Shawn R. Noren

Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration

Cetaceans exhibit an exceptionally wide range of body mass that influence both the capacities for oxygen storage and utilization; the balance of these factors is important for defining dive limits. Furthermore, myoglobin content is a key oxygen store in the muscle as it is many times higher in marine mammals than terrestrial mammals. Yet little consideration has been given to the effects of myoglobin content or body mass on cetacean dive capacity. To determine the importance of myoglobin content and body mass on cetacean diving performance, we measured myoglobin content of the longissimus dorsi for ten odontocete (toothed whales) and one mysticete (baleen whales) species ranging in body mass from 70 to 80000 kg. The results showed that myoglobin content in cetaceans ranged from 1.81 to 5.78 g (100 g wet muscle)(-1). Myoglobin content and body mass were both positively and significantly correlated to maximum dive duration in odontocetes; this differed from the relationship for mysticetes. Overall, the combined effects of body mass and myoglobin content accounts for 50% of the variation in cetacean diving performance. While independent analysis of the odontocetes showed that body mass and myoglobin content accounts for 83% of the variation in odontocete dive capacity.

The development of diving in marine endotherms: preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence

Abstract. Myoglobin is an important oxygen store for supporting aerobic diving in endotherms, yet little is known about its role during postnatal development. Therefore, we compared the postnatal development of myoglobin in marine endotherms that develop at sea (cetaceans) to those that develop on land (penguins and pinnipeds). We measured myoglobin concentrations in the major locomotor muscles of mature and immature bottlenose dolphins (Tursiops truncatus) and king penguins (Aptenodytes patagonicus) and compared the data to previously reported values for northern elephant seals (Mirounga angustirostris). Neonatal dolphins, penguins, and seals lack the myoglobin concentrations required for prolonged dive durations, having 10%, 9%, and 31% of adult values, respectively. Myoglobin contents increased significantly during subsequent development. The increases in myoglobin content with age may correspond to increases in activity levels, thermal demands, and time spent in apnea during swimming and diving. Across these phylogenetically diverse taxa (cetaceans, penguins, and pinnipeds), the final stage of postnatal development of myoglobin occurs during the initiation of independent foraging, regardless of whether development takes place at sea or on land.

The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): implications for diving capacity

Enhanced oxygen reserves in the blood facilitate diving in marine mammals. For pinnipeds (seals and sea lions), a developmental period of 4 to 24 months is required for blood oxygen stores to reach adult capacities. We investigated whether a similar developmental period for the blood occurs in cetaceans (dolphins and whales), a group of mammals that are exposed to diving immediately after birth. Blood samples were collected from wild and zoological park bottlenose dolphins Tursiops truncatus aged 0–12 years. Red blood cell number (RBC), haemoglobin content (Hb), haematocrit (Hct), mean corpuscular volume (MCV), mean cell haemoglobin (MCH), and mean corpuscular haemoglobin concentration (MCHC) were determined for each sample. We found that during postnatal development, RBC, Hb and Hct decreased from 0 to 1.5 months and then increased from 1.5 to 6 months, reaching adult levels by 3 years. MCV and MCH both increased from birth. MCHC decreased from 0 to 3.2 months and then increased. Adult levels for MCV were attained as early as 2 months of age while adult levels for MCH and MCHC were attained by 6 months of age. These results indicate that, for bottlenose dolphins, the development of the blood and its capacity to store oxygen is not complete with weaning, which generally occurs at 1.5 years old. The lower oxygen storage capacity of immature dolphins is likely to limit dive capabilities. Calculated aerobic dive limits (cADLs) for 0- to 2-year-old dolphin calves are 1.9–3.6 min, compared to 4.8–5.4 min for 3- to 12-year-old dolphins. Increases in cADLs from 0 to 3 years are attributed to increases in both body mass and mass specific oxygen stores while body mass alone explains the increases in cADLs from 3 to 9 years. The limited diving capacity of young dolphins may influence the foraging behaviours of newly weaned juveniles and females accompanied by calves.

Ontogeny of swim performance and mechanics in bottlenose dolphins(Tursiops truncatus)

SUMMARY Morphological and physiological development impacts swimming performance throughout ontogeny. Our investigation of the ontogeny of swim performance (mean and maximum swim speed) and swim effort (stroke amplitude and tailbeat frequency) of independently swimming bottlenose dolphins (Tursiops truncatus) demonstrated that swimming capabilities are extremely limited in calves. Mean and maximum swim speeds of 0-1-month-old calves were only 37% and 52% of that for adults, respectively, and levels similar to those of adults were not achieved until one year post-partum. Limitations in swim speed were associated with an inability to achieve mature thrusting capabilities, as stroke amplitude and distance covered per stroke remained significantly lower than adult levels during the first-year post-partum. Although calves were expected to require less thrusting power to propel their smaller bodies through water, size-specific stroke amplitudes of 0-3-month-olds (23-26% of body length) were smaller than those of dolphins ≥10 months post-partum (29-30% of body length). As a result, swim speed standardized by body length was significantly slower for 0-3-month-old dolphins compared with dolphins≥ 10 months post-partum. These results suggest that other factors, such as underdeveloped physiology, act synergistically with small body size to limit independent swim performance in dolphins during ontogeny.

Body condition at weaning affects the duration of the postweaning fast in gray seal pups(Halichoerus grypus)

Gray seals (Halichoerus grypus) undergo a terrestrial postweaning fast (PWF) that depletes energy reserves acquired during the suckling interval. Plasticity in PWF duration may ensure that pups of variable body condition depart for sea with adequate energy reserves. To test this hypothesis, we examined body condition of 30 gray seal pups at weaning and monitored their PWF duration. On average, fat accounted for 47.3% ± 0.7% of their 53.2 ± 1.3‐kg weaning mass. Although fasting duration averaged 21 ± 1.1 d (n = 28), there was considerable variation in fasting duration (9 to >31 d) and the resulting age when pups departed to sea (26 to >49 d). Percent fat at weaning (38.6%–54.6%) was positively correlated with fasting duration (n = 28, r = 0.376, P = 0.0489). In contrast, total body gross energy (735.3–1,447.4 MJ) and body mass (39.0–66.0 kg) were not correlated with fasting duration. Thus, body composition, not overall body reserves, predicted fasting duration, but the effect was weak, indicating that other factors also account for the observed variation in fasting duration. We speculate that pups with greater percent fat more effectively utilized lipid and conserved protein while meeting metabolic costs throughout the PWF. As a result, fatter pups extended the PWF duration, which may be critical for development of diving physiology and may have facilitated their survivorship to age 1.

Running energetics of the North American river otter: do short legs necessarily reduce efficiency on land?

Semi-aquatic mammals move between two very different media (air and water), and are subject to a greater range of physical forces (gravity, buoyancy, drag) than obligate swimmers or runners. This versatility is associated with morphological compromises that often lead to elevated locomotor energetic costs when compared to fully aquatic or terrestrial species. To understand the basis of these differences in energy expenditure, this study examined the interrelationships between limb morphology, cost of transport and biomechanics of running in a semi-aquatic mammal, the North American river otter. Oxygen consumption, preferred locomotor speeds, and stride characteristics were measured for river otters (body mass=11.1 kg, appendicular/axial length=29%) trained to run on a treadmill. To assess the effects of limb length on performance parameters, kinematic measurements were also made for a terrestrial specialist of comparable stature, the Welsh corgi dog (body mass=12.0 kg, appendicular/axial length=37%). The results were compared to predicted values for long legged terrestrial specialists. As found for other semi-aquatic mammals, the net cost of transport of running river otters (6.63 J kg(-1)min(-1) at 1.43 ms(-1)) was greater than predicted for primarily terrestrial mammals. The otters also showed a marked reduction in gait transition speed and in the range of preferred running speeds in comparison to short dogs and semi-aquatic mammals. As evident from the corgi dogs, short legs did not necessarily compromise running performance. Rather, the ability to incorporate a period of suspension during high speed running was an important compensatory mechanism for short limbs in the dogs. Such an aerial period was not observed in river otters with the result that energetic costs during running were higher and gait transition speeds slower for this versatile mammal compared to locomotor specialists.

The dive response redefined: underwater behavior influences cardiac variability in freely diving dolphins

SUMMARY A hallmark of the dive response, bradycardia, promotes the conservation of onboard oxygen stores and enables marine mammals to submerge for prolonged periods. A paradox exists when marine mammals are foraging underwater because activity should promote an elevation in heart rate (fH) to support increased metabolic demands. To assess the effect of the interaction between the diving response and underwater activity on fH, we integrated interbeat fH with behavioral observations of adult bottlenose dolphins diving and swimming along the coast of the Bahamas. As expected for the dive response, fH while resting during submergence (40±6 beats min−1) was significantly lower than fH while resting at the water surface (105±8 beats min−1). The maximum recorded fH (fH,max) was 128±7 beats min−1, and occurred during post-dive surface intervals. During submergence, the level of bradycardia was modified by activity. Behaviors such as simple head bobbing at depth increased fH by 40% from submerged resting levels. Higher heart rates were observed for horizontal swimming at depth. Indeed, the dolphins operated at 37–58% of their fH,max while active at depth and approached 57–79% of their fH,max during anticipatory tachycardia as the animals glided to the surface. fH was significantly correlated with stroke frequency (range=0–2.5 strokes s−1, r=0.88, N=25 dives) and calculated swim speed (range=0–5.4 m s−1, r=0.88, N=25 dives). We find that rather than a static reflex, the dive response is modulated by behavior and exercise in a predictable manner.

Pregnancy is a drag: hydrodynamics, kinematics and performance in pre- and post-parturition bottlenose dolphins (Tursiops truncatus).

SUMMARY Constraints on locomotion could be an important component of the cost of reproduction as carrying an increased load associated with eggs or developing fetuses may contribute to decreased locomotor performance for females across taxa and environments. Diminished performance could increase susceptibility to predation, yet the mechanism(s) by which gravidity and pregnancy affect locomotion remains largely unexplored. Here we demonstrate that morphology, hydrodynamics and kinematics were altered during pregnancy, providing a mechanism for diminished locomotor performance in two near-term pregnant (10 days pre-parturition) bottlenose dolphins (Tursiops truncatus). Near-term pregnancy resulted in a 51±14% increase in frontal surface area, coinciding with dramatic increases in drag forces while gliding. For example, pregnant females encountered 80 N of drag at 1.7 m s–1 whereas that magnitude of drag was not encountered until speed doubled for females 18 months post-parturition. Indeed, drag coefficients based on frontal surface area were significantly greater during pregnancy (Cd,F=0.22±0.04) than at 18 months post-parturition (Cd,F=0.09±0.01). Pregnancy also induced a gait change as stroke amplitude and distance per stroke were reduced by 13 and 14%, respectively, compared with non-pregnant periods (1–24 months post-parturition). This was concomitant with a 62 and 44% reduction in mean and maximum swim speeds, respectively, during the pregnancy period. Interestingly, attack speeds of known predators of dolphins surpass maximum speeds for the pregnant dolphins in this study. Thus, pregnant dolphins may be more susceptible to predation. This study demonstrates unequivocally that changes in morphology, hydrodynamics and kinematics are associated with diminished performance during pregnancy in dolphins.

Age-related differences in skeletal muscle lipid profiles of Weddell seals: clues to developmental changes

SUMMARY Our objective was to elucidate age-related changes in lipids associated with skeletal muscle of Weddell seals and to suggest possible physiological implications. Muscle biopsies were collected from pups, juveniles and adults in McMurdo Sound, Antarctica and analyzed for intramuscular lipid (IML) and triacylglyceride (IMTG) amounts, fatty acid groups, as well as individual fatty acid profiles. The results from this study suggest a switch from primarily saturated fatty acids (SFAs) and monounsaturated fatty acids (MUFAs) in the skeletal muscle of young pups to increases in polyunsaturated fatty acids (PUFAs) as the percentage of blubber increases, resulting in possible thermoregulatory benefits. As Weddell pups continue to develop into juveniles, fatty acids associated with the skeletal muscle changes such that MUFA levels are relatively higher, which may be in response to energy depletion associated with their restricted diving ability and rapid growth. As juveniles transform into adults, a reduction in n-3 PUFA levels in the muscle as the percentage of blubber increases may be indicative of a trigger to prepare for deep diving or could be a mechanism for oxygen conservation during long-duration dives. We speculate that the observed change in lipids associated with the skeletal muscle of Weddell seals is related to ontogenetic differences in thermoregulation and locomotion.

Blubber Deposition During Ontogeny in Free-Ranging Bottlenose Dolphins: Balancing Disparate Roles of Insulation and Locomotion

Abstract Blubber is a critical component of thermoregulation for marine mammals, particularly for cetaceans. However, the cost of overcoming blubbers buoyant force during descent could constrain blubber deposition. One- to 12-year-old healthy, free-ranging common bottlenose dolphins (Tursiops truncatus) were studied in Sarasota Bay, Florida, during summer (mean water temperature: 29.7°C ± 0.1 SE) and winter (mean water temperature: 19.2 ± 0.4°C) to examine ontogenetic and seasonal trends in morphology and blubber deposition. Surface-area-to-volume ratio decreased significantly with age. During summer, yearlings had significantly thicker blubber than 2- to 12-year-old animals but this difference diminished by winter because blubber deposition in response to the colder water temperature was smaller in yearlings (2-mm increase) compared to 2- to 12-year-old animals (3- to 6-mm increase). During summer, buoyancy was highest in yearlings (6.24 N ± 0.41 SE), compared to a buoyant force of −0.98 ± 0.90 N (neutrally buoyant) for 12-year-old animals. Conversely, all dolphins converged upon a similar buoyant force (8.01 ± 0.56 N) in winter. The elevated buoyancy of yearlings in summer presumably limits seasonal blubber adjustments, because all yearlings (regardless of season) converged upon a similar calculated mass-specific cost of descent that was greater than all other age classes. Balancing energetic demands of thermoregulation and locomotion may limit the flexibility of yearlings to adjust blubber deposition in response to fluctuating water temperatures.