This review concentrates on the physiological responses, and their control, in freely diving birds and mammals that enable them to remain submerged and sometimes quite active for extended periods of time. Recent developments in technology have provided much detailed information on the behavior of these fascinating animals. Unfortunately, the advances in technology have been insufficient to enable physiologists to obtain anything like the same level of detail on the metabolic rate and physiological adjustments that occur during natural diving. This has led to much speculation and calculations based on many assumptions concerning usable oxygen stores and metabolic rate during diving, in an attempt to explain the observed behavior. Despite their shortcomings, these calculations have provided useful insights into the degree of adaptations of various species of aquatic birds and mammals. Many of them, e.g., ducks, smaller penguins, fur seals, and Weddell seals, seem able to metabolize aerobically, when diving, at approximately the same (if not greater) rate as they do at the surface. Their enhanced oxygen stores are able to support aerobic metabolism, at what would not be considered unusually low levels, for the duration of the dives, although there are probably circulatory readjustments to ensure that the oxygen stores are managed judiciously. For other species, such as the larger penguins, South Georgian shag, and female elephant seals, there is a general consensus that they must either be reducing their aerobic metabolic rate when diving, possibly by way of regional hypothermia, and/or producing ATP, at least partly, by anaerobiosis and metabolizing the lactic acid when at the surface (although this is hardly likely in the case of the female elephant seals). Circulation is the proximate regulator of metabolism during aerobic diving, and heart rate is the best single indicator of circulatory adjustment. During voluntary dives, heart rates range from extreme bradycardia to well above resting, reflecting metabolic performance. Efferent cardiac control is largely parasympathetic. Reflex cardiorespiratory responses are modulated by conditioning and habituation, but reflexes predominate during extended dives and during recovery, when gas exchange is maximized.

Physiology of diving of birds and mammals

There is wide diversity in the animals that dive to depth and in the distribution of their body oxygen stores. A hallmark of animals diving to depth is a substantial elevation of muscle myoglobin concentration. In deep divers, more than 80% of the oxygen store is in the blood and muscles. How these oxygen stores are managed, particularly within muscle, is unclear. The aerobic endurance of four species has now been measured. These measurements provide a standard for other species in which the limits cannot be measured. Diving to depth requires several adaptations to the effects of pressure. In mammals, one adaptation is lung collapse at shallow depths, which limits absorption of nitrogen. Blood N2 levels remain below the threshold for decompression sickness. No such adaptive model is known for birds. There appear to be two diving strategies used by animals that dive to depth. Seals, for example, seldom rely on anaerobic metabolism. Birds, on the other hand, frequently rely on anaerobic metabolism to exploit prey-rich depths otherwise unavailable to them.

THE PHYSIOLOGICAL BASIS OF DIVING TO DEPTH: Birds and Mammals

▪ Abstract Understanding adaptation in morphological and physiological traits requires elucidation of how traits relate to whole-organism performance and how performance relates to fitness. A common assumption is that performance capacities are utilized by and important to organisms. For some systems, it is assumed that high levels of physical fitness, as indexed by measures of locomotor performance, lead to high fitness levels. Although biologists have appreciated this, little attention has been paid to quantifying how organisms use their performance capacities in nature. We argue that for the study of adaptation to proceed, greater integration of laboratory studies of performance and behavioral/ecological studies is needed, and we illustrate this approach by examining two questions. First, how does the environment affect locomotor function in nature? Second, what percentage of locomotor capacities do animals use in nature? A review of studies in several animal groups shows widespread effects of the envi...

Integrating function and ecology in studies of adaptation: Investigations of locomotor capacity as a model system

An animal's behaviour is a response to its environment and physiological condition, and as such, gives vital clues as to its well-being, which is highly relevant in conservation issues. Behaviour can generally be typified by body motion and body posture, parameters that are both measurable using animal-attached accelerometers. Interpretation of acceleration data, however, can be complex, as the static (indicative of posture) and dynamic (motion) components are derived from the total acceleration values, which should ideally be recorded in all 3-dimensional axes. The principles of triaxial accelerometry are summarised and discussed in terms of the commonalities that arise in patterns of acceleration across species that vary in body pattern, life-history strategy, and the medium they inhabit. Using tri-axial acceleration data from deployments on captive and free-living animals (n = 12 species), behaviours were identified that varied in complexity, from the rhythmic patterns of locomotion, to feeding, and more variable patterns including those relating to social interactions. These data can be combined with positional information to qualify patterns of area-use and map the distribution of target behaviours. The range and distribution of behaviour may also provide insight into the transmission of disease. In this way, the measurement of tri-axial acceleration can provide insight into individual and population level processes, which may ultimately influence the effectiveness of conservation practice. © 2008 Inter-Research.

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Identification of animal movement patterns using tri-axial accelerometry

Locomotor activity by diving marine mammals is accomplished while breath-holding and often exceeds predicted aerobic capacities. Video sequences of freely diving seals and whales wearing submersible cameras reveal a behavioral strategy that improves energetic efficiency in these animals. Prolonged gliding (greater than 78% descent duration) occurred during dives exceeding 80 meters in depth. Gliding was attributed to buoyancy changes with lung compression at depth. By modifying locomotor patterns to take advantage of these physical changes, Weddell seals realized a 9.2 to 59.6% reduction in diving energetic costs. This energy-conserving strategy allows marine mammals to increase aerobic dive duration and achieve remarkable depths despite limited oxygen availability when submerged.

https://science.sciencemag.org/content/sci/288/5463/133.full.pdf

Sink or swim: strategies for cost-efficient diving by marine mammals.

Velocities during surface swimming and diving were measured with microprocessor recorders in four otariid species: northern fur seals (Callorhinus ursinus), Galapagos sea lions (Zalophus californianus wollebaeki), Galapagos fur seals (Arctocephalus galapagoensis), and Hooker's sea lions (Phocarctos hookeri). Mean surface swimming velocities ranged from 0.6 to 1.9 m/s. Transit distances to feeding sites (1.2–90 km) were calculated using these velocities. Dive velocities, recorded every 15 s, ranged from 0.9 to 1.9 m/s. These velocities were consistent with calculated minimal cost of transport velocities in the smaller species. Using time partitioning, the metabolic cost of a northern fur seal foraging trip is estimated on the basis of recorded velocities and their calculated energy costs. This value is within 6% of that previously made with doubly labeled water techniques.

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Swimming velocities in otariids

Heart rate during overnight rest and while diving were recorded from five emperor penguins with a microprocessor-controlled submersible recorder. Heart rate, cardiac output and stroke volume were also measured in two resting emperor penguins using standard electrocardiography and thermodilution measurements. Swim velocities from eight birds were obtained with the submersible recorder. The resting average of the mean heart rates was 72 beats min-1. Diving heart rates were about 15% lower than resting rates. Cardiac outputs of 1.9-2.9 ml kg-1 s-1 and stroke volumes of 1.6-2.7 ml kg-1 were similar to values recorded from mammals of the same body mass. Swim velocities averaged 3 m s-1. The swim speeds and heart rates suggest that muscle O2 depletion must occur frequently: therefore, many dives require a significant energy contribution from anaerobic glycolysis.

Heart rates and swim speeds of emperor penguins diving under sea ice

Temperatures were recorded at several body sites in emperor penguins (Aptenodytes forsteri) diving at an isolated dive hole in order to document temperature profiles during diving and to evaluate the role of hypothermia in this well-studied model of penguin diving physiology. Grand mean temperatures (+/-S.E.) in central body sites during dives were: stomach: 37.1+/-0.2 degrees C (n=101 dives in five birds), pectoral muscle: 37.8+/-0.1 degrees C (n=71 dives in three birds) and axillary/brachial veins: 37.9+/-0.1 degrees C (n=97 dives in three birds). Mean diving temperature and duration correlated negatively at only one site in one bird (femoral vein, r=-0.59, P<0.05; range <1 degrees C). In contrast, grand mean temperatures in the wing vein, foot vein and lumbar subcutaneous tissue during dives were 7.6+/-0.7 degrees C (n=157 dives in three birds), 20.2+/-1.2 degrees C (n=69 in three birds) and 35.2+/-0.2 degrees C (n=261 in six birds), respectively. Mean limb temperature during dives negatively correlated with diving duration in all six birds (r=-0.29 to -0.60, P<0.05). In two of six birds, mean diving subcutaneous temperature negatively correlated with diving duration (r=-0.49 and -0.78, P<0.05). Sub-feather temperatures decreased from 31 to 35 degrees C during rest periods to a grand mean of 15.0+/-0.7 degrees C during 68 dives of three birds; mean diving temperature and duration correlated negatively in one bird (r=-0.42, P<0.05). In general, pectoral, deep venous and even stomach temperatures during diving reflected previously measured vena caval temperatures of 37-39 degrees C more closely than the anterior abdominal temperatures (19-30 degrees C) recently recorded in diving emperors. Although prey ingestion can result in cooling in the stomach, these findings and the lack of negative correlations between internal temperatures and diving duration do not support a role for hypothermia-induced metabolic suppression of the abdominal organs as a mechanism of extension of aerobic dive time in emperor penguins diving at the isolated dive hole. Such high temperatures within the body and the observed decreases in limb, anterior abdomen, subcutaneous and sub-feather temperatures are consistent with preservation of core temperature and cooling of an outer body shell secondary to peripheral vasoconstriction, decreased insulation of the feather layer, and conductive/convective heat loss to the water environment during the diving of these emperor penguins.

Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice.

To investigate the diving heart rate (f(H)) response of the emperor penguin (Aptenodytes forsteri), the consummate avian diver, birds diving at an isolated dive hole in McMurdo Sound, Antarctica were outfitted with digital electrocardiogram recorders, two-axis accelerometers and time depth recorders (TDRs). In contrast to any other freely diving bird, a true bradycardia (f(H) significantly <f(H) at rest) occurred during diving [dive f(H) (total beats/duration)=57+/-2 beats min(-1), f(H) at rest=73+/-2 beats min(-1) (mean +/- s.e.m.)]. For dives less than the aerobic dive limit (ADL; duration beyond which [blood lactate] increases above resting levels), dive f(H)=85+/-3 beats min(-1), whereas f(H) in dives greater than the ADL was significantly lower (41+/-1 beats min(-1)). In dives greater than the ADL, f(H) reached extremely low values: f(H) during the last 5 mins of an 18 min dive was 6 beats min(-1). Dive f(H) and minimum instantaneous f(H) during dives declined significantly with increasing dive duration. Dive f(H) was independent of swim stroke frequency. This suggests that progressive bradycardia and peripheral vasoconstriction (including isolation of muscle) are primary determinants of blood oxygen depletion in diving emperor penguins. Maximum instantaneous surface interval f(H) in this study is the highest ever recorded for emperor penguins (256 beats min(-1)), equivalent to f(H) at V(O(2)) max., presumably facilitating oxygen loading and post-dive metabolism. The classic Scholander-Irving dive response in these emperor penguins contrasts with the absence of true bradycardia in diving ducks, cormorants, and other penguin species.

Heart rate regulation and extreme bradycardia in diving emperor penguins.

SUMMARY Blood gas analyses from emperor penguins ( Aptenodytes forsteri ) at
rest, and intravascular P O 2 profiles from
free-diving birds were obtained in order to examine hypoxemic tolerance and
utilization of the blood O 2 store during dives. Analysis of blood
samples from penguins at rest revealed arterial
 P O 2 s and O 2 contents of 68±7
mmHg (1 mmHg= 133.3 Pa) and 22.5±1.3 ml O 2 
dl –1 ( N =3) and venous values of 41±10 mmHg
and 17.4±2.9 ml O 2 dl –1 ( N =9).
Corresponding arterial and venous Hb saturations for a hemoglobin (Hb)
concentration of 18 g dl –1 were >91% and 70%,
respectively. Analysis of P O 2 profiles obtained
from birds equipped with intravascular P O 2 
electrodes and backpack recorders during dives revealed that (1) the decline
of the final blood P O 2 of a dive in relation to
dive duration was variable, (2) final venous
 P O 2 values spanned a 40-mmHg range at the
previously measured aerobic dive limit (ADL; dive duration associated with
onset of post-dive blood lactate accumulation), (3) final arterial, venous and
previously measured air sac P O 2 values were
indistinguishable in longer dives, and (4) final venous
 P O 2 values of longer dives were as low as
1–6 mmHg during dives. Although blood O 2 is not depleted at
the ADL, nearly complete depletion of the blood O 2 store occurs in
longer dives. This extreme hypoxemic tolerance, which would be catastrophic in
many birds and mammals, necessitates biochemical and molecular adaptations,
including a shift in the O 2 –Hb dissociation curve of the
emperor penguin in comparison to those of most birds. A relatively
higher-affinity Hb is consistent with blood P O 2 
values and O 2 contents of penguins at rest.

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K. V. Ponganis

Papers

Swimming velocities in otariids

Heart rates and swim speeds of emperor penguins diving under sea ice

Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice.

Heart rate regulation and extreme bradycardia in diving emperor penguins.

Returning on empty: extreme blood O2 depletion underlies dive capacity of emperor penguins.