Randall W. Davis

The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke.

SUMMARY Foraging by mammals is a complex suite of behaviors that can entail high energetic costs associated with supporting basal metabolism, locomotion and the digestion of prey. To determine the contribution of these various costs in a free-ranging marine mammal, we measured the post-dive oxygen consumption of adult Weddell seals (N=9) performing foraging and non-foraging dives from an isolated ice hole in McMurdo Sound, Antarctica. Dives were classified according to behavior as monitored by an attached video-data logging system (recording activity, time, depth, velocity and stroking). We found that recovery oxygen consumption showed a biphasic relationship with dive duration that corresponded to the onset of plasma lactate accumulation at approximately 23 min. Locomotor costs for diving Weddell seals increased linearly with the number of strokes taken according to the relationship: locomotor cost =– 3.78+0.04 × stroke number (r2=0.74, N=90 dives), where locomotor cost is in ml O2 kg–1. Foraging dives in which seals ingested Pleuragramma antarcticum resulted in a 44.7% increase in recovery oxygen consumption compared to non-foraging dives, which we attributed to the digestion and warming of prey. The results show that the energy expended in digestion for a free-ranging marine mammal are additive to locomotor and basal costs. By accounting for each of these costs and monitoring stroking mechanics, it is possible to estimate the aerobic cost of diving in free-ranging seals where cryptic behavior and remote locations prevent direct energetic measurements.

Swimming Metabolism of Yearling and Adult Harbor Seals Phoca vitulina

The swimming metabolism of yearling and adult harbor seals was measured by indirect calorimetry in a flow channel at speeds ranging from 0.5 to 1.4 m·s−1. Minimum resting metabolic rates in still water were 5.1 and 4.6 ml O2·min−1·kg−1 for the two yearling seals (body mass [Mb] = 33 kg) and one adult seal (Mb = 63 kg), respectively. Minimum resting metabolic rates were about 1.1 × the predicted standard metabolic rate for mammals of equivalent size. During steady-state swimming, metabolism increased curvilinearly with speed and was best described by the equation V̇o2 (ml O2·min−1·kg−1) = 5.1 + 6.25 velocity (m·s−1)1.42 for the yearling seals and V̇o2 = 4.6 + 3.1 velocity1.42 for the adult seal. Stroke frequency increased linearly as a function of swimming speed. Cost of transport decreased asymptotically with swim velocity, approaching a minimum at 1.0–1.4 m·s−1 of 3.6 J·m−1·kg−1 for yearling and 2.3 J·m−1·kg−1 for adult seals. The minimum cost of transport was less than for other semiaquatic birds and mammals but 3–4 × the predicted value for salmonid fish of equivalent size at 25 C.

A killer appetite: metabolic consequences of carnivory in marine mammals ☆

Among terrestrial mammals, the morphology of the gastrointestinal tract reflects the metabolic demands of the animal and individual requirements for processing, distributing, and absorbing nutrients. To determine if gastrointestinal tract morphology is similarly correlated with metabolic requirements in marine mammals, we examined the relationship between basal metabolic rate (BMR) and small intestinal length in pinnipeds and cetaceans. Oxygen consumption was measured for resting bottlenose dolphins and Weddell seals, and the results combined with data for four additional species of carnivorous marine mammal. Data for small intestinal length were obtained from previously published reports. Similar analyses were conducted for five species of carnivorous terrestrial mammal, for which BMR and intestinal length were known. The results indicate that the BMRs of Weddell seals and dolphins resting on the water surface are 1.6 and 2.3 times the predicted levels for similarly sized domestic terrestrial mammals, respectively. Small intestinal lengths for carnivorous marine mammals depend on body size and are comparatively longer than those of terrestrial carnivores. The relationship between basal metabolic rate (kcal day(-1)) and small intestinal length (m) for both marine and terrestrial carnivores was, BMR=142.5 intestinal length(1.20) (r(2)=0.83). We suggest that elevated metabolic rates among marine mammal carnivores are associated with comparatively large alimentary tracts that are presumably required for supporting the energetic demands of an aquatic lifestyle and for feeding on vertebrate and invertebrate prey.

Validation of heart rate and doubly labelled water as measures of metabolic rate during swimming in California sea lions

1. The measurement of energy expenditures in free-ranging animals is essential if we are to understand fully the interaction between a species and its environment. This study examined the validity of heart rate (fH) and doubly labelled water (DLW) as measures of field metabolic rate (FMR) in California Sea Lions (Zalophus californianus). 2. Oxygen consumption and CO2 production were measured over 24 h by direct respirometry in six juvenile sea lions. The respirometer consisted of a hood over a flume in which the sea lions were exercised to various levels for 15 min periods throughout each experiment. The exercise regime produced a mean metabolic rate which was 2.3 times the predicted basal metabolic rate (BMR) with mean maxima of 6.27 times the predicted BMR. 3. Simultaneously with direct respirometry, mean CO2 production was estimated using DLW and O2 consumption was estimated using fH, which had previously been calibrated against O2 consumption. 4. The mean\pmSD O2 consumptions from direct respirometry, fH and DLW were 11.80\pm2.40, 11.95\pm2.17 and 15.01\pm3.77 ml min-1 kg-1 respectively. Paired Students t-tests showed no significant difference between O2 consumption by direct respirometry and the estimates from DLW and fH. DLW measurements ranged from -10% to +86% of the direct respirometry measurements (mean +36.4%) and fH measurements ranged from -28% to +23% of the direct respirometry measurements (mean +2.7%). 5. The range of estimated metabolic rates from fH was largely owing to individual differences in the slopes of the linear relationship between fH and O2 consumption. The range of metabolic rates from DLW could be partly attributed to the short duration of the experiments (24-25 h) but this was shown not to be the cause of the tendency to overestimate metabolic rate from DLW. It was concluded that both DLW and fH are valid methods for measuring FMR in California Sea Lions although it is possible that FMR could be overestimated when using DLW.

Blood Chemistry Regulation during Repetitive Diving in Weddell Seals

During serial diving periods in Weddell seals, whole-blood lactate and glucose levels do not indicate a metabolic demand for extended recovery time at the surface. In fact, in some rare cases, the seals continue to dive even if blood lactate is elevated from a previous long dive. In addition, hematocrit (Hct) levels increase significantly and remain elevated until the dive bout has ended. These combined responses indicate that the seal will maximize its foraging time underwater by establishing a diving routine that does not significantly alter its blood chemistry. Instead, by minimizing blood glucose and lactate variations, occasionally continuing to dive in spite of excess blood lactate levels, and enhancing its blood oxygen carrying capacity, the seal can minimize time at the surface. These behavioral and metabolic correlates are unique observations on how seals can dive repetitively for hours or even days.

The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals.

SUMMARY Our objective was to determine the ontogenetic changes in the skeletal muscles of Weddell seals that transform a non-diving pup into an elite diving adult. Muscle biopsies were collected from pups, juveniles and adults and analyzed for changes in fiber type, mitochondrial density, myoglobin concentrations and aerobic, lipolytic and anaerobic enzyme activities. The fiber type results demonstrated a decrease in slow-twitch oxidative (Type I) fibers and a significant increase in fast-twitch oxidative (Type IIA) fibers as the animals mature. In addition, the volume density of mitochondria and the activity of lipolytic enzymes significantly decreased as the seals matured. To our knowledge, this is the first quantitative account describing a decrease in aerobic fibers shifting towards an increase in fast-twitch oxidative fibers with a significant decrease in mitochondrial density as animals mature. These differences in the muscle physiology of Weddell seals are potentially due to their three very distinct stages of life history: non-diving pup, novice diving juvenile, and elite deep diving adult. During the first few weeks of life, pups are a non-diving terrestrial mammal that must rely on lanugo (natal fur) for thermoregulation in the harsh conditions of Antarctica. The increased aerobic capacity of pups, associated with increased mitochondrial volumes, acts to provide additional thermogenesis. As these future elite divers mature, their skeletal muscles transform to a more sedentary state in order to maintain the low levels of aerobic metabolism associated with long-duration diving.

Movements and Behavior of Satellite- tagged Spotted Seals (Phoca largha) in the Bering and Chukchi Seas

Abstract Satellite-linked tags were attached to 12 spotted seals (Phoca largha) captured at a coastal lagoon in the eastern Chukchi Sea during August 1991–1993. Movements of seals were tracked for 32–298 days using the Argos system. Of 9,651 total location records obtained, 7,268 were usable. Individual seals were located on 41–96% of the days that tags were operational. During August–November, tagged seals alternated haul-outs at coastal sites lasting 1–304 h with trips to sea of 14–901 h. Coastal haul-outs occurred at 14 sites in western Alaska and eastern Russia. On several trips to sea, seals covered distances of more than 1,000 km. Movement southward from the Chukchi Sea generally began in October, with most of the seals passing through the Bering Strait during November. Seals first hauled out on sea ice in October (Chukchi Sea) or November (Bering Sea), and generally moved southward during October–December as sea-ice coverage increased. Seven seals, whose transmitters were still operating, spent December to June in the Bering Sea region between Kuskokwim Bay and Anadyr Gulf, which corresponded to the location of the ice front. The seals made active east-west movements within the ice front. Spotted seals are unlike other ice-breeding seals in that they regularly use coastal haul-outs during summer and autumn. Compared to the closely related Pacific harbor seal (Phoca vitulina richardsi), spotted seals make much longer trips to sea and spend longer continuous periods at their haul-outs during summer and autumn.

Water flux and estimated metabolism of free-ranging gentoo and macaroni penguins at South Georgia

SummaryWater turnover rates were measured in gentoo and macaroni penguins breeding sympatrically on South Georgia Island. At the time of this study, adult male macaronis were attending the nest while female macaronis and both sexes of adult gentoos were making regular foraging trips to sea and returning to feed their chicks. Both species feed principally on krill, Euphausia superba, although gentoos also feed on fish. The average water turnover rate in 2 fasting male macaronis was 12.5 ml·kg-1·day-1 with a half-time for water turnover of 36 days. The mean water flux rate in feeding birds was 155 ml·kg-1·day-1 in gentoos and 184 ml·kg-1·day-1 in macaronis. The half-times for water turnover were 2.8 days, and 2.6 days, respectively. The average metabolic rate of fasting macaronis calculated from water turnover rates was 5.6 W·kg-1 or 1.8 x the standard metabolic rate (SMR). In order to calculate prey consumption and average daily metabolic rate (ADMR) from water flux rates in feeding birds, it was assumed that a) the only sources of water are from metabolism and performed water in the diet and b) the composition of the diet is known. Based on the type of prey consumed, the calculated ADMR was 7.1 W·kg-1 or 2.6×SMR (n=5) for gentoos and 9.1 W·kg-1 or 2.9×SMR (n=3) for macaronis. The ADMR of female macaronis making regular trips to sea was 1.6 x greater than the fasting metabolism of males brooding the chick.

Fuel homeostasis in the harbor seal during submerged swimming.

Summary1.The turnover rates and oxidation rates of plasma glucose, lactate, and free fatty acids (FFA) were measured in three harbor seals (average mass=40 kg) at rest or during voluntary submerged swimming in a water flume at 35% (1.3 m·s-1) and 50% (2 m·s-1) of maximum oxygen consumption (MO2max).2.For seals resting in water, the total turnover rates for glucose, lactate, and FFA were 23.2, 26.2, and 7.5 μmol·min-1·kg-1, respectively. Direct oxidation of these metabolites accounted for approximately 7%, 27%, and 33% of their turnover and 3%, 7%, and 18% of the total ATP production, respectively.3.For swimming seals,MO2max was achieved at a drag load equivalent to a speed of 3 m·s-1 and averaged 1.85 mmol O2·min-1·kg-1, which is 9-fold greater than resting metabolism in water at 18°C.4.At 35% and 50%MO2max, glucose turnover and oxidation rates did not change from resting levels. Glucose oxidation contributed about 1% of the total ATP production during swimming.5.At 50%MO2max, lactate turnover and anaerobic ATP production doubled, but the steady state plasma lactate concentration remained low at 1.1 mM. Lactate oxidation increased 63% but still contributed only 4% of the total ATP production. Anaerobic metabolism contributed about 1% of the total ATP production at rest and during swimming.6.The plasma FFA concentration and turnover rate inereased only 24% and 37% over resting levels, respectively, at 50%MO2max. However, the oxidation rate increased almost 3.5-fold and accounted for 85% of the turnover. The percentage of total ATP produced (21%) from FFA oxidation at 35% and 50%MO2max did not increase greatly over that at rest.7.Dive duration decreased from 78 s while resting in water to 28 s at 50%MO2max.8.The RQ ranged from 0.78 at rest to 0.74 at 50%MO2max, indicating that fat was an important source of energy during submerged swimming.9.By adjusting breath-hold duration during strenuous underwater swimming, harbor seals are able to maintain an aerobic, fat-based metabolism.

A review of the multi-level adaptations for maximizing aerobic dive duration in marine mammals: from biochemistry to behavior.

Marine mammals exhibit multi-level adaptations, from cellular biochemistry to behavior, that maximize aerobic dive duration. A dive response during aerobic dives enables the efficient use of blood and muscle oxygen stores, but it is exercise modulated to maximize the aerobic dive limit at different levels of exertion. Blood volume and concentrations of blood hemoglobin and muscle myoglobin are elevated and serve as a significant oxygen store that increases aerobic dive duration. However, myoglobin is not homogeneously distributed in the locomotory muscles and is highest in areas that produce greater force and consume more oxygen during aerobic swimming. Muscle fibers are primarily fast and slow twitch oxidative with elevated mitochondrial volume densities and enhanced oxidative enzyme activities that are highest in areas that produce more force generation. Most of the muscle mitochondria are interfibriller and homogeneously distributed. This reduces the diffusion distance between mitochondria and helps maintain aerobic metabolism under hypoxic conditions. Mitochondrial volume densities and oxidative enzyme activities are also elevated in certain organs such as liver, kidneys, and stomach. Hepatic and renal function along with digestion and assimilation continue during aerobic dives to maintain physiological homeostasis. Most ATP production comes from aerobic fat metabolism in carnivorous marine mammals. Glucose is derived mostly from gluconeogenesis and is conserved for tissues such as red blood cells and the central nervous system. Marine mammals minimize the energetic cost of swimming and diving through body streamlining, efficient, lift-based propulsive appendages, and cost-efficient modes of locomotion that reduce drag and take advantage of changes in buoyancy with depth. Most dives are within the animal’s aerobic dive limit, which maximizes time underwater and minimizes recovery time at the surface. The result of these adaptations is increased breath-hold duration and enhanced foraging ability that maximizes energy intake and minimizes energy output while making aerobic dives to depth. These adaptations are the long, evolutionary legacy of an aquatic lifestyle that directly affects the fitness of marine mammal species for different diving abilities and environments.