Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice.

Temperatures were recorded at several body sites in emperor penguins (Aptenodytes forsteri) diving at an isolated dive hole in order to document temperature profiles during diving and to evaluate the role of hypothermia in this well-studied model of penguin diving physiology. Grand mean temperatures (+/-S.E.) in central body sites during dives were: stomach: 37.1+/-0.2 degrees C (n=101 dives in five birds), pectoral muscle: 37.8+/-0.1 degrees C (n=71 dives in three birds) and axillary/brachial veins: 37.9+/-0.1 degrees C (n=97 dives in three birds). Mean diving temperature and duration correlated negatively at only one site in one bird (femoral vein, r=-0.59, P<0.05; range <1 degrees C). In contrast, grand mean temperatures in the wing vein, foot vein and lumbar subcutaneous tissue during dives were 7.6+/-0.7 degrees C (n=157 dives in three birds), 20.2+/-1.2 degrees C (n=69 in three birds) and 35.2+/-0.2 degrees C (n=261 in six birds), respectively. Mean limb temperature during dives negatively correlated with diving duration in all six birds (r=-0.29 to -0.60, P<0.05). In two of six birds, mean diving subcutaneous temperature negatively correlated with diving duration (r=-0.49 and -0.78, P<0.05). Sub-feather temperatures decreased from 31 to 35 degrees C during rest periods to a grand mean of 15.0+/-0.7 degrees C during 68 dives of three birds; mean diving temperature and duration correlated negatively in one bird (r=-0.42, P<0.05). In general, pectoral, deep venous and even stomach temperatures during diving reflected previously measured vena caval temperatures of 37-39 degrees C more closely than the anterior abdominal temperatures (19-30 degrees C) recently recorded in diving emperors. Although prey ingestion can result in cooling in the stomach, these findings and the lack of negative correlations between internal temperatures and diving duration do not support a role for hypothermia-induced metabolic suppression of the abdominal organs as a mechanism of extension of aerobic dive time in emperor penguins diving at the isolated dive hole. Such high temperatures within the body and the observed decreases in limb, anterior abdomen, subcutaneous and sub-feather temperatures are consistent with preservation of core temperature and cooling of an outer body shell secondary to peripheral vasoconstriction, decreased insulation of the feather layer, and conductive/convective heat loss to the water environment during the diving of these emperor penguins.

Temperature regulation in emperor penguins foraging under sea ice.

Inferior vena caval (IVC) and anterior abdominal (AA) temperatures were recorded in seven emperor penguins (Aptenodytes forsteri) 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 degrees C. 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.

Sub-ice foraging behavior of emperor penguins.

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 1 h 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.

Red muscle activation patterns in yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas during steady swimming.

To learn about muscle function in two species of tuna (yellowfin Thunnus albacares and skipjack Katsuwonus pelamis), a series of electromyogram (EMG) electrodes was implanted down the length of the body in the internal red (aerobic) muscle. Additionally, a buckle force transducer was fitted around the deep caudal tendons on the same side of the peduncle as the electrodes. Recordings of muscle activity and caudal tendon forces were made while the fish swam over a range of steady, sustainable cruising speeds in a large water tunnel treadmill. In both species, the onset of red muscle activation proceeds sequentially in a rostro-caudal direction, while the offset (or deactivation) is nearly simultaneous at all sites, so that EMG burst duration decreases towards the tail. Muscle duty cycle at each location remains a constant proportion of the tailbeat period (T), independent of swimming speed, and peak force is registered in the tail tendons just as all ipsilateral muscle deactivates. Mean duty cycles in skipjack are longer than those in yellowfin. In yellowfin red muscle, there is complete segregation of contralateral activity, while in skipjack there is slight overlap. In both species, all internal red muscle on one side is active simultaneously for part of each cycle, lasting 0.18T in yellowfin and 0.11T in skipjack. (Across the distance encompassing the majority of the red muscle mass, 0.35-0.65L, where L is fork length, the duration is 0.25T in both species.) When red muscle activation patterns were compared across a variety of fish species, it became apparent that the EMG patterns grade in a progression that parallels the kinematic spectrum of swimming modes from anguilliform to thunniform. The tuna EMG pattern, underlying the thunniform swimming mode, culminates this progression, exhibiting an activation pattern at the extreme opposite end of the spectrum from the anguilliform mode.

Muscle dynamics in skipjack tuna: timing of red muscle shortening in relation to activation and body curvature during steady swimming.

Cyclic length changes in the internal red muscle of skipjack tuna (Katsuwonus pelamis) were measured using sonomicrometry while the fish swam in a water tunnel at steady speeds of 1.1-2.3 L s(-)(1), where L is fork length. These data were coupled with simultaneous electromyographic (EMG) recordings. The onset of EMG activity occurred at virtually the same phase of the strain cycle for muscle at axial locations between approximately 0.4L and 0.74L, where the majority of the internal red muscle is located. Furthermore, EMG activity always began during muscle lengthening, 40-50 ° prior to peak length, suggesting that force enhancement by stretching and net positive work probably occur in red muscle all along the body. Our results support the idea that positive contractile power is derived from all the aerobic swimming muscle in tunas, while force transmission is provided primarily by connective tissue structures, such as skin and tendons, rather than by muscles performing negative work. We also compared measured muscle length changes with midline curvature (as a potential index of muscle strain) calculated from synchronised video image analysis. Unlike contraction of the superficial red muscle in other fish, the shortening of internal red muscle in skipjack tuna substantially lags behind changes in the local midline curvature. The temporal separation of red muscle shortening and local curvature is so pronounced that, in the mid-body region, muscle shortening at each location is synchronous with midline curvature at locations that are 7-8 cm (i.e. 8-10 vertebral segments) more posterior. These results suggest that contraction of the internal red muscle causes deformation of the body at more posterior locations, rather than locally. This situation represents a unique departure from the model of a homogeneous bending beam, which describes red muscle strain in other fish during steady swimming, but is consistent with the idea that tunas produce thrust by motion of the caudal fin rather than by undulation of segments along the body.