Fur seals do, but sea lions don't - cross taxa insights into exhalation during ascent from dives.

Management of gases during diving is not well understood across marine mammal species. Prior to diving, phocid (true) seals generally exhale, a behaviour thought to assist with the prevention of decompression sickness. Otariid seals (fur seals and sea lions) have a greater reliance on their lung oxygen stores, and inhale prior to diving. One otariid, the Antarctic fur seal (Arctocephalus gazella), then exhales during the final 50-85% of the return to the surface, which may prevent another gas management issue: shallow-water blackout. Here, we compare data collected from animal-attached tags (video cameras, hydrophones and conductivity sensors) deployed on a suite of otariid seal species to examine the ubiquity of ascent exhalations for this group. We find evidence for ascent exhalations across four fur seal species, but that such exhalations are absent for three sea lion species. Fur seals and sea lions are no longer genetically separated into distinct subfamilies, but are morphologically distinguished by the thick underfur layer of fur seals. Together with their smaller size and energetic dives, we suggest their air-filled fur might underlie the need to perform these exhalations, although whether to reduce buoyancy and ascent speed, for the avoidance of shallow-water blackout or to prevent other cardiovascular management issues in their diving remains unclear. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Physiological, morphological, and ecological tradeoffs influence vertical habitat use of deep-diving toothed-whales in the Bahamas.

Dive capacity among toothed whales (suborder: Odontoceti) has been shown to generally increase with body mass in a relationship closely linked to the allometric scaling of metabolic rates. However, two odontocete species tagged in this study, the Blainville's beaked whale Mesoplodon densirostris and the Cuvier's beaked whale Ziphius cavirostris, confounded expectations of a simple allometric relationship, with exceptionally long (mean: 46.1 min & 65.4 min) and deep dives (mean: 1129 m & 1179 m), and comparatively small body masses (med.: 842.9 kg & 1556.7 kg). These two species also exhibited exceptionally long recovery periods between successive deep dives, or inter-deep-dive intervals (M. densirostris: med. 62 min; Z. cavirostris: med. 68 min). We examined competing hypotheses to explain observed patterns of vertical habitat use based on body mass, oxygen binding protein concentrations, and inter-deep-dive intervals in an assemblage of five sympatric toothed whales species in the Bahamas. Hypotheses were evaluated using dive data from satellite tags attached to the two beaked whales (M. densirostris, n = 12; Z. cavirostris, n = 7), as well as melon-headed whales Peponocephala electra (n = 13), short-finned pilot whales Globicephala macrorhynchus (n = 15), and sperm whales Physeter macrocephalus (n = 27). Body mass and myoglobin concentration together explained only 36% of the variance in maximum dive durations. The inclusion of inter-deep-dive intervals, substantially improved model fits (R2 = 0.92). This finding supported a hypothesis that beaked whales extend foraging dives by exceeding aerobic dive limits, with the extension of inter-deep-dive intervals corresponding to metabolism of accumulated lactic acid. This inference points to intriguing tradeoffs between body size, access to prey in different depth strata, and time allocation within dive cycles. These tradeoffs and resulting differences in habitat use have important implications for spatial distribution patterns, and relative vulnerabilities to anthropogenic impacts.

Diving behaviour of Cuvier's beaked whales exposed to two types of military sonar.

Cuvier's beaked whales (Ziphius cavirostris) have stranded in association with mid-frequency active sonar (MFAS) use, and though the causative mechanism linking these events remains unclear, it is believed to be behaviourally mediated. To determine whether MFAS use was associated with behavioural changes in this species, satellite tags were used to record the diving and movements of 16 Cuvier's beaked whales for up to 88 days in a region of frequent MFAS training off the coast of Southern California. Tag data were combined with summarized records of concurrent bouts of high-power, surface-ship and mid-power, helicopter-deployed MFAS use, along with other potential covariates, in generalized additive mixed-effects models. Deep dives, shallow dives and surface intervals tended to become longer during MFAS use, with some variation associated with the total amount of overlapping MFAS during the behaviour. These changes in dives and surface intervals contributed to a longer interval between deep dives, a proxy for foraging disruption in this species. Most responses intensified with proximity and were more pronounced during mid-power than high-power MFAS use at comparable distances within approximately 50 km, despite the significantly lower source level of mid-power MFAS. However, distance-mediated responses to high-power MFAS, and increased deep dive intervals during mid-power MFAS, were evident up to approximately 100 km away.

Diving physiology of seabirds and marine mammals: Relevance, challenges and some solutions for field studies.

To fully understand how diving seabirds and marine mammals balance the potentially conflicting demands of holding their breath while living their lives underwater (and maintaining physiological homeostasis during exercise, feeding, growth, and reproduction), physiological studies must be conducted with animals in their natural environments. The purpose of this article is to review the importance of making physiological measurements on diving animals in field settings, while acknowledging the challenges and highlighting some solutions. The most extreme divers are great candidates for study, especially in a comparative and mechanistic context. However, physiological data are also required of a wide range of species for problems relating to other disciplines, in particular ecology and conservation biology. Physiological data help with understanding and predicting the outcomes of environmental change, and the direct impacts of anthropogenic activities. Methodological approaches that have facilitated the development of field-based diving physiology include the isolated diving hole protocol and the translocation paradigm, and while there are many techniques for remote observation, animal-borne biotelemetry, or "biologging", has been critical. We discuss issues related to the attachment of instruments, the retrieval of data and sensing of physiological variables, while also considering negative impacts of tagging. This is illustrated with examples from a variety of species, and an in-depth look at one of the best studied and most extreme divers, the emperor penguin (Aptenodytes forsteri). With a variety of approaches and high demand for data on the physiology of diving seabirds and marine mammals, the future of field studies is bright.

Characterizing a Foraging Hotspot for Short-Finned Pilot Whales and Blainville's Beaked Whales Located off the West Side of Hawai'i Island by Using Tagging and Oceanographic Data.

Satellite tagging data for short-finned pilot whales (Globicephala macrorhynchus) and Blainville's beaked whales (Mesoplodon densirostris) were used to identify core insular foraging regions off the Kona (west) Coast of Hawai'i Island. Ship-based active acoustic surveys and oceanographic model output were used in generalized additive models (GAMs) and mixed models to characterize the oceanography of these regions and to examine relationships between whale density and the environment. The regions of highest density for pilot whales and Blainville's beaked whales were located between the 1000 and 2500 m isobaths and the 250 and 2000 m isobaths, respectively. Both species were associated with slope waters, but given the topography of the area, the horizontal distribution of beaked whales was narrower and located in shallower waters than that of pilot whales. The key oceanographic parameters characterizing the foraging regions were bathymetry, temperature at depth, and a high density of midwater micronekton scattering at 70 kHz in 400-650 m depths that likely represent the island-associated deep mesopelagic boundary community and serve as prey for the prey of the whales. Thus, our results suggest that off the Kona Coast, and potentially around other main Hawaiian Islands, the deep mesopelagic boundary community is key to a food web that supports insular cetacean populations.

Age specific survival rates of Steller sea lions at rookeries with divergent population trends in the Russian Far East.

After a dramatic population decline, Steller sea lions have begun to recover throughout most of their range. However, Steller sea lions in the Western Aleutians and Commander Islands are continuing to decline. Comparing survival rates between regions with different population trends may provide insights into the factors driving the dynamics, but published data on vital rates have been extremely scarce, especially in regions where the populations are still declining. Fortunately, an unprecedented dataset of marked Steller sea lions at rookeries in the Russian Far East is available, allowing us to determine age and sex specific survival in sea lions up to 22 years old. We focused on survival rates in three areas in the Russian range with differing population trends: the Commander Islands (Medny Island rookery), Eastern Kamchatka (Kozlov Cape rookery) and the Kuril Islands (four rookeries). Survival rates differed between these three regions, though not necessarily as predicted by population trends. Pup survival was higher where the populations were declining (Medny Island) or not recovering (Kozlov Cape) than in all Kuril Island rookeries. The lowest adult (> 3 years old) female survival was found on Medny Island and this may be responsible for the continued population decline there. However, the highest adult survival was found at Kozlov Cape, not in the Kuril Islands where the population is increasing, so we suggest that differences in birth rates might be an important driver of these divergent population trends. High pup survival on the Commander Islands and Kamchatka Coast may be a consequence of less frequent (e.g. biennial) reproduction there, which may permit females that skip birth years to invest more in their offspring, leading to higher pup survival, but this hypothesis awaits measurement of birth rates in these areas.

Satellite tagging and biopsy sampling of killer whales at subantarctic Marion Island: effectiveness, immediate reactions and long-term responses.

Remote tissue biopsy sampling and satellite tagging are becoming widely used in large marine vertebrate studies because they allow the collection of a diverse suite of otherwise difficult-to-obtain data which are critical in understanding the ecology of these species and to their conservation and management. Researchers must carefully consider their methods not only from an animal welfare perspective, but also to ensure the scientific rigour and validity of their results. We report methods for shore-based, remote biopsy sampling and satellite tagging of killer whales Orcinus orca at Subantarctic Marion Island. The performance of these methods is critically assessed using 1) the attachment duration of low-impact minimally percutaneous satellite tags; 2) the immediate behavioural reactions of animals to biopsy sampling and satellite tagging; 3) the effect of researcher experience on biopsy sampling and satellite tagging; and 4) the mid- (1 month) and long- (24 month) term behavioural consequences. To study mid- and long-term behavioural changes we used multievent capture-recapture models that accommodate imperfect detection and individual heterogeneity. We made 72 biopsy sampling attempts (resulting in 32 tissue samples) and 37 satellite tagging attempts (deploying 19 tags). Biopsy sampling success rates were low (43%), but tagging rates were high with improved tag designs (86%). The improved tags remained attached for 26±14 days (mean ± SD). Individuals most often showed no reaction when attempts missed (66%) and a slight reaction-defined as a slight flinch, slight shake, short acceleration, or immediate dive-when hit (54%). Severe immediate reactions were never observed. Hit or miss and age-sex class were important predictors of the reaction, but the method (tag or biopsy) was unimportant. Multievent trap-dependence modelling revealed considerable variation in individual sighting patterns; however, there were no significant mid- or long-term changes following biopsy sampling or tagging.

First long-term behavioral records from Cuvier's beaked whales (Ziphius cavirostris) reveal record-breaking dives.

Cuvier's beaked whales (Ziphius cavirostris) are known as extreme divers, though behavioral data from this difficult-to-study species have been limited. They are also the species most often stranded in association with Mid-Frequency Active (MFA) sonar use, a relationship that remains poorly understood. We used satellite-linked tags to record the diving behavior and locations of eight Ziphius off the Southern California coast for periods up to three months. The effort resulted in 3732 hr of dive data with associated regional movements--the first dataset of its kind for any beaked whale--and included dives to 2992 m depth and lasting 137.5 min, both new mammalian dive records. Deep dives had a group mean depth of 1401 m (s.d. = 137.8, n = 1142) and duration of 67.4 min (s.d. = 6.9). The group mean time between deep dives was 102.3 min (s.d. = 30.8, n = 783). While the previously described stereotypic pattern of deep and shallow dives was apparent, there was considerable inter- and intra-individual variability in most parameters. There was significant diel behavioral variation, including increased time near the surface and decreased shallow diving at night. However, maximum depth and the proportion of time spent on deep dives (presumed foraging), varied little from day to night. Surprisingly, tagged whales were present within an MFA sonar training range for 38% of days locations were received, and though comprehensive records of sonar use during tag deployments were not available, we discuss the effects frequent acoustic disturbance may have had on the observed behaviors. These data better characterize the true behavioral range of this species, and suggest caution should be exercised when drawing conclusions about behavior using short-term datasets.

Acoustic tracking of sperm whales in the Gulf of Alaska using a two-element vertical array and tags.

Between 15 and 17 August 2010, a simple two-element vertical array was deployed off the continental slope of Southeast Alaska in 1200 m water depth. The array was attached to a vertical buoy line used to mark each end of a longline fishing set, at 300 m depth, close to the sound-speed minimum of the deep-water profile. The buoy line also served as a depredation decoy, attracting seven sperm whales to the area. One animal was tagged with both a LIMPET dive depth-transmitting satellite and bioacoustic "B-probe" tag. Both tag datasets were used as an independent check of various passive acoustic schemes for tracking the whale in depth and range, which exploited the elevation angles and relative arrival times of multiple ray paths recorded on the array. Analytical tracking formulas were viable up to 2 km range, but only numerical propagation models yielded accurate locations up to at least 35 km range at Beaufort sea state 3. Neither localization approach required knowledge of the local bottom bathymetry. The tracking system was successfully used to estimate the source level of an individual sperm whale's "clicks" and "creaks" and predict the maximum detection range of the signals as a function of sea state.

Trackline and point detection probabilities for acoustic surveys of Cuvier's and Blainville's beaked whales.

Acoustic survey methods can be used to estimate density and abundance using sounds produced by cetaceans and detected using hydrophones if the probability of detection can be estimated. For passive acoustic surveys, probability of detection at zero horizontal distance from a sensor, commonly called g(0), depends on the temporal patterns of vocalizations. Methods to estimate g(0) are developed based on the assumption that a beaked whale will be detected if it is producing regular echolocation clicks directly under or above a hydrophone. Data from acoustic recording tags placed on two species of beaked whales (Cuvier's beaked whale-Ziphius cavirostris and Blainville's beaked whale-Mesoplodon densirostris) are used to directly estimate the percentage of time they produce echolocation clicks. A model of vocal behavior for these species as a function of their diving behavior is applied to other types of dive data (from time-depth recorders and time-depth-transmitting satellite tags) to indirectly determine g(0) in other locations for low ambient noise conditions. Estimates of g(0) for a single instant in time are 0.28 [standard deviation (s.d.) = 0.05] for Cuvier's beaked whale and 0.19 (s.d. = 0.01) for Blainville's beaked whale.

The effects of experimentally induced hyperthyroidism on the diving physiology of harbor seals (Phoca vitulina).

Many phocid seals are expert divers that remain submerged longer than expected based on estimates of oxygen storage and utilization. This discrepancy is most likely due to an overestimation of diving metabolic rate. During diving, a selective redistribution of blood flow occurs, which may result in reduced metabolism in the hypoperfused tissues and a possible decline in whole-body metabolism to below the resting level (hypometabolism). Thyroid hormones are crucial in regulation of energy metabolism in vertebrates and therefore their control might be an important part of achieving a hypometabolic state during diving. To investigate the effect of thyroid hormones on diving physiology of phocid seals, we measured oxygen consumption, heart rate, and post-dive lactate concentrations in five harbor seals (Phoca vitulina) conducting 5 min dives on command, in both euthyroid and experimentally induced hyperthyroid states. Oxygen consumption during diving was significantly reduced (by 25%) in both euthyroid and hyperthyroid states, confirming that metabolic rate during diving falls below resting levels. Hyperthyroidism increased oxygen consumption (by 7-8%) when resting in water and during diving, compared with the euthyroid state, illustrating the marked effect of thyroid hormones on metabolic rate. Consequently, post-dive lactate concentrations were significantly increased in the hyperthyroid state, suggesting that the greater oxygen consumption rates forced seals to make increased use of anaerobic metabolic pathways. During diving, hyperthyroid seals also exhibited a more profound decline in heart rate than seals in the euthyroid state, indicating that these seals were pushed toward their aerobic limit and required a more pronounced cardiovascular response. Our results demonstrate the powerful role of thyroid hormones in metabolic regulation and support the hypothesis that thyroid hormones play a role in modulating the at-sea metabolism of phocid seals.

Development of the aerobic dive limit and muscular efficiency in northern fur seals (Callorhinus ursinus).

Northern fur seal (Callorhinus ursinus; NFS) populations have been declining, perhaps due to limited foraging ability of pups. Because a marine mammal's proficiency at exploiting underwater prey resources is based on the ability to store large amounts of oxygen (O(2)) and to utilize these reserves efficiently, this study was designed to determine if NFS pups had lower blood, muscle, and total body O(2) stores than adults. Pups (<1-month old) had a calculated aerobic dive limit only ~40% of adult females due to lower blood and, to a much greater extent, muscle O(2) stores. Development of the Pectoralis (Pec) and Longissimus dorsi (LD) skeletal muscles was further examined by determining their myosin heavy chain (MHC) composition and enzyme activities. In all animals, the slow MHC I and fast-twitch IIA proteins typical of oxidative fiber types were dominant, but adult muscles contained more (Pec ~50%; LD ~250% higher) fast-twitch MHC IID/X protein characteristic of glycolytic muscle fibers, than pup muscles. This suggests that adults have greater ability to generate muscle power rapidly and/or under anaerobic conditions. Pup muscles also had lower aerobic and anaerobic ATP production potential, as indicated by lower metabolically scaled citrate synthase, ß-hydroxyacyl CoA dehydrogenase, and lactate dehydrogenase activities (all P values ≤0.001). In combination, these findings indicate that pups are biochemically and physiologically limited in their diving capabilities relative to adults. This may contribute to lower NFS first year survival.

Differentiating between Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus) scats through analysis of faecal DNA.

We describe a method to determine the species of pinniped from faeces collected from sympatric Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus) rookeries using newly developed species-specific primers that amplify a 667-669-base pair segment from the mitochondrial DNA (mtDNA) cytochrome B (cytB) gene region. The primers yielded the correct species in 100% of tissue samples from 10 known animals and 100% of faecal samples from 13 known animals. Species could be identified unequivocally for 87.7% of faecal samples from 122 unknown individuals. The ability to differentiate between scats of sympatrically breeding Steller sea lions and northern fur seals will contribute to the range-wide knowledge of the foraging strategies of both species as well as allow researchers to examine the niche partitioning and potential resource competition between the two predators.

Hematology of free-ranging, lactating northern fur seals, Callorhinus ursinus.

Thirteen standard hematology values were determined for a healthy and growing population of free-ranging, lactating northern fur seals (Callorhinus ursinus) from Lovushki Island in the Kuril Islands of far-east Russia. Results are presented from 24 females sampled between June and August during the 3-yr period of 2006-08. Hematologic values have been made available for future comparisons with the declining population of northern fur seals on the Pribilof Islands, Alaska, and are compared with published values for other otariid species.

Three-dimensional resting behaviour of northern elephant seals: drifting like a falling leaf.

During their long migrations through the Pacific, northern elephant seals, Mirounga angustirostris, never haul out on land and they rarely spend more than a few minutes at a time at the surface. They are almost constantly making repetitive, deep dives, raising the question of when do they rest? One type of dive, the drift dive, characterized by a time-depth profile with a phase of lower than average descent speed is believed to be a resting dive. To examine the behaviour of seals during drift dives, we measured body position and three-dimensional diving paths of six juvenile seals. We found that seals rolled over and sank on their backs during the drift phase, wobbling periodically so that they resembled a falling leaf. This enabled seals to drastically slow their descent rate, possibly so that negatively buoyant seals can rest without ending up in the abyss. This reduces the work required to return to the surface to breath, and allows them time to rest, process food or possibly sleep during the descent phase of these dives where they are probably less susceptible to predation.

Validation of the use of doubly labeled water for estimating metabolic rate in the green turtle (Chelonia mydas L.): a word of caution.

Marine turtles often have extremely high water turnover accompanied by a low field metabolic rate (FMR), a combination that can contraindicate the use of doubly labelled water (DLW). Therefore, we conducted a validation study to assess the suitability of the DLW technique for determining FMR of marine turtles. Six green turtles (22.42+/-3.13 kg) were injected with DLW and placed in a tank of seawater with a respirometer for continuous monitoring of oxygen consumption (MR) over a 5-day period. Trials were conducted for turtles in both fed and fasted states. Respiratory exchange ratio (RER) was determined in a dry respirometer and used to calculate energy expenditure. For fed and fasted turtles, total body water (TBW) was 66.67+/-3.37% and 58.70+/-7.63% of body mass, and water flux rates were 9.57+/-1.33% and 6.14+/-0.65% TBW day(-1), respectively. Water turnover in fasted turtles was 36% lower than that of fed turtles but MR (from oxygen consumption) of fasted turtles (13.77+/-1.49 kJ kg(-1) day(-1)) was 52% lower than in fed turtles (28.66+/-5.31 kJ kg(-1) day(-1)). Deuterium to oxygen-18 turnover rate (k(d):k(o)) ratios averaged 0.91+/-0.02 for fed turtles and 1.07+/-0.16 for fasted turtles. Fed turtles had a mean group difference of 8% and a mean individual difference of 53% between DLW and respirometry. The DLW method gave negative MR values in fasted turtles and could not be compared with respirometry data. Researchers should use caution when applying the DLW method in marine reptiles, especially when high water flux causes >90% of the labeled oxygen turnover to be due to water exchange.

A novel method for identifying behavioural changes in animal movement data.

A goal of animal movement analysis is to reveal behavioural mechanisms by which organisms utilize complex and variable environments. Statistical analysis of movement data is complicated by the fact that the data are multidimensional, autocorrelated and often marked by error and irregular measurement intervals or gappiness. Furthermore, movement data reflect behaviours that are themselves heterogeneous. Here, we model movement data as a subsampling of a continuous stochastic processes, and introduce the behavioural change point analysis (BCPA), a likelihood-based method that allows for the identification of significant structural changes. The BCPA is robust to gappiness and measurement error, computationally efficient, easy to implement and reveals structure that is otherwise difficult to discern. We apply the analysis to a GPS movement track of a northern fur seal (Callorhinus ursinus), revealing an unexpectedly complex diurnal behavioural profile, and demonstrate its robustness to the greater errors associated with the ARGOS tracking system. By informing empirical interpretation of movement data, we suggest that the BCPA can eventually motivate the development of mechanistic behavioural models.

Biotelemetry: a mechanistic approach to ecology.

Remote measurement of the physiology, behaviour and energetic status of free-living animals is made possible by a variety of techniques that we refer to collectively as 'biotelemetry'. This set of tools ranges from transmitters that send their signals to receivers up to a few kilometers away to those that send data to orbiting satellites and, more frequently, to devices that log data. They enable researchers to document, for long uninterrupted periods, how undisturbed organisms interact with each other and their environment in real time. In spite of advances enabling the monitoring of many physiological and behavioural variables across a range of taxa of various sizes, these devices have yet to be embraced widely by the ecological community. Our review suggests that this technology has immense potential for research in basic and applied animal ecology. Efforts to incorporate biotelemetry into broader ecological research programs should yield novel information that has been challenging to collect historically from free-ranging animals in their natural environments. Examples of research that would benefit from biotelemetry include the assessment of animal responses to different anthropogenic perturbations and the development of life-time energy budgets.

Allometric cascade: a model for resolving body mass effects on metabolism.

Expanding upon a preliminary communication (Nature 417 (2002) 166), we here further develop a "multiple-causes model" of allometry, where the exponent b is the sum of the influences of multiple contributors to control. The relative strength of each contributor, with its own characteristic value of b(i), is determined by c(i), the control contribution or control coefficient. A more realistic equation for the scaling of metabolism with body size thus can be written as BMR=MR(0)Sigmac(i)(M/M(0))(bi), where MR(0) is the "characteristic metabolic rate" of an animal with a "characteristic body mass", M(0). With M(0) of 1 unit mass (usually kg), MR(0) takes the place of the value a, found in the standard scaling equation, b(i) is the scaling exponent of the process i, and c(i) is its control contribution to overall flux, or the control coefficient of the process i. One can think of this as an allometric cascade, with the b exponent for overall energy metabolism being determined by the b(i) and c(i) values for key steps in the complex pathways of energy demand and energy supply. Key intrinsic factors (such as neural and endocrine processes) or ecological extrinsic factors are considered to act through this system in affecting allometric scaling of energy turnover. Applying this model to maximum vs. BMR data for the first time explains the differing scaling behaviour of these two biological states in mammals, both in the absence and presence of intrinsic regulators such as thyroid hormones (for BMR) and catecholamines (for maximum metabolic rate).