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2017
Kooyman, GL, Ponganis PJ.  2017.  Rise and fall of Ross Sea emperor penguin colony populations: 2000 to 2012. Antarctic Science. 29:201-208.   10.1017/s0954102016000559   AbstractWebsite

There are seven emperor penguin (Aptenodytes forsteri) colonies distributed throughout the traditional boundaries of the Ross Sea from Cape Roget to Cape Colbeck. This coastline is c. 10% of the entire coast of Antarctica. From 2000 to 2012, there has been a nearly continuous record of population size of most, and sometimes all, of these colonies. Data were obtained by analysing aerial photographs. We found large annual variations in populations of individual colonies, and conclude that a trend from a single emperor penguin colony may not be a good environmental sentinel. There are at least four possibilities for census count fluctuations: i) this species is not bound to a nesting site like other penguins, and birds move within the colony and possibly to other colonies, ii) harsh environmental conditions cause a die-off of chicks in the colony or of adults elsewhere, iii) the adults skip a year of breeding if pre-breeding foraging is inadequate and iv) if sea ice conditions are unsatisfactory at autumn arrival of the adults, they skip breeding or go elsewhere. Such variability indicates that birds at all Ross Sea colonies should be counted annually if there is to be any possibility of understanding the causes of population changes.

Tift, MS, Huckstadt LA, McDonald BI, Thorson PH, Ponganis PJ.  2017.  Flipper stroke rate and venous oxygen levels in free-ranging California sea lions. Journal of Experimental Biology. 220:1533-1540.   10.1242/jeb.152314   AbstractWebsite

The depletion rate of the blood oxygen store, development of hypoxemia and dive capacity are dependent on the distribution and rate of blood oxygen delivery to tissues while diving. Although blood oxygen extraction by working muscle would increase the blood oxygen depletion rate in a swimming animal, there is little information on the relationship between muscle workload and blood oxygen depletion during dives. Therefore, we examined flipper stroke rate, a proxy of muscle workload, and posterior vena cava oxygen profiles in four adult female California sea lions (Zalophus californianus) during foraging trips at sea. Flipper stroke rate analysis revealed that sea lions minimized muscle metabolism with a stroke-glide strategy when diving, and exhibited prolonged glides during the descent of deeper dives (>100 m). During the descent phase of these deep dives, 55 +/- 21% of descent was spent gliding, with the longest glides lasting over 160 s and covering a vertical distance of 340 m. Animals also consistently glided to the surface from 15 to 25 m depth during these deeper dives. Venous hemoglobin saturation (SO2) profiles were highly variable throughout dives, with values occasionally increasing during shallow dives. The relationship between SO2 and flipper stroke rate was weak during deeper dives, while this relationship was stronger during shallow dives. We conclude that (1) the depletion of oxygen in the posterior vena cava in deep-diving sea lions is not dependent on stroke effort, and (2) stroke-glide patterns during dives contribute to a reduction of muscle metabolic rate.

Ponganis, PJ, McDonald BI, Tift MS, Williams CL.  2017.  Heart rate regulation in diving sea lions: the vagus nerve rules. Journal of Experimental Biology. 220:1372-1381.   10.1242/jeb.146779   AbstractWebsite

Recent publications have emphasized the potential generation of morbid cardiac arrhythmias secondary to autonomic conflict in diving marine mammals. Such conflict, as typified by cardiovascular responses to cold water immersion in humans, has been proposed to result from exercise-related activation of cardiac sympathetic fibers to increase heart rate, combined with depth-related changes in parasympathetic tone to decrease heart rate. After reviewing the marine mammal literature and evaluating heart rate profiles of diving California sea lions (Zalophus californianus), we present an alternative interpretation of heart rate regulation that de-emphasizes the concept of autonomic conflict and the risk of morbid arrhythmias in marine mammals. We hypothesize that: (1) both the sympathetic cardiac accelerator fibers and the peripheral sympathetic vasomotor fibers are activated during dives even without exercise, and their activities are elevated at the lowest heart rates in a dive when vasoconstriction is maximal, (2) in diving animals, parasympathetic cardiac tone via the vagus nerve dominates over sympathetic cardiac tone during all phases of the dive, thus producing the bradycardia, (3) adjustment in vagal activity, which may be affected by many inputs, including exercise, is the primary regulator of heart rate and heart rate fluctuations during diving, and (4) heart beat fluctuations (benign arrhythmias) are common in marine mammals. Consistent with the literature and with these hypotheses, we believe that the generation of morbid arrhythmias because of exercise or stress during dives is unlikely in marine mammals.

2016
Cristofari, R, Bertorelle G, Ancel A, Benazzo A, Lemaho Y, Ponganis PJ, Stenseth NC, Trathan PN, Whittington JD, Zanetti E, Zitterbart DP, Le Bohec C, Trucchi E.  2016.  Full circumpolar migration ensures evolutionary unity in the Emperor penguin. Nature Communications. 7   10.1038/ncomms11842   AbstractWebsite

Defining reliable demographic models is essential to understand the threats of ongoing environmental change. Yet, in the most remote and threatened areas, models are often based on the survey of a single population, assuming stationarity and independence in population responses. This is the case for the Emperor penguin Aptenodytes forsteri, a flagship Antarctic species that may be at high risk continent-wide before 2100. Here, using genome-wide data from the whole Antarctic continent, we reveal that this top-predator is organized as one single global population with a shared demography since the late Quaternary. We refute the view of the local population as a relevant demographic unit, and highlight that (i) robust extinction risk estimations are only possible by including dispersal rates and (ii) colony-scaled population size is rather indicative of local stochastic events, whereas the species' response to global environmental change is likely to follow a shared evolutionary trajectory.

2015
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.

2014
McDonald, BI, Ponganis PJ.  2014.  Deep-diving sea lions exhibit extreme bradycardia in long-duration dives. Journal of Experimental Biology. 217:1525-1534.   10.1242/jeb.098558   AbstractWebsite

Heart rate and peripheral blood flow distribution are the primary determinants of the rate and pattern of oxygen store utilisation and ultimately breath-hold duration in marine endotherms. Despite this, little is known about how otariids (sea lions and fur seals) regulate heart rate (f(H)) while diving. We investigated dive f(H) in five adult female California sea lions (Zalophus californianus) during foraging trips by instrumenting them with digital electrocardiogram (ECG) loggers and time depth recorders. In all dives, dive f(H) (number of beats/duration; 50 +/- 9 beats min(-1)) decreased compared with surface rates (113 +/- 5 beats min(-1)), with all dives exhibiting an instantaneous f(H) below resting (<54 beats min(-1)) at some point during the dive. Both dive f(H) and minimum instantaneous f(H) significantly decreased with increasing dive duration. Typical instantaneous f(H) profiles of deep dives (>100 m) consisted of: (1) an initial rapid decline in f(H) resulting in the lowest instantaneous f(H) of the dive at the end of descent, often below 10 beats min-1 in dives longer than 6 min in duration; (2) a slight increase in f(H) to similar to 10-40 beats min(-1) during the bottom portion of the dive; and (3) a gradual increase in f(H) during ascent with a rapid increase prior to surfacing. Thus, f(H) regulation in deep-diving sea lions is not simply a progressive bradycardia. Extreme bradycardia and the presumed associated reductions in pulmonary and peripheral blood flow during late descent of deep dives should (a) contribute to preservation of the lung oxygen store, (b) increase dependence of muscle on the myoglobin-bound oxygen store, (c) conserve the blood oxygen store and (d) help limit the absorption of nitrogen at depth. This f(H) profile during deep dives of sea lions may be characteristic of deep-diving marine endotherms that dive on inspiration as similar f(H) profiles have been recently documented in the emperor penguin, another deep diver that dives on inspiration.

Tift, MS, Ponganis PJ, Crocker DE.  2014.  Elevated carboxyhemoglobin in a marine mammal, the northern elephant seal. Journal of Experimental Biology. 217:1752-1757.   10.1242/jeb.100677   AbstractWebsite

Low concentrations of endogenous carbon monoxide (CO), generated primarily through degradation of heme from hemeproteins, have been shown to maintain physiological function of organs and to exert cytoprotective effects. However, high concentrations of carboxyhemoglobin (COHb), formed by CO binding to hemoglobin, potentially prevent adequate O-2 delivery to tissues by lowering arterial O-2 content. Elevated heme-protein concentrations, as found in marine mammals, are likely associated with greater heme degradation, more endogenous CO production and, consequently, elevated COHb concentrations. Therefore, we measured COHb in elephant seals, a species with large blood volumes and elevated hemoglobin and myoglobin concentrations. The levels of COHb were positively related to the total hemoglobin concentration. The maximum COHb value was 10.4% of total hemoglobin concentration. The mean (+/- s.e.m.) value in adult seals was 8.7 +/- 0.3% (N=6), while juveniles and pups (with lower heme-protein contents) had lower mean COHb values of 7.6 +/- 0.2% and 7.1 +/- 0.3%, respectively (N=9 and N=9, respectively). Serial samples over several hours revealed little to no fluctuation in COHb values. This consistent elevation in COHb suggests that the magnitude and/ or rate of heme-protein turnover is much higher than in terrestrial mammals. The maximum COHb values from this study decrease total body O-2 stores by 7%, thereby reducing the calculated aerobic dive limit for this species. However, the constant presence of elevated CO in blood may also protect against potential ischemia-reperfusion injury associated with the extreme breath-holds of elephant seals. We suggest the elephant seal represents an ideal model for understanding the potential cytoprotective effects, mechanisms of action and evolutionary adaptation associated with chronically elevated concentrations of endogenously produced CO.

Kooyman, GL, Ponganis PJ.  2014.  Chick production at the largest emperor penguin colony decreases by 50% from 2008-10. Antarctic Science. 26:33-37.   10.1017/s0954102013000515   AbstractWebsite

The emperor penguin colony at Coulman Island is reputedly the largest known. This reputation is based on intermittent ground and aerial surveys performed since 1958. From an aerial survey obtained on 28 October 2010 we discovered that the total number of chicks was 56% of the lowest previous estimate of 2006 and only 41% of the most recent estimate in 2008. All of the counts tallied since 1983 were determined either by ground counts or from aerial film or digital photographs, or estimates from adult counts. We also determined the sea ice conditions in autumn, which is close to the time the adults arrive to breed. We present three hypotheses of what might have happened from 2008-10 to cause the step change in chick production, the small recovery of chick numbers in 2011, and the complete recovery of number of adults from 2010-11. We conclude that local circumstances may have strongly influenced the breeding behaviour of the emperor penguins in 2010 and to a lesser degree in 2011 when many adults elected not to breed.

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.

2013
McDonald, BI, Ponganis PJ.  2013.  Insights from venous oxygen profiles: oxygen utilization and management in diving California sea lions. Journal of Experimental Biology. 216:3332-3341.   10.1242/jeb.085985   AbstractWebsite

The management and depletion of O-2 stores underlie the aerobic dive capacities of marine mammals. The California sea lion (Zalophus californianus) presumably optimizes O-2 store management during all dives, but approaches its physiological limits during deep dives to greater than 300. m depth. Blood O-2 comprises the largest component of total body O-2 stores in adult sea lions. Therefore, we investigated venous blood O-2 depletion during dives of California sea lions during maternal foraging trips to sea by: (1) recording venous partial pressure of O-2 (PO2) profiles during dives, (2) characterizing the O-2-hemoglobin (Hb) dissociation curve of sea lion Hb and (3) converting the PO2 profiles into percent Hb saturation (SO2) profiles using the dissociation curve. The O-2-Hb dissociation curve was typical of other pinnipeds (P-50=28 +/- 2mmHg at pH 7.4). In 43% of dives, initial venous SO2 values were greater than 78% (estimated resting venous SO2), indicative of arterialization of venous blood. Blood O-2 was far from depleted during routine shallow dives, with minimum venous SO2 values routinely greater than 50%. However, in deep dives greater than 4. min in duration, venous SO2 reached minimum values below 5% prior to the end of the dive, but then increased during the last 30-60s of ascent. These deep dive profiles were consistent with transient venous blood O-2 depletion followed by partial restoration of venous O-2 through pulmonary gas exchange and peripheral blood flow during ascent. These differences in venous O-2 profiles between shallow and deep dives of sea lions reflect distinct strategies of O-2 store management and suggest that underlying cardiovascular responses will also differ.

Meir, JU, Robinson PW, Vilchis LI, Kooyman GL, Costa DP, Ponganis PJ.  2013.  Blood oxygen depletion is independent of dive function in a deep diving vertebrate, the northern elephant seal. Plos One. 8   10.1371/journal.pone.0083248   AbstractWebsite

Although energetics is fundamental to animal ecology, traditional methods of determining metabolic rate are neither direct nor instantaneous. Recently, continuous blood oxygen (O-2) measurements were used to assess energy expenditure in diving elephant seals (Mirounga angustirostris), demonstrating that an exceptional hypoxemic tolerance and exquisite management of blood O-2 stores underlie the extraordinary diving capability of this consummate diver. As the detailed relationship of energy expenditure and dive behavior remains unknown, we integrated behavior, ecology, and physiology to characterize the costs of different types of dives of elephant seals. Elephant seal dive profiles were analyzed and O-2 utilization was classified according to dive type (overall function of dive: transit, foraging, food processing/rest). This is the first account linking behavior at this level with in vivo blood O-2 measurements in an animal freely diving at sea, allowing us to assess patterns of O-2 utilization and energy expenditure between various behaviors and activities in an animal in the wild. In routine dives of elephant seals, the blood O-2 store was significantly depleted to a similar range irrespective of dive function, suggesting that all dive types have equal costs in terms of blood O-2 depletion. Here, we present the first physiological evidence that all dive types have similarly high blood O-2 demands, supporting an energy balance strategy achieved by devoting one major task to a given dive, thereby separating dive functions into distinct dive types. This strategy may optimize O-2 store utilization and recovery, consequently maximizing time underwater and allowing these animals to take full advantage of their underwater resources. This approach may be important to optimizing energy expenditure throughout a dive bout or at-sea foraging trip and is well suited to the lifestyle of an elephant seal, which spends >90% of its time at sea submerged making diving its most "natural" state.

2012
Watanabe, S, Sato K, Ponganis PJ.  2012.  Activity time budget during foraging trips of emperor penguins. Plos One. 7   10.1371/journal.pone.0050357   AbstractWebsite

We developed an automated method using depth and one axis of body acceleration data recorded by animal-borne data loggers to identify activities of penguins over long-term deployments. Using this technique, we evaluated the activity time budget of emperor penguins (n = 10) both in water and on sea ice during foraging trips in chick-rearing season. During the foraging trips, emperor penguins alternated dive bouts (4.8 +/- 4.5 h) and rest periods on sea ice (2.5 +/- 2.3 h). After recorder deployment and release near the colony, the birds spent 17.9 +/- 8.4% of their time traveling until they reached the ice edge. Once at the ice edge, they stayed there more than 4 hours before the first dive. After the first dive, the mean proportions of time spent on the ice and in water were 30.8 +/- 7.4% and 69.2 +/- 7.4%, respectively. When in the water, they spent 67.9 +/- 3.1% of time making dives deeper than 5 m. Dive activity had no typical diurnal pattern for individual birds. While in the water between dives, the birds had short resting periods (1.2 +/- 1.7 min) and periods of swimming at depths shallower than 5 m (0.25 +/- 0.38 min). When the birds were on the ice, they primarily used time for resting (90.3 +/- 4.1% of time) and spent only 9.7 +/- 4.1% of time traveling. Thus, it appears that, during foraging trips at sea, emperor penguins traveled during dives >5 m depth, and that sea ice was primarily used for resting. Sea ice probably provides refuge from natural predators such as leopard seals. We also suggest that 24 hours of sunlight and the cycling of dive bouts with short rest periods on sea ice allow emperor penguins to dive continuously throughout the day during foraging trips to sea.

Williams, CL, Sato K, Shiomi K, Ponganis PJ.  2012.  Muscle energy stores and stroke rates of emperor penguins: implications for muscle metabolism and dive performance. Physiological and Biochemical Zoology. 85:120-133.   10.1086/664698   AbstractWebsite

In diving birds and mammals, bradycardia and peripheral vasoconstriction potentially isolate muscle from the circulation. During complete ischemia, ATP production is dependent on the size of the myoglobin oxygen (O-2) store and the concentrations of phosphocreatine (PCr) and glycogen (Gly). Therefore, we measured PCr and Gly concentrations in the primary underwater locomotory muscle of emperor penguin and modeled the depletion of muscle O-2 and those energy stores under conditions of complete ischemia and a previously determined muscle metabolic rate. We also analyzed stroke rate to assess muscle workload variation during dives and evaluate potential limitations on the model. Measured PCr and Gly concentrations, 20.8 and 54.6 mmol kg(-1), respectively, were similar to published values for nondiving animals. The model demonstrated that PCr and Gly provide a large anaerobic energy store, even for dives longer than 20 min. Stroke rate varied throughout the dive profile, indicating muscle workload was not constant during dives as was assumed in the model. The stroke rate during the first 30 s of dives increased with increased dive depth. In extremely long dives, lower overall stroke rates were observed. Although O-2 consumption and energy store depletion may vary during dives, the model demonstrated that PCr and Gly, even at concentrations typical of terrestrial birds and mammals, are a significant anaerobic energy store and can play an important role in the emperor penguin's ability to perform long dives.

Shiomi, K, Sato K, Ponganis PJ.  2012.  Point of no return in diving emperor penguins: is the timing of the decision to return limited by the number of strokes? Journal of Experimental Biology. 215:135-140.   10.1242/jeb.064568   AbstractWebsite

At some point in a dive, breath-hold divers must decide to return to the surface to breathe. The issue of when to end a dive has been discussed intensively in terms of foraging ecology and behavioral physiology, using dive duration as a temporal parameter. Inevitably, however, a time lag exists between the decision of animals to start returning to the surface and the end of the dive, especially in deep dives. In the present study, we examined the decision time in emperor penguins under two different conditions: during foraging trips at sea and during dives at an artificial isolated dive hole. It was found that there was an upper limit for the decision-to-return time irrespective of dive depth in birds diving at sea. However, in a large proportion of dives at the isolated dive hole, the decision-to-return time exceeded the upper limit at sea. This difference between the decision times in dives at sea versus the isolated dive hole was accounted for by a difference in stroke rate. The stroke rates were much lower in dives at the isolated hole and were inversely correlated with the upper limit of decision times in individual birds. Unlike the decision time to start returning, the cumulative number of strokes at the decision time fell within a similar range in the two experiments. This finding suggests that the number of strokes, but not elapsed time, constrained the decision of emperor penguins to return to the surface. While the decision to return and to end a dive may be determined by a variety of ecological, behavioral and physiological factors, the upper limit to that decision time may be related to cumulative muscle workload.

McDonald, BI, Ponganis PJ.  2012.  Lung collapse in the diving sea lion: hold the nitrogen and save the oxygen. Biology Letters. 8:1047-1049.   10.1098/rsbl.2012.0743   AbstractWebsite

Lung collapse is considered the primary-mechanism that limits nitrogen absorption and decreases the risk of decompression sickness in deep-diving marine mammals. Continuous arterial partial pressure of oxygen (P-O2) profiles in a free-diving female California sea lion (Zalophus californianus) revealed that (i) depth of lung collapse was near 225 m as evidenced by abrupt changes in P-O2 during descent and ascent, (ii) depth of lung collapse was positively related to maximum dive depth, suggesting that the sea lion increased inhaled air volume in deeper dives and (iii) lung collapse at depth preserved a pulmonary oxygen reservoir that supplemented blood oxygen during ascent so that mean end-of-dive arterial P-O2 was 74+/-17 mmHg (greater than 85% haemoglobin saturation). Such information is critical to the understanding and the modelling of both nitrogen and oxygen transport in diving marine mammals.

2011
Sato, K, Shiomi K, Marshall G, Kooyman GL, Ponganis PJ.  2011.  Stroke rates and diving air volumes of emperor penguins: implications for dive performance. Journal of Experimental Biology. 214:2854-2863.   10.1242/jeb.055723   AbstractWebsite

Emperor penguins (Aptenodytes forsteri), both at sea and at an experimental dive hole, often have minimal surface periods even after performance of dives far beyond their measured 5.6 min aerobic dive limit (ADL: dive duration associated with the onset of post-dive blood lactate accumulation). Accelerometer-based data loggers were attached to emperor penguins diving in these two different situations to further evaluate the capacity of these birds to perform such dives without any apparent prolonged recovery periods. Minimum surface intervals for dives as long as 10 min were less than 1 min at both sites. Stroke rates for dives at sea were significantly greater than those for dives at the isolated dive hole. Calculated diving air volumes at sea were variable, increased with maximum depth of dive to a depth of 250 m, and decreased for deeper dives. It is hypothesized that lower air volumes for the deepest dives are the result of exhalation of air underwater. Mean maximal air volumes for deep dives at sea were approximately 83% greater than those during shallow (<50 m) dives. We conclude that (a) dives beyond the 5.6. min ADL do not always require prolongation of surface intervals in emperor penguins, (b) stroke rate at sea is greater than at the isolated dive hole and, therefore, a reduction in muscle stroke rate does not extend the duration of aerobic metabolism during dives at sea, and (c) a larger diving air volume facilitates performance of deep dives by increasing the total body O(2) store to 68 ml O(2) kg(-1). Although increased O(2) storage and cardiovascular adjustments presumably optimize aerobic metabolism during dives, enhanced anaerobic capacity and hypoxemic tolerance are also essential for longer dives. This was exemplified by a 27.6 min dive, after which the bird required 6 min before it stood up from a prone position, another 20 min before it began to walk, and 8.4 h before it dived again.

Ponganis, PJ, Meir JU, Williams CL.  2011.  In pursuit of Irving and Scholander: a review of oxygen store management in seals and penguins. Journal of Experimental Biology. 214:3325-3339.   10.1242/jeb.031252   AbstractWebsite

Since the introduction of the aerobic dive limit (ADL) 30 years ago, the concept that most dives of marine mammals and sea birds are aerobic in nature has dominated the interpretation of their diving behavior and foraging ecology. Although there have been many measurements of body oxygen stores, there have been few investigations of the actual depletion of those stores during dives. Yet, it is the pattern, rate and magnitude of depletion of O(2) stores that underlie the ADL. Therefore, in order to assess strategies of O(2) store management, we review (a) the magnitude of O(2) stores, (b) past studies of O(2) store depletion and (c) our recent investigations of O(2) store utilization during sleep apnea and dives of elephant seals (Mirounga angustirostris) and during dives of emperor penguins (Aptenodytes forsteri). We conclude with the implications of these findings for (a) the physiological responses underlying O(2) store utilization, (b) the physiological basis of the ADL and (c) the value of extreme hypoxemic tolerance and the significance of the avoidance of re-perfusion injury in these animals.

Williams, CL, Meir JU, Ponganis PJ.  2011.  What triggers the aerobic dive limit? Patterns of muscle oxygen depletion during dives of emperor penguins Journal of Experimental Biology. 214:1802-1812.   10.1242/jeb.052233   AbstractWebsite

The physiological basis of the aerobic dive limit (ADL), the dive duration associated with the onset of post-dive blood lactate elevation, is hypothesized to be depletion of the muscle oxygen (O(2)) store. A dual wavelength near-infrared spectrophotometer was developed and used to measure myoglobin (Mb) O(2) saturation levels in the locomotory muscle during dives of emperor penguins (Aptenodytes forsteri). Two distinct patterns of muscle O(2) depletion were observed. Type A dives had a monotonic decline, and, in dives near the ADL, the muscle O(2) store was almost completely depleted. This pattern of Mb desaturation was consistent with lack of muscle blood flow and supports the hypothesis that the onset of post-dive blood lactate accumulation is secondary to muscle O(2) depletion during dives. The mean type A Mb desaturation rate allowed for calculation of a mean muscle O(2) consumption of 12.4. ml O(2). kg(-1) muscle. min(-1), based on a Mb concentration of 6.4. g 100. g(-1) muscle. Type B desaturation patterns demonstrated a more gradual decline, often reaching a mid-dive plateau in Mb desaturation. This mid-dive plateau suggests maintenance of some muscle perfusion during these dives. At the end of type B dives, Mb desaturation rate increased and, in dives beyond the ADL, Mb saturation often reached near 0%. Thus, although different physiological strategies may be used during emperor penguin diving, both Mb desaturation patterns support the hypothesis that the onset of post-dive lactate accumulation is secondary to muscle O(2) store depletion.

Ponganis, PJ.  2011.  Diving Mammals. Comprehensive Physiology. 1: John Wiley & Sons, Inc.   10.1002/cphy.c091003   AbstractWebsite

The ability of diving mammals to forage at depth on a breath hold of air is dependent on gas exchange, both in the lung and in peripheral tissues. Anatomical and physiological adaptations in the respiratory system, cardiovascular system, blood and peripheral tissues contribute to the remarkable breath-hold capacities of these animals. The end results of these adaptations include efficient ventilation, enhanced oxygen storage, regulated transport and delivery of respiratory gases, extreme hypoxemic/ischemic tolerance, and pressure tolerance. © 2011 American Physiological Society. Compr Physiol 1:447-465, 2011.

2010
Meir, JU, Ponganis PJ.  2010.  Blood temperature profiles of diving elephant seals. Physiological and Biochemical Zoology. 83:531-540.   10.1086/651070   AbstractWebsite

Hypothermia-induced reductions in metabolic rate have been proposed to suppress metabolism and prolong the duration of aerobic metabolism during dives of marine mammals and birds. To determine whether core hypothermia might contribute to the repetitive long-duration dives of the northern elephant seal Mirounga angustirostris, blood temperature profiles were obtained in translocated juvenile elephant seals equipped with a thermistor and backpack recorder. Representative temperature (the y-intercept of the mean temperature vs. dive duration relationship) was 37.2 degrees +/- 0.6 degrees C (n=3 seals) in the extradural vein, 38.1 degrees +/- 0.7 degrees C (n=4 seals) in the hepatic sinus, and 38.8 degrees +/- 16 degrees C (n=6 seals) in the aorta. Mean temperature was significantly though weakly negatively related to dive duration in all but one seal. Mean venous temperatures of all dives of individual seals ranged between 36 degrees and 38 degrees C, while mean arterial temperatures ranged between 35 degrees and 39 degrees C. Transient decreases in venous and arterial temperatures to as low as 30 degrees-33 degrees C occurred in some dives >30 min (0.1% of dives in the study). The lack of significant core hypothermia during routine dives (10-30 min) and only a weak negative correlation of mean temperature with dive duration do not support the hypothesis that a cold-induced Q(10) effect contributes to metabolic suppression of central tissues during dives. The wide range of arterial temperatures while diving and the transient declines in temperature during long dives suggest that alterations in blood flow patterns and peripheral heat loss contribute to thermoregulation during diving.

Sato, K, Shiomi K, Watanabe Y, Watanuki Y, Takahashi A, Ponganis PJ.  2010.  Scaling of swim speed and stroke frequency in geometrically similar penguins: they swim optimally to minimize cost of transport. Proceedings of the Royal Society B-Biological Sciences. 277:707-714.   10.1098/rspb.2009.1515   AbstractWebsite

It has been predicted that geometrically similar animals would swim at the same speed with stroke frequency scaling with mass(-1/3). In the present study, morphological and behavioural data obtained from free-ranging penguins (seven species) were compared. Morphological measurements support the geometrical similarity. However, cruising speeds of 1.8-2.3 m s(-1) were significantly related to mass(0.08) and stroke frequencies were proportional to mass(-0.29). These scaling relationships do not agree with the previous predictions for geometrically similar animals. We propose a theoretical model, considering metabolic cost, work against mechanical forces (drag and buoyancy), pitch angle and dive depth. This new model predicts that: (i) the optimal swim speed, which minimizes the energy cost of transport, is proportional to (basal metabolic rate/drag)(1/3) independent of buoyancy, pitch angle and dive depth; (ii) the optimal speed is related to mass(0.05); and (iii) stroke frequency is proportional to mass(-0.28). The observed scaling relationships of penguins support these predictions, which suggest that breath-hold divers swam optimally to minimize the cost of transport, including mechanical and metabolic energy during dive.

Zenteno-Savin, T, Leger JS, Ponganis PJ.  2010.  Hypoxemic and ischemic tolerance in emperor penguins. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology. 152:18-23.   10.1016/j.cbpc.2010.02.007   AbstractWebsite

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. (C) 2010 Elsevier Inc. All rights reserved.

Ponganis, PJ, Welch TJ, Welch LS, Stockard TK.  2010.  Myoglobin production in emperor penguins. Journal of Experimental Biology. 213:1901-1906.   10.1242/jeb.042093   AbstractWebsite

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.

Houser, DS, Dankiewicz-Talmadge LA, Stockard TK, Ponganis PJ.  2010.  Investigation of the potential for vascular bubble formation in a repetitively diving dolphin. Journal of Experimental Biology. 213:52-62.   10.1242/jeb.028365   AbstractWebsite

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 60s surface intervals to depths of 30, 50, 70 or 100m. The dolphin remained at the bottom depth for 90s 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(N2)) 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(N2) 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.

Blight, LK, Ainley DG, Ackley SF, Ballard G, Ballerini T, Brownell RL, Cheng CHC, Chiantore M, Costa D, Coulter MC, Dayton P, Devries AL, Dunbar R, Earle S, Eastman JT, Emslie SD, Evans CW, Garrott RA, Kim S, Kooyman G, Lescroel A, Lizotte M, Massaro M, Olmastroni S, Ponganis PJ, Russell J, Siniff DB, Smith WO, Stewart BS, Stirling I, Willis J, Wilson P, Woehler EJ.  2010.  Fishing for data in the Ross Sea. Science. 330:1316-1316.   10.1126/science.330.6009.1316   AbstractWebsite
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