Extreme bradycardia and tachycardia in the world's largest animal.

The biology of the blue whale has long fascinated physiologists because of the animal's extreme size. Despite high energetic demands from a large body, low mass-specific metabolic rates are likely powered by low heart rates. Diving bradycardia should slow blood oxygen depletion and enhance dive time available for foraging at depth. However, blue whales exhibit a high-cost feeding mechanism, lunge feeding, whereby large volumes of prey-laden water are intermittently engulfed and filtered during dives. This paradox of such a large, slowly beating heart and the high cost of lunge feeding represents a unique test of our understanding of cardiac function, hemodynamics, and physiological limits to body size. Here, we used an electrocardiogram (ECG)-depth recorder tag to measure blue whale heart rates during foraging dives as deep as 184 m and as long as 16.5 min. Heart rates during dives were typically 4 to 8 beats min-1 (bpm) and as low as 2 bpm, while after-dive surface heart rates were 25 to 37 bpm, near the estimated maximum heart rate possible. Despite extreme bradycardia, we recorded a 2.5-fold increase above diving heart rate minima during the powered ascent phase of feeding lunges followed by a gradual decrease of heart rate during the prolonged glide as engulfed water is filtered. These heart rate dynamics explain the unique hemodynamic design in rorqual whales consisting of a large-diameter, highly compliant, elastic aortic arch that allows the aorta to accommodate blood ejected by the heart and maintain blood flow during the long and variable pauses between heartbeats.

Penguin lungs and air sacs: implications for baroprotection, oxygen stores and buoyancy.

The anatomy and volume of the penguin respiratory system contribute significantly to pulmonary baroprotection, the body O2 store, buoyancy and hence the overall diving physiology of penguins. Therefore, three-dimensional reconstructions from computerized tomographic (CT) scans of live penguins were utilized to measure lung volumes, air sac volumes, tracheobronchial volumes and total body volumes at different inflation pressures in three species with different dive capacities [Adélie (Pygoscelis adeliae), king (Aptenodytes patagonicus) and emperor (A. forsteri) penguins]. Lung volumes scaled to body mass according to published avian allometrics. Air sac volumes at 30 cm H2O (2.94 kPa) inflation pressure, the assumed maximum volume possible prior to deep dives, were two to three times allometric air sac predictions and also two to three times previously determined end-of-dive total air volumes. Although it is unknown whether penguins inhale to such high volumes prior to dives, these values were supported by (a) body density/buoyancy calculations, (b) prior air volume measurements in free-diving ducks and (c) previous suggestions that penguins may exhale air prior to the final portions of deep dives. Based upon air capillary volumes, parabronchial volumes and tracheobronchial volumes estimated from the measured lung/airway volumes and the only available morphometry study of a penguin lung, the presumed maximum air sac volumes resulted in air sac volume to air capillary/parabronchial/tracheobronchial volume ratios that were not large enough to prevent barotrauma to the non-collapsing, rigid air capillaries during the deepest dives of all three species, and during many routine dives of king and emperor penguins. We conclude that volume reduction of airways and lung air spaces, via compression, constriction or blood engorgement, must occur to provide pulmonary baroprotection at depth. It is also possible that relative air capillary and parabronchial volumes are smaller in these deeper-diving species than in the spheniscid penguin of the morphometry study. If penguins do inhale to this maximum air sac volume prior to their deepest dives, the magnitude and distribution of the body O2 store would change considerably. In emperor penguins, total body O2 would increase by 75%, and the respiratory fraction would increase from 33% to 61%. We emphasize that the maximum pre-dive respiratory air volume is still unknown in penguins. However, even lesser increases in air sac volume prior to a dive would still significantly increase the O2 store. More refined evaluations of the respiratory O2 store and baroprotective mechanisms in penguins await further investigation of species-specific lung morphometry, start-of-dive air volumes and body buoyancy, and the possibility of air exhalation during dives.

Myoglobin production in emperor penguins.

Increased oxygen storage is essential to the diving capacities of marine mammals and seabirds. However, the molecular mechanisms underlying this adaptation are unknown. Myoglobin (Mb) and Mb mRNA concentrations were analyzed in emperor penguin (Aptenodytes forsteri) adults and chicks with spectrophotometric and RNase protection assays to evaluate production of their large Mb-bound O(2) stores. Mean pectoral Mb concentration and Mb mRNA content increased throughout the pre-fledging period and were 15-fold and 3-fold greater, respectively, in adults than in 3.5 month old chicks. Mean Mb concentration in 5.9 month old juveniles was 2.7+/-0.4 g 100 g(-1) muscle (44% that of wild adults), and in adults that had been captive all their lives it was 3.7+/-0.1 g 100 g(-1) muscle. The Mb and Mb mRNA data are consistent with regulation of Mb production at the level of transcription as in other animals. Significant Mb and Mb mRNA production occurred in chicks and young juveniles even without any diving activity. The further increase in adult Mb concentrations appears to require the exercise/hypoxia of diving because Mb concentration in captive, non-diving adults only reached 60% of that of wild adults. The much greater relative increase in Mb concentration than in Mb mRNA content between young chicks and adults suggests that there is not a simple 1:1 relationship between Mb mRNA content and Mb concentration. Nutritional limitation in young chicks and post-transcriptional regulation of Mb concentration may also be involved.

Hypoxemic and ischemic tolerance in emperor penguins.

Oxygen store depletion and a diving bradycardia in emperor penguins (Aptenodytes forsteri) expose tissues to critical levels of hypoxemia and ischemia. To assess the prevention of re-perfusion injury and reactive oxygen species (ROS) damage in emperor penguins, superoxide radical production, lipid peroxidation (thiobarbituric acid reactive substances (TBARS)), and antioxidant enzyme activity profiles in biopsy samples from muscle and liver were determined and compared to those in the chicken and 8 species of flighted marine birds (non-divers and plunge divers). In muscle of emperor penguins, superoxide production and TBARS levels were not distinctly different from those in the other species; among the antioxidant enzymes, catalase (CAT) and glutathione-S-transferase (GST) activities were significantly elevated above all species. In the liver of emperor penguins, TBARS levels were not significantly different from other species; only CAT activity was significantly elevated, although GST and glutathione peroxidase (GPX) activities were 2-3 times higher than those in other species. The potential for ROS formation and lipid peroxidation is not reduced in the pectoral muscle or liver of the emperor penguin. Scavenging of hydrogen peroxide by CAT and the conjugation of glutathione with reactive intermediates and peroxides by GST and GPX appear to be important in the prevention of ROS damage and re-perfusion injury in these birds.

Investigation of the potential for vascular bubble formation in a repetitively diving dolphin.

The production of venous gas emboli (VGE) resulting from altered dive behavior is postulated as contributing to the stranding of beaked whales exposed to mid-frequency active sonar. To test whether nitrogen gas uptake during repetitive breath-hold diving is sufficient for asymptomatic VGE formation in odontocetes, a bottlenose dolphin (Tursiops truncatus Montagu) was trained to perform 10-12 serial dives with 60 s surface intervals to depths of 30, 50, 70 or 100 m. The dolphin remained at the bottom depth for 90 s on each dive. Doppler and/or two-dimensional imaging ultrasound did not detect VGE in the portal and brachiocephalic veins following a dive series. Van Slyke analyses of serial, post-dive blood samples drawn from the fluke yielded blood nitrogen partial pressure (P(N(2))) values that were negligibly different from control samples. Mean heart rate (HR; +/-1 s.d.) recorded during diving was 50+/-3 beats min(-1) and was not significantly different between the 50, 70 and 100 m dive sessions. The absence of VGE and elevated blood P(N(2)) during post-dive periods do not support the hypothesis that N(2) supersaturation during repetitive dives contributes to VGE formation in the dolphin. The diving HR pattern and the presumed rapid N(2) washout during the surface-interval tachycardia probably minimized N(2) accumulation in the blood during dive sessions.

O2 store management in diving emperor penguins.

In order to further define O(2) store utilization during dives and understand the physiological basis of the aerobic dive limit (ADL, dive duration associated with the onset of post-dive blood lactate accumulation), emperor penguins (Aptenodytes forsteri) were equipped with either a blood partial pressure of oxygen (P(O(2))) recorder or a blood sampler while they were diving at an isolated dive hole in the sea ice of McMurdo Sound, Antarctica. Arterial P(O(2)) profiles (57 dives) revealed that (a) pre-dive P(O(2)) was greater than that at rest, (b) P(O(2)) transiently increased during descent and (c) post-dive P(O(2)) reached that at rest in 1.92+/-1.89 min (N=53). Venous P(O(2)) profiles (130 dives) revealed that (a) pre-dive venous P(O(2)) was greater than that at rest prior to 61% of dives, (b) in 90% of dives venous P(O(2)) transiently increased with a mean maximum P(O(2)) of 53+/-18 mmHg and a mean increase in P(O(2)) of 11+/-12 mmHg, (c) in 78% of dives, this peak venous P(O(2)) occurred within the first 3 min, and (d) post-dive venous P(O(2)) reached that at rest within 2.23+/-2.64 min (N=84). Arterial and venous P(O(2)) values in blood samples collected 1-3 min into dives were greater than or near to the respective values at rest. Blood lactate concentration was less than 2 mmol l(-1) as far as 10.5 min into dives, well beyond the known ADL of 5.6 min. Mean arterial and venous P(N(2)) of samples collected at 20-37 m depth were 2.5 times those at the surface, both being 2.1+/-0.7 atmospheres absolute (ATA; N=3 each), and were not significantly different. These findings are consistent with the maintenance of gas exchange during dives (elevated arterial and venous P(O(2)) and P(N(2)) during dives), muscle ischemia during dives (elevated venous P(O(2)), lack of lactate washout into blood during dives), and arterio-venous shunting of blood both during the surface period (venous P(O(2)) greater than that at rest) and during dives (arterialized venous P(O(2)) values during descent, equivalent arterial and venous P(N(2)) values during dives). These three physiological processes contribute to the transfer of the large respiratory O(2) store to the blood during the dive, isolation of muscle metabolism from the circulation during the dive, a decreased rate of blood O(2) depletion during dives, and optimized loading of O(2) stores both before and after dives. The lack of blood O(2) depletion and blood lactate elevation during dives beyond the ADL suggests that active locomotory muscle is the site of tissue lactate accumulation that results in post-dive blood lactate elevation in dives beyond the ADL.

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

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.

Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirostris).

Blood gases (P(O)2, P(CO)2, pH), oxygen content, hematocrit and hemoglobin concentration were measured during rest-associated apneas of nine juvenile northern elephant seals. In conjunction with blood volume determinations, these data were used to determine total blood oxygen stores, the rate and magnitude of blood O(2) depletion, the contribution of the blood O(2) store to apneic metabolic rate, and the degree of hypoxemia that occurs during these breath-holds. Mean body mass was 66+/-9.7 kg (+/- s.d.); blood volume was 196+/-20 ml kg(-1); and hemoglobin concentration was 23.5+/-1.5 g dl(-1). Rest apneas ranged in duration from 3.1 to 10.9 min. Arterial P(O)2 declined exponentially during apnea, ranging between a maximum of 108 mmHg and a minimum of 18 mmHg after a 9.1 min breath-hold. Venous P(O)2 values were indistinguishable from arterial values after the first minute of apnea; the lowest venous P(O)2 recorded was 15 mmHg after a 7.8 min apnea. O(2) contents were also similar between the arterial and venous systems, declining linearly at rates of 2.3 and 2.0 ml O(2) dl(-1) min(-1), respectively, from mean initial values of 27.2 and 26.0 ml O(2) dl(-1). These blood O(2) depletion rates are approximately twice the reported values during forced submersion and are consistent with maintenance of previously measured high cardiac outputs during rest-associated breath-holds. During a typical 7-min apnea, seals consumed, on average, 56% of the initial blood O(2) store of 52 ml O(2) kg(-1); this contributed 4.2 ml O(2) kg(-1) min(-1) to total body metabolic rate during the breath-hold. Extreme hypoxemic tolerance in these seals was demonstrated by arterial P(O)2 values during late apnea that were less than human thresholds for shallow-water blackout. Despite such low P(O)2s, there was no evidence of significant anaerobic metabolism, as changes in blood pH were minimal and attributable to increased P(CO)2. These findings and the previously reported lack of lactate accumulation during these breath-holds are consistent with the maintenance of aerobic metabolism even at low oxygen tensions during rest-associated apneas. Such hypoxemic tolerance is necessary in order to allow dissociation of O(2) from hemoglobin and provide effective utilization of the blood O(2) store.

Intravascular pressure profiles in elephant seals: hypotheses on the caval sphincter, extradural vein and venous return to the heart.

In order to evaluate hemodynamics in the complex vascular system of phocid seals, intravascular pressure profiles were measured during periods of rest-associated apnea in young elephant seals (Mirounga angustirostris). There were no significant differences between apneic and eupneic mean arterial pressures. During apnea, venous pressure profiles (pulmonary artery, thoracic portion of the vena cava (thoracic vena cava), extradural vein, and hepatic sinus) demonstrated only minor, transient fluctuations. During eupnea, all venous pressure profiles were dominated by respiratory fluctuations. During inspiration, pressures in the thoracic vena cava and extradural vein decreased -9 to -21 mm Hg, and -9 to -17 mm Hg, respectively. In contrast, hepatic sinus pressure increased 2-6 mm Hg during inspiration. Nearly constant hepatic sinus and intrathoracic vascular pressure profiles during the breath-hold period are consistent with incomplete constriction of the caval sphincter during these rest-associated apneas. During eupnea, negative inspiratory intravascular pressures in the chest ("the respiratory pump") should augment venous return via both the venae cavae and the extradural vein. It is hypothesized that, in addition to the venae cavae, the prominent para-caval venous system of phocid seals (i.e., the extradural vein) is necessary to allow adequate venous return for maintenance of high cardiac outputs and blood pressure during eupnea.

Cardiac output and muscle blood flow during rest-associated apneas of elephant seals.

In order to evaluate hemodynamics and blood flow during rest-associated apnea in young elephant seals (Mirounga angustirostris), cardiac outputs (CO, thermodilution), heart rates (HR), and muscle blood flow (MBF, laser Doppler flowmetry) were measured. Mean apneic COs and HRs of three seals were 46% and 39% less than eupneic values, respectively (2.1+/-0.3 vs. 4.0+/-0.1 mL kg(-1) s(-1), and 54+/-6 vs. 89+/-14 beats min(-1)). The mean apneic stroke volume (SV) was not significantly different from the eupneic value (2.3+/-0.2 vs. 2.7+/-0.5 mL kg(-1)). Mean apneic MBF of three seals was 51% of the eupneic value. The decline in MBF during apnea was gradual, and variable in both rate and magnitude. In contrast to values previously documented in seals during forced submersions (FS), CO and SV during rest-associated apneas were maintained at levels characteristic of previously published values in similarly-sized terrestrial mammals at rest. Apneic COs of such magnitude and incomplete muscle ischemia during the apnea suggest that (1) most organs are not ischemic during rest-associated apneas, (2) the blood O(2) depletion rate is greater during rest-associated apneas than during FS, and (3) the blood O(2) store is not completely isolated from muscle during rest-associated apneas.

Air sac PO2 and oxygen depletion during dives of emperor penguins.

In order to determine the rate and magnitude of respiratory O2 depletion during dives of emperor penguins (Aptenodytes forsteri), air sac O2 partial pressure (PO2) was recorded in 73 dives of four birds at an isolated dive hole. These results were evaluated with respect to hypoxic tolerance, the aerobic dive limit (ADL; dive duration beyond which there is post-dive lactate accumulation) and previously measured field metabolic rates (FMRs). 55% of dives were greater in duration than the previously measured 5.6-min ADL. PO2 and depth profiles revealed compression hyperoxia and gradual O2 depletion during dives. 42% of final PO2s during the dives (recorded during the last 15 s of ascent) were <20 mmHg (<2.7 kPa). Assuming that the measured air sac PO2 is representative of the entire respiratory system, this implies remarkable hypoxic tolerance in emperors. In dives of durations greater than the ADL, the calculated end-of-dive air sac O2 fraction was <4%. The respiratory O2 store depletion rate of an entire dive, based on the change in O2 fraction during a dive and previously measured diving respiratory volume, ranged from 1 to 5 ml O2 kg(-1) min(-1) and decreased exponentially with diving duration. The mean value, 2.1+/-0.8 ml O2 kg(-1) min(-1), was (1) 19-42% of previously measured respiratory O(2) depletion rates during forced submersions and simulated dives, (2) approximately one-third of the predicted total body resting metabolic rate and (3) approximately 10% of the measured FMR. These findings are consistent with a low total body metabolic rate during the dive.

Regional heterothermy and conservation of core temperature in 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.

Stroke frequencies of emperor penguins diving under sea ice.

During diving, intermittent swim stroke patterns, ranging from burst/coast locomotion to prolonged gliding, represent potential energy conservation mechanisms that could extend the duration of aerobic metabolism and, hence, increase the aerobic dive limit (ADL, dive duration associated with onset of lactate accumulation). A 5.6 min ADL for emperor penguins had been previously determined with lactate measurements after dives of <50 m depth. In order to assess locomotory patterns during such dives, longitudinal acceleration was measured with an attached accelerometer in 44 dives of seven adult birds diving from an isolated dive hole in the sea ice of McMurdo Sound, Antarctica. Detection of wing strokes in processed accelerometer data was verified in selected birds with analysis of simultaneous Crittercam underwater video footage. Mean dive duration of birds equipped with the accelerometer and a time-depth recorder (TDR) was 5.7+/-2.2 min; 48% of these dives were greater than the measured 5.6 min ADL (ADL(M)). Highest stroke frequencies (0.92+/-0.31 Hz, N=981) occurred during the initial descent to 12 m depth. Swimming effort was reduced to a mean stroke frequency <0.70 Hz during other phases of the dive (while traveling below 12 m depth, during foraging ascents/descents to and from the sub-ice surface, and during final ascents to exit). The longest stroke interval (8.6 s) occurred during a feeding excursion to the undersurface of the ice. In dives >ADL(M), mean stroke frequency during travel segments was significantly less than that in dives 10 s) periods of prolonged gliding during these shallow (<60 m) foraging dives. However, a stroke/glide pattern was evident with more than 50% of strokes associated with a stroke interval >1.6 s, and with lower stroke frequency associated with increased dive duration.

Energetic cost of foraging in free-diving emperor penguins.

Hypothesizing that emperor penguins (Aptenodytes forsteri) would have higher daily energy expenditures when foraging for their food than when being hand-fed and that the increased expenditure could represent their foraging cost, we measured field metabolic rates (FMR; using doubly labeled water) over 4-d periods when 10 penguins either foraged under sea ice or were not allowed to dive but were fed fish by hand. Surprisingly, penguins did not have higher rates of energy expenditure when they dove and captured their own food than when they did not forage but were given food. Analysis of time-activity and energy budgets indicated that FMR was about 1.7 x BMR (basal metabolic rate) during the 12 h d(-1) that penguins were lying on sea ice. During the remaining 12 h d(-1), which we termed their "foraging period" of the day, the birds were alert and active (standing, preening, walking, and either free diving or being hand-fed), and their FMR was about 4.1 x BMR. This is the lowest cost of foraging estimated to date among the eight penguin species studied. The calculated aerobic diving limit (ADL(C)), determined with the foraging period metabolic rate of 4.1 x BMR and known O(2) stores, was only 2.6 min, which is far less than the 6-min ADL previously measured with postdive lactate analyses in emperors diving under similar conditions. This indicates that calculating ADL(C) from an at-sea or foraging-period metabolic rate in penguins is not appropriate. The relatively low foraging cost for emperor penguins contributes to their relatively low total daily FMR (2.9 x BMR). The allometric relationship for FMR in eight penguin species, including the smallest and largest living representatives, is kJ d(-1)=1,185 kg(0.705).

Temperature regulation in emperor penguins foraging under sea ice.

Inferior vena caval (IVC) and anterior abdominal (AA) temperatures were recorded in seven emperor penguins (Aptenodytes forsteri) foraging under sea ice in order to evaluate the hypothesis that hypothermia-induced metabolic suppression might extend aerobic diving time. Diving durations ranged from 1 to 12.5 min, with 39% of dives greater than the measured aerobic dive limit of 5.6 min. Anterior abdominal temperature decreased progressively throughout dives, and partially returned to pre-dive values during surface intervals. The lowest AA temperature was 19 degrees C. However, mean AA temperatures during dives did not correlate with diving durations. In six of seven penguins, only minor fluctuations in IVC temperatures occurred during diving. These changes were often elevations in temperature. In the one exception, although IVC temperatures decreased, the reductions were less than those in the anterior abdomen and did not correlate with diving durations. Because of these findings, we consider it unlikely that regional hypothermia in emperor penguins leads to a significant reduction in oxygen consumption of the major organs within the abdominal core. Rather, temperature profiles during dives are consistent with a model of regional heterothermy with conservation of core temperature, peripheral vasoconstriction, and cooling of an outer body shell.

Effects of training on forced submersion responses in harbor seals.

In several pinniped species, the heart rates observed during unrestrained dives are frequently higher than the severe bradycardias recorded during forced submersions. To examine other physiological components of the classic 'dive response' during such moderate bradycardias, a training protocol was developed to habituate harbor seals (Phoca vitulina) to short forced submersions. Significant changes were observed between physiological measurements made during naive and trained submersions (3-3.5 min). Differences were found in measurements of heart rate during submersion (naive 18+/-4.3 beats min(-1) versus trained 35+/-3.4 beats min(-1)), muscle blood flow measured using laser-Doppler flowmetry (naive 1.8+/-0.8 ml min(-1) 100 g(-1) versus trained 5.8+/-3.9 ml min(-1) 100 g(-1)), change in venous P(O(2)) (naive -0.44+/-1.25 kPa versus trained -1.48+/-0.76 kPa) and muscle deoxygenation rate (naive -0.67+/-0.27 mvd s(-1) versus trained -0.51+/-0.18 mvd s(-1), a relative measure of muscle oxygenation provided by the Vander Niroscope, where mvd are milli-vander units). In contrast to the naive situation, the post-submersion increase in plasma lactate levels was only rarely significant in trained seals. Resting eupneic (while breathing) heart rate and total oxygen consumption rates (measured in two seals) were not significantly different between the naive and trained states. This training protocol revealed that the higher heart rate and greater muscle blood flow in the trained seals were associated with a lower muscle deoxygenation rate, presumably secondary to greater extraction of blood O(2) during trained submersions. Supplementation of muscle oxygenation by blood O(2) delivery during diving would increase the rate of blood O(2) depletion but could prolong the duration of aerobic muscle metabolism during diving. This alteration of the dive response may increase the metabolic efficiency of diving.

Energetics of surface swimming in Brandt's cormorants (Phalacrocorax penicillatus brandt).

The energy requirements of Brandt's cormorants (Phalacrocorax penicillatus) during surface swimming were measured in birds swimming under a metabolic chamber in a water flume. From the oxygen consumption recordings, we extrapolated the metabolic rate and cost of transport at water speeds ranging from 0 to 1.3 m s(-)(1). In still water, the birds' mean mass-specific rate of oxygen consumption ( V(O2)) while floating at the surface was 20.2 ml O(2 )min(-)(1 )kg(-)(1), 2.1 times the predicted resting metabolic rate. During steady-state voluntary swimming against a flow, their V(O2) increased with water speed, reaching 74 ml O(2 )min(-)(1 )kg(-)(1) at 1.3 m s(-)(1), which corresponded to an increase in metabolic rate from 11 to 25 W kg(-)(1). The cost of transport decreased with swimming velocity, approaching a minimum of 19 J kg(-)(1 )m(-)(1) for a swimming speed of 1.3 m s(-)(1). Surface swimming in the cormorant costs approximately 18 % less than sub-surface swimming. This confirms similar findings in tufted ducks (Aythya fuligula) and supports the hypothesis that increased energy requirements are necessary in these birds during diving to overcome buoyancy and heat loss during submergence.

Sub-ice foraging behavior of emperor penguins.

Emperor penguins (Aptenodytes forsteri) were equipped with a remote underwater video camera, the Crittercam, to evaluate sub-ice foraging behavior while the birds dived from an isolated dive hole. Three birds dived and foraged successfully for 1 h periods after being trained to wear and to dive with a harness for camera attachment. Video and depth profile recordings revealed that emperor penguins travel at shallow depths (<50 m), ascend to the undersurface of the ice to feed on fish, and descend back to depth to return to the exit hole. Although the mean durations of dives of individual birds with the Crittercam were 21-35 % shorter than the diving durations of these same birds without the camera, the dive profiles in both situations were similar, thus demonstrating a similar foraging strategy in birds diving without the camera. Despite shorter diving durations with the camera, the penguins were still successful at prey capture in 80 % of 91 dives greater than 1 min in duration. Prey included the sub-ice fish Pagothenia borchgrevinki. Hunting ascents (from depth to within 5 m of the surface) occurred in 85 % of dives, ranged from zero to three per dive, and were associated with successful prey capture in 77 % of 128 ascents. Occasionally, several fish were captured during a single ascent. These observations and this application of video technology create a model for further physiological and behavioral studies of foraging, and also emphasize the potential importance of shallow dives as sources of food intake for emperor penguins during foraging trips to sea.

Diving physiology of birds: a history of studies on polar species.

Our knowledge of avian diving physiology has been based primarily on research with polar species. Since Scholander's 1940 monograph, research has expanded from examination of the 'diving reflex' to studies of free-diving birds, and has included laboratory investigations of oxygen stores, muscle adaptations, pressure effects, and cardiovascular/metabolic responses to swimming exercise. Behavioral and energetic studies at sea have shown that common diving durations of many avian species exceed the calculated aerobic diving limits (ADL). Current physiological research is focused on factors, such as heart rate and temperature, which potentially affect the diving metabolic rate and duration of aerobic diving.

Development of diving capacity in emperor penguins.

To compare the diving capacities of juvenile and adult emperor penguins Aptenodytes forsteri, and to determine the physiological variables underlying the diving ability of juveniles, we monitored diving activity in juvenile penguins fitted with satellite-linked time/depth recorders and examined developmental changes in body mass (Mb), hemoglobin concentration, myoglobin (Mb) content and muscle citrate synthase and lactate dehydrogenase activities. Diving depth, diving duration and time-at-depth histograms were obtained from two fledged juveniles during the first 2.5 months after their depature from the Cape Washingon colony in the Ross Sea, Antarctica. During this period, values of all three diving variables increased progressively. After 8-10 weeks at sea, 24-41 % of transmitted maximum diving depths were between 80 and 200 m. Although most dives lasted less than 2 min during the 2 month period, 8-25 % of transmitted dives in the last 2 weeks lasted 2-4 min. These values are lower than those previously recorded in adults during foraging trips. Of the physiological variables examined during chick and juvenile development, only Mb and Mb content did not approach adult values. In both near-fledge chicks and juveniles, Mb was 50-60 % of adult values and Mb content was 24-31 % of adult values. This suggests that the increase in diving capacity of juveniles at sea will be most dependent on changes in these factors.