Limits and constraints on the duration of dives in nature: why are many dives so short and others so long?

Mike Fedak, Dave Thompson, Bernie McConnell and Kimberly Bennett

NERC Sea Mammal Research Unit, School of Environmental and Evolutionary Biology, University of St Andrews, Scotland UK KY16 8LB

The diving behaviour displayed by seals is highly variable in duration. What sets the durations of dives? Why are most dives much shorter than estimates of physiological capability suggest they could be and can we use the upper limits of duration observed in nature to tell us anything about the physiological processes that set limits to duration?
We present a simple model of dive behaviour that may help to explain why most dives performed by seals are short. We show that by giving up early and returning to the surface while O2 stores are only partially utilized, seals can improve foraging success in relatively shallow dives. Deep diving seal species have little to gain by adopting this strategy; they make very long dives. We also examine seasonal patterns in extreme dive behaviour in elephant seals and show that dives are consistently longer in early morning and mid-winter, regardless of depth, the habitat or the sex and age of the animal. The underlying physiological capacity for diving changes diurnally and seasonally and may explain these consistent patterns in the durations of the longest dives. We speculate on what might mediate these patterns.
Simplistic notions of a "dive response" have given way to the realization that diving represents a complex range of responses that operate within physiological constraints but are tuned to the behavioural context in which they are performed. Combined physiological and behavioural models and detailed behavioural observations can help us to put forward stimulating hypotheses and explanations of the patterns we observe.

The Role of Physiological Constraint in the Acquisition of Foraging Ability: The Development of Diving Capacity in Juvenile Phocid Seals

Jennifer Burns

Department of Biological Sciences, 3211 Providence Drive, University of Alaska Anchorage, Anchorage, AK 99708

Knowledge of the mechanisms by which neonatal mammals acquire the tools necessary to become competent predators is crucial to understanding how
physiological processes influence behavioral strategies. While such questions can be addressed in many species, because oxygen stores and use rates determine foraging capacity, the study of how pinniped neonates become marine predators offers several unique advantages. In phocids, the rapid transition from terrestrial neonate to diving juvenile is accomplished by differential maturation of blood and muscle oxygen stores and a shift in the relative contribution of these stores to total reserves. Blood oxygen stores develop rapidly over the lactation and postweaning fast period, such that by independence, the mass specific blood oxygen stores of juveniles are 70-90% of adult values (Weddell, harbor, hooded, harp, northern elephant seals). In contrast, muscle mass and muscle myoglobin loads are much slower to develop, such that mass specific oxygen stores are only 30-50% of adult values. In addition, it appears that foraging is only initiated after approximately 25% of total oxygen stores are held in muscle tissue (as opposed to ~15% at birth, and ~35% in adults). The similar pattern of physiological development among these species is remarkable given interspecific differences in the length of the lactation and postweaning fast periods, the relative maturity of pups at birth, and the size of adult stores. These findings suggest that the rate and extent of muscle development may be a critical factor in determining when phocid pups are able to begin diving and foraging efficiently.

Remote monitoring of the behavior and physiology of diving mammals

Russel D. Andrews.

Dept. of Zoology, Univ. of British Columbia, Vancouver, B.C.
(e-mail: andrews@zoology.ubc.ca)

After 60 years of intensive research efforts, the mechanistic basis of the diving response of mammals is well understood. Many unanswered questions, however, still remain in the field of diving physiology. Some problems may only be resolved with the application of new tools and techniques for remotely monitoring animals in their natural environments. Despite the immense challenges of trying to deploy miniature electronic devices on large animals that spend most of their time exposed to corrosive seawater, investigators have had some recent, outstanding successes. I will illustrate such approaches with a study of northern elephant seals. The elephant seal is an ideal subject for studying how divers balance the conflicting demands of diving, exercise, and thermoregulation in cold water, because, unlike most other pinnipeds, elephant seals routinely dive for periods (up to 2 hours) that exceed the capacity of the oxygen stores to provide for aerobic metabolism. We recorded dive depth, field metabolic rate (FMR), heart and respiratory rate, and regional body temperatures in juvenile elephant seals freely diving in the open ocean. Pronounced bradycardia and regional hypothermia were unexpected features of voluntary diving. Surprisingly, the FMR of seals at sea, actively swimming in cold water, was the same as while resting on land. Such low FMRs are apparently due to low swim speed, reduced heat loss, and low core temperature. Exactly how seals redistribute blood flow and oxygen to maintain function is unclear. We hope to answer this and many other questions with new instrumentation currently in development, including a miniature, animal-mounted blood flow/ blood pressure monitor, controlled by a new generation data logger capable of large (300 Mbyte) data storage.

A comparison between the antioxidant status of terrestrial and diving mammals.

Danilo Wilhelm Filho

Depto. Ecologia & Zoologia, Universidade Federal de Santa Catarina, Florianspolis, Brazil

Oxygen metabolism in all aerobic organisms, from bacteria to mammals, implies the generation of reactive oxygen species (ROS). These ROS can oxidize all kinds of biologically relevant molecules including proteins, lipids, and DNA, leading to alterations in normal cell and organ functions. This damage is functionally minimized by a complex panoply of antioxidant defences (AD). Therefore, ROS generation, molecule oxidation, and antioxidant consumption exist in a steady-state in aerobic organisms, and this functional interaction needs to be understood if comparisons between different vertebrate species are to be made. Diving mammals are known for their ability to deal with nitrogen supersaturation and to tolerate apnea for extended periods of time. They are all characterized by a high oxygen-carrying capacity in blood together with a high oxygen storage in their muscle mass. The above properties theoretically also imply a high tissue antioxidant capacity to counteract the ROS generation associated with the rapid transition from apnea to reoxygenation. Different enzymatic (superoxide dismutase, catalase, glutathione reductase, glutathione peroxidase), and non-enzymatic (different forms of glutathione) concentrations, as well as cellular damage (TBARS contents as a measure of lipoperoxidation) were measured in fresh blood samples from anesthetized healthy animals, and also in samples from brain, liver, and skeletal muscles of dead animals. Blood samples from diving mammals (especially from sea elephants) were compared with those obtained from non-diving mammals. The results obtained clearly indicate that diving mammals have, in general, higher antioxidant capacity compared to non-diving mammals. Apparently, to avoid sudden exposure of the tissues to high oxygen levels, and therefore to avoid an oxidative stress condition related to antioxidant consumption and ROS production, diving mammals possess a high AD system. These data are in agreement with AD adaptations related to arrested states in other animals that undergo hibernation, estivation, torpor (microchiropteran bats), and fish and moluscs that experience large daily or seasonal changes in oxygen consumption. In summary, animals that routinely face high changes in oxygen availability seem to show a general strategy to prevent oxidative damage by having appropiate high constitutive AD.

Adaptations for tolerance to deep diving in marine mammals

M.A. Castellini, J.M. Castellini and P.M. Rivera

University of Alaska Fairbanks, USA

It is now known that both whales and seals can dive repeatedly up to 2000m, well beyond the limits where both physiological and biochemical "problems" should arise. While routine dives are shallower, seals can still approach multiple dives per day to over 800m. The adaptations to withstand elevated pressure include anatomical respiratory changes to allow lung collapse and thus inhibit gas equilibration at depth, and sinus and ear modifications. However, at the biochemical level, the necessary adaptations to withstand pressure modification of membrane properties, enzyme mechanics, metabolic pathway regulation and high pressure gas damage are not as clear.
Work in our laboratory on RBC metabolism in marine mammals and on tissue enzyme kinetics, suggests that marine mammal tissues exhibit biochemical modifications at several levels. First, compared to marine mammals, the overall glycolytic of RBCs from terrestrial mammals is inhibited by elevated hydrostatic pressure. Second, it appears that this occurs in both metabolic pathway alteration and at cell membrane transport mechanisms. However, the enzyme kinetics for lactate production and consumption at pressure show a clear change in the affinities of the enzyme lactate dehydrogenase for its substrates in both marine and terrestrial mammals. Thus, marine mammals may exhibit supra-enzyme biochemical alterations that allow metabolic flux to continue unabated at pressure, since their enzyme properties may not be different than terrestrial mammals. While many more enzymes should be investigated at pressure, we believe this evidence suggests that mechanisms involving pressure modifications of membrane properties may be of great importance.