Vincent A. Viblanc

Reliability of flipper-banded penguins as indicators of climate change

In 2007, the Intergovernmental Panel on Climate Change highlighted an urgent need to assess the responses of marine ecosystems to climate change. Because they lie in a high-latitude region, the Southern Ocean ecosystems are expected to be strongly affected by global warming. Using top predators of this highly productive ocean (such as penguins) as integrative indicators may help us assess the impacts of climate change on marine ecosystems. Yet most available information on penguin population dynamics is based on the controversial use of flipper banding. Although some reports have found the effects of flipper bands to be deleterious, some short-term (one-year) studies have concluded otherwise, resulting in the continuation of extensive banding schemes and the use of data sets thus collected to predict climate impact on natural populations. Here we show that banding of free-ranging king penguins (Aptenodytes patagonicus) impairs both survival and reproduction, ultimately affecting population growth rate. Over the course of a 10-year longitudinal study, banded birds produced 39% fewer chicks and had a survival rate 16% lower than non-banded birds, demonstrating a massive long-term impact of banding and thus refuting the assumption that birds will ultimately adapt to being banded. Indeed, banded birds still arrived later for breeding at the study site and had longer foraging trips even after 10 years. One of our major findings is that responses of flipper-banded penguins to climate variability (that is, changes in sea surface temperature and in the Southern Oscillation index) differ from those of non-banded birds. We show that only long-term investigations may allow an evaluation of the impact of flipper bands and that every major life-history trait can be affected, calling into question the banding schemes still going on. In addition, our understanding of the effects of climate change on marine ecosystems based on flipper-band data should be reconsidered.

Kin selection in Columbian ground squirrels ( Urocitellus columbianus ): littermate kin provide individual fitness benefits

Since W. D. Hamiltons seminal work on the evolution of sociality, a large body of research has accumulated on how kin selection might explain the evolution of cooperation in many group-living species. Our study examined the evolutionary basis of philopatry and cooperation; specifically, whether individuals benefit from the presence of close kin. We applied an individual fitness approach to a 16-year study of Columbian ground squirrels (Urocitellus columbianus) to investigate potential causal paths by which the presence of kin might act on individual fitness. Our results indicate that individual fitness benefits resulted from associations of philopatric female kin, and support the hypothesis that increased tolerance of proximity of kin is a proximate mechanism for these benefits. The major life-history influence of kin on individual fitness was through improved reproductive success, and this benefit may have been owing to philopatric settlement of kin that were recognized through familiarization in the natal burrow. Thus, we demonstrated an evolutionary basis necessary for ongoing kin-selected cooperation in Columbian ground squirrels, though the mechanism of familiarity may determine which kin individuals benefit from cooperative behaviours.

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be ‘genial neighbours’. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.

It costs to be clean and fit: energetics of comfort behavior in breeding-fasting penguins.

Background Birds may allocate a significant part of time to comfort behavior (e.g., preening, stretching, shaking, etc.) in order to eliminate parasites, maintain plumage integrity, and possibly reduce muscular ankylosis. Understanding the adaptive value of comfort behavior would benefit from knowledge on the energy costs animals are willing to pay to maintain it, particularly under situations of energy constraints, e.g., during fasting. We determined time and energy devoted to comfort activities in freely breeding king penguins (Aptenodytes patagonicus), seabirds known to fast for up to one month during incubation shifts ashore. Methodology/Principal Findings A time budget was estimated from focal and scan sampling field observations and the energy cost of comfort activities was calculated from the associated increase in heart rate (HR) during comfort episodes, using previously determined equations relating HR to energy expenditure. We show that incubating birds spent 22% of their daily time budget in comfort behavior (with no differences between day and night) mainly devoted to preening (73%) and head/body shaking (16%). During comfort behavior, energy expenditure averaged 1.24 times resting metabolic rate (RMR) and the corresponding energy cost (i.e., energy expended in excess to RMR) was 58 kJ/hr. Energy expenditure varied greatly among various types of comfort behavior, ranging from 1.03 (yawning) to 1.78 (stretching) times RMR. Comfort behavior contributed 8.8–9.3% to total daily energy expenditure and 69.4–73.5% to energy expended daily for activity. About half of this energy was expended caring for plumage. Conclusion/Significance This study is the first to estimate the contribution of comfort behavior to overall energy budget in a free-living animal. It shows that although breeding on a tight energy budget, king penguins devote a substantial amount of time and energy to comfort behavior. Such findings underline the importance of comfort behavior for the fitness of colonial seabirds.

Active territory defence at a low energy cost in a colonial seabird

Aggressive behaviour associated with the defence of a territory is thought to impose substantial energy costs and thus to represent a trade-off with other energy-demanding activities. The energy costs of aggressive behaviours, however, have rarely been estimated in the wild, and the overall contribution of territorial defence to daily energy expenditure has never been determined. We studied the activity budget of breeding king penguins, Aptenodytes patagonicus, equipped with heart rate data loggers to estimate the energy costs associated with territory defence in this colonial bird exhibiting very high rates of agonistic interactions. We also assessed whether threat displays imposed lower energy costs than attacks with body contact. During territorial defence (i.e. threats and physical attacks combined), energy expenditure averaged 1.27 times resting metabolic rate. Defence accounted for 13% of the daily time budget and contributed to 2.7% of the total daily energy expenditure. Interactions with body contact cost three times more than threat displays, but accounted for only 16% of the aggressive behaviours recorded. Neither did body mass, body size, penguin sex or breeding stage affect the cost of aggressiveness. Our results are consistent with previous research reporting that fighting imposes significant metabolic costs. However, we found that aggressive behaviour in king penguins was not an expensive activity compared to the total energy budget. Because king penguins go without food and are sleep deprived while breeding, they may have developed behavioural strategies (e.g. lower rates of attacks with body contact) allowing them to defend their territory efficiently at a low energy cost.

Telomere length reflects individual quality in free-living adult king penguins

Growing evidence suggests that telomeres, non-coding DNA sequences that shorten with age and stress, are related in an undefined way to individual breeding performances and survival rates in several species. Short telomeres and elevated shortening rates are typically associated with life stress and low health. As such, telomeres could serve as an integrative proxy of individual quality, describing the overall biological state of an individual at a given age. Telomere length could be associated with the decline of an array of physiological traits in age-controlled individuals. Here, we investigated the links between individuals’ relative telomere length, breeding performance and various physiological (body condition, natural antibody levels) and life history (age, past breeding success) parameters in a long-lived seabird species, the king penguin Aptenodytes patagonicus. While we observed no link between relative telomere length and age, we found that birds with longer telomeres arrived earlier for breeding at the colony, and had higher breeding performances (i.e. the amount of time adults managed to maintain their chicks alive, and ultimately breeding success) than individuals with shorter telomeres. Further, we observed a positive correlation between telomere length and natural antibody levels. Taken together, our results add to the growing evidence that telomere length is likely to reflect individual quality difference in wild animal.

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.

An ethical issue in biodiversity science: the monitoring of penguins with flipper bands

Individual marking is essential to study the life-history traits of animals and to track them in all kinds of ecological, behavioural or physiological studies. Unlike other birds, penguins cannot be banded on their legs due to their leg joint anatomy and a band is instead fixed around a flipper. However, there is now detailed evidence that flipper-banding has a detrimental impact on individuals. It can severely injure flipper tissues, and the drag effect of their flipper bands results in a higher energy expenditure when birds are moving through the water. It also results in lower efficiency in foraging, since they require longer foraging trips, as well as in lower survival and lower breeding success. Moreover, due to the uncertainty of the rate of band loss, flipper bands induce a scientific bias. These problems, which obviously have serious ethical implications, can be avoided with alternative methods such as radiofrequency identification techniques.

Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (Urocitellus columbianus)

In polyandrous and polygynandrous species where females mate with multiple partners, males are expected to maximize their fitness by exhibiting an array of reproductive behaviors to ensure fertilization success, such as competing for the best mating order within a mating sequence, optimizing their investment in copulation, and mate guarding. Though there is genetic evidence of a first-male precedence in siring success for many mammalian species, the causes of this effect are poorly understood. We studied influences on first-male precedence in Columbian ground squirrels (Urocitellus columbianus). We found that the time a male spent consorting and mate guarding declined with his mating order (both the highest for the first male to mate). Mate guarding by the first male significantly reduced, but did not exclude, the number of additional males a female accepted. Later mating males reduced the time spent consorting, suggesting a perceived decreased chance of fertilization success. Consortship and mate guarding durations were positively related to the male’s siring success and to each other, suggesting that males adjusted these behaviors strategically to increase their chances of fertilization success. Our results suggest that besides being the first male to consort, first-male sperm precedence is further enhanced through longer mating bouts and by suppressing the chances and/or efforts of later mating males.

The oxidative debt of fasting: evidence for short- to medium-term costs of advanced fasting in adult king penguins

ABSTRACT In response to prolonged periods of fasting, animals have evolved metabolic adaptations helping to mobilize body reserves and/or reduce metabolic rate to ensure a longer usage of reserves. However, those metabolic changes can be associated with higher exposure to oxidative stress, raising the question of how species that naturally fast during their life cycle avoid an accumulation of oxidative damage over time. King penguins repeatedly cope with fasting periods of up to several weeks. Here, we investigated how adult male penguins deal with oxidative stress after an experimentally induced moderate fasting period (PII) or an advanced fasting period (PIII). After fasting in captivity, birds were released to forage at sea. We measured plasmatic oxidative stress on the same individuals at the start and end of the fasting period and when they returned from foraging at sea. We found an increase in activity of the antioxidant enzyme superoxide dismutase along with fasting. However, PIII individuals showed higher oxidative damage at the end of the fast compared with PII individuals. When they returned from re-feeding at sea, all birds had recovered their initial body mass and exhibited low levels of oxidative damage. Notably, levels of oxidative damage after the foraging trip were correlated to the rate of mass gain at sea in PIII individuals but not in PII individuals. Altogether, our results suggest that fasting induces a transitory exposure to oxidative stress and that effort to recover in body mass after an advanced fasting period may be a neglected carryover cost of fasting. Summary: Fasting induces a transitory exposure to oxidative stress, and effort to recover in body mass after an advanced fasting period may be a neglected carryover cost of fasting in king penguins.