Impact of predation on king penguin Aptenodytes patagonicus in Crozet Archipelago

Predation can have major effects on population dynamics, but predator–prey interactions in marine ecosystems have rarely been studied. While the king penguin is one of the most studied seabirds, little is known about the impact of predation on its population dynamics. Here, we determine the impact of the main predators (giant petrels and skuas) on king penguin breeding success taking into account the nocturnal predation of petrels. We found that predation is the most important source of breeding failure for king penguins. The smallest chicks within crèches are the most hunted. The periphery of the colony suffers the highest risk of predation during summer. Our study shows the unequal quality of some areas inside the colony in terms of predation risk and breeding success, and points out the importance of timing in successful breeding.     

Prevalence of Borrelia burgdorferi (the Lyme disease agent) antibodies in king penguin Aptenodytes patagonicus in Crozet Archipelago

The seabird tick Ixodes uriae (White) is common in subantarctic areas and is likely to be a vector of pathogenic agents. This paper reports on the prevalence of tick-infested adult king penguins (Aptenodytes patagonicus) and on antibodies to the Lyme disease agent (Borrelia burgdorferi sensu lato) in adult and chick penguins. Fifteen percent of the adults of the colony studied were tick infested. B. burgdorferi antibodies were detected in 14% of tick-infested adults' and in 6% of chicks' sera. The percentage of tick-infested adults differed significantly according to location in the colony, the highest density occurring on the upper slopes of the colony. The potential role of king penguins as B. burgdorferi reservoirs and the effect of this agent on king penguin populations remain unknown. The consequences for human health are discussed. Accepted: 15 March 1999     

Spheniscins, avian beta-defensins in preserved stomach contents of the king penguin, Aptenodytes patagonicus

During the last part of egg incubation in king penguins, the male can preserve undigested food in the stomach for several weeks. This ensures survival of the newly hatched chick, in cases where the return of the foraging female from the sea is delayed. In accordance with the characterization of stress-induced bacteria, we demonstrate the occurrence of strong antimicrobial activities in preserved stomach contents. We isolated and fully characterized two isoforms of a novel 38-residue antimicrobial peptide (AMP), spheniscin, belonging to the beta-defensin subfamily. Spheniscin concentration was found to strongly increase during the period of food storage. Using a synthetic version of one of two spheniscin isoforms, we established that this peptide has a broad activity spectrum, affecting the growth of both pathogenic bacteria and fungi. Altogether, our data suggest that spheniscins and other, not yet identified, antimicrobial substances may play a role in the long term preservation of stored food in the stomach of king penguins.     

Ontogeny of thermoregulatory mechanisms in king penguin chicks (Aptenodytes patagonicus)

The rapid maturation of thermoregulatory mechanisms may be of critical importance for optimising chick growth and survival and parental energy investment under harsh climatic conditions. The ontogeny of thermoregulatory mechanisms was studied in growing king penguin chicks from hatching to the full emancipation observed at 1 month of age in the sub-Antarctic area (Crozet Archipelago). Newly hatched chicks showed small, but significant regulatory thermogenesis (21% rise in heat production assessed by indirect calorimetry), but rapidly became hypothermic. Within a few days, both resting (+32%) and peak (+52%) metabolic rates increased. The first week of life was characterised by a two-fold rise in thermogenic capacity in the cold, while thermal insulation was not improved. During the second and third weeks of age, thermal insulation markedly rose (two-fold drop in thermal conductance) in relation to down growth, while resting heat production was slightly reduced (-13%). Shivering (assessed by electromyography) was visible right after hatching, although its efficiency was limited. Thermogenic efficiency of shivering increased five-fold with age during the first weeks of life, but there was no sign of non-shivering thermogenesis. We conclude that thermal emancipation of king penguin chicks may be primarily determined by improvement of thermal insulation after thermogenic processes have become sufficiently matured. Both insulative and metabolic adaptations are required for the rapid ontogeny of thermoregulation and thermal emancipation in growing king penguin chicks.     

Ticks Ixodes uriae and the breeding performance of a colonial seabird, king penguin Aptenodytes patagonicus

High densities of penguins in their colonies and the continuous use of these sites over consecutive reproductive periods increase the risk of development of tick populations. We have studied the effects of tick parasitism by Ixodes uriae in a colony of king penguins Aptenodytes patagonicus at Possession Island during three breeding seasons. We investigated the prevalence and periods of tick infestation during the one-year breeding cycle of penguins. The effects of tick parasitism on penguin breeding performance were assessed from photographs of the colony and with an automatic penguin identification system. We compared two groups of penguins carrying individual subcutaneous electronic tags, one group breeding in an infested area and the other in a non-infested area. Tick feeding activity was coincident with the periods when adult penguins stayed ashore for six days or more, i.e. during the incubating period. This duration corresponds to the duration of a tick meal on the host. The level of infestation varied between years. Penguins showed a lower incubating success in infested areas during a year of high infestation. In an infested area, individuals seen with ticks had a lower breeding success in rearing a one-year old chick than those seen without ticks.     

The endocrine basis of the reproductive cycle in the king penguin (Aptenodytes patagonicus)

What is the breeding frequency of the king penguin? More than 30 years of study and five major investigations, did not answer this question owing to the length (14 months) and the spreading (four months of laying) of reproductive events.
Following intensively during three consecutive years nearly 1000 tagged birds in a small colony, we obtained the individual history of a large part of the population. To these demographic and phenological studies, we have associated an endocrinological study validating blood samples and experiments in another colony.
The success or failure of a breeding cycle determines the timing of the subsequent breeding attempt. At Crozet Islands, the king penguin can rear one chick every two years at best: a successful breeding is followed by unsuccessful late breeding (or by non-breeding). So a large part of the population displays an annual periodicity of breeding attempts but with low individual breeding success.
The restarting of the reproductive cycle appears basically to be annual, the pituitary responding to the photoperiod. Steroid patterns present classical variations of level according to the reproductive stage. Prolactin (PRL) and luteinizing hormone (LH) are antagonists but, in this species, PRL remains high without external stimulation. To relay after failure in the field. we have experimentally to break down endogenous PRL. So, we have demonstrated that PRL has a key role in the reproductive cycle.
Paradoxically, the king penguin is an irregular breeder, quasi-biennial, although physiologically an annual breeder. In winter, there is not enough food at sea to rear the chick and during four months, the chick fasts. So a successful breeding cycle, which can be shortened to only nine months in captivity, is extended to more than a year for ecological reasons.     

Responses of king penguin Aptenodytes patagonicus adults and chicks to two food‐related odours

Increasing evidence suggests that penguins are sensitive to dimethyl sulphide (DMS), a scented airborne compound that a variety of marine animals use to find productive areas of the ocean where prey is likely to be found. Here we present data showing that king penguins Aptenodytes patagonicus are also sensitive to DMS. We deployed DMS on a lake near a king penguin colony at Ratmanoff beach in the Kerguelen archipelago. We also presented DMS to ‘sleeping’ adults on the beach. On the lake, penguins responded to the DMS deployments by swimming more, while on the beach, penguins twitched their heads and woke up more for the DMS than for the control presentations. Interestingly, penguins did not respond to cod liver oil deployments on the lake; mirroring at‐sea studies of other penguins. Although at‐sea studies are needed to confirm that king penguins use DMS as a surface cue that informs them of productivity under the water, this study is an important first step in understanding how these birds locate prey over significant distances.     

Nutrient reserve dynamics and energetics during long-term fasting in the king penguin (Aptenodytes patagonicus)

Males of king penguins (Aptenodytes patagonicus) naturally fast during one month at the beginning of their breeding cycle in the sub-Antarctic islands. Previous qualitative data have shown that this species adapts to prolonged fasting by mobilizing fat stores and minimizing protein loss and that this strategy ends with a progressive increase in protein utilization. In the present study, the quantification of nutrient utilization from body composition of captive birds indicates that, during the phase of protein conservation, 93% of the energy produced derives from the oxidation of fat stores, body protein accounting for the remainder (7%). Tissue composition analysis shows that integument (feathers, skin and subdermal fat) is the main lipid source (65% of the fat loss) during this period, and that pectoral muscles provide the majority of body protein (57% of the total loss). If the fast is prolonged until a body mass below 10 kg is reached, there is a progressive four-fold increase (from 1 68 to 6.50 gN/24h) in nitrogen excretion, together with a progressive exhaustion of fat stores. This shift in fuel metabolism is not a direct consequence of total lipid depletion, because 22% of the initial fat content still remains when proteins are no longer spared. During this later metabolic phase, protein is not only provided by pectoral muscles (71% of the loss), but also by hindlimb muscles (13%), and there remains only 2% of the initial amount of lipid in the integument at the end of the fast. Total energy expenditure is close to the fasting basal metabolic rate during the phase of protein conservation (2.52 W/kg), but it increases by 33% (3.36 W/kg) during the phase of protein wasting. This difference is probably due to a rise in locomotor activity, that is interpreted as reflecting a stimulation of food foraging behaviour before the lethal depletion of nutrient reserves.     

Transfer of Vitamins E and A from yolk to embryo during development of the king penguin (Aptenodytes patagonicus).

Since the yolk lipids of the king penguin (Aptenodytes patagonicus) are rich in n-3 fatty acids, which are potentially susceptible to peroxidative damage, the yolk contents and yolk-to-embryo transfer of antioxidants and lipid-soluble vitamins were investigated under conditions of natural incubation in the wild. The concentration of vitamin E in the unincubated egg was 155 microg/g wet yolk, of which 88% was alpha-tocopherol and the rest was gamma-tocopherol. Vitamin A (2.9 microg/g) was present in the yolk entirely as retinol; no retinyl esters were detected. Throughout the latter half of the incubation period, vitamins E and A were taken up from the yolk into the yolk sac membrane (YSM) and later accumulated in the liver, with vitamin A being transferred in advance of vitamin E. In the YSM, vitamin A was present almost entirely as retinyl ester, indicating that the free retinol of the yolk is rapidly esterified following uptake. Retinyl esters were also the predominant form in the liver. The retinyl esters of the liver and YSM displayed different fatty acid profiles. At hatching, the brain contained relatively little vitamin E (4.7 microg/g) compared to the much higher concentration in the liver (482.9 microg/g) at this stage. Ascorbic acid was not detected in the yolk but was present at a high concentration in the brain at day 27 (404.6 microg/g), decreasing to less than half this value by the time of hatching. This report is the first to delineate the yolk-to-embryo transfer of lipid-soluble vitamins for a free-living avian species. The yolk fatty acids of the king penguin provide an extreme example of potential oxidative susceptibility, forming a basis for comparative studies on embryonic antioxidant requirements among species of birds whose yolk lipids differ in their degree of unsaturation.     

Seasonal variation in the diet of the king penguin (Aptenodytes patagonicus) at sub-Antarctic Marion Island

King penguins are important consumers of marine resources, throughout the year, at the Prince Edward Islands. Meal size varied from 8.5–12.6% of adult mass, depending on the method of determination. In spite of the biases in the analysis favouring the overestimation of squid, fish and, in particular, myctophid fish accounted for the largest proportion of the stomach samples, 87% by wet mass, 75% by numbers and 69% by reconstituted mass. The relative abundance of fish in the diet dropped markedly in winter followed by a subsequent rise to nearly 100% in summer. This rise coincided with an increase in the chick growth rate and the king penguin population at the island and suggests the rise in relative abundance offish reflects a real increase in the availability of fish around the islands.
Juvenile and adult Krefftichthys anderssoni/Protomyctophum tenisoni and adult Electrona carlsbergi were the most common fish consumed. There was an increase in the modal size of K. anderssoni/P. tenisoni throughout the year which we interpret as growth of a single fish population. Juvenile Kondakoviu longimana was the important squid species taken by king penguins. Crustaceans were only rarely recorded in the diet and may have come from digestion of fish and squid stomachs.
This is the first study of the diet of a Southern Ocean pelagic predator that has identified myctophid fish as a major component of its diet. All three important fish species taken by king penguins at Marion Island have a wide distribution throughout the Southern Ocean and consequently may prove to be important dietary components of other Southern Ocean pelagic predators.     

Projected poleward shift of king penguins' (Aptenodytes patagonicus) foraging range at the Crozet Islands, southern Indian Ocean

Seabird populations of the Southern Ocean have been responding to climate change for the last three decades and demographic models suggest that projected warming will cause dramatic population changes over the next century. Shift in species distribution is likely to be one of the major possible adaptations to changing environmental conditions. Habitat models based on a unique long-term tracking dataset of king penguin (Aptenodytes patagonicus) breeding on the Crozet Islands (southern Indian Ocean) revealed that despite a significant influence of primary productivity and mesoscale activity, sea surface temperature consistently drove penguins' foraging distribution. According to climate models of the Intergovernmental Panel on Climate Change (IPCC), the projected warming of surface waters would lead to a gradual southward shift of the more profitable foraging zones, ranging from 25 km per decade for the B1 IPCC scenario to 40 km per decade for the A1B and A2 scenarios. As a consequence, distances travelled by incubating and brooding birds to reach optimal foraging zones associated with the polar front would double by 2100. Such a shift is far beyond the usual foraging range of king penguins breeding and would negatively affect the Crozet population on the long term, unless penguins develop alternative foraging strategies.     

Effect of fasting on the VO2-fh relationship in king penguins, Aptenodytes patagonicus

King penguins (Aptenodytes patagonicus) may fast for up to 30 days during their breeding period. As such extended fasting may affect the relationship between the rate of O(2) consumption (Vo(2)) and heart rate (f(H)), five male king penguins were exercised at various speeds on repeated occasions during a fasting period of 24-31 days. In addition, Vo(2) and f(H) were measured in the same animals during rest in cold air and water (4 degrees C). Vo(2) and f(H) at rest and Vo(2) during exercise decreased with fasting. There was a significant relation between Vo(2) and f(H) (r(2) = 0.56) that was improved by including speed, body mass (M(b)), number of days fasting (t), and a cross term between f(H) and t (r(2) = 0.92). It was concluded that there was a significant change in the Vo(2)-f(H) relationship with fasting during exercise. As t is measurable in the field and was shown to be significant and, therefore, a practical covariate, a regression equation for use when birds are ashore was obtained by removing speed and M(b). When this equation was used, predicted Vo(2) was in good agreement with the observed data, with an overall error of 3.0%. There was no change in the Vo(2)-f(H) relationship in penguins at rest in water.     

Metabolism and thermoregulation during fasting in king penguins, Aptenodytes patagonicus, in air and water

We measured oxygen consumption rate (Vo(2)) and body temperatures in 10 king penguins in air and water. Vo(2) was measured during rest and at submaximal and maximal exercise before (fed) and after (fasted) an average fasting duration of 14.4 +/- 2.3 days (mean +/- 1 SD, range 10-19 days) in air and water. Concurrently, we measured subcutaneous temperature and temperature of the upper (heart and liver), middle (stomach) and lower (intestine) abdomen. The mean body mass (M(b)) was 13.8 +/- 1.2 kg in fed and 11.0 +/- 0.6 kg in fasted birds. After fasting, resting Vo(2) was 93% higher in water than in air (air: 86.9 +/- 8.8 ml/min; water: 167.3 +/- 36.7 ml/min, P < 0.01), while there was no difference in resting Vo(2) between air and water in fed animals (air: 117.1 +/- 20.0 ml O(2)/min; water: 114.8 +/- 32.7 ml O(2)/min, P > 0.6). In air, Vo(2) decreased with M(b), while it increased with M(b) in water. Body temperature did not change with fasting in air, whereas in water, there were complex changes in the peripheral body temperatures. These latter changes may, therefore, be indicative of a loss in body insulation and of variations in peripheral perfusion. Four animals were given a single meal after fasting and the temperature changes were partly reversed 24 h after refeeding in all body regions except the subcutaneous, indicating a rapid reversal to a prefasting state where body heat loss is minimal. The data emphasize the importance in considering nutritional status when studying king penguins and that the fasting-related physiological changes diverge in air and water.     

Survival in king penguins Aptenodytes patagonicus: temporal and sex-specific effects of environmental variability

We investigated annual adult survival rates of king penguins Aptenodytes patagonicus breeding at South Georgia during 6 years in relation to age/breeding experience, sex, and food availability. During the first 3 years of the study, when food availability was good, survival was 97.7% for experienced breeders, which confirmed the very high survival rates observed in penguins in general. In these years survival did not differ between the sexes, presumably because parental investment is shared equally between the sexes, and the sexual dimorphism is small in king penguins. Survival was lower for young, first-time breeders (83.0%). In experienced birds the annual survival rate decreased to 68-82% following a catastrophic year when food availability was extremely low. We address the question how parents balance their current investment in offspring against their chances to reproduce in the future. We argue that the high mortality rate among breeding individuals after the year of food stress provides support for previous suggestions that the response to increased costs in seabirds might be complex to predict and does not always follow intuitive expectations according to general life-history theory. We also found that females survived significantly less well than males following the bad year. We explain this result as follows: the male-biased sex ratio (56:44) that we observed in our study colony clearly does not result from lower female survival during normal conditions. An already existing skewed sex ratio forces males to delay the onset of breeding because of a lack of breeding partners. This in turn causes breeding females to be, on average, younger and less experienced than males and to have lower survival following a year of food shortage. In this study survival was linked with food availability and we suggest that this was connected to climatic/oceanographic features, such as the position of the Antarctic Polar Front Zone. We could, however, not verify this by anomalies in sea surface temperature data.     

Accounting for body condition improves allometric estimates of resting metabolic rates in fasting king penguins, Aptenodytes patagonicus

We describe a method that allows prediction of resting metabolic rate (RMR, ml O₂ · min⁻¹) in adult male and female king penguins on shore by measuring body mass (M _b) and the length of the foot, flipper and beak. This method is accurate, underestimating measured RMR (n=114) by 4% in a data set consisting of 44 birds (33 males and 11 females). Measurement error was unbiased with respect to fasting duration and can therefore estimate RMR during any stage of fasting. This new method provides significant cost and logistical savings when estimating RMR during fieldwork, allowing RMR of a large number of birds to be measured quickly. These findings suggest the possibility that the use of M _b and morphometrics will allow development of general and specific equations to estimate RMR in other species.     

Effects of weather on activity and sleep in brooding king penguins (Aptenodytes patagonicus)

Avian sleep is sensitive to thermal challenges. Brooding king penguins (Aptenodytes patagonicus) defending a territory are exposed to wide daily fluctuations in ambient temperature and wind conditions. We studied the daytime behavioural time budget of 89 groups of territorial adults brooding a 1- to 5-week-old chick on Crozet Island during summer 1998. Scans were performed every 10 min and each bird was categorized as either active, resting or sleeping. Three ranges of ambient temperatures (T1=5-9°C, T2=10-13°C, T3=14-19°C) and wind conditions (calm-light, moderate, strong) were distinguished. Wind conditions did not affect the behavioural time budget of king penguins during summer. Resting, which represented about half of the daytime behavioural time budget, increased by 17% when ambient temperature increased from T1 to T3, mostly at the expense of active behaviours. The percentage of time spent sleeping was low, but was reduced by 66% when ambient temperature increased over 10°C. Thus, behavioural sleep was mainly observed in a range of temperatures within which resting metabolic rate of adult king penguins is minimal, i.e. between -1 and 11°C. It is also interesting to note that the range of ambient temperatures in which sleeping was high coincides with the most common microclimatology prevailing at the colony during summer, i.e. ambient temperatures between 5 and 10°C.     

Satellite remote sensing in monitoring change of seabirds: use of Spot Image in king penguin population increase at Ile aux Cochons,Crozet Archipelago

The king penguin colony at Ile aux Cochons, Crozet Archipelago (southern Indian Ocean) is the largest in the world. The change in its surface area was investigated by means of satellite remote sensing using spot scene. The satellite picture enabled us to locate the colony and to determine that the surface area occupied by the colony has increased by 56% between 1962 and 1988. The increase in the surface area occupied by the colony was confirmed by a map realised in 1982 (by the Institut Géographique National). The high resolution system available on the spot system which allows at present at 10 m ground resolution, and 5 m in the near future, can thus be a useful tool for monitoring medium to long-term changes in marine bird populations breeding in colonies composed of birds spaced a constant distance from one another. Based on the surface area occupied by the colony and the published data on the population size on Possession Island, as well as information on the breeding frequency of the species, we estimated that the total breeding population is about 1,000,000 pairs for the whole archipelago and that about 70% of birds breed at Ile aux Cochons.     

Summer diet of king penguins (Aptenodytes patagonicus) at the Falkland Islands, southern Atlantic Ocean

The diet of king penguins (Aptenodytes patagonicus) brooding chicks was investigated during February 2001 at the Falkland Islands, where a small but increasing population is located at the limit of the breeding range of this species. Fish was the most important food source by number (98.0%) and reconstituted mass (97.8%), squids accounting for the remainder. Myctophid fishes represented the main part of the diet (97.7% by number and 96.6% by reconstituted mass), Protomyctophum choriodon being by far the main prey item (84.2% and 88.1%, respectively). Four other myctophids and one squid species each contributed to more than 1% of the diet by number: Krefftichthys anderssoni (4.8%), Electrona carlsbergi (4.6%), Gymnoscopelus nicholsi (2.2%) and Protomyctophum tenisoni (1.8%), together with small juveniles of Gonatus antarcticus (1.8%). Twelve squid species were identified from accumulated lower beaks, including the ommastrephid Martialia hyadesi (48.3% by number), the onychoteuthids Moroteuthis ingens (15.6%), Kondakovia longimana (10.5%) and Moroteuthis knipovitchi (7.3%), and Gonatus antarcticus (9.2%). The stable-carbon and stable-nitrogen isotopic composition of chick food and adult blood differed in a way that suggests that, during the same trip, adult birds fed for themselves in distant foraging grounds, and fed for their chicks on their way back to the colony. The study emphasizes that king penguins are specialist myctophid eaters throughout their breeding range in summer, and highlights the importance of Protomyctophum choriodon as a link between zooplankton and top predators in the pelagic ecosystem of the southwestern Atlantic Ocean.     

How do king penguins (Aptenodytes patagonicus apply the mathematical theory of information to communicate in windy conditions?

In the king penguin (Aptenodytes patagonicus), both pair members alternate in incubating and rearing their chick. Mates can recognize each other among thousands of other birds in the hubbub of the colony using only acoustic signalling: the display call. Large penguin colonies are found on sub-Antarctic islands where strong winds blow throughout the year. We have shown by experiments under natural conditions that the level of background noise increases in windy conditions and thus leads to a diminution of the signal-to-noise ratio. Moreover the emergence level of the signal revealed by entropy calculation is statistically weaker in windy conditions. To achieve breeding success, birds must continue communicating in spite of the significant decrease in the total amount of information that can be transmitted in windy situations. For the first time, to our knowledge, we have shown that a bird species takes into account the constraints imposed by wind on their acoustic communication. In windy conditions, birds try to maintain the efficiency of communication by increasing both the number of calls emitted and the number of syllables per call. This result conforms with predictions from the mathematical theory of communication: increased redundancy in a signal improves the probability of receiving a message in a noisy channel.