Convergence of marine megafauna movement patterns in coastal and open oceans.

The extent of increasing anthropogenic impacts on large marine vertebrates partly depends on the animals' movement patterns. Effective conservation requires identification of the key drivers of movement including intrinsic properties and extrinsic constraints associated with the dynamic nature of the environments the animals inhabit. However, the relative importance of intrinsic versus extrinsic factors remains elusive. We analyze a global dataset of ∼2.8 million locations from >2,600 tracked individuals across 50 marine vertebrates evolutionarily separated by millions of years and using different locomotion modes (fly, swim, walk/paddle). Strikingly, movement patterns show a remarkable convergence, being strongly conserved across species and independent of body length and mass, despite these traits ranging over 10 orders of magnitude among the species studied. This represents a fundamental difference between marine and terrestrial vertebrates not previously identified, likely linked to the reduced costs of locomotion in water. Movement patterns were primarily explained by the interaction between species-specific traits and the habitat(s) they move through, resulting in complex movement patterns when moving close to coasts compared with more predictable patterns when moving in open oceans. This distinct difference may be associated with greater complexity within coastal microhabitats, highlighting a critical role of preferred habitat in shaping marine vertebrate global movements. Efforts to develop understanding of the characteristics of vertebrate movement should consider the habitat(s) through which they move to identify how movement patterns will alter with forecasted severe ocean changes, such as reduced Arctic sea ice cover, sea level rise, and declining oxygen content.

The importance of sample size in marine megafauna tagging studies.

Telemetry is a key, widely used tool to understand marine megafauna distribution, habitat use, behavior, and physiology; however, a critical question remains: "How many animals should be tracked to acquire meaningful data sets?" This question has wide-ranging implications including considerations of statistical power, animal ethics, logistics, and cost. While power analyses can inform sample sizes needed for statistical significance, they require some initial data inputs that are often unavailable. To inform the planning of telemetry and biologging studies of marine megafauna where few or no data are available or where resources are limited, we reviewed the types of information that have been obtained in previously published studies using different sample sizes. We considered sample sizes from one to >100 individuals and synthesized empirical findings, detailing the information that can be gathered with increasing sample sizes. We complement this review with simulations, using real data, to show the impact of sample size when trying to address various research questions in movement ecology of marine megafauna. We also highlight the value of collaborative, synthetic studies to enhance sample sizes and broaden the range, scale, and scope of questions that can be answered.

Tracking apex marine predator movements in a dynamic ocean.

Pelagic marine predators face unprecedented challenges and uncertain futures. Overexploitation and climate variability impact the abundance and distribution of top predators in ocean ecosystems. Improved understanding of ecological patterns, evolutionary constraints and ecosystem function is critical for preventing extinctions, loss of biodiversity and disruption of ecosystem services. Recent advances in electronic tagging techniques have provided the capacity to observe the movements and long-distance migrations of animals in relation to ocean processes across a range of ecological scales. Tagging of Pacific Predators, a field programme of the Census of Marine Life, deployed 4,306 tags on 23 species in the North Pacific Ocean, resulting in a tracking data set of unprecedented scale and species diversity that covers 265,386 tracking days from 2000 to 2009. Here we report migration pathways, link ocean features to multispecies hotspots and illustrate niche partitioning within and among congener guilds. Our results indicate that the California Current large marine ecosystem and the North Pacific transition zone attract and retain a diverse assemblage of marine vertebrates. Within the California Current large marine ecosystem, several predator guilds seasonally undertake north-south migrations that may be driven by oceanic processes, species-specific thermal tolerances and shifts in prey distributions. We identify critical habitats across multinational boundaries and show that top predators exploit their environment in predictable ways, providing the foundation for spatial management of large marine ecosystems.

Foraging strategies of a generalist marine predator inhabiting a dynamic environment.

Intraspecific variability is increasingly recognized as an important component of foraging behavior that can have implications for both population and community dynamics. We used an individual-level approach to describe the foraging behavior of an abundant, generalist predator that inhabits a dynamic marine ecosystem, focusing specifically on the different foraging strategies used by individuals in the same demographic group. We collected data on movements and diving behavior of adult female California sea lions (Zalophus californianus) across multiple foraging trips to sea. Sea lions (n = 35) used one of three foraging strategies that primarily differed in their oceanic zone and dive depth: a shallow, epipelagic strategy, a mixed epipelagic/benthic strategy, and a deep-diving strategy. Individuals varied in their degree of fidelity to a given strategy, with 66 % of sea lions using only one strategy on all or most of their foraging trips across the two-month tracking period. All foraging strategies were present in each of the sampling years, but there were inter-annual differences in the population-level importance of each strategy that may reflect changes in prey availability. Deep-diving sea lions traveled shorter distances and spent a greater proportion of time at the rookery than sea lions using the other two strategies, which may have energetic and reproductive implications. These results highlight the importance of an individual-based approach in describing the foraging behavior of female California sea lions and understanding how they respond to the seasonal and annual changes in prey availability that characterize the California Current System.

Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion.

Despite global declines in the abundance of marine predators, knowledge of foraging ecology, necessary to predict the ecological consequences of large changes in marine predator abundance, remains enigmatic for many species. Given that populations suffering severe declines are of conservation concern, we examined the foraging ecology of southern sea lions (SSL) (Otaria flavescens)-one of the least studied otariids (fur seal and sea lions)-which have declined by over 90% at the Falkland Islands since the 1930s. Using a combination of biologging devices and stable isotope analysis of vibrissae, we redress major gaps in the knowledge of SSL ecology and quantify patterns of individual specialization. Specifically, we revealed two discrete foraging strategies, these being inshore (coastal) and offshore (outer Patagonian Shelf). The majority of adult female SSL (72% or n = 21 of 29 SSL) foraged offshore. Adult female SSL that foraged offshore travelled further (92 ± 20 vs. 10 ± 4 km) and dived deeper (75 ± 23 vs. 21 ± 8 m) when compared to those that foraged inshore. Stable isotope analysis revealed long-term fidelity (years) to these discrete foraging habitats. In addition, we found further specialization within the offshore group, with adult female SSL separated into two clusters on the basis of benthic or mixed (benthic and pelagic) dive behavior (benthic dive proportion was 76 ± 9 vs. 51 ± 8%, respectively). We suggest that foraging specialization in depleted populations such as SSL breeding at the Falkland Islands, are influenced by foraging site fidelity, and could be independent of intraspecific competition. Finally, the behavioral differences we describe are crucial to understanding population-level dynamics, impediments to population recovery, and threats to population persistence.

Deadly diving? Physiological and behavioural management of decompression stress in diving mammals.

Decompression sickness (DCS; 'the bends') is a disease associated with gas uptake at pressure. The basic pathology and cause are relatively well known to human divers. Breath-hold diving marine mammals were thought to be relatively immune to DCS owing to multiple anatomical, physiological and behavioural adaptations that reduce nitrogen gas (N(2)) loading during dives. However, recent observations have shown that gas bubbles may form and tissue injury may occur in marine mammals under certain circumstances. Gas kinetic models based on measured time-depth profiles further suggest the potential occurrence of high blood and tissue N(2) tensions. We review evidence for gas-bubble incidence in marine mammal tissues and discuss the theory behind gas loading and bubble formation. We suggest that diving mammals vary their physiological responses according to multiple stressors, and that the perspective on marine mammal diving physiology should change from simply minimizing N(2) loading to management of the N(2) load. This suggests several avenues for further study, ranging from the effects of gas bubbles at molecular, cellular and organ function levels, to comparative studies relating the presence/absence of gas bubbles to diving behaviour. Technological advances in imaging and remote instrumentation are likely to advance this field in coming years.

Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal.

Identifying individuals' foraging strategies is critical to understanding the ecology of a species, and can provide the means to predict possible ecological responses to environmental change. Our study combines stable isotope analysis and satellite telemetry to study the variability in individual foraging strategies of adult female southern elephant seals (Mirounga leonina). Our hypothesis is that female elephant seals from the Western Antarctica Peninsula (WAP) display individual specialization in their diets. We captured adult female elephant seals (n = 56, 2005-2009) at Livingston Island (Antarctica), and instrumented them with SMRU-CTD satellite tags. We collected blood, fur, and vibrissae samples for δ(13)C and δ(15)N analyses. The mean values for all vibrissae were -21.0 ± 0.7‰ for δ(13)C, and 10.4 ± 0.8‰, for δ(15)N. The individual variability of δ(13)C (60%) was more important than the within-individual variability (40%) in explaining the total variance observed in our data. For δ(15)N, the results showed the opposite trend, with the within-individual variability (64%) contributing more to the total variance than the individual variability (36%), likely associated with the effect that the fasting periods have on δ(15)N values. Most individuals were specialists, as inferred from the low intra-individual variability of δ(13)C values with respect to the population variability, with half the individuals utilizing 31% or less of their available niche. We found eight different foraging strategies for these animals. Female elephant seals from the WAP are a diverse group of predators with individuals utilizing only a small portion of the total available niche, with the consequent potential to expand their foraging habits to exploit other resources or environments in the Southern Ocean.

Parasitological examination for presence of hookworms (Uncinaria spp.) in northern elephant seals (Mirounga angustirostris) at Año Nuevo State Reserve, California (2012).

Northern elephant seals (Mirounga angustirostris Gill, 1866), inhabiting rookeries on the mainland of Año Nuevo State Reserve in central California, were investigated in 2012 for presence of hookworms (Uncinaria spp.). Material collected and examined for hookworms included: blubber (n = 15), stomach and intestines (n = 21) from dead pups; feces from the rectum of weaned pups (n = 23); sand containing apparent feces in areas of weaned pups (n = 28) and sand without apparent feces in areas of weaned pups (n = 54); milk from females (n =23) at 5 days and about 23 to 26 days postpartum; and placenta from one female. Evidence of hookworm presence was not detected in any of the samples examined. Possible reasons why hookworms were not found in northern elephant seals on the mainland of Año Nuevo State Reserve are discussed.

Variation in blubber cortisol levels in a recovering humpback whale population inhabiting a rapidly changing environment.

Glucocorticoids are regularly used as biomarkers of relative health for individuals and populations. Around the Western Antarctic Peninsula (WAP), baleen whales have and continue to experience threats, including commercial harvest, prey limitations and habitat change driven by rapid warming, and increased human presence via ecotourism. Here, we measured demographic variation and differences across the foraging season in blubber cortisol levels of humpback whales (Megaptera novaeangliae) over two years around the WAP. Cortisol concentrations were determined from 305 biopsy samples of unique individuals. We found no significant difference in the cortisol concentration between male and female whales. However, we observed significant differences across demographic groups of females and a significant decrease in the population across the feeding season. We also assessed whether COVID-19-related reductions in tourism in 2021 along the WAP correlated with lower cortisol levels across the population. The decline in vessel presence in 2021 was associated with a significant decrease in humpback whale blubber cortisol concentrations at the population level. Our findings provide critical contextual data on how these hormones vary naturally in a population over time, show direct associations between cortisol levels and human presence, and will enable comparisons among species experiencing different levels of human disturbance.

Condition and mass impact oxygen stores and dive duration in adult female northern elephant seals.

The range of foraging behaviors available to deep-diving, air-breathing marine vertebrates is constrained by their physiological capacity to breath-hold dive. We measured body oxygen stores (blood volume and muscle myoglobin) and diving behavior in adult female northern elephant seals, Mirounga angustirostris, to investigate age-related effects on diving performance. Blood volume averaged 74.4+/-17.0 liters in female elephant seals or 20.2+/-2.0% of body mass. Plasma volume averaged 32.2+/-7.8 liters or 8.7+/-0.7% of body mass. Absolute plasma volume and blood volume increased independently with mass and age. Hematocrit decreased weakly with mass but did not vary with age. Muscle myoglobin concentration, while higher than previously reported (7.4+/-0.7 g%), did not vary with mass or age. Pregnancy status did not influence blood volume. Mean dive duration, a proxy for physiological demand, increased as a function of how long seals had been at sea, followed by mass and hematocrit. Strong effects of female body mass (range, 218-600 kg) on dive duration, which were independent of oxygen stores, suggest that larger females had lower diving metabolic rates. A tendency for dives to exceed calculated aerobic limits occurred more frequently later in the at-sea migration. Our data suggest that individual physiological state variables and condition interact to determine breath-hold ability and that both should be considered in life-history studies of foraging behavior.

Measurements of foraging success in a highly pelagic marine predator, the northern elephant seal.

1. Identification of foraging behaviour and the ability to assess foraging success is critical to understanding individual and between-species variation in habitat use and foraging ecology. For pelagic predators, behaviour-dependent foraging metrics are commonly used to identify important foraging areas, yet few of these metrics have been validated. 2. Using the northern elephant seal as a model species, we validated the use of a behaviour-independent measure of foraging success (changes in drift rate) at the scale of the entire foraging migration, and then used this to assess a variety of common foraging metrics that are based on movement patterns and dive behaviour. Transit rate consistently provided the best estimate of daily foraging success, although the addition of other metrics provides insight into different foraging behaviours or strategies. 3. While positive changes in buoyancy occurred throughout most of the migrations, implying successful feeding across much of the north Pacific, the areas of most rapid changes in buoyancy occurred along a latitudinal band (40-50° N) corresponding to a dynamic hydrographic region including Subarctic Gyre and Transition Zone waters. 4. These results support the use of transit rate as an index of foraging success: a metric that is easily derived from tracking measurements on a wide range of marine species.

Diving depths and energy requirements of king penguins.

During 4- to 8-day periods at sea, half of 2595 dives of three king penguins were more than 50 meters and two dives exceeded 240 meters. The at-sea metabolic rate, estimated from the turnover of tritiated water, was 2.8 times the standard metabolic rate and requires about 2.5 kilograms of squid per day. Ten percent or less of the dives may result in prey capture.

The effects of water temperature on the energetic costs of juvenile and adult California sea lions (Zalophus californianus): the importance of skeletal muscle thermogenesis for thermal balance.

As highly mobile marine predators, many pinniped species routinely encounter a wide range of water temperatures during foraging and in association with seasonal, geographical and climatic changes. To determine how such variation in environmental temperature may impact energetic costs in otariids, we determined the thermal neutral zone of adult and juvenile California sea lions (Zalophus californianus) by measuring resting metabolic rate using open-flow respirometry. Five adult female (body mass range =82.2-107.2 kg) and four juvenile (body mass=26.2-36.5 kg) sea lions were examined over experimental water temperatures ranging from 0 to 20 degrees C (adults) or 5 to 20 degrees C (juveniles). The metabolic rate of adult sea lions averaged 6.4+/-0.64 ml O(2) kg(-1) min(-1) when resting within the thermal neutral zone. The lower critical temperature of adults was 6.4+/-2.2 degrees C, approximately 4 degrees C lower than sea surface temperatures routinely encountered off coastal California. In comparison, juvenile sea lions did not demonstrate thermal neutrality within the range of water temperatures examined. Resting metabolic rate of the younger animals, 6.3+/-0.53 ml O(2) kg(-1) min(-1), increased as water temperature approached 12 degrees C, and suggested a potential thermal limitation in the wild. To determine whether muscle thermogenesis during activity could mitigate this limitation, we measured the active metabolic rate of juveniles swimming at water temperature (T(water))=5, 12 and 20 degrees C. No significant difference (F=0.377, P=0.583) in swimming metabolic rate was found among water temperatures, suggesting that thermal disadvantages due to small body size in juvenile sea lions may be circumvented by recycling endogenous heat during locomotor activity.

Dive behaviour and foraging effort of female Cape fur seals Arctocephalus pusillus pusillus.

While marine top predators can play a critical role in ecosystem structure and dynamics through their effects on prey populations, how the predators function in this role is often not well understood. In the Benguela region of southern Africa, the Cape fur seal (Arctocephalus pusillus pusillus) population constitutes the largest marine top predator biomass, but little is known of its foraging ecology other than its diet and some preliminary dive records. Dive information was obtained from 32 adult females instrumented with dive recorders at the Kleinsee colony (29°34.17' S, 16°59.80' E) in South Africa during 2006-2008. Most dives were in the depth range of epipelagic prey species (less than 50 m deep) and at night, reflecting the reliance of Cape fur seals on small, vertically migrating, schooling prey. However, most females also performed benthic dives, and benthic diving was prevalent in some individuals. Benthic diving was significantly associated with the frequency with which females exceeded their aerobic dive limit. The greater putative costs of benthic diving highlight the potential detrimental effects to Cape fur seals of well-documented changes in the availability of epipelagic prey species in the Benguela.

High-energy, high-fat lifestyle challenges an Arctic apex predator, the polar bear.

Regional declines in polar bear (Ursus maritimus) populations have been attributed to changing sea ice conditions, but with limited information on the causative mechanisms. By simultaneously measuring field metabolic rates, daily activity patterns, body condition, and foraging success of polar bears moving on the spring sea ice, we found that high metabolic rates (1.6 times greater than previously assumed) coupled with low intake of fat-rich marine mammal prey resulted in an energy deficit for more than half of the bears examined. Activity and movement on the sea ice strongly influenced metabolic demands. Consequently, increases in mobility resulting from ongoing and forecasted declines in and fragmentation of sea ice are likely to increase energy demands and may be an important factor explaining observed declines in body condition and survival.

Effects of El Niño-driven changes in wind patterns on North Pacific albatrosses.

Changes to patterns of wind and ocean currents are tightly linked to climate change and have important implications for cost of travel and energy budgets in marine vertebrates. We evaluated how El Niño-Southern Oscillation (ENSO)-driven wind patterns affected breeding Laysan and black-footed albatross across a decade of study. Owing to latitudinal variation in wind patterns, wind speed differed between habitat used during incubation and brooding; during La Niña conditions, wind speeds were lower in incubating Laysan (though not black-footed) albatross habitat, but higher in habitats used by brooding albatrosses. Incubating Laysan albatrosses benefited from increased wind speeds during El Niño conditions, showing increased travel speeds and mass gained during foraging trips. However, brooding albatrosses did not benefit from stronger winds during La Niña conditions, instead experiencing stronger cumulative headwinds and a smaller proportion of trips in tailwinds. Increased travel costs during brooding may contribute to the lower reproductive success observed in La Niña conditions. Furthermore, benefits of stronger winds in incubating habitat may explain the higher reproductive success of Laysan albatross during El Niño conditions. Our findings highlight the importance of considering habitat accessibility and cost of travel when evaluating the impacts of climate-driven habitat change on marine predators.

Development of body oxygen stores in harbor seals: effects of age, mass, and body composition.

Harbor seal pups are highly precocial and can swim and dive at birth. Such behavioral maturity suggests that they may be born with mature body oxygen stores or that stores develop quickly during the nursing period. To test this hypothesis, we compared the blood and muscle oxygen stores of harbor seal pups, yearlings, and adults. We found that pups had smaller oxygen stores than adults (neonates 57%, weaned pups 75%, and yearlings 90% those of adults), largely because neonatal myoglobin concentrations were low (1.6+/-0.2 g% vs. 3.8+/-0.3 g% for adults) and changed little during the nursing period. In contrast, blood oxygen stores were relatively mature, with nursing pups having hematocrit (55%+/-0.2%), hemoglobin (21.7+/-0.4 g%), and blood volume (12.3+/-0.5 mL/kg) only slightly lower than the corresponding values for adults (57%+/-0.2%, 23.8+/-0.3 g %, and 15.0+/-0.5 mL/kg). Because neonatal pups had relatively high metabolic rates (11.0 mL O2/kg min), their calculated aerobic dive limit was less than 50% that of adults. These results suggest that harbor seals' early aquatic activity is primarily supported by rapid development of blood, with immature muscle oxygen stores and elevated use rates limiting aerobic diving ability.

Summing the strokes: energy economy in northern elephant seals during large-scale foraging migrations.

BACKGROUND: The energy requirements of free-ranging marine mammals are challenging to measure due to cryptic and far-ranging feeding habits, but are important to quantify given the potential impacts of high-level predators on ecosystems. Given their large body size and carnivorous lifestyle, we would predict that northern elephant seals (Mirounga angustirostris) have elevated field metabolic rates (FMRs) that require high prey intake rates, especially during pregnancy. Disturbance associated with climate change or human activity is predicted to further elevate energy requirements due to an increase in locomotor costs required to accommodate a reduction in prey or time available to forage. In this study, we determined the FMRs, total energy requirements, and energy budgets of adult, female northern elephant seals. We also examined the impact of increased locomotor costs on foraging success in this species. RESULTS: Body size, time spent at sea and reproductive status strongly influenced FMR. During the short foraging migration, FMR averaged 90.1 (SE = 1.7) kJ kg(-1)d(-1) - only 36 % greater than predicted basal metabolic rate. During the long migration, when seals were pregnant, FMRs averaged 69.4 (±3.0) kJ kg(-1)d(-1) - values approaching those predicted to be necessary to support basal metabolism in mammals of this size. Low FMRs in pregnant seals were driven by hypometabolism coupled with a positive feedback loop between improving body condition and reduced flipper stroking frequency. In contrast, three additional seals carrying large, non-streamlined instrumentation saw a four-fold increase in energy partitioned toward locomotion, resulting in elevated FMRs and only half the mass gain of normally-swimming study animals. CONCLUSIONS: These results highlight the importance of keeping locomotion costs low for successful foraging in this species. In preparation for lactation and two fasting periods with high demands on energy reserves, migrating elephant seals utilize an economical foraging strategy whereby energy savings from reduced locomotion costs are shuttled towards somatic growth and fetal gestation. Remarkably, the energy requirements of this species, particularly during pregnancy, are 70-80 % lower than expected for mammalian carnivores, approaching or even falling below values predicted to be necessary to support basal metabolism in mammals of this size.

Fast and fuel efficient? Optimal use of wind by flying albatrosses.

The influence of wind patterns on behaviour and effort of free-ranging male wandering albatrosses (Diomedea exulans) was studied with miniaturized external heart-rate recorders in conjunction with satellite transmitters and activity recorders. Heart rate was used as an instantaneous index of energy expenditure. When cruising with favourable tail or side winds, wandering albatrosses can achieve high flight speeds while expending little more energy than birds resting on land. In contrast, heart rate increases concomitantly with increasing head winds, and flight speeds decrease. Our results show that effort is greatest when albatrosses take off from or land on the water. On a larger scale, we show that in order for birds to have the highest probability of experiencing favourable winds, wandering albatrosses use predictable weather systems to engage in a stereotypical flight pattern of large looping tracks. When heading north, albatrosses fly in anticlockwise loops, and to the south, movements are in a clockwise direction. Thus, the capacity to integrate instantaneous eco-physiological measures with records of large-scale flight and wind patterns allows us to understand better the complex interplay between the evolution of morphological, physiological and behavioural adaptations of albatrosses in the windiest place on earth.

Amino acid composition of pinniped milk.

The total amino acid concentration and the amino acid pattern, i.e. the relative proportion of each amino acid (protein-bound plus free) to the total amino acids, in the milks of the Northern elephant seal, Antarctic fur seal, California sea lion, and Australian sea lion were determined. Total amino acid concentration was 10% (w/v) or greater and did not vary significantly among species. The most abundant amino acids in the milks of all species were glutamate, proline and leucine. Essential amino acids were 40%, branched-chain amino acids were 20%, and sulfur amino acids were 4% of the total milk amino acids in all species. There were differences among the pinnipeds in some of the individual amino acids; the milk of the Northern elephant seal was the most distinct among the pinnipeds with higher histidine, serine and cystine contents and a lower methionine content than that of other pinnipeds. There was little effect of stage of lactation on total amino acid concentration or amino acid pattern in pinniped milk. Comparison of milk from the four pinniped species with that of 14 other mammalian species suggests commonality in milk amino acid pattern despite the wide variation in total amino acid concentration among the species.