The role of glucocorticoids in naturally fasting grey seal (Halichoerus grypus) pups: dexamethasone stimulates mass loss and protein utilisation, but not departure from the colony.

Seals must manage their energy reserves carefully while they fast on land to ensure that they go to sea with sufficient fuel to sustain them until they find food. Glucocorticoids (GCs) have been implicated in the control of fuel metabolism and termination of fasting in pinnipeds. Here we tested the hypothesis that dexamethasone, an artificial GC, increases fat and protein catabolism, and induces departure from the breeding colony in wild, fasting grey seal pups. A single intramuscular dose of dexamethasone completely suppressed cortisol production for 24-72 h, demonstrating activation of GC receptors. In experiment 1, we compared the effects of a single dose of dexamethasone or saline administered 10 days after weaning on fasting mass and body composition changes, cortisol, blood urea nitrogen (BUN) and glucose levels, and timing of departure from the colony. In experiment 2, we investigated the effects of dexamethasone on short-term (5 days) changes in mass loss, body composition and BUN levels. In experiment 1, dexamethasone induced a short-lived increase in mass loss, but there was no difference in timing of departure between dexamethasone- and saline-treated pups (N=10). In experiment 2, dexamethasone increased protein and water loss and prevented a decrease in BUN levels (N=11). Our data suggest changes in cortisol contribute to regulation of protein catabolism in fasting seal pups, irrespective of the sex of the animal, but do not terminate fasting. By affecting the rate of protein depletion, lasting changes in cortisol levels could influence the amount of time seal pups have to find food, and thus may have important consequences for their survival.

Effects of age and body mass on development of diving capabilities of gray seal pups: costs and benefits of the postweaning fast.

Development of adequate diving capabilities is crucial for survival of seal pups and may depend on age and body size. We tracked the diving behavior of 20 gray seal pups during their first 3 mo at sea using satellite relay data loggers. We employed quantile analysis to track upper limits of dive duration and percentage time spent diving, and lower limits of surface intervals. When pups first left the breeding colony, extreme (ninety-fifth percentile) dive duration and percentage time spent diving were positively correlated with age, but not mass, at departure. Extreme dive durations and percentage time spent diving peaked at [Formula: see text] d of age at values comparable with those of adults, but were not sustained. Greater peaks in extreme percentage time spent diving occurred in pups that had higher initial values, were older at their peak, and were heavier at departure. Pups that were smaller and less capable divers when they left the colony improved extreme dive durations and percentage time spent diving more rapidly, once they were at sea. Minimum survival time correlated positively with departure mass. Pups that were heavier at weaning thus benefitted from being both larger and older at departure, but smaller pups faced a trade-off. While age at departure had a positive effect on early dive performance, departure mass impacted on peak percentage time spent diving and longer-term survival. We speculate that once small pups have attained a minimum degree of physiological development to support diving, they would benefit by leaving the colony when younger but larger to maximize limited fuel reserves, rather than undergoing further maturation on land away from potential food resources, because poor divers may be able to "catch up" once at sea.

Southern Ocean frontal structure and sea-ice formation rates revealed by elephant seals.

Polar regions are particularly sensitive to climate change, with the potential for significant feedbacks between ocean circulation, sea ice, and the ocean carbon cycle. However, the difficulty in obtaining in situ data means that our ability to detect and interpret change is very limited, especially in the Southern Ocean, where the ocean beneath the sea ice remains almost entirely unobserved and the rate of sea-ice formation is poorly known. Here, we show that southern elephant seals (Mirounga leonina) equipped with oceanographic sensors can measure ocean structure and water mass changes in regions and seasons rarely observed with traditional oceanographic platforms. In particular, seals provided a 30-fold increase in hydrographic profiles from the sea-ice zone, allowing the major fronts to be mapped south of 60 degrees S and sea-ice formation rates to be inferred from changes in upper ocean salinity. Sea-ice production rates peaked in early winter (April-May) during the rapid northward expansion of the pack ice and declined by a factor of 2 to 3 between May and August, in agreement with a three-dimensional coupled ocean-sea-ice model. By measuring the high-latitude ocean during winter, elephant seals fill a "blind spot" in our sampling coverage, enabling the establishment of a truly global ocean-observing system.

Variations in behavior and condition of a Southern Ocean top predator in relation to in situ oceanographic conditions.

Responses by marine top predators to environmental variability have previously been almost impossible to observe directly. By using animal-mounted instruments simultaneously recording movements, diving behavior, and in situ oceanographic properties, we studied the behavioral and physiological responses of southern elephant seals to spatial environmental variability throughout their circumpolar range. Improved body condition of seals in the Atlantic sector was associated with Circumpolar Deep Water upwelling regions within the Antarctic Circumpolar Current, whereas High-Salinity Shelf Waters or temperature/salinity gradients under winter pack ice were important in the Indian and Pacific sectors. Energetic consequences of these variations could help explain recently observed population trends, showing the usefulness of this approach in examining the sensitivity of top predators to global and regional-scale climate variability.

Unsteady-state gas exchange and storage in diving marine mammals: the harbor porpoise and gray seal.

Breath-by-breath measurements of end-tidal O(2) and CO(2) concentrations in harbor porpoise reveal that the respiratory gas exchange ratio (R(R); CO(2) output/O(2) uptake) of the first lung ventilation in a breathing bout after a prolonged breath-hold is always well below the animal's metabolic respiratory quotient (RQ) of 0.85. Thus the longest apneic pauses are always followed by an initial breath having a very low R(R) (0.6-0.7), which thereafter increases with each subsequent breath to values in excess of 1.2. Although the O(2) stores of the body are fully readjusted after the first three to four breaths following a prolonged apneic pause, a further three to four ventilations are always needed, not to load more O(2) but to eliminate built-up levels of CO(2). The slower readjustment of CO(2) stores relates to their greater magnitude and to the fact that they must be mobilized from comparatively large and chemically complex HCO/CO(2) stores that are built up in the blood and tissues during the breath-hold. These data, and similar measurements on gray seals (12), indicate that it is the readjustment of metabolic RQ and not O(2) stores per se that governs the amount of time an animal must spend ventilating at the surface after a dive.

Diurnal and seasonal variations in the duration and depth of the longest dives in southern elephant seals (Mirounga leonina): possible physiological and behavioural constraints.

This study seeks to understand how the physiological constraints of diving may change on a daily and seasonal basis. Dive data were obtained from southern elephant seals (Mirounga leonina) from South Georgia using satellite relay data loggers. We analysed the longest (95th percentile) dive durations as proxies for physiological dive limits. A strong, significant relationship existed between the duration of these dives and the time of day and week of year in which they were performed. The depth of the deepest dives also showed a significant, but far less consistent, relationship with local time of day and season. Changes in the duration of the longest dives occurred irrespective of their depth. Dives were longest in the morning (04:00-12:00 h) and shortest in the evening (16:00-00:00 h). The size of the fluctuation varied among animals from 4.0 to 20.0 min. The daily pattern in dive depth was phase-shifted in relation to the diurnal rhythm in dive duration. Dives were deeper at midday and shallower around midnight. Greater daily changes in duration occurred in seals feeding in the open ocean than in those foraging on the continental shelf. The seasonal peak in the duration of the longest dives coincided with austral midwinter. The size of the increase in dive duration from autumn/spring to winter ranged from 11.5 to 30.0 min. Changes in depth of the longest dives were not consistently associated with particular times of year. The substantial diurnal and seasonal fluctuations in maximum dive duration may be a result of changes in the physiological capacity to remain submerged, in addition to temporal changes in the ecological constraints on dive behaviour. We speculate about the role of melatonin as a hormonal mediator of diving capability.

Gas exchange and heart rate in the harbour porpoise, Phocoena phocoena.

The respiratory physiology, heart rates and metabolic rates of two captive juvenile male harbour porpoises (both 28 kg) were measured using a rapid-response respiratory gas analysis system in the laboratory. Breath-hold durations in the laboratory (12 +/- 0.3 s, mean +/- SEM) were shorter than field observations, although a few breath-holds of over 40 s were recorded. The mean percentage time spent submerged was 89 +/- 0.4%. Relative to similarly-sized terrestrial mammals, the respiratory frequency was low (4.9 +/- 0.19 breaths.min-1) but with high tidal volumes (1.1 +/- 0.011), enabling a comparatively high minute rate of gas exchange. Oxygen consumption under these experimental conditions (247 +/- 13.8 ml O2.min-1) was 1.9-fold higher than predicted by standard scaling relations. These data together with an estimate of the total oxygen stores predicted an aerobic dive limit of 5.4 min. The peak end-tidal O2 values were related to the length of the previous breath-hold, demonstrating the increased oxygen uptake from the lung for the longer dives. Blood oxygen capacity was 23.5 +/- 1.0 ml.100 ml-1, and the oxygen affinity was high, enabling rapid oxygen loading during ventilation.

The metabolic characteristics of the locomotory muscles of grey seals (Halichoerus grypus), harbour seals (Phoca vitulina) and Antarctic fur seals (Arctocephalus gazella).

It is not known precisely how marine mammals are able to maintain muscle function during active swimming in breath-hold dives, when ventilation stops and heart rate falls. Examination of muscle biochemistry and histochemistry can provide information on the relative importance of different metabolic pathways, the contractile potential of the muscle fibres, the oxygen storage capacity of the muscle and the capillary distribution in these animals. In this study, samples of locomotory muscle were taken from wild grey seals (Halichoerus grypus), harbour seals (Phoca vitulina) and Antarctic fur seals (Arctocephalus gazella); Wistar rat muscle was analysed for comparative purposes. Activities of citrate synthase and beta-hydroxyacyl CoA dehydrogenase were higher in the harbour seal muscle than in the grey seal muscle, suggesting that harbour seals have a greater aerobic capacity. Both phocid muscles had a greater reliance on fatty acid oxidation than the fur seal or rat muscles. The myoglobin data demonstrate that the grey seals have the highest oxygen storage capacity of the three pinniped species, which correlates with their greater diving ability. Myoglobin levels were higher in all three pinniped species than in the Wistar rat. The fibre type compositions suggest that the muscles from the fur seals have higher glycolytic capacities than those of the phocid seals [fur seal pectoralis, 7% slow-twitch oxidative fibres (SO), 25% fast-twitch oxidative glycolytic fibres (FOG), 68% fast-twitch glycolytic fibres (FG); grey seal 57% SO, 5% FOG, 38% FG; area per cents]. However, the pectoralis muscle of the fur seal, although the most glycolytic of the pinniped muscles studied, has the highest capillary density, which indicates a high capacity for fuel distribution. These results show that, while pinniped muscle has an increased oxygen storage potential compared with the muscle of a typical terrestrial mammal, there are no distinct adaptations for diving in the enzyme pathways or fibre type distributions of the pinniped muscle. However, the muscle characteristics of each species can be related to its diving behaviour and foraging strategy.

Gas exchange of captive freely diving grey seals (Halichoerus grypus).

When at sea, phocids dive for long periods and spend a high percentage of their time submerged. This behaviour requires some combination of an increased oxygen storage capacity, rapid oxygen loading at the surface and reduced oxygen utilisation when submerged. To assess these adaptations, breath-by-breath ventilation was studied in four adult grey seals (two male, two female, 160-250 kg), freely diving in a large outdoor tank where surface access was restricted to one breathing hole. The dive patterns obtained were similar to those recorded from freely diving wild grey seals. Respiratory frequency during the surface periods was 40% higher than that estimated from allometric relationships (19.4 +/- 0.7 breaths min-1), and tidal volume (6.3 +/- 1.21) was approximately five times higher than that estimated from allometric relationships. These adaptations produce a high minute volume and enable gas exchange to occur at the surface. Mean oxygen consumption rate (VO2, measured for a dive+surface cycle) decreased with increasing dive duration. The aerobic dive limit was estimated as 9.6 min for a 150 kg grey seal (using the overall average VO2 of 5.2 ml O2 min-1 kg-1), which is consistent with results from freely diving wild grey seals (only 6% of dives exceeded 10 min). End-tidal oxygen values varied during a surface period, following a U-shaped curve, which suggests that there is limited oxygen uptake from the lung and/or blood oxygen stores during dives. This result was unexpected and indicates that these seals are utilising substantial physiological responses to conserve oxygen, even during shallow voluntary diving.

Cardiac responses of grey seals during diving at sea.

Heart rate, swimming speed and diving depth data were collected from free-ranging grey seals, Halichoerus grypus, as they foraged and travelled in the sea around the Hebrides Islands off western Scotland. Information was collected on a tracking yacht using a combination of sonic and radio telemetry. Diving heart rate declined as a function of dive duration. In long dives, grey seals employed extreme bradycardia, with heart rates falling to 4 beats min-1 for extended periods, despite the animal being free to breath at will. This extreme dive response is part of the normal foraging behaviour. Seals spent 89% of the time submerged during bouts of long dives; swimming was restricted to ascent and descent. Dive durations exceeded estimated aerobic dive limit, even assuming resting metabolic rates. These results indicate that behavioural, and possibly cellular, energy-sparing mechanisms play an important role in diving behaviour of grey seals. This has implications not only for studies of mammalian energetics but also for our understanding of the foraging tactics and prey selection of marine mammals. If some seals are using energy-sparing mechanisms to reduce metabolic costs while at depth, they may be forced to wait for and ambush prey rather than to search for and chase it.

Measurement of the body composition of living gray seals by hydrogen isotope dilution.

The body composition of living gray seals (Halichoerus grypus) can be accurately predicted from a two-step model that involves measurement of total body water (TBW) by 2H or 3H dilution and application of predictive relationships between body components and TBW that were derived empirically by slaughter chemical analysis. TBW was overestimated by both 2HHO and 3HHO dilution; mean overestimates were 2.8 +/- 0.9% (SE) with 2H and 4.0 +/- 0.6% with 3H. The relationships for prediction of total body fat (TBF), protein (TBP), gross energy (TBGE), and ash (TBA) were as follows: %TBF = 105.1 - 1.47 (%TBW); %TBP = 0.42 (%TBW) - 4.75; TBGE (MJ) = 40.8 (mass in kg) - 48.5 (TBW in kg) - 0.4; and TBA (kg) = 0.1 - 0.008 (mass in kg) + 0.05 (TBW in kg). These relationships are applicable to gray seals of both sexes over a wide range of age and body conditions, and they predict the body composition of gray seals more accurately than the predictive equations derived from ringed seals (Pusa hispida) (Stirling et al., Can. J. Zool. 53: 1021-1027, 1975) and from the equation of Pace and Rathbun (J. Biol. Chem. 158: 685-691, 1945), which has been reported to be generally applicable to mammals.

Use of a tiletamine-zolazepam mixture to immobilise wild grey seals and southern elephant seals.

A mixture of tiletamine and zolazepam at a combined dose of 1 mg/kg was a reliable and safe agent for immobilising wild grey seals (Halichoerus grypus) and southern elephant seals (Mirouga leonina). The agent had a number of advantages over all the other agents used previously.

The use of a ketamine-diazepam mixture to immobilise wild grey seals (Halichoerus grypus) and southern elephant seals (Mirounga leonina).

A mixture of ketamine and diazepam, at doses of 6 mg/kg and 0.30 mg/kg respectively, proved to be a reliable and reasonably safe immobilisation agent for field work on grey and southern elephant seals. It was better than previously reported drugs used either singly or in combination.

Energetics and mechanics of terrestrial locomotion. II. Kinetic energy changes of the limbs and body as a function of speed and body size in birds and mammals.

This is the second paper in a series examining the link between energetics and mechanics of terrestrial locomotion. In this paper, the changes in the kinetic energy of the limbs and body relative to the centre of mass of an animal (EKE, tot) are measured as functions of speed and body size. High-speed films (light or X-ray) of four species of quadrupeds and four species of bipeds running on a treadmill were analysed to determine EKE, tot. A mass-specific power term, EKE, tot/Mb was calculated by adding all of the increments in EKE during an integral number of strides and dividing by the time interval for the strides and body mass. The equations relating EKE, tot/Mb and speed were similar for all bipeds and quadrupeds regardless of size. One general equation for the rate at which muscle and tendons must supply energy to accelerate the limbs and body relative to the centre of mass seems to apply for all of the animals: E'KE, tot/Mb = 0.478 vg1.53 where E'KE, tot/Mb has the units W kg-1 and vg is ground speed in m s-1. Therefore, E'KE, tot/Mb does not change in parallel with the mass-specific rate at which animals consume energy (Emetab/Mb), either as a function of speed or as a function of body size.

Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals.

This is the final paper in or series examining the link between the energetics and mechanics of terrestrial locomotion. In this paper the kinetic energy of the limbs and body relative to the centre of mass (EKE, tot of paper two) is combined with the potential plus kinetic energy of the centre of mass (ECM, tot of paper three) to obtain the total mechanical energy (excluding elastic energy) of an animal during constant average-speed locomotion. The minimum mass-specific power required of the muscles and tendons to maintain the observed oscillations in total energy, Etot/Mb, can be described by one equation: Etot/Mb = 0.478 . vg 1.53 + 0.685 . vg + 0.072 where Etot/Mb is in W kg-1 and vg is in m s-1. This equation is independent of body size, applying equally as well to a chipmunk or a quail as to a horse or an ostrich. In marked contrast, the metabolic energy consumed by each gram of an animal as it moves along the ground at a constant speed increases linearly with speed and is proportional to Mb-0.3. Thus, we have found that each gram of tissue of a 30 g quail or chipmunk running at 3 m s-1 consumes metabolic energy at a rate about 15 times that of a 100 kg ostrich, horse or human running at the same speed while their muscles are performing work at the same rate. Our measurements demonstrate the importance of storage and recovery of elastic energy in larger animals, but they cannot confirm or exclude the possibility of elastic storage of energy in small animals. It seems clear that the rate at which animals consume energy during locomotion cannot be explained by assuming a constant efficiency between the energy consumed and the mechanical work performed by the muscles. It is suggested that the intrinsic velocity of shortening of the active muscle motor units (which is related to the rate of cycling of the cross bridges between actin and myosin) and the rate at which the muscles are turned on and off are the most important factors in determining the metabolic cost of constant-speed locomotion. Faster motor units are recruited as animals increase speed, and equivalent muscles of small animals have faster fibres than those of larger animals. Also, the muscles are turned on and off more quickly as an animal increases speed, and at the same speed a small animal will be turning muscles on and off at a much higher rate. These suggestions are testable, and future studies should determine if they are correct.

One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems.

A simple one-step procedure that eliminates the need to calibrate the O2 analyzer or measure the flow past the animal is described for calibrating an open-flow respirometry system. The technique is particularly useful for situations of high ambient humidity and for large or active animals where a mask is employed to capture expired gases. A measured N2 flow is used to calibrate the system. The equations describing the technique are given, and the accuracy of the method is discussed in detail. The errors associated with the technique are compared with those of more conventional procedures and are usually smaller.

Terrestrial locomotion in penguins: it costs more to waddle.

The energetic cost for walking is relatively higher for penguins than for other birds or for quadrupeds of similar body mass. The morphology of penguins seems to represent a compromise between aquatic and terrestrial locomotion wherein both energy economy and speed suffer when the birds move on land.

Energy expenditure for thermoregulation and locomotion in emperor penguins.

During the antarctic winter emperor penguins (Aptenodytes forsteri) spend up to four mo fasting while they breed at rookeries 80 km or more from the sea, huddling close together in the cold. This breeding cycle makes exceptional demands on their energy reserves, and we therefore studied their thermoregulation and locomotion. Rates of metabolism were measured in five birds (mean body mass, 23.37 kg) at ambient temperatures ranging from 25 to -47 degrees C. Between 20 and -10 degrees C the metabolic rate (standard metabolic rate (SMR)) remained neraly constant, about 42.9 W. Below -10 degrees C metabolic rate increased lineraly with decreasing ambient temperature and at -47 degrees C it was 70% above the SMR. Mean thermal conductance below -10 degrees C was 1.57 W m-2 degrees C-1. Metabolic rate during treadmill walking increased linearly with increasing speed. Our data suggest that walking 200 km (from the sea to the rookery and back) requires less than 15% of the energy reserves of a breeding male emperor penguin initially weighing 35 kg. The high energy requirement for thermoregulation (about 85%) would, in the absence of huddling, probably exceed the total energy reserves.