Deep dives and aortic temperatures of emperor penguins: new directions for bio-logging at the isolated dive hole

In order to document deep (>100 m) dives and aortic temperature responses of emperor penguins (Aptenodytes forsteri) at an isolated dive hole, and also to evaluate a new catheterization technique, three birds were equipped with time depth recorders, temperature data loggers, and percutaneously-inserted aortic thermistors. After recovery from anesthesia, they were provided access for one day to the dive hole. The birds tolerated the experiment without complication. Mean diving duration (+ SE) of 83 dives was 5.9 + 3.1 min; 55% of dives were > 5.6 min, the previously determined aerobic dive limit; 36% were > 100 m in depth. Mean aortic temperatures during 3-h rest periods ranged from 37.3 + 0.2oC to 38.0 + 0.1oC. Mean dive temperature did not correlate with dive duration, and the grand mean of mean dive temperatures in each bird ranged from 38.3 + 0.2oC to 39.0 + 0.2oC; there was no evidence of core hypothermia during dives. Reliable, safe catheterizations, and the large percentage of deep/long dives of these birds should provide the basis both for future studies of pressure adaptation and hypoxemic tolerance in diving emperor penguins, and for investigation of deep-dive foraging behavior

Blood Oxygen Depletion Is Independent of Dive Function in a Deep Diving Vertebrate, the Northern Elephant Seal

Although energetics is fundamental to animal ecology, traditional methods of determining metabolic rate are neither direct nor instantaneous. Recently, continuous blood oxygen (O2) measurements were used to assess energy expenditure in diving elephant seals (Mirounga angustirostris), demonstrating that an exceptional hypoxemic tolerance and exquisite management of blood O2 stores underlie the extraordinary diving capability of this consummate diver. As the detailed relationship of energy expenditure and dive behavior remains unknown, we integrated behavior, ecology, and physiology to characterize the costs of different types of dives of elephant seals. Elephant seal dive profiles were analyzed and O2 utilization was classified according to dive type (overall function of dive: transit, foraging, food processing/rest). This is the first account linking behavior at this level with in vivo blood O2 measurements in an animal freely diving at sea, allowing us to assess patterns of O2 utilization and energy expenditure between various behaviors and activities in an animal in the wild. In routine dives of elephant seals, the blood O2 store was significantly depleted to a similar range irrespective of dive function, suggesting that all dive types have equal costs in terms of blood O2 depletion. Here, we present the first physiological evidence that all dive types have similarly high blood O2 demands, supporting an energy balance strategy achieved by devoting one major task to a given dive, thereby separating dive functions into distinct dive types. This strategy may optimize O2 store utilization and recovery, consequently maximizing time underwater and allowing these animals to take full advantage of their underwater resources. This approach may be important to optimizing energy expenditure throughout a dive bout or at-sea foraging trip and is well suited to the lifestyle of an elephant seal, which spends > 90% of its time at sea submerged making diving its most “natural” state

Time domains of hypoxia responses and -omics insights

The ability to respond rapidly to changes in oxygen tension is critical for many forms of life. Challenges to oxygen homeostasis, specifically in the contexts of evolutionary biology and biomedicine, provide important insights into mechanisms of hypoxia adaptation and tolerance. Here we synthesize findings across varying time domains of hypoxia in terms of oxygen delivery, ranging from early animal to modern human evolution and examine the potential impacts of environmental and clinical challenges through emerging multi-omics approaches. We discuss how diverse animal species have adapted to hypoxic environments, how humans vary in their responses to hypoxia (i.e., in the context of high-altitude exposure, cardiopulmonary disease, and sleep apnea), and how findings from each of these fields inform the other and lead to promising new directions in basic and clinical hypoxia research

doi:10.1098/rspb.2006.0005

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 animalborne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass K0.29 (R 2 Z0.99, nZ17 groups), while propulsive swimming speeds of 1-2 m s K1 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. Keywords: accelerometer; power spectral density; dive; free-ranging; scaling; optimal INTRODUCTION In a Friday Evening Discourse given at the Royal Institution in 1949 Direct observations have often been used to record movements of flying animals MATERIAL AND METHODS We compared the stroke frequencies and swimming speeds of a range of animals in relation to their body sizes. Owing to morphological differences among species, body mass was used as an index of body size. Morphological measurements were used to estimate mass for adult Weddell seals , leatherback turtles and sperm whales Field experiments using accelerometers were conducted from tropical to Antarctic regions. Detailed protocols of the field experiments were already published for the sperm whale (French Guiana, South America, May 2001. Study protocols followed those of the above-mentioned published studies. We used acceleration data loggers (D2GT and PD2GT, Little Leonardo Ltd, Tokyo; Dtag, the Woods Hole Oceanographic Institution; We could detect the duration of each stroke cycle from the time-series data, but our goal was to determine the dominant stroke cycle frequency for each animal. The periodic properties of the acceleration signal allowed us to apply a Fourier Transform to determine the dominant frequency. Power spectral density (PSD) was calculated from the entire acceleration dataset of each animal, or a subsample during identified foraging or migration behaviour to determine the dominant stroke cycle frequency using a Fast Fourier Transformation with a computer program package, IGOR PRO (WaveMetric, Inc., Lake Oswego, OR, USA). For the sperm whale, the bottom phase of the dive was not used as it is typified by body rotations, which can occur at similar rates to the fluking action. Stroke frequency and body size of animals K. Sato et al. 473 Proc. R. Soc. B (2007) 3. RESULTS Seals move their rear flippers side-to-side and these movements are detected as fluctuations in lateral acceleration along the transverse axis of the body (Mirounga angustirostris; with R 2 Z0.99 (nZ17, p!0.0001). The 95% confidence interval for the exponent was from K0.28 to K0.30. In contrast, the mean propulsive swim speed (U ) among these species was independent of body mass in the log-log analysis (UZ1.88 m K0.05 , R 2 Z0.18, nZ17, pZ0.09). Sperm whales of more than 30 tons, 300 kg seals and 0.5 kg seabirds all swam at mean swim speeds around 1-2 m s K1 during transit between the sea surface and the foraging depths (table 1). DISCUSSION According to experimental measurements based on respirometers in water tunnels and the doubly labelled water technique, the optimum swim speed was proportional to mass 0.27 Stroke frequency and body size of animals K. Sato et al. 475 Proc. R. Soc. B K1 ). Why these free-ranging animals did not follow the theoretical and experimental predictions for optimal swimming speed is a question we cannot answer now. The constructal model The isometric model proposed by According to the present study, swim speed (U ) was independent of body size, therefore the frequency is expected to be proportional to area divided by mass (S/m), which is expected to be proportional to the length K1 or mass K1/3 . Results of the present study were obtained from morphologically diverse animals. Nonetheless, f is inversely proportional to m K0.29 , close to the predicted value of mass K1/3 , implying that diving specialists among seabirds and marine mammals have evolved similar proportions of propulsive muscles and muscle contraction rates during cruising travel. The scaling relationship was very strong among swimming specialists during contexts when they were predicted to swim efficiently. Moreover, interesting deviations from the regression line (see Japanese flounders Paralichthys olivaceus had lower stroke frequencies than other swimming specialists (open pink circle i

Evaluating the impact of handling and logger attachment on foraging parameters and physiology in southern rockhopper penguins

Logger technology has revolutionised our knowledge of the behaviour and physiology of free-living animals but handling and logger attachments may have negative effects on the behaviour of the animals and their welfare. We studied southern rockhopper penguin ( Eudyptes chrysocome ) females during the guard stage in three consecutive breeding seasons (2008/09−2010/11) to evaluate the effects of handling and logger attachment on foraging trip duration, dive behaviour and physiological parameters. Smaller dive loggers (TDRs) were used in 2010/11 for comparison to larger GPS data loggers used in all three seasons and we included two categories of control birds: handled controls and PIT control birds that were previously marked with passive integrative transponders (PITs), but which had not been handled during this study. Increased foraging trip duration was only observed in GPS birds during 2010/11, the breeding season in which we also found GPS birds foraging further away from the colony and travelling longer distances. Compared to previous breeding seasons, 2010/11 may have been a period with less favourable environmental conditions, which would enhance the impact of logger attachments. A comparison between GPS and TDR birds showed a significant difference in dive depth frequencies with birds carrying larger GPS data loggers diving shallower. Mean and maximum dive depths were similar between GPS and TDR birds. We measured little impact of logger attachments on physiological parameters (corticosterone, protein, triglyceride levels and leucocyte counts). Overall, handling and short-term logger attachments (1-3 days) showed limited impact on the behaviour and physiology of the birds but care must be taken with the size of data loggers on diving seabirds. Increased drag may alter their diving behaviour substantially, thus constraining them in their ability to catch prey. Results obtained in this study indicate that data recorded may also not represent their normal dive behaviour

Step by step: reconstruction of terrestrial animal movement paths by dead-reckoning

Background: Research on wild animal ecology is increasingly employing GPS telemetry in order to determine animal movement. However, GPS systems record position intermittently, providing no information on latent position or track tortuosity. High frequency GPS have high power requirements, which necessitates large batteries (often effectively precluding their use on small animals) or reduced deployment duration. Dead-reckoning is an alternative approach which has the potential to ‘fill in the gaps’ between less resolute forms of telemetry without incurring the power costs. However, although this method has been used in aquatic environments, no explicit demonstration of terrestrial dead-reckoning has been presented.Results: We perform a simple validation experiment to assess the rate of error accumulation in terrestrial dead-reckoning. In addition, examples of successful implementation of dead-reckoning are given using data from the domestic dog Canus lupus, horse Equus ferus, cow Bos taurus and wild badger Meles meles.Conclusions: This study documents how terrestrial dead-reckoning can be undertaken, describing derivation of heading from tri-axial accelerometer and tri-axial magnetometer data, correction for hard and soft iron distortions on the magnetometer output, and presenting a novel correction procedure to marry dead-reckoned paths to ground-truthed positions. This study is the first explicit demonstration of terrestrial dead-reckoning, which provides a workable method of deriving the paths of animals on a step-by-step scale. The wider implications of this method for the understanding of animal movement ecology are discussed

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities

Adult Weddell seals (Leptonychotes weddellii) haul-out on the ice in October/November (austral spring) for the breeding season and reduce foraging activities for ~4 months until their molt in the austral fall (January/February). After these periods, animals are at their leanest and resume actively foraging for the austral winter. In mammals, decreased exercise and hypoxia exposure typically lead to decreased production of O2-carrying proteins and muscle wasting, while endurance training increases aerobic potential. To test whether similar effects were present in marine mammals, this study compared the physiology of 53 post-molt female Weddell seals in the austral fall to 47 pre-breeding females during the spring in McMurdo Sound, Antarctica. Once body mass and condition (lipid) were controlled for, there were no seasonal changes in total body oxygen (TBO2) stores. Within each season, hematocrit and hemoglobin values were negatively correlated with animal size, and larger animals had lower mass-specific TBO2 stores. But because larger seals had lower mass-specific metabolic rates, their calculated aerobic dive limit was similar to smaller seals. Indicators of muscular efficiency, myosin heavy chain composition, myoglobin concentrations, and aerobic enzyme activities (citrate synthase and β-hydroxyacyl CoA dehydrogenase) were likewise maintained across the year. The preservation of aerobic capacity is likely critical to foraging capabilities, so that following the molt Weddell seals can rapidly regain body mass at the start of winter foraging. In contrast, muscle lactate dehydrogenase activity, a marker of anaerobic metabolism, exhibited seasonal plasticity in this diving top predator and was lowest after the summer period of reduced activity