss in 1178 individuals. We found that an exceptionally rapid visible moult (7 days, the shortest of any mammals or birds), and a wide range of moult start dates (spanning 6-10× the event duration) facilitated high asynchrony across individuals (only 20% of individuals in the population moulting at the same time). Some of the variation was due to reproductive state, as reproductively mature females that skipped a breeding season moulted a week earlier than reproductive females. Moreover, individual variation in timing and duration within age-sex categories far outweighed (76-80%) variation among age-sex categories. Individuals arriving at the end of the moult season spent 50% less time on the beach, which allowed them to catch up in their annual cycles and reduce population-level variance during breeding. These findings underscore the importance of individual variation in annual cycles.

Selected and shared hematological responses to apnea in elite human free divers and northern elephant seals (Mirounga angustirostris).

Despite elite human free divers achieving incredible feats in competitive free diving, there has yet to be a study that compares consummate divers, (i.e. northern elephant seals) to highly conditioned free divers (i.e., elite competitive free-diving humans). Herein, we compare these two diving models and suggest that hematological traits detected in seals reflect species-specific specializations, while hematological traits shared between the two species are fundamental mammalian characteristics. Arterial blood samples were analyzed in elite human free divers (n = 14) during a single, maximal volitional apnea and in juvenile northern elephant seals (n = 3) during rest-associated apnea. Humans and elephant seals had comparable apnea durations (∼6.5 min) and end-apneic arterial Po2 [humans: 40.4 ± 3.0 mmHg (means ± SE); seals: 27.1 ± 5.9 mmHg; P = 0.2]. Despite similar increases in arterial Pco2 (humans: 33 ± 5%; seals: 16.3 ± 5%; P = 0.2), only humans experienced reductions in pH from baseline (humans: 7.45 ± 0.01; seals: 7.39 ± 0.02) to end apnea (humans: 7.37 ± 0.01; seals: 7.38 ± 0.02; P < 0.0001). Hemoglobin P50 was greater in humans compared to elephant seals (29.9 ± 1.5 and 28.7 ± 0.6 mmHg, respectively; P = 0.046). Elephant seals overall had higher carboxyhemoglobin (COHb) levels (5.9 ± 2.6%) compared to humans (0.8 ± 1.2%; P < 0.0001); however, following apnea, COHb was reduced in seals (baseline: 6.1 ± 0.3%; end apnea: 5.6 ± 0.3%) and was slightly elevated in humans (baseline: 0.7 ± 0.1%; end apnea: 0.9 ± 0.1%; P < 0.0002, both comparisons). Our data indicate that during static apnea, seals have reduced hemoglobin P50, greater pH buffering, and increased COHb levels. The differences in hemoglobin P50 are likely due to the differences in the physiological environment between the two species during apnea, whereas enhanced pH buffering and higher COHb may represent traits selected for in elephant seals.NEW & NOTEWORTHY This study uses similar methods and protocols in elite human free divers and northern elephant seals. Using highly conditioned divers (elite free-diving humans) and highly adapted divers (northern elephant seals), we explored which hematological traits are fundamentally mammalian and which may have been selected for. We found differences in P50, which may be due to different physiological environments between species, while elevated pH buffering and carbon monoxide levels might have been selected for in seals.

Physiological tipping points in the relationship between foraging success and lifetime fitness of a long-lived mammal.

Although anthropogenic change is often gradual, the impacts on animal populations may be precipitous if physiological processes create tipping points between energy gain, reproduction or survival. We use 25 years of behavioural, diet and demographic data from elephant seals to characterise their relationships with lifetime fitness. Survival and reproduction increased with mass gain during long foraging trips preceding the pupping seasons, and there was a threshold where individuals that gained an additional 4.8% of their body mass (26 kg, from 206 to 232 kg) increased lifetime reproductive success three-fold (from 1.8 to 4.9 pups). This was due to a two-fold increase in pupping probability (30% to 76%) and a 7% increase in reproductive lifespan (6.0 to 6.4 years). The sharp threshold between mass gain and reproduction may explain reproductive failure observed in many species and demonstrates how small, gradual reductions in prey from anthropogenic disturbance could have profound implications for animal populations.

Adrenal response to ACTH challenge alters thyroid and immune function and varies with body reserves in molting adult female northern elephant seals.

Intrinsic stressors associated with life-history stages may alter the responsiveness of the hypothalamic-pituitary-adrenal axis and responses to extrinsic stressors. We administered adrenocorticotropic hormone (ACTH) to 24 free-ranging adult female northern elephant seals (NESs) at two life-history stages: early and late in their molting period and measured a suite of endocrine, immune, and metabolite responses. Our objective was to evaluate the impact of extended, high-energy fasting on adrenal responsiveness. Animals were blood sampled every 30 min for 120 min post-ACTH injection, then blood was sampled 24 h later. In response to ACTH injection, cortisol levels increased 8- to 10-fold and remained highly elevated compared with baseline at 24 h. Aldosterone levels increased 6- to 9-fold before returning to baseline at 24 h. The magnitude of cortisol and aldosterone release were strongly associated, and both were greater after extended fasting. We observed an inverse relationship between fat mass and the magnitude of cortisol and aldosterone responses, suggesting that body reserves influenced adrenal responsiveness. Sustained elevation in cortisol was associated with alterations in thyroid hormones; both tT3 and tT4 concentrations were suppressed at 24 h, while rT3 increased. Immune cytokine IL-1ß was also suppressed after 24 h of cortisol elevation, and numerous acute and sustained impacts on substrate metabolism were evident. Our data suggest that female NESs are more sensitive to stress after the molt fast and that acute stress events can have important impacts on metabolism and immune function. These findings highlight the importance of considering life-history context when assessing the impacts of anthropogenic stressors on wildlife.

A surplus no more? Variation in krill availability impacts reproductive rates of Antarctic baleen whales.

The krill surplus hypothesis of unlimited prey resources available for Antarctic predators due to commercial whaling in the 20th century has remained largely untested since the 1970s. Rapid warming of the Western Antarctic Peninsula (WAP) over the past 50 years has resulted in decreased seasonal ice cover and a reduction of krill. The latter is being exacerbated by a commercial krill fishery in the region. Despite this, humpback whale populations have increased but may be at a threshold for growth based on these human-induced changes. Understanding how climate-mediated variation in prey availability influences humpback whale population dynamics is critical for focused management and conservation actions. Using an 8-year dataset (2013-2020), we show that inter-annual humpback whale pregnancy rates, as determined from skin-blubber biopsy samples (n = 616), are positively correlated with krill availability and fluctuations in ice cover in the previous year. Pregnancy rates showed significant inter-annual variability, between 29% and 86%. Our results indicate that krill availability is in fact limiting and affecting reproductive rates, in contrast to the krill surplus hypothesis. This suggests that this population of humpback whales may be at a threshold for population growth due to prey limitations. As a result, continued warming and increased fishing along the WAP, which continue to reduce krill stocks, will likely impact this humpback whale population and other krill predators in the region. Humpback whales are sentinel species of ecosystem health, and changes in pregnancy rates can provide quantifiable signals of the impact of environmental change at the population level. Our findings must be considered paramount in developing new and more restrictive conservation and management plans for the Antarctic marine ecosystem and minimizing the negative impacts of human activities in the region.

Field physiology in the aquatic realm: ecological energetics and diving behavior provide context for elucidating patterns and deviations.

Comparative physiology has developed a rich understanding of the physiological adaptations of organisms, from microbes to megafauna. Despite extreme differences in size and a diversity of habitats, general patterns are observed in their physiological adaptations. Yet, many organisms deviate from the general patterns, providing an opportunity to understand the importance of ecology in determining the evolution of unusual adaptations. Aquatic air-breathing vertebrates provide unique study systems in which the interplay between ecology, physiology and behavior is most evident. They must perform breath-hold dives to obtain food underwater, which imposes a physiological constraint on their foraging time as they must resurface to breathe. This separation of two critical resources has led researchers to investigate these organisms' physiological adaptations and trade-offs. Addressing such questions on large marine animals is best done in the field, given the difficulty of replicating the environment of these animals in the lab. This Review examines the long history of research on diving physiology and behavior. We show how innovative technology and the careful selection of research animals have provided a holistic understanding of diving mammals' physiology, behavior and ecology. We explore the role of the aerobic diving limit, body size, oxygen stores, prey distribution and metabolism. We then identify gaps in our knowledge and suggest areas for future research, pointing out how this research will help conserve these unique animals.

Deep dives and high tissue density increase mean dive costs in California sea lions (Zalophus californianus).

Diving is central to the foraging strategies of many marine mammals and seabirds. Still, the effect of dive depth on foraging cost remains elusive because energy expenditure is difficult to measure at fine temporal scales in wild animals. We used depth and acceleration data from eight lactating California sea lions (Zalophus californianus) to model body density and investigate the effect of dive depth and tissue density on rates of energy expenditure. We calculated body density in 5 s intervals from the rate of gliding descent. We modeled body density across depth in each dive, revealing high tissue densities and diving lung volumes (DLVs). DLV increased with dive depth in four individuals. We used the buoyancy calculated from dive-specific body-density models and drag calculated from swim speed to estimate metabolic power and cost of transport in 5 s intervals during descents and ascents. Deeper dives required greater mean power for round-trip vertical transit, especially in individuals with higher tissue density. These trends likely follow from increased mean swim speed and buoyant hinderance that increasingly outweighs buoyant aid in deeper dives. This suggests that deep diving is either a 'high-cost, high-reward' strategy or an energetically expensive option to access prey when prey in shallow waters are limited, and that poor body condition may increase the energetic costs of deep diving. These results add to our mechanistic understanding of how foraging strategy and body condition affect energy expenditure in wild breath-hold divers.

Feeding morphology and body size shape resource partitioning in an eared seal community.

Body size and feeding morphology influence how animals partition themselves within communities. We tested the relationships among sex, body size, skull morphology and foraging in sympatric otariids (eared seals) from the eastern North Pacific Ocean, the most diverse otariid community in the world. We recorded skull measurements and stable carbon (δ13C) and nitrogen (δ15N) isotope values (proxies for foraging) from museum specimens in four sympatric species: California sea lions (Zalophus californianus), Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus ursinus) and Guadalupe fur seals (Arctocephalus townsendi). Species and sexes had statistical differences in size, skull morphology and foraging significantly affecting the δ13C values. Sea lions had higher δ13C values than fur seals, and males of all species had higher values than females. The δ15N values were correlated with species and feeding morphology; individuals with stronger bite forces had higher δ15N values. We also found a significant community-wide correlation between skull length (indicator of body length), and foraging, with larger individuals having nearshore habitat preferences, and consuming higher trophic level prey than smaller individuals. Still, there was no consistent association between these traits at the intraspecific level, indicating that other factors might account for foraging variability.

Mercury Bioaccumulation and Cortisol Interact to Influence Endocrine and Immune Biomarkers in a Free-Ranging Marine Mammal.

Mercury bioaccumulation from deep-ocean prey and the extreme life history strategies of adult female northern elephant seals (Mirounga angustirostris) provide a unique system to assess the interactive effects of mercury and stress on animal health by quantifying blood biomarkers in relation to mercury (skeletal muscle and blood mercury) and cortisol concentrations. The thyroid hormone thyroxine (tT4) and the antibody immunoglobulin E (IgE) were associated with mercury and cortisol concentrations interactively, where the magnitude and direction of the association of each biomarker with mercury or cortisol changed depending on the concentration of the other factor. For example, when cortisol concentrations were lowest, tT4 was positively related to muscle mercury, whereas tT4 had a negative relationship with muscle mercury in seals that had the highest cortisol concentrations. Additionally, we observed that two thyroid hormones, triiodothyronine (tT3) and reverse triiodothyronine (rT3), were negatively (tT3) and positively (rT3) associated with mercury concentrations and cortisol in an additive manner. As an example, tT3 concentrations in late breeding seals at the median cortisol concentration decreased by 14% across the range of observed muscle mercury concentrations. We also observed that immunoglobulin M (IgM), the pro-inflammatory cytokine IL-6 (IL-6), and a reproductive hormone, estradiol, were negatively related to muscle mercury concentrations but were not related to cortisol. Specifically, estradiol concentrations in late molting seals decreased by 50% across the range of muscle mercury concentrations. These results indicate important physiological effects of mercury on free-ranging apex marine predators and interactions between mercury bioaccumulation and extrinsic stressors. Deleterious effects on animals' abilities to maintain homeostasis (thyroid hormones), fight off pathogens and disease (innate and adaptive immune system), and successfully reproduce (endocrine system) can have significant individual- and population-level consequences.

Managing the effects of multiple stressors on wildlife populations in their ecosystems: developing a cumulative risk approach.

Assessing cumulative effects of human activities on ecosystems is required by many jurisdictions, but current science cannot meet regulatory demands. Regulations define them as effect(s) of one human action combined with other actions. Here we argue for an approach that evaluates the cumulative risk of multiple stressors for protected wildlife populations within their ecosystems. Monitoring effects of each stressor is necessary but not sufficient to estimate how multiple stressors interact to affect wildlife populations. Examining the mechanistic pathways, from cellular to ecological, by which stressors affect individuals can help prioritize stressors and interpret how they interact. Our approach uses health indicators to accumulate the effects of stressors on individuals and to estimate changes in vital rates, driving population status. We advocate using methods well-established in human health and integrating them into ecosystem-based management to protect the health of commercially and culturally important wildlife populations and to protect against risk of extinction for threatened species. Our approach will improve abilities to conserve and manage ecosystems but will also demand significant increases in research and monitoring effort. We advocate for increased investment proportional to the economic scale of human activities in the Anthropocene and their pervasive effects on ecology and biodiversity.

Changes in apolipoprotein abundance dominate proteome responses to prolonged fasting in elephant seals.

Unlike many animals that reduce activity during fasting, northern elephant seals (NES) undergo prolonged fasting during energy-intensive life-history stages such as reproduction and molting, fueling fasting energy needs by mobilizing fat stores accrued during foraging. NES display several unique metabolic features such as high fasting metabolic rates, elevated blood lipid and high-density lipoprotein (HDL) cholesterol levels, efficient protein sparing and resistance to oxidative stress during fasting. However, the cellular mechanisms that regulate these adaptations are still not fully understood. To examine how metabolic coordination is achieved during prolonged fasting, we profiled changes in blubber, skeletal muscle and plasma proteomes of adult female NES over a 5 week fast associated with molting. We found that while blubber and muscle proteomes were remarkably stable over fasting, over 50 proteins changed in abundance in plasma, including those associated with lipid storage, mobilization, oxidation and transport. Apolipoproteins dominated the blubber, plasma and muscle proteome responses to fasting. APOA4, APOE and APOC3, which are associated with lipogenesis and triglyceride accumulation, decreased, while APOA1, APOA2 and APOM, which are associated with lipid mobilization and HDL function, increased over fasting. Our findings suggest that changes in apolipoprotein composition may underlie the maintenance of high HDL levels and, together with adipokines and hepatokines that facilitate lipid catabolism, may mediate the metabolic transitions between feeding and fasting in NES. Many of these proteins have not been previously studied in this species and provide intriguing hypotheses about metabolic regulation during prolonged fasting in mammals.

Effects of the use of synthetic astaxanthin in the feeding of Lophiosilurus alexandri, a neotropical siluriform fish.

Aiming to test the capacity of retention of carotenoids in tissues, Lophiosilurus alexandri juveniles were fed diets containing 0, 25, 50, 100, 200, and 400 mg/kg of synthetic astaxanthin for 62 days. The inclusion of astaxanthin did not result in significant differences in growth, weight gain, apparent feed conversion, and feed efficiency of the fish. Blood biochemistry and liver histology did not change with the different treatments. At the level of 100 mg/kg of inclusion, there were the highest levels of carotenoids in the blood, and muscle and the smallest difference between the muscle x integument ratio.

Emerging themes in Population Consequences of Disturbance models.

Assessing the non-lethal effects of disturbance from human activities is necessary for wildlife conservation and management. However, linking short-term responses to long-term impacts on individuals and populations is a significant hurdle for evaluating the risks of a proposed activity. The Population Consequences of Disturbance (PCoD) framework conceptually describes how disturbance can lead to changes in population dynamics, and its real-world application has led to a suite of quantitative models that can inform risk assessments. Here, we review PCoD models that forecast the possible consequences of a range of disturbance scenarios for marine mammals. In so doing, we identify common themes and highlight general principles to consider when assessing risk. We find that, when considered holistically, these models provide valuable insights into which contextual factors influence a population's degree of exposure and sensitivity to disturbance. We also discuss model assumptions and limitations, identify data gaps and suggest future research directions to enable PCoD models to better inform risk assessments and conservation and management decisions. The general principles explored can help wildlife managers and practitioners identify and prioritize the populations most vulnerable to disturbance and guide industry in planning activities that avoid or mitigate population-level effects.

Density-dependent effects on reproductive output in a capital breeding carnivore, the northern elephant seal (Mirounga angustirostris).

All organisms face resource limitations that will ultimately restrict population growth, but the controlling mechanisms vary across ecosystems, taxa, and reproductive strategies. Using four decades of data, we examine how variation in the environment and population density affect reproductive outcomes in a capital-breeding carnivore, the northern elephant seal (Mirounga angustirostris). This species provides a unique opportunity to examine the relative importance of resource acquisition and density-dependence on breeding success. Capital breeders accrue resources over large temporal and spatial scales for use during an abbreviated reproductive period. This strategy may have evolved, in part, to confer resilience to short-term environmental variability. We observed density-dependent effects on weaning mass, and maternal age (experience) was more important than oceanographic conditions or maternal mass in determining offspring weaning mass. Together these findings show that the mechanisms controlling reproductive output are conserved across terrestrial and marine systems and vary with population dynamics, an important consideration when assessing the effect of extrinsic changes, such as climate change, on a population.

Predicting the population consequences of acoustic disturbance, with application to an endangered gray whale population.

Acoustic disturbance is a growing conservation concern for wildlife populations because it can elicit physiological and behavioral responses that can have cascading impacts on population dynamics. State-dependent behavioral and life history models implemented via Stochastic Dynamic Programming (SDP) provide a natural framework for quantifying biologically meaningful population changes resulting from disturbance by linking environment, physiology, and metrics of fitness. We developed an SDP model using the endangered western gray whale (Eschrichtius robustus) as a case study because they experience acoustic disturbance on their summer foraging grounds. We modeled the behavior and physiological dynamics of pregnant females as they arrived on the feeding grounds and predicted the probability of female and offspring survival, with and without acoustic disturbance and in the presence/absence of high prey availability. Upon arrival in mid-May, pregnant females initially exhibited relatively random behavior before they transitioned to intensive feeding that resulted in continual fat mass gain until departure. This shift in behavior co-occurred with a change in spatial distribution; early in the season, whales were more equally distributed among foraging areas with moderate to high energy availability, whereas by mid-July whales transitioned to predominate use of the location that had the highest energy availability. Exclusion from energy-rich offshore areas led to reproductive failure and in extreme cases, mortality of adult females that had lasting impacts on population dynamics. Simulated disturbances in nearshore foraging areas had little to no impact on female survival or reproductive success at the population level. At the individual level, the impact of disturbance was unequally distributed across females of different lengths, both with respect to the number of times an individual was disturbed and the impact of disturbance on vital rates. Our results highlight the susceptibility of large capital breeders to reductions in prey availability, and indicate that who, where, and when individuals are disturbed are likely to be important considerations when assessing the impacts of acoustic activities. This model provides a framework to inform planned acoustic disturbances and assess the effectiveness of mitigation strategies for large capital breeders.

Changes in serum adipokines during natural extended fasts in female northern elephant seals.

Adipose tissue is essential to endotherms for thermoregulation and energy storage as well as functioning as an endocrine organ. Adipose derived hormones, or adipokines, regulate metabolism, energy expenditure, reproduction, and immune function in model systems but are less well studied in wildlife. Female northern elephant seals (NES) achieve high adiposity during foraging and then undergo natural fasts up to five weeks long during haul-outs associated with reproduction and molting, resulting in large changes in adipose reserves. We measured circulating levels of four adipokines: leptin, resistin, adiponectin, and kisspeptin-54, in 196 serum samples from female NES at the beginning and end of their breeding and molting fasts. We examined the relationships between these adipokines and life-history stage, adiposity, mass, cortisol, and an immune cytokine involved in the innate immune response interleukin 6 (IL-6). All four adipokines varied with life-history stage. Leptin concentrations were highest at the beginning of the breeding haul-out. Resistin concentrations were higher throughout the breeding haul-out compared to the molt haul-out. Adiponectin concentrations were highest at the beginning of both haul-outs. Kisspeptin-54 concentrations were highest at the end of the breeding haul-out. Leptin, resistin, and adiponectin were associated with measures of body condition, either adiposity, mass, or both. Resistin, adiponectin, and kisspeptin-54 were associated with circulating cortisol concentrations. Resistin was strongly associated with circulating IL-6, a multifunctional cytokine. Adiponectin was associated with glucose concentrations, suggesting a potential role in tissue-specific insulin sensitivity during life-history stages categorized by high adiposity. Increased cortisol concentrations late in lactation were associated with increased kisspeptin-54, suggesting a link to ovulation initiation in NES. This study suggests dramatic changes in circulating adipokines with life-history and body condition that may exert important regulatory roles in NES. The positive relationship between adiponectin and adiposity as well as the lack of a relationship between leptin and kisspeptin-54 differed from model systems. These differences from biomedical model systems suggest the potential for modifications of expression and function of adipose-derived hormones in species that undergo natural changes in adiposity as part of their life-history.

Propensity for Risk in Reproductive Strategy Affects Susceptibility to Anthropogenic Disturbance.

AbstractAnimals initiate, interrupt, or invest resources in reproduction in light of their physiology and the environment. The energetic risks entailed in an individual's reproductive strategy can influence the ability to cope with additional stressors, such as anthropogenic climate change and disturbance. To explore the trade-offs between internal state, external resource availability, and reproduction, we applied state-dependent life-history theory (SDLHT) to a dynamic energy budget (DEB) model for long-finned pilot whales (Globicephala melas). We investigated the reproductive strategies emerging from the interplay between fitness maximization and propensity to take energetic risks, as well as the resulting susceptibility of individual vital rates to disturbance. Without disturbance, facultative reproductive behavior from SDLHT and fixed rules in the DEB model led to comparable individual fitness. However, under disturbance, the reproductive strategies emerging from SDLHT increased vulnerability to energetic risks, resulting in lower fitness than fixed rules. These fragile strategies might therefore be unlikely to evolve in the first place. Heterogeneous resource availability favored more cautious (and thus more robust) strategies, particularly when knowledge of resource variation was accurate. Our results demonstrate that the assumptions regarding the dynamic trade-offs underlying an individual's decision-making can have important consequences for predicting the effects of anthropogenic stressors on wildlife populations.

Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies.

Understanding the environmental and behavioral factors that influence how organisms maintain energy balance can inform us about their potential resiliency to rapid environmental changes. Flexibility in maintaining energy balance is particularly important to long-lived, central-place foraging seabirds that are constrained when locating food for offspring in a dynamic ocean environment. To understand the role of environmental interactions, behavioral flexibility and morphological constraints on energy balance, we used doubly labeled water to measure the at-sea daily energy expenditure (DEE) of two sympatrically breeding seabirds, Campbell (Thalassarche impavida) and grey-headed (Thalassarchechrysostoma) albatrosses. We found that species and sexes had similar foraging costs, but DEE varied between years for both species and sexes during early chick rearing in two consecutive seasons. For both species, greater DEE was positively associated with larger proportional mass gain, lower mean wind speeds during water take-offs, greater proportions of strong tailwinds (>12 m s-1), and younger chick age. Greater proportional mass gains were marginally more costly in male albatrosses that already have higher wing loading. DEE was higher during flights with a greater proportion of strong headwinds for grey-headed albatrosses only. Poleward winds are forecasted to intensify over the next century, which may increase DEE for grey-headed albatrosses that heavily use this region during early chick rearing. Female Campbell albatrosses may be negatively affected by forecasted slackening winds at lower latitudes due to an expected greater reliance on less energy efficient sit-and-wait foraging strategies. Behavioral plasticity associated with environmental variation may influence future population responses to climate change of both species.