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.     

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.     

Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host

To examine the potential importance of the spatial subdivision of hosts for the functioning of parasite populations, we analysed patterns of local genetic structure within natural populations of the seabird ectoparasite, Ixodes uriae, at the scale of the host breeding cliff. The seabird hosts of this parasite nest in dense colonies with a hierarchical spatial organisation (individual nests-breeding cliffs-colony). Using eight microsatellite markers and samples from three breeding cliffs of the Black-legged kittiwake (Rissa tridactyla), we found that tick populations were indeed genetically structured at this spatial scale. However, the nature of this structuring depended on the characteristics of the cliffs considered. Both the host nest and cliff topography seemed to be important factors in the isolation of tick groups, but their relative roles may depend on the size of the local parasite population. We found no evidence of isolation by distance within a cliff suggesting that independent tick dispersal may not be a significant force influencing population structure in highly infested cliffs. However, genetic structure seemed to decrease with tick life stage, nymphal ticks being more strongly structured than adult ticks. These results may be related to the clustering of tick progeny combined with differential mortality and dispersal probabilities of each life stage. Overall, results indicate that the spatial organisation of hosts can indeed have important consequences for the population genetic structure of their parasites and, thus, may modify parasite dynamics and the scale at which local coevolutionary processes occur.     

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.     

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.     

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.     

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.     

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.     

Foraging strategies of incubating and brooding king penguins Aptenodytes patagonicus

For oceanic birds like king penguins, a major constraint is the separation of foraging areas from the breeding colony, largely because swimming increases foraging costs. However, the relationship between foraging strategy and breeding stage has been poorly investigated. Using time-depth recorders, we studied the diving behaviour of two groups of king penguins that were either incubating or brooding chicks at Crozet Islands (Southern Indian Ocean) at the same period of the year. Although birds with chicks had the highest predicted energy demand, they made foraging trips half as long as incubating birds (6 vs. 14 days) and modified their time and depth utilisation. Birds with chicks dived deeper during daylight (mean maximum depth of 280 m vs. 205 m for those incubating). At night, birds with chicks spent twice as much time diving as those incubating, but birds at both stages never dived beyond 30 m. Movements to greater depths by brooding birds are consistent with the vertical distribution of myctophid fish which are the main prey. As chick provisioning limits trip duration, it is suggested that it is more efficient for parents to change their diving patterns rather than to restrict their foraging range. Received: 23 June 1997 / Accepted: 3 November 1997     

Endocrine correlates of parental care in an Antarctic winter breeding seabird, the emperor penguin, Aptenodytes forsteri

Plasma levels of luteinizing hormone (LH) and prolactin associated with parental behavior were measured in the Antarctic winter breeding emperor penguin, Aptenodytes forsteri. Males exclusively incubate the egg while females exclusively brood the nonhomeothermic young; both sexes alternate in rearing the homeothermic young. Birds were sampled on arrival from the sea through egg laying, incubation, and brooding. All parent birds lost their chicks at the end of the brooding period due to harsh weather but sampling continued. In females, LH titers dropped after egg laying but levels were restored when the birds returned from the sea to brood the chicks and were not depressed by high prolactin levels. Plasma prolactin remained low in males captured on arrival and kept until the free-living males finished incubation. In breeders, prolactin secretion increased during the prelaying period when day length decreased. Prolactin levels stayed elevated in males during incubation and in brooding females returning after a 2-month absence at sea. Prolactin values were higher in brooding females than in males ending incubation or returning in late brooding. These levels did not drop after chick loss, and the sexual difference in prolactin values was maintained after breeding failure. In emperor penguins, increased prolactin secretion appears to be triggered around the time of egg laying and continues, driven by an endogenous mechanism, through incubation and brooding until rearing is completed. Prolactin secretion independent of external stimuli may have evolved in pelagic seabirds to maintain parental care despite long absences at sea from the breeding colony.     

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     

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.     

Tracing the colonization and diversification of the worldwide seabird ectoparasite Ixodes uriae

Historical patterns of dispersal and population isolation are key components shaping contemporary genetic diversity across landscapes and require explicit consideration when examining the relative role of different factors in driving the evolution of host specificity in parasitic organisms. In this study, we investigate the worldwide colonization history of a common ectoparasite of seabirds, the tick Ixodes uriae. This tick has a circumpolar distribution across both hemispheres but has repeatedly formed host‐specific races within different regions. By combining mitochondrial and nuclear data, we infer how this species spread to its present‐day distribution and how the colonization process may have affected the geographic and host‐associated structure of this tick within regions. We demonstrate that I. uriae is highly structured at a global scale and isolates into four genetic groups that correspond to well‐defined geographical regions. Molecular dating suggests that the diversification of I. uriae began in the early Miocene (22 Myr) and that this tick colonized most of the southern hemisphere before moving into northern latitudes via two independent routes. However, no relationship between the degree of host race divergence and colonization history was evident, supporting previous hypotheses that host specialization evolves relatively rapidly in this parasite, but does not typically lead to speciation. We discuss the possible historical and contemporary mechanisms of large‐scale dispersal for this ectoparasite and how its biological characteristics may condition current patterns of genetic diversity. More generally, our results illustrate how combining broad‐scale sampling and modern molecular tools can help disentangle complex patterns of diversification in widespread parasites.     

Life cycle of the tick Ixodes uriae in penguin colonies: relationships with host breeding activity.

A survey of the temporal pattern of population structure and feeding activity of the seabird tick Ixodes uriae was conducted for the first time in two host species colonies: King penguin (Aptenodytes patagonicus halli) and Macaroni penguin (Eudyptes chrysolophus chrysolophus). The life cycle of the tick was investigated over 3 years in a King penguin colony and 2 years in a Macaroni penguin colony at Possession Island (Crozet Archipelago). There was a marked seasonal feeding activity pattern of ticks in both host species, connected with the presence of birds during the breeding season. Although the King penguin colonies were occupied throughout the year by birds, the favourable period for engorgement was limited to 3.5-4.5 months, and almost all the ticks overwintered in the unengorged state. Consequently, I. uriae probably completed its life cycle over 3 years in King penguin colonies. In contrast, this life cycle could be shortened to 2 years in Macaroni penguin colonies, as a result of a different timetable of the presence of birds for breeding and moulting. The relationships between such plasticity and the host behaviour and subantarctic climatic conditions are discussed.     

Recent evolution of host-associated divergence in the seabird tick Ixodes uriae

Ecological interactions are an important source of rapid evolutionary change and thus may generate a significant portion of novel biodiversity. Such changes may be particularly prevalent in parasites, where hosts can induce strong selection for adaptation. To understand the relative frequency at which host-associated divergences occur, it is essential to examine the evolutionary history of the divergence process, particularly when it is occurring over large geographical scales where both geographical and host-associated isolation may playa part. In this study, we use population genetics and phylogeography to study the evolutionary history of host-associated divergence in the seabird tick Ixodes uriae (Acari, Ixodidae). We compare results from microsatellite markers that reflect more ecological timescales with a conserved mitochondrial gene (COIII) that reflects more ancient divergence events. Population structure based on microsatellites showed clear evidence of host-associated divergence in all colonies examined. However, isolated populations of the same host type did not always group together in overall analyses and the genetic differentiation among sympatric host races was highly variable. In contrast, little host or geographical structure was found for the mitochondrial gene fragment. These results suggest that host race formation in I. uriae is a recent phenomenon, that it may have occurred several times and that local interactions are at different points in the divergence process. Rapid divergence in I. uriae implies a strong interaction with its local host species, an interaction that will alter the ecological dynamics of the system and modify the epidemiological landscape of circulating micropathogens.