Rovers minimize human disturbance in research on wild animals.

Investigating wild animals while minimizing human disturbance remains an important methodological challenge. When approached by a remote-operated vehicle (rover) which can be equipped to make radio-frequency identifications, wild penguins had significantly lower and shorter stress responses (determined by heart rate and behavior) than when approached by humans. Upon immobilization, the rover-unlike humans-did not disorganize colony structure, and stress rapidly ceased. Thus, rovers can reduce human disturbance of wild animals and the resulting scientific bias.

King penguins adjust their diving behaviour with age.

Increasing experience in long-lived species is fundamental to improving breeding success and ultimately individual fitness. Diving efficiency of marine animals is primarily determined by their physiological and mechanical characteristics. This efficiency may be apparent via examination of biomechanical performance (e.g. stroke frequency and amplitude, change in buoyancy or body angle, etc.), which itself may be modulated according to resource availability, particularly as a function of depth. We investigated how foraging and diving abilities vary with age in a long-lived seabird. During two breeding seasons, small accelerometers were deployed on young (5 year old) and older (8/9 year old) brooding king penguins (Aptenodytes patagonicus) at the Crozet Archipelago, Indian Ocean. We used partial dynamic body acceleration (PDBA) to quantify body movement during dive and estimate diving cost. During the initial part of the descent, older birds exerted more effort for a given speed but younger penguins worked harder in relation to performance at greater depths. Younger birds also worked harder per unit speed for virtually the whole of the ascent. We interpret these differences using a model that takes into account the upthrust and drag to which the birds are subjected during the dive. From this, we suggest that older birds inhale more at the surface but that an increase in the drag coefficient is the factor leading to the increased effort to swim at a given speed by the younger birds at greater depths. We propose that this higher drag may be the result of young birds adopting less hydrodynamic postures or less direct trajectories when swimming or even having a plumage in poorer condition.

Effects of individual pre-fledging traits and environmental conditions on return patterns in juvenile king penguins.

Despite the importance of early life stages in individuals' life history and population dynamics, very few studies have focused on the constraints to which these juvenile traits are subjected. Based on 10 years of automatic monitoring of over 2500 individuals, we present the first study on the effects of environmental conditions and individual pre-fledging traits on the post-fledging return of non-banded king penguins to their natal colony. Juvenile king penguins returned exclusively within one of the three austral summers following their departure. A key finding is that return rates (range 68-87%) were much higher than previously assumed for this species, importantly meaning that juvenile survival is very close to that of adults. Such high figures suggest little juvenile dispersal, and selection occurring mostly prior to fledging in king penguins. Pre-fledging conditions had a strong quadratic impact on juvenile return rates. As expected, cohorts reared under very unfavourable years (as inferred by the breeding success of the colony) exhibited low return rates but surprisingly, so did those fledged under very favourable conditions. Juvenile sojourns away from the colony were shorter under warm conditions and subsequent return rates higher, suggesting a positive effect of climate warming. The longer the post-fledging trip (1, 2 or 3 years), the earlier in the summer birds returned to their natal colony and the longer they stayed before leaving for the winter journey. The presence of juveniles in the colony was more than twice the duration required for moulting purposes, yet none attempted breeding in the year of their first return. Juvenile presence in the colony may be important for acquiring knowledge on the social and physical colonial environment and may play an important part in the learning process of mating behaviour. Further studies are required to investigate its potential implications on other life-history traits such as recruitment age.

Measuring foraging activity in a deep-diving bird: comparing wiggles, oesophageal temperatures and beak-opening angles as proxies of feeding.

Quantification of prey consumption by marine predators is key to understanding the organisation of ecosystems. This especially concerns penguins, which are major consumers of southern food webs. As direct observation of their feeding activity is not possible, several indirect methods have been developed that take advantage of miniaturised data logging technology, most commonly: detection of (i) anomalies in diving profiles (wiggles), (ii) drops in oesophageal temperature and (iii) the opening of mouth parts (recorded with a Hall sensor). In the present study, we used these three techniques to compare their validity and obtain information about the feeding activity of two free-ranging king penguins (Aptenodytes patagonicus). Crucially, and for the first time, two types of beak-opening events were identified. Type A was believed to correspond to failed prey-capture attempts and type B to successful attempts, because, in nearly all cases, only type B was followed by a drop in oesophageal temperature. The number of beak-opening events, oesophageal temperature drops and wiggles per dive were all correlated. However, for a given dive, the number of wiggles and oesophageal temperature drops were lower than the number of beak-opening events. Our results suggest that recording beak opening is a very accurate method for detecting prey ingestions by diving seabirds at a fine scale. However, these advantages are counterbalanced by the difficulty, and hence potential adverse effects, of instrumenting birds with the necessary sensor/magnet, which is in contrast to the less accurate but more practicable methods of measuring dive profiles or, to a lesser extent, oesophageal temperature.

Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins.

Juvenile king penguins develop adaptive thermogenesis after repeated immersion in cold water. However, the mechanisms of such metabolic adaptation in birds are unknown, as they lack brown adipose tissue and uncoupling protein-1 (UCP1), which mediate adaptive non-shivering thermogenesis in mammals. We used three different groups of juvenile king penguins to investigate the mitochondrial basis of avian adaptive thermogenesis in vitro. Skeletal muscle mitochondria isolated from penguins that had never been immersed in cold water showed no superoxide-stimulated proton conductance, indicating no functional avian UCP. Skeletal muscle mitochondria from penguins that had been either experimentally immersed or naturally adapted to cold water did possess functional avian UCP, demonstrated by a superoxide-stimulated, GDP-inhibitable proton conductance across their inner membrane. This was associated with a markedly greater abundance of avian UCP mRNA. In the presence (but not the absence) of fatty acids, these mitochondria also showed a greater adenine nucleotide translocase-catalysed proton conductance than those from never-immersed penguins. This was due to an increase in the amount of adenine nucleotide translocase. Therefore, adaptive thermogenesis in juvenile king penguins is linked to two separate mechanisms of uncoupling of oxidative phosphorylation in skeletal muscle mitochondria: increased proton transport activity of avian UCP (dependent on superoxide and inhibited by GDP) and increased proton transport activity of the adenine nucleotide translocase (dependent on fatty acids and inhibited by carboxyatractylate).

Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus).

We present the partial nucleotide sequence of the avian uncoupling protein (avUCP) gene from king penguin (Aptenodytes patagonicus), showing that the protein is 88-92% identical to chicken (Gallus gallus), turkey (Meleagris gallopavo), and hummingbird (Eupetomena macroura). We show that superoxide activates the proton conductance of mitochondria isolated from king penguin skeletal muscle. GDP abolishes the superoxide-activated proton conductance, indicating that it is mediated via avUCP. In the absence of superoxide there is no GDP-sensitive component of the proton conductance from penguin muscle mitochondria demonstrating that avUCP plays no role in the basal proton leak.