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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.

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.

2010
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.

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
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.

2007
Barber-Meyer, SM, Kooyman GL, Ponganis PJ.  2007.  Estimating the relative abundance of emperor penguins at inaccessible colonies using satellite imagery. Polar Biology. 30:1565-1570.   10.1007/s00300-007-0317-8   AbstractWebsite

Emperor penguin (Aptenodytes forsteri) populations are useful environmental indicators due to the bird's extreme reliance on sea ice. We used remote sensing technology to estimate relative adult bird abundance at two inaccessible emperor penguin colonies in the Ross Sea, Antarctica. We performed supervised classification of 12 panchromatic satellite images of the seven known Ross Sea colonies. We used regression to predict adult bird counts at the inaccessible colonies by relating the number of pixels classified as "penguin" in the satellite images of the accessible colonies to corresponding known adult bird counts from aerial photographs or ground counts. While our analysis was hampered by excessive guano and shadows, we used satellite imagery to differentiate between relatively small (< 3,000 adult birds) and larger colonies (> 5,000 adult birds). Remote sensing technology is logistically less intense and less costly than aerial or ground censuses when the objective is to document penguin presence and/or large emperor penguin population changes (e.g., catastrophic changes). Improvements expected soon in the resolution of the satellite images should allow for more accurate abundance estimates.

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, 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.

2005
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.

2002
Van Dam, RP, Ponganis PJ, Ponganis KV, Levenson DH, Marshall G.  2002.  Stroke frequencies of emperor penguins diving under sea ice. Journal of Experimental Biology. 205:3769-3774. AbstractWebsite

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

2000
Ponganis, PJ, Van Dam RP, Marshall G, Knower T, Levenson DH.  2000.  Sub-ice foraging behavior of emperor penguins. Journal of Experimental Biology. 203:3275-3278. AbstractWebsite

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

1999
Ponganis, PJ, Starke LN, Horning M, Kooyman GL.  1999.  Development of diving capacity in emperor penguins. Journal of Experimental Biology. 202:781-786. AbstractWebsite

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

1997
Ponganis, PJ, Kooyman GL, Starke LN, Kooyman CA, Kooyman TG.  1997.  Post-dive blood lactate concentrations in emperor penguins, Aptenodytes forsteri. Journal of Experimental Biology. 200:1623-1626. AbstractWebsite

In order to determine an aerobic diving limit (ADL) in emperor penguins (Aptenodytes forsteri), post-dive blood lactate concentrations were measured in penguins foraging at an isolated sea ice hole. Resting lactate concentrations were 1.2-2.7 mmol l(-1). Serial samples revealed that lactate level usually peaked within 5 min after dives and that 7-12 min was required for lactate concentrations to decrease from 5-8 mmol l(-1) to less than 2.5 mmol l(-1). Post-dive lactate level was not elevated above 3 mmol l(-1) for dives shorter than 5 min. Two-phase regression analysis revealed a transition at 5.6 min in the post-dive lactate level versus diving duration relationship. All dives longer than 7 min were associated with lactate concentrations greater than 5 mmol l(-1). We conclude that the ADL in emperor penguins ranges between 5 and 7 min. These are the first determinations of post-dive lactate concentrations in any free-diving bird and are currently the only physiological assessment of an ADL in an avian species.