K. V. Ponganis

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.

Heart rate regulation and extreme bradycardia in diving emperor penguins

SUMMARY To investigate the diving heart rate (fH) 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 (fH significantly<fH at rest) occurred during diving [dive fH (total beats/duration)=57±2 beats min–1, fH 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 fH=85±3 beats min–1, whereas fH in dives greater than the ADL was significantly lower (41±1 beats min–1). In dives greater than the ADL, fH reached extremely low values: fH during the last 5 mins of an 18 min dive was 6 beats min–1. Dive fH and minimum instantaneous fH during dives declined significantly with increasing dive duration. Dive fH 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 fH in this study is the highest ever recorded for emperor penguins (256 beats min–1), equivalent to fH at V̇O2 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.

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

SUMMARY Blood gas analyses from emperor penguins (Aptenodytes forsteri) at rest, and intravascular PO2 profiles from free-diving birds were obtained in order to examine hypoxemic tolerance and utilization of the blood O2 store during dives. Analysis of blood samples from penguins at rest revealed arterial PO2s and O2 contents of 68±7 mmHg (1 mmHg= 133.3 Pa) and 22.5±1.3 ml O2 dl–1 (N=3) and venous values of 41±10 mmHg and 17.4±2.9 ml O2 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 PO2 profiles obtained from birds equipped with intravascular PO2 electrodes and backpack recorders during dives revealed that (1) the decline of the final blood PO2 of a dive in relation to dive duration was variable, (2) final venous PO2 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 PO2 values were indistinguishable in longer dives, and (4) final venous PO2 values of longer dives were as low as 1–6 mmHg during dives. Although blood O2 is not depleted at the ADL, nearly complete depletion of the blood O2 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 O2–Hb dissociation curve of the emperor penguin in comparison to those of most birds. A relatively higher-affinity Hb is consistent with blood PO2 values and O2 contents of penguins at rest.

O2 store management in diving emperor penguins

SUMMARY In order to further define O2 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 (PO2) recorder or a blood sampler while they were diving at an isolated dive hole in the sea ice of McMurdo Sound, Antarctica. Arterial PO2 profiles (57 dives) revealed that (a) pre-dive PO2 was greater than that at rest, (b) PO2 transiently increased during descent and (c) post-dive PO2 reached that at rest in 1.92±1.89 min (N=53). Venous PO2 profiles (130 dives) revealed that (a) pre-dive venous PO2 was greater than that at rest prior to 61% of dives, (b) in 90% of dives venous PO2 transiently increased with a mean maximum PO2 of 53±18 mmHg and a mean increase in PO2 of 11±12 mmHg, (c) in 78% of dives, this peak venous PO2 occurred within the first 3 min, and (d) post-dive venous PO2 reached that at rest within 2.23±2.64 min (N=84). Arterial and venous PO2 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 PN2 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 PO2 and PN2 during dives), muscle ischemia during dives (elevated venous PO2, lack of lactate washout into blood during dives), and arterio-venous shunting of blood both during the surface period (venous PO2 greater than that at rest) and during dives (arterialized venous PO2 values during descent, equivalent arterial and venous PN2 values during dives). These three physiological processes contribute to the transfer of the large respiratory O2 store to the blood during the dive, isolation of muscle metabolism from the circulation during the dive, a decreased rate of blood O2 depletion during dives, and optimized loading of O2 stores both before and after dives. The lack of blood O2 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.

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

SUMMARY 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 O2 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.