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Ponganis, PJ, St Leger J, Scadeng M.  2015.  Penguin lungs and air sacs: implications for baroprotection, oxygen stores and buoyancy. Journal of Experimental Biology. 218:720-730.   10.1242/jeb.113647   AbstractWebsite

The anatomy and volume of the penguin respiratory system contribute significantly to pulmonary baroprotection, the body O-2 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 [Adelie (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 O-2 store would change considerably. In emperor penguins, total body O-2 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 O-2 store. More refined evaluations of the respiratory O-2 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.

Wright, AK, Ponganis KV, McDonald BI, Ponganis PJ.  2014.  Heart rates of emperor penguins diving at sea: implications for oxygen store management. Marine Ecology Progress Series. 496:85-98.   10.3354/meps10592   AbstractWebsite

Heart rate (f(H)) contributes to control of blood oxygen (O-2) depletion through regulation of the magnitude of pulmonary gas exchange and of peripheral blood flow in diving vertebrates such as penguins. Therefore, we measured H during foraging trip dives of emperor penguins Aptenodytes forsteri equipped with digital electrocardiogram (ECG) recorders and time depth recorders (TDRs). Median dive f(H) (total heartbeats/duration, 64 beats min(-1)) was higher than resting H (56 beats min(-1)) and was negatively related to dive duration. Median dive f(H) in dives greater than the 5.6 min aerobic dive limit (ADL; dive duration associated with the onset of a net accumulation of lactic acid above resting levels) was significantly less than the median dive f(H) of dives less than the ADL (58 vs. 66 beats min(-1)). f(H) profile patterns differed between shallow (<50 m) and deep dives (>250 m), with values usually declining to levels near resting f(H) in shallow, short-duration dives, and to levels as low as 10 beats min(-1) during the deepest segments of deep dives. The total number of heartbeats in a dive was variable in shallow dives and consistently high in deep dives. A true bradycardia (f(H) below resting levels) during segments of 31% of shallow and deep dives of emperor penguins is consistent with reliance on myoglobin-bound O-2 stores for aerobic muscle metabolism that is especially accentuated during the severe bradycardias of deep dives. Although f(H) is low during the deepest segments of deep dives, the total number and distribution of heartbeats in deep, long dives suggest that pulmonary gas exchange and peripheral blood flow primarily occur at shallow depths.

Ponganis, PJ, Meir JU, Williams CL.  2010.  Oxygen store depletion and the aerobic dive limit in emperor penguins. Aquatic Biology. 8:237-245.   10.3354/ab00216   AbstractWebsite

The aerobic dive limit (ADL), dive duration associated with the onset of post-dive blood lactate elevation, has been widely used in the interpretation of diving physiology and diving behavior. However, its physiological basis is incompletely understood, and in most studies, ADLs are simply calculated with an O(2) store/O(2) consumption formula. To better understand the ADL, research has been conducted on emperor penguins diving at an isolated dive hole. This work has revealed that O(2) stores are greater than previously estimated, and that the rate of depletion of those O(2) stores appears to be regulated primarily through a diving bradycardia and the efficiency of swimming. Blood and respiratory O(2) stores are not depleted at the 5.6 min ADL determined by post-dive blood lactate measurements. It is hypothesized that muscle, isolated from the circulation during a dive, is the primary source of lactate accumulation. To predict this 5.6 min ADL for these shallow dives at the isolated dive hole with the classic O(2) store/O(2) consumption formula, an O(2) consumption rate of 2x the predicted metabolic rate of a penguin at rest is required. In contrast, if the formula is used to calculate an ADL that is defined as the time for all consumable O(2) stores to be depleted, then a 23.1 min dive, in which final venous partial pressure of oxygen (P(O2)) was 6 mm Hg (0.8 kPa), represents such a maximum limit and demonstrates that an O(2) consumption rate of about 0.5x the predicted rate of an emperor penguin at rest is required in the formula.

Ponganis, PJ, Stockard TK, Meir JU, Williams CL, Ponganis KV, Howard R.  2009.  O-2 store management in diving emperor penguins. Journal of Experimental Biology. 212:217-224.   10.1242/jeb.026096   AbstractWebsite

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-O2) recorder or a blood sampler while they were diving at an isolated dive hole in the sea ice of McMurdo Sound, Antarctica. Arterial P-O2 profiles (57 dives) revealed that (a) pre-dive P-O2 was greater than that at rest, (b) P-O2 transiently increased during descent and (c) post-dive P-O2 reached that at rest in 1.92 +/- 1.89 min (N=53). Venous P-O2 profiles (130 dives) revealed that (a) pre-dive venous P-O2 was greater than that at rest prior to 61% of dives, (b) in 90% of dives venous P-O2 transiently increased with a mean maximum P-O2 of 53 +/- 18 mmHg and a mean increase in P-O2 of 11 +/- 12 mmHg, (c) in 78% of dives, this peak venous P-O2 occurred within the first 3 min, and (d) post-dive venous P-O2 reached that at rest within 2.23 +/- 2.64 min (N=84). Arterial and venous P-O2 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-N2 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-O2 and P-N2 during dives), muscle ischemia during dives (elevated venous P-O2, lack of lactate washout into blood during dives), and arterio-venous shunting of blood both during the surface period (venous P-O2 greater than that at rest) and during dives (arterialized venous P-O2 values during descent, equivalent arterial and venous P-N2 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.

Meir, JU, Stockard TK, Williams CL, Ponganis KV, Ponganis PJ.  2008.  Heart rate regulation and extreme bradycardia in diving emperor penguins. Journal of Experimental Biology. 211:1169-1179.   10.1242/jeb.013235   AbstractWebsite

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 (fH significantly < f(H) at rest) occurred during diving [dive fH (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-O2 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.

Kooyman, GL, Ponganis PJ.  2007.  The initial journey of juvenile emperor penguins. Aquatic Conservation-Marine and Freshwater Ecosystems. 17:S37-S43.   10.1002/aqc.930   AbstractWebsite

1. The first major journey of emperor penguins, among several in their lifetime, is the juveniles' dispersal from their natal colony on a trip that takes them beyond Antarctic waters. The route taken by fledglings from Cape Washington (74.5 degrees S; 165.4 degrees E) was Studied by applying satellite transmitters to ten individuals during December 1994-1996. In January 2001 transmitters with longer transmission capacity were also applied to six hand-fed fledglings, which had been held captive for one month while attaining a body mass exceeding that of wild birds. These post-captive birds were released at the ice edge of McMurdo Sound (77.5 degrees S; 165.0 degrees E), which is in the vicinity of other emperor penguin colonies, and 320km south of their natal colony of Cape Washington. 2. Independent of their parents, the wild birds travelled north-east for the next two months, reaching locations as low as 57 degrees S. The post-captive birds travelled north also, but their trek reached only to about 63 degrees S before they turned south, or remained near their most northerly position from March through May. 3. It was concluded that among colonies in the southern Ross Sea: (a) most healthy fledglings Survive at least the first two months at sea, feeding themselves as they go; (b) the Cape Washington fledglings travelled as far north as 57 degrees S, and much of this journey was in ice free waters; (c) by April, the post-captive birds reached at least as far as the large-scale pack ice edge and possibly beyond the edge Lit 63 degrees S; (d) by early March the trend north ends, and by about late March the birds travel to, or remain near the northern ice edge. 4. The reason the birds travel so far north remains a mystery. Copyright (c) 2008 John Wiley & Sons, Ltd.

Ponganis, PJ, Van Dam RP, Levenson DH, Knower T, Ponganis KV, Marshall G.  2003.  Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology. 135:477-487.   10.1016/s1095-6433(03)00133-8   AbstractWebsite

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 degreesC (n = 101 dives in five birds), pectoral muscle: 37.8 +/- 0.1 degreesC (n = 71 dives in three birds) and axillary/brachial veins: 37.9 +/- 0.1 degreesC (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 degreesC). In contrast, grand mean temperatures in the wing vein, foot vein and lumbar subcutaneous tissue during dives were 7.6 +/- 0.7 degreesC (n = 157 dives in three birds), 20.2 +/- 1.2 degreesC (n = 69 in three birds) and 35.2 +/- 0.2 degreesC (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 T during rest periods to a grand mean of 15.0 +/- 0.7 degreesC 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 degreesC more closely than the anterior abdominal temperatures (19-30 degreesC) 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. (C) 2003 Elsevier Science Inc. All fights reserved.

Ponganis, PJ, Kooyman GL.  2000.  Diving physiology of birds: a history of studies on polar species. Comparative Biochemistry and Physiology a-Molecular and Integrative Physiology. 126:143-151.   10.1016/s1095-6433(00)00208-7   AbstractWebsite

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. (C) 2000 Elsevier Science Inc. All rights reserved.