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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.

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.

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.

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.

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.

Ponganis, PJ, Van Dam RP, Knower T, Levenson DH.  2001.  Temperature regulation in emperor penguins foraging under sea ice. Comparative Biochemistry and Physiology a-Molecular and Integrative Physiology. 129:811-820.   10.1016/s1095-6433(01)00349-x   AbstractWebsite

Inferior vena caval (IVC) and anterior abdominal (AA) temperatures were recorded in seven emperor penguins (Aptenodytes foresteri) foraging under sea ice in order to evaluate the hypothesis that hypothermia-induced metabolic suppression might extend aerobic diving time. Diving durations ranged from 1 to 12.5 min, with 39% of dives greater than the measured aerobic dive limit of 5.6 min. Anterior abdominal temperature decreased progressively throughout dives, and partially returned to pre-dive values during surface intervals. The lowest AA temperature was 19 degreesC. However, mean AA temperatures during dives did not correlate with diving durations. In six of seven penguins, only minor fluctuations in IVC temperatures occurred during diving. These changes were often elevations in temperature. In the one exception, although IVC temperatures decreased, the reductions were less than those in the anterior abdomen and did not correlate with diving durations. Because of these findings, we consider it unlikely that regional hypothermia in emperor penguins leads to a significant reduction in oxygen consumption of the major organs within the abdominal core. Rather, temperature profiles during dives are consistent with a model of regional heterothermy with conservation of core temperature, peripheral vasoconstriction, and cooling of an outer body shell. (C) 2001 Elsevier Science Inc. All rights reserved.

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

Our knowledge of avian diving physiology has been based primarily on research with polar species. Since Scholander's 1940 monograph, research has expanded from examination of the 'diving reflex' to studies of free-diving birds, and has included laboratory investigations of oxygen stores, muscle adaptations, pressure effects, and cardiovascular/metabolic responses to swimming exercise. Behavioral and energetic studies at sea have shown that common diving durations of many avian species exceed the calculated aerobic diving limits (ADL). Current physiological research is focused on factors, such as heart rate and temperature, which potentially affect the diving metabolic rate and duration of aerobic diving. (C) 2000 Elsevier Science Inc. All rights reserved.

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.