Manfred R. Enstipp

Energy expenditure of freely swimming adult green turtles ( Chelonia mydas ) and its link with body acceleration

SUMMARY Marine turtles are globally threatened. Crucial for the conservation of these large ectotherms is a detailed knowledge of their energy relationships, especially their at-sea metabolic rates, which will ultimately define population structure and size. Measuring metabolic rates in free-ranging aquatic animals, however, remains a challenge. Hence, it is not surprising that for most marine turtle species we know little about the energetic requirements of adults at sea. Recently, accelerometry has emerged as a promising tool for estimating activity-specific metabolic rates of animals in the field. Accelerometry allows quantification of the movement of animals (ODBA/PDBA, overall/partial dynamic body acceleration), which, after calibration, might serve as a proxy for metabolic rate. We measured oxygen consumption rates () of adult green turtles (Chelonia mydas; 142.1±26.9 kg) at rest and when swimming within a 13 m-long swim channel, using flow-through respirometry. We investigated the effect of water temperature (Tw) on turtle and tested the hypothesis that turtle body acceleration can be used as a proxy for . Mean mass-specific () of six turtles when resting at a Tw of 25.8±1.0°C was 0.50±0.09 ml min–1 kg–0.83. increased significantly with Tw and activity level. Changes in were paralleled by changes in respiratory frequency (fR). Deploying bi-axial accelerometers in conjunction with respirometry, we found a significant positive relationship between and PDBA that was modified by Tw. The resulting predictive equation was highly significant (r2=0.83, P<0.0001) and associated error estimates were small (mean algebraic error 3.3%), indicating that body acceleration is a good predictor of in green turtles. Our results suggest that accelerometry is a suitable method to investigate marine turtle energetics at sea.

Exogenous corticosterone mimics a late fasting stage in captive Adelie penguins (Pygoscelis adeliae)

Fasting is part of penguins breeding constraints. During prolonged fasting, three metabolic phases occur successively. Below a threshold in body reserves, birds enter phase III (PIII), which is characterized by hormonal and metabolic shifts. These changes are concomitant with egg abandonment in the wild and increased locomotor activity in captivity. Because corticosterone (CORT) enhances foraging activity, we investigated the variations of endogenous CORT, and the effects of exogenous CORT on the behavioral, hormonal, and metabolic responses of failed breeder Adélie penguins. Untreated and treated captive male birds were regularly weighed and sampled for blood while fasting, and locomotor activity was recorded daily. Treated birds were implanted with various doses of CORT during phase II. Untreated penguins entering PIII had increased CORT (3.5-fold) and uric acid (4-fold; reflecting protein catabolism) levels, concomitantly with a rise in locomotor activity (2-fold), while prolactin (involved in parental care in birds) levels declined by 33%. In CORT-treated birds, an inverted-U relationship was obtained between CORT levels and locomotor activity. The greatest increase in locomotor activity was observed in birds implanted with a high dose of CORT (C100), locomotor activity showing a 2.5-fold increase, 4 days after implantation to a level similar to that of birds in PIII. Moreover, uric acid levels increased three-fold in C100-birds, while prolactin levels declined by 30%. The experimentally induced rise in CORT levels mimicked metabolic, hormonal, and behavioral changes, characterizing late fasting, thus supporting a role for this hormone in the enhanced drive for refeeding occurring in long-term fasting birds.

Reassessment of the cardio-respiratory stress response, using the king penguin as a model.

Abstract Research in to short-term cardio-respiratory changes in animals in reaction to a psychological stressor typically describes increases in rate of oxygen consumption () and heart rate. Consequently, the broad consensus is that they represent a fundamental stressor response generalizable across adult species. However, movement levels can also change in the presence of a stressor, yet studies have not accounted for this possible confound on heart rate. Thus the direct effects of psychological stressors on the cardio-respiratory system are not resolved. We used an innovative experimental design employing accelerometers attached to king penguins (Aptenodytes patagonicus) to measure and thus account for movement levels in a sedentary yet free-to-move animal model during a repeated measures stress experiment. As with previous studies on other species, incubating king penguins (N = 6) exhibited significant increases in both and heart rate when exposed to the stressor. However, movement levels, while still low, also increased in response to the stressor. Once this was accounted for by comparing periods of time during the control and stress conditions when movement levels were similar as recorded by the accelerometers, only significantly increased; there was no change in heart rate. These findings offer evidence that changing movement levels have an important effect on the measured stress response and that the cardio-respiratory response per se to a psychological stressor (i.e. the response as a result of physiological changes directly attributable to the stressor) is an increase in without an increase in heart rate.

Apparent changes in body insulation of juvenile king penguins suggest an energetic challenge during their early life at sea

ABSTRACT Little is known about the early life at sea of marine top predators, like deep-diving king penguins (Aptenodytes patagonicus), although this dispersal phase is probably a critical phase in their life. Apart from finding favourable foraging sites, they have to develop effective prey search patterns as well as physiological capacities that enable them to capture sufficient prey to meet their energetic needs. To investigate the ontogeny of their thermoregulatory responses at sea, we implanted 30 juvenile king penguins and 8 adult breeders with a small data logger that recorded pressure and subcutaneous temperature continuously for up to 2.5 years. We found important changes in the development of peripheral temperature patterns of foraging juvenile king penguins throughout their first year at sea. Peripheral temperature during foraging bouts fell to increasingly lower levels during the first 6 months at sea, after which it stabilized. Most importantly, these changes re-occurred during their second year at sea, after birds had fasted for ∼4 weeks on land during their second moult. Furthermore, similar peripheral temperature patterns were also present in adult birds during foraging trips throughout their breeding cycle. We suggest that rather than being a simple consequence of concurrent changes in dive effort or an indication of a physiological maturation process, these seasonal temperature changes mainly reflect differences in thermal insulation. Heat loss estimates for juveniles at sea were initially high but declined to approximately half after ∼6 months at sea, suggesting that juvenile king penguins face a strong energetic challenge during their early oceanic existence. Summary: Important changes in peripheral temperature patterns during foraging occur in juvenile king penguins throughout their first year at sea, probably reflecting changes in body insulation that suggest an energetic challenge.

High peripheral temperatures in king penguins while resting at sea: thermoregulation versus fat deposition

ABSTRACT Marine endotherms living in cold water face an energetically challenging situation. Unless properly insulated, these animals will lose heat rapidly. The field metabolic rate of king penguins at sea is about twice that on land. However, when at sea, their metabolic rate is higher during extended resting periods at the surface than during foraging, when birds descend to great depth in pursuit of their prey. This is most likely explained by differences in thermal status. During foraging, peripheral vasoconstriction leads to a hypothermic shell, which is rewarmed during extended resting bouts at the surface. Maintaining peripheral perfusion during rest in cold water, however, will greatly increase heat loss and, therefore, thermoregulatory costs. Two hypotheses have been proposed to explain the maintenance of a normothermic shell during surface rest: (1) to help the unloading of N2 accumulated during diving; and (2) to allow the storage of fat in subcutaneous tissue, following the digestion of food. We tested the latter hypothesis by maintaining king penguins within a shallow seawater tank, while we recorded tissue temperature at four distinct sites. When king penguins were released into the tank during the day, their body temperature immediately declined. However, during the night, periodic rewarming of abdominal and peripheral tissues occurred, mimicking temperature patterns observed in the wild. Body temperatures, particularly in the flank, also depended on body condition and were higher in ‘lean’ birds (after 10 days of fasting) than in ‘fat’ birds. While not explicitly tested, our observation that nocturnal rewarming persists in the absence of diving activity during the day does not support the N2 unloading hypothesis. Rather, differences in temperature changes throughout the day and night, and the effect of body condition/mass supports the hypothesis that tissue perfusion during rest is required for nutritional needs. Summary: Periodic peripheral rewarming occurs when king penguins rest at night in a shallow seawater tank, probably reflecting perfusion changes required for the deposition of subcutaneous fat.

Energy expenditure of adult green turtles (Chelonia mydas) at their foraging grounds and during simulated oceanic migration

Measuring the energy requirements of animals under natural conditions and determining how acquired energy is allocated to specific activities is a central theme in ecophysiology. Turtle reproductive output is fundamentally linked with their energy balance so a detailed understanding of marine turtle energy requirements during the different phases of their life cycle at sea is essential for their conservation. We used the non-invasive accelerometry technique to investigate the activity patterns and energy expenditure (EE) of adult green turtles (Chelonia mydas) foraging year-round at a seagrass meadow in Mayotte (n = 13) and during simulated oceanic migration (displacement from the nesting beach) off Moheli (n = 1), in the south-western Indian Ocean. At the foraging site, turtles divided their days between foraging benthically on the shallow seagrass meadow during daylight hours and resting at greater depth on the inner side of the reef slope at night. Estimated oxygen consumption rates (sinline image) and daily energy expenditures (DEE) at the foraging site were low (sinline image during the day was 1·6 and 1·9 times the respective resting rate at night during the austral summer and winter, respectively), which is consistent with the requirement to build up substantial energy reserves at the foraging site, to sustain the energy-demanding breeding migration and reproduction. Dive duration (but not dive depth) at the foraging site shifted significantly with season (dive duration increased with declining water temperatures, Tw), while overall activity levels remained unchanged. In parallel with a significant seasonal decline in Tw (from 28·9 ± 0·1 °C to 25·3 ± 0·4 °C), there was a moderate (˜19%) but significant decline in DEE of turtles during the austral winter (901 ± 111 kJ day−1), when compared with the austral summer (1117 ± 66 kJ day−1). By contrast, the turtle moved continuously during simulated oceanic migration, conducting short/shallow dives in the day, which (predominately at night) were interspersed with longer and deeper ‘pelagic’ dives. Estimated oxygen consumption rates during a simulated migration (1·25 ± 0·16 mL O2 min−1 kg−0·83) were found to be significantly increased over the foraging condition, equal to ˜3 times the resting rate at night (0·42 ± 0·02 mL O2 min−1 kg−0·83), and daily energy expenditure amounted to 2327 ± 292 kJ day−1, underlining the tremendous energetic effort associated with breeding migration. Our study indicates that the accelerometry technique provides a new and promising opportunity to study marine turtle energy relations in great detail and under natural conditions.

Why implantation of bio-loggers may improve our understanding of how animals cope within their natural environment

Bio-loggers are miniaturized autonomous devices that record quantitative data on the state of free-ranging animals (e.g. behavior, position and physiology) and their natural environment. This is especially relevant for species where direct visual observation is difficult or impossible. Today, ongoing technical development allows the monitoring of numerous parameters in an increasing range of species over extended periods. However, the external attachment of devices might affect various aspects of animal performance (energetics, thermoregulation, foraging as well as social and reproductive behavior), which ultimately affect fitness. External attachment might also increase entanglement risk and the conspicuousness of animals, leaving them more vulnerable to predation. By contrast, implantation of devices can mitigate many of these undesirable effects and might be preferable, especially for long-term studies, provided that the many challenges associated with surgical procedures can be mastered. Implantation may then allow us to gather data that would be impossible to obtain otherwise and thereby may provide new and ecologically relevant insights into the life of wild animals. Here, we: (i) discuss the pros and cons of attachment methods; (ii) highlight recent field studies that used implanted bio-loggers to address eco-physiological questions in a wide range of species; and (iii) discuss logger implantation in light of ethical considerations.

Thermal strategies of king penguins during prolonged fasting in water

ABSTRACT Most animals experience periods of unfavourable conditions, challenging their daily energy balance. During breeding, king penguins fast voluntarily for up to 1.5 months in the colony, after which they replenish their energy stores at sea. However, at sea, birds might encounter periods of low foraging profitability, forcing them to draw from previously stored energy (e.g. subcutaneous fat). Accessing peripheral fat stores requires perfusion, increasing heat loss and thermoregulatory costs. Hence, how these birds balance the conflicting demands of nutritional needs and thermoregulation is unclear. We investigated the physiological responses of king penguins to fasting in cold water by: (1) monitoring tissue temperatures, as a proxy of tissue perfusion, at four distinct sites (deep and peripheral); and (2) recording their oxygen consumption rate while birds floated inside a water tank. Despite frequent oscillations, temperatures of all tissues often reached near-normothermic levels, indicating that birds maintained perfusion to peripheral tissues throughout their fasting period in water. The oxygen consumption rate of birds increased with fasting duration in water, while it was also higher when the flank tissue was warmer, indicating greater perfusion. Hence, fasting king penguins in water maintained peripheral perfusion, despite the associated greater heat loss and, therefore, thermoregulatory costs, probably to access subcutaneous fat stores. Hence, the observed normothermia in peripheral tissues of king penguins at sea, upon completion of a foraging bout, is likely explained by their nutritional needs: depositing free fatty acids (FFA) in subcutaneous tissues after profitable foraging or mobilizing FFA to fuel metabolism when foraging success was insufficient. Summary: Maintenance of near-normothermic temperatures in peripheral tissues of king penguins when fasting in cold water suggests maintained perfusion, presumably to mobilize free fatty acids from subcutaneous adipose tissue.