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2019
Williams, CL, Sato K, Ponganis PJ.  2019.  Activity, not submergence, explains diving heart rates of captive loggerhead sea turtles. Journal of Experimental Biology. 222   10.1242/jeb.200824   AbstractWebsite

Marine turtles spend their life at sea and can rest on the seafloor for hours. As air-breathers, the breath-hold capacity of marine turtles is a function of oxygen (O-2) stores, O-2 consumption during dives and hypoxia tolerance. However, some physiological adaptations to diving observed in mammals are absent in marine turtles. This study examined cardiovascular responses in loggerhead sea turtles, which have even fewer adaptations to diving than other marine turtles, but can dive for extended durations. Heart rates (f(H)) of eight undisturbed loggerhead turtles in shallow tanks were measured using self-contained ECG data loggers under five conditions: spontaneous dives, resting motionless on the tank bottom, resting in shallow water with their head out of water, feeding on squid, and swimming at the surface between dives. There was no significant difference between resting f(H) while resting on the bottom of the tank, diving or resting in shallow water with their head out of water. f(H) rose as soon as turtles began to move and was highest between dives when turtles were swimming at the surface. These results suggest cardiovascular responses in captive loggerhead turtles are driven by activity and apneic f(H) is not reduced by submergence under these conditions.

2017
Ponganis, PJ, McDonald BI, Tift MS, Gonzalez SC, DaValle B, Gliniecki RA, Stehman CC, Hauff N, Ruddick B, Howard R.  2017.  Effects of inhalational anesthesia on blood gases and pH in California sea lions. Marine Mammal Science. 33:726-737.   10.1111/mms.12388   AbstractWebsite

Despite the widespread use of inhalational anesthesia with spontaneous ventilation in many studies of otariid pinnipeds, the effects and risks of anesthetic-induced respiratory depression on blood gas and pH regulation are unknown in these animals. During such anesthesia in California sea lions (Zalophus californianus), blood gas and pH analyses of opportunistic blood samples revealed routine hypercarbia (highest P-CO2 = 128 mm Hg [17.1 kPa]), but adequate arterial oxygenation (P-O2 > 100 mm Hg [13.3 kPa] on 100% inspiratory oxygen). Respiratory acidosis (lowest pH = 7.05) was limited by the increased buffering capacity of sea lion blood. Amarkedly widened alveolar-to-arterial P-O2 difference was indicative of atelectasis and ventilation-perfusion mismatch in the lung secondary to hypoventilation during anesthesia. Despite the generally safe track record of this anesthetic regimen in the past, these findings demonstrate the value of high inspiratory O-2 concentrations and the necessity of constant vigilance and caution. In order to avoid hypoxemia, we emphasize the importance of late extubation or at least maintenance of mask ventilation on O-2 until anesthetic-induced respiratory depression is resolved. In this regard, whether for planned or emergency application, we also describe a simple, easily employed intubation technique with the Casper zalophoscope for sea lions.

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.

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.

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.

2010
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.

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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Shiomi, K, Narazaki T, Sato K, Shimatani K, Arai N, Ponganis PJ, Miyazaki N.  2010.  Data-processing artefacts in three-dimensional dive path reconstruction from geomagnetic and acceleration data. Aquatic Biology. 8:299-304.   10.3354/ab00239   AbstractWebsite

Tri-axis magnetism and acceleration data loggers have recently been used to obtain time-series headings and, consequently, the 3-dimensional dive paths of aquatic animals. However, problems may arise in the resulting calculation process with multiple parameters. In this study, the dive paths of loggerhead turtles and emperor penguins were reconstructed. For both species, apparently unrealistic movements were found. Time-series heading data of turtles showed small regular fluctuations synchronous with stroking. In the dive paths of penguins, infrequent abrupt changes in heading were observed during stroke cycles. These were unlikely to represent true behaviours according to observations of underwater behaviour and tri-axis magnetism and acceleration data. Based on the relationship between sampling frequency and frequency of body posture change, we suggest that (1) the changes in the animals' posture concurrent with strokes and (2) the mismatched treatment (i.e. filtering and non-filtering) of the acceleration and magnetism data caused the artefacts. These inferences are supported by the results of simulations. For data sets obtained at a given sampling frequency, the error pattern in calculated dive paths is likely to differ depending on the frequency and amplitude of body posture changes and in swim speed. In order to avoid misinterpretation, it is necessary to understand the assumptions and inherent problems of the calculation methods as well as the behavioural characteristics of the study animals.

2009
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.

2008
Ponganis, PJ, Kreutzer U, Stockard TK, Lin PC, Sailasuta N, Tran TK, Hurd R, Jue T.  2008.  Blood flow and metabolic regulation in seal muscle during apnea. Journal of Experimental Biology. 211:3323-3332.   10.1242/jeb.018887   AbstractWebsite

In order to examine myoglobin (Mb) function and metabolic responses of seal muscle during progressive ischemia and hypoxemia, Mb saturation and high-energy phosphate levels were monitored with NMR spectroscopy during sleep apnea in elephant seals (Mirounga angustirostris). Muscle blood flow (MBF) was measured with laser-Doppler flowmetry (LDF). During six, spontaneous, 8-12 min apneas of an unrestrained juvenile seal, apneic MBF decreased to 46 +/- 10% of the mean eupneic MBF. By the end of apnea, MBF reached 31 +/- 8% of the eupneic value. The t(1/2) for 90% decline in apneic MBF was 1.9 +/- 1.2 min. The initial post-apneic peak in MBF occurred within 0.20 +/- 0.04 min after the start of eupnea. NMR measurements revealed that Mb desaturated rapidly from its eupenic resting level to a lower steady state value within 4 min after the onset of apnea at rates between 1.7 +/- 1.0 and 3.8 +/- 1.5% min(-1), which corresponded to a muscle O(2) depletion rate of 1-2.3 ml O(2)kg(-1) min(-1). High-energy phosphate levels did not change with apnea. During the transition from apnea to eupnea, Mb resaturated to 95% of its resting level within the first minute. Despite the high Mb concentration in seal muscle, experiments detected Mb diffusing with a translational diffusion coefficient of 4.5 x 10(-7) cm(2) s(-1), consistent with the value observed in rat myocardium. Equipoise P(O2) analysis revealed that Mb is the predominant intracellular O(2) transporter in elephant seals during eupnea and apnea.

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.

Shiomi, K, Sato K, Mitamura H, Arai N, Naito Y, Ponganis PJ.  2008.  Effect of ocean current on the dead-reckoning estimation of 3-D dive paths of emperor penguins. Aquatic Biology. 3:265-270.   10.3354/ab00087   AbstractWebsite

The dead-reckoning technique is a useful method for obtaining 3-D movement data of aquatic animals. However, such positional data include an accumulative error. Understanding the source of the error is important for proper data interpretation. In order to determine whether ocean currents affect dive paths calculated by dead-reckoning, as has previously been hypothesized, we examined the directions of the estimated positions relative to the known real points (error direction) and the relationship between the error direction and the current direction. 3-D dive paths of emperor penguins Aptenodytes forsteri diving at isolated dive holes in eastern McMurdo Sound were reconstructed by dead-reckoning, and the net error and error direction were calculated. The net error correlated positively with the dive duration. The error directions were not distributed uniformly, and the mean error direction tended to be north of the starting point of dives. Because there was a southward-flowing current in eastern McMurdo Sound, the ocean current was likely to affect the calculated dive paths. Therefore, the method of error correction generally used, in which the net error divided by the dive duration is applied to each estimated position, is realistically appropriate, provided that the current does not change significantly during a dive.

2007
Sato, K, Watanuki Y, Takahashi A, Miller PJO, Tanaka H, Kawabe R, Ponganis PJ, Handrich Y, Akamatsu T, Watanabe Y, Mitani Y, Costa DP, Bost CA, Aoki K, Amano M, Trathan P, Shapiro A, Naito Y.  2007.  Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans. Proceedings of the Royal Society B-Biological Sciences. 274:471-477.   10.1098/rspb.2006.0005   AbstractWebsite

It is obvious, at least qualitatively, that small animals move their locomotory apparatus faster than large animals: small insects move their wings invisibly fast, while large birds flap their wings slowly. However, quantitative observations have been difficult to obtain from free-ranging swimming animals. We surveyed the swimming behaviour of animals ranging from 0.5 kg seabirds to 30 000 kg sperm whales using animal-borne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass(-0.29) (R-2=0.99, n=17 groups), while propulsive swimming speeds of 1-2 m s(-1) were independent of body size. This scaling relationship, obtained from breath-hold divers expected to swim optimally to conserve oxygen, does not agree with recent theoretical predictions for optimal swimming. Seabirds that use their wings for both swimming and flying stroked at a lower frequency than other swimming specialists of the same size, suggesting a morphological trade-off with wing size and stroke frequency representing a compromise. In contrast, foot-propelled diving birds such as shags had similar stroke frequencies as other swimming specialists. These results suggest that muscle characteristics may constrain swimming during cruising travel, with convergence among diving specialists in the proportions and contraction rates of propulsive muscles.

Ponganis, PJ, Stockard TK.  2007.  The Antarctic toothfish: how common a prey for Weddell seals? Antarctic Science. 19:441-442.   10.1017/s0954102007000715   AbstractWebsite

The Antarctic toothfish (Dissostichus mawsoni Norman) has been considered an occasional large prey item of the Weddell seal (Leptonychotes weddellii Lesson) (Kooyman 1967, Calhaem & Christoffel 1969, Testa et al. 1985, Castellini et al. 1992, Davis et al. 1999, Fuiman et al. 2002). The seal's most common prey is the Antarctic silverfish (Pleuragramma antarcticum Boulenger) as well as benthic and sub-ice fish, cephalopods, and crustaceans (Dearborn 1965, Green & Burton 1987, Plotz 1987, Plotz et al. 1991, Castellini et al. 1992, Burns et al. 1998).

Ponganis, PJ, Stockard TK, Meir JU, Williams CL, Ponganis KV, Van Dam RP, Howard R.  2007.  Returning on empty: extreme blood O-2 depletion underlies dive capacity of emperor penguins. Journal of Experimental Biology. 210:4279-4285.   10.1242/jeb.011221   AbstractWebsite

Blood gas analyses from emperor penguins (Aptenodytes forsteri) at rest, and intravascular P-O2 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(O2)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-O2 profiles obtained from birds equipped with intravascular P-O2 electrodes and backpack recorders during dives revealed that (1) the decline of the final blood P-O2 of a dive in relation to dive duration was variable, (2) final venous P-O2 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-O2 values were indistinguishable in longer dives, and (4) final venous P-O2 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-O2 values and O-2 contents of penguins at rest.

Stockard, TK, Levenson DH, Berg L, Fransioli JR, Baranov EA, Ponganis PJ.  2007.  Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirostris). Journal of Experimental Biology. 210:2607-2617.   10.1242/jeb.008078   AbstractWebsite

Blood gases (P-O2, P-CO2, 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 egree 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-O2 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-O2 values were indistinguishable from arterial values after the first minute of apnea; the lowest venous P-O2 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-O2 values during late apnea that were less than human thresholds for shallow-water blackout. Despite such low P-O2s, there was no evidence of significant anaerobic metabolism, as changes in blood pH were minimal and attributable to increased P-CO2. 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.

2006
Ponganis, PJ, Stockard TK, Levenson DH, Berg L, Baranov EA.  2006.  Intravascular pressure profiles in elephant seals: Hypotheses on the caval sphincter, extradural vein and venous return to the heart. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology. 145:123-130.   10.1016/j.cbpa.2006.05.012   AbstractWebsite

In order to evaluate bemodynamics 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. (c) 2006 Elsevier Inc. All rights reserved.

Ponganis, PJ, Stockard TK, Levenson DH, Berg L, Baranov EA.  2006.  Cardiac output and muscle blood flow during rest-associated apneas of elephant seals. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology. 144:105-111.   10.1016/j.cbpa.2006.02.009   AbstractWebsite

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. (c) 2006 Elsevier Inc. All rights reserved.

2005
Sato, K, Ponganis PJ, Habara Y, Naito Y.  2005.  Emperor penguins adjust swim speed according to the above-water height of ice holes through which they exit. Journal of Experimental Biology. 208:2549-2554.   10.1242/jeb.01665   AbstractWebsite

Emperor penguins leap from the water onto the sea ice. Their ability to reach above-water height depends critically on initial vertical speed of their leaping, assuming that the kinetic energy is converted to gravitational potential energy. We deliberately changed the above-water heights of ice hole exits, in order to examine whether penguins adjusted swim speed in accordance with the above-water height of the ice. Penguins were maintained in a corral on the fast ice in Antarctica, and voluntarily dived through two artificial ice holes. Data loggers were deployed on the penguins to monitor under water behavior. Nine instrumented penguins performed 386 leaps from the holes during experiments. The maximum swim speeds within 1 s before the exits through the holes correlated significantly with the above-water height of the holes. Penguins adopted higher speed to exit through the higher holes than through the lower holes. Speeds of some failed exits were lower than the theoretical minimum values to reach a given height. Penguins failed to exit onto the sea ice in a total of 37 of the trials. There was no preference to use lower holes after they failed to exit through the higher holes. Rather, swim speed was increased for subsequent attempts after failed leaps. These data demonstrated that penguins apparently recognized the above-water height of holes and adopted speeds greater than the minimal vertical speeds to reach the exit height. It is likely, especially in the case of higher holes (>40 cm), that they chose minimum speeds to exit through the holes to avoid excess energy for swimming before leaping. However, some exceptionally high speeds were recorded when they directly exited onto the ice from lower depths. In those cases, birds could increase swim speed without strokes for the final seconds before exit and they only increased the steepness of their body angles as they surfaced, which indicates that the speed required for leaps by emperor penguins were aided by buoyancy, and that penguins can sometimes exit through the ice holes without any stroking effort before leaping.

Knower Stockard, T, Heil J, Meir JU, Sato K, Ponganis KV, Ponganis PJ.  2005.  Air sac P-O2 and oxygen depletion during dives of emperor penguins. Journal of Experimental Biology. 208:2973-2980.   10.1242/jeb.01687   AbstractWebsite

In order to determine the rate and magnitude of respiratory O-2 depletion during dives of emperor penguins (Aptenodytes forsteri), air sac O-2 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. P-O2 and depth profiles revealed compression hyperoxia and gradual O-2 depletion during dives. 42% of final P(O2)s during the dives (recorded during the last 15 s of ascent) were < 20 mmHg (< 2.7 kPa). Assuming that the measured air sac P-O2 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 O-2 fraction was < 4%. The respiratory O-2 store depletion rate of an entire dive, based on the change in O-2 fraction during a dive and previously measured diving respiratory volume, ranged from I to 5 ml O-2 kg(-1) min(-1) and decreased exponentially with diving duration. The mean value, 2.1 +/- 0.8 ml O-2 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.