Molecular sexing of unusually large numbers of Spheniscus magellanicus (Spheniscidae) washed ashore along the Brazilian coast in 2008

There have been few studies on Magellanic penguins (Spheniscus magellanicus). In 2008, these penguins washed ashore along the Brazilian coast in unusually high numbers, some reaching as far as northeast Brazil. As Magellanic penguins show little sexual dimorphism, sex determination by morphological features is not accurate. Here, we tested a molecular procedure for sexing specimens of S. magellanicus washed ashore along the coasts of Sergipe, Rio de Janeiro and Rio Grande do Sul in 2008, comparing the sex ratio between these localities. Tissue samples were collected from 135 dead, beached specimens. We carried out total genomic DNA extraction and CHD-Z/CHD-W gene amplification by PCR using P2 and P8 primers. Amplicons were separated by 12% acrylamide gel electrophoresis. We found a greater proportion of females (70%). Sex could be determined because females have two intronic regions of CHD gene of different size in the sex chromosomes, visualized as two bands on the gel (380 and 400 bp approximately), while males have only one (400 bp). Therefore, this method proved to be effective and sensitive for sex determination of S. magellanicus individuals. Data on sex ratios are useful for understanding the dynamics and ecology of Magellanic penguin populations.     

Behavioural time budget of breeding king penguins (Aptenodytes patagonica)

As do so many other seabirds, penguins fast when ashore for breeding. For penguins in dense colonies, territory defence seems to imply conflicting energetic requirements because of its assumed high energy cost, when the birds need to limit energy expenditure to cope with their fast. In this context, behavioural time budget over 24 h was investigated during breeding in the king penguin, Aptenodytes putugonicu , by using a remote-controlled videocamera. The comparison of day-night activity was performed in relation to breeding status (incubation vs. brooding) and duration of fasting (beginning vs. end of incubation shift). Five categories of behaviours were quantified: territoly defence, comfort, resting, sleeping and chick-feeding. Breeding king penguins remain active by day as well as by night. Between incubation and brooding we found a three-fold increase in the energy consuming temtory defence, together with a drastic decrease in that posture which corresponds to deep sleep, is. when most energy is saved. These increases in aggressiveness and vigilance may be related to protection of the newly hatched chick. Between the onset and the end of an incubation shift, the time spent in sleep increases three-fold, whereas territory defence remains unchanged. These data for penguins under natural conditions accord with previous studies on captive birds which have shown that an increasing proportion of sleep during the course of fasting may contribute to energy saving. On the other hand, both resting (which is the main component of penguins'time budget; about 65%) and comfort (about 16% of time) show no change either between incubation and brooding or during the course of fasting.     

Effect of fog on the arrival time of little penguins Eudyptula minor: a clue for visual orientation?

We report a dramatic change in the arrival time of little penguins Eudyptula minor at their breeding colony when a heavy low-level fog was present on the southern beaches of Phillip Island, Australia. On the evening of 21 December 2002, only 5% of penguins arrived at the expected time, and the peak time at arrival that night was 2 h behind the peak arrival times of previous and subsequent days. It appears that little penguins were unable or unwilling to return to the colony under the low visibility caused by the fog. Only half (52%) of the average number of penguins returned to the colony on the evening of the fog. We propose two explanations for our observation. First, penguins could have been close to the colony but did not come ashore in conditions of poor visibility to avoid predation. Secondly, the extensive fog may have affected the orientation of the penguins and they were unable to find their way back home. Our results could serve as indirect evidence for both hypotheses.     

Behavioral and physiological significance of minimum resting metabolic rate in king penguins

Because fasting king penguins (Aptenodytes patagonicus) need to conserve energy, it is possible that they exhibit particularly low metabolic rates during periods of rest. We investigated the behavioral and physiological aspects of periods of minimum metabolic rate in king penguins under different circumstances. Heart rate (f(H)) measurements were recorded to estimate rate of oxygen consumption during periods of rest. Furthermore, apparent respiratory sinus arrhythmia (RSA) was calculated from the f(H) data to determine probable breathing frequency in resting penguins. The most pertinent results were that minimum f(H) achieved (over 5 min) was higher during respirometry experiments in air than during periods ashore in the field; that minimum f(H) during respirometry experiments on water was similar to that while at sea; and that RSA was apparent in many of the f(H) traces during periods of minimum f(H) and provides accurate estimates of breathing rates of king penguins resting in specific situations in the field. Inferences made from the results include that king penguins do not have the capacity to reduce their metabolism to a particularly low level on land; that they can, however, achieve surprisingly low metabolic rates at sea while resting in cold water; and that during respirometry experiments king penguins are stressed to some degree, exhibiting an elevated metabolism even when resting.     

Energetic cost of foraging in free-diving emperor penguins.

Hypothesizing that emperor penguins (Aptenodytes forsteri) would have higher daily energy expenditures when foraging for their food than when being hand-fed and that the increased expenditure could represent their foraging cost, we measured field metabolic rates (FMR; using doubly labeled water) over 4-d periods when 10 penguins either foraged under sea ice or were not allowed to dive but were fed fish by hand. Surprisingly, penguins did not have higher rates of energy expenditure when they dove and captured their own food than when they did not forage but were given food. Analysis of time-activity and energy budgets indicated that FMR was about 1.7 x BMR (basal metabolic rate) during the 12 h d(-1) that penguins were lying on sea ice. During the remaining 12 h d(-1), which we termed their "foraging period" of the day, the birds were alert and active (standing, preening, walking, and either free diving or being hand-fed), and their FMR was about 4.1 x BMR. This is the lowest cost of foraging estimated to date among the eight penguin species studied. The calculated aerobic diving limit (ADL(C)), determined with the foraging period metabolic rate of 4.1 x BMR and known O(2) stores, was only 2.6 min, which is far less than the 6-min ADL previously measured with postdive lactate analyses in emperors diving under similar conditions. This indicates that calculating ADL(C) from an at-sea or foraging-period metabolic rate in penguins is not appropriate. The relatively low foraging cost for emperor penguins contributes to their relatively low total daily FMR (2.9 x BMR). The allometric relationship for FMR in eight penguin species, including the smallest and largest living representatives, is kJ d(-1)=1,185 kg(0.705).     

Pedestrian locomotion energetics and gait characteristics of a diving bird, the great cormorant, Phalacrocorax carbo

Great cormorants Phalacrocorax carbo are foot propelled diving birds that seem poorly suited to locomotion on land. They have relatively short legs, which are presumably adapted for the generation of high forces during the power stroke of aquatic locomotion, and walk with a pronounced "clumsy waddle". We hypothesise (1) that the speed, independent minimum cost of locomotion (C min, ml O2 m(-1)) will be high for cormorants during treadmill exercise, and (2) that cormorants will have a relatively limited speed range in comparison to more cursorial birds. We measured the rate of oxygen consumption (V02) of cormorants during pedestrian locomotion on a treadmill, and filmed them to determine duty factor (the fraction of stride period that the foot is in contact with the ground), foot contact time (tc), stride frequency (f), swing phase duration and stride length. C min was 2.1-fold higher than that predicted by their body mass and phylogenetic position, but was not significantly different from the C min of runners (Galliformes and Struthioniformes). The extrapolated gamma-intercept of the relationship between V02 and speed was 1.9-fold higher than that predicted by allometry. Again, cormorants were not significantly different from runners. Contrary to our hypothesis, we therefore conclude that cormorants do not have high pedestrian transport costs. Cormorants were observed to use a grounded gait with two double support phases at all speeds measured, and showed an apparent gait transition between 0.17 and 0.25 m s(-1). This transition occurs at a Froude number between 0.016 and 0.037, which is lower than the value of approximately 0.5 observed for many other species. However, despite the use of a limited speed range, and a gait transition at relatively low speed, we conclude that the pedestrian locomotion of these foot propelled diving birds is otherwise generally similar to that of cursorial birds at comparable relative velocities.     

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.     

Moulting fast and time constraint for reproduction in the king penguin

King penguins (Aptenodytes patagonicus) replace their complete plumage during a 3- to 4-week moulting fast on shore. After moulting, birds forage at sea for 2-3 weeks to store energy reserves for reproduction. Using an automatic identification and weighing system coupled with visual observations, we investigated the trade-off between the moulting fast and the following breeding attempt, in terms of body condition and in relation to time constraints, in free-living king penguins. King penguins reached their lowest body mass of the yearly cycle at the end of the moulting fast; this was lower than that at the end of the incubation fasts and not different from the body mass at egg desertion. Later in the season, the duration of the moulting fast became shorter and old feather loss occurred earlier after arrival ashore. Postmoulting foraging trips were shorter, but at the expense of body condition at the beginning of courtship. These results are discussed in relation to the synchronisation of the breeding cycle with food availability and mate choice.     

Behaviour and breeding success of gentoo penguins Pygoscelis papua in areas of low and high human activity

A key factor influencing wildlife responses to human activity is the degree to which animals have been previously exposed to human stimuli. On subantarctic Macquarie Island, gentoo penguins Pygoscelis papua breed in areas of high and low human activity (on and off-station, respectively). We investigated the behaviour and breeding success of gentoo penguins on and off-station, by a) comparing the behavioural responses of guarding gentoos before, during and after exposure to standardised pedestrian approaches, and b) employing an observational study to determine how human activity may have contributed to within-season breeding success in light of other environmental and site variables. Behavioural responses to pedestrian visitation by gentoos off-station were significantly stronger than those of birds breeding on-station. However, no relationship was found between pedestrian activity and breeding success off-station. Breeding success was, however, positively related to colony size, and negatively related to the activity of other penguins, the number of nearby southern elephant seal Mirounga leonina harems and the location of colonies within short grassland. On-station, breeding success was amongst the highest recorded for that season. Habituation, predator exclusion and the relevance of these findings for management are discussed.     

How accurately can we estimate energetic costs in a marine top predator,the king penguin?

King penguins (Aptenodytes patagonicus) are one of the greatest consumers of marine resources. However, while their influence on the marine ecosystem is likely to be significant, only an accurate knowledge of their energy demands will indicate their true food requirements. Energy consumption has been estimated for many marine species using the heart rate-rate of oxygen consumption (f(H) - V(O2)) technique, and the technique has been applied successfully to answer eco-physiological questions. However, previous studies on the energetics of king penguins, based on developing or applying this technique, have raised a number of issues about the degree of validity of the technique for this species. These include the predictive validity of the present f(H) - V(O2) equations across different seasons and individuals and during different modes of locomotion. In many cases, these issues also apply to other species for which the f(H) - V(O2) technique has been applied. In the present study, the accuracy of three prediction equations for king penguins was investigated based on validity studies and on estimates of V(O2) from published, field f(H) data. The major conclusions from the present study are: (1) in contrast to that for walking, the f(H) - V(O2) relationship for swimming king penguins is not affected by body mass; (2) prediction equation (1), log(V(O2) = -0.279 + 1.24log(f(H) + 0.0237t - 0.0157log(f(H)t, derived in a previous study, is the most suitable equation presently available for estimating V(O2) in king penguins for all locomotory and nutritional states. A number of possible problems associated with producing an f(H) - V(O2) relationship are discussed in the present study. Finally, a statistical method to include easy-to-measure morphometric characteristics, which may improve the accuracy of f(H) - V(O2) prediction equations, is explained.     

Energetic costs of surface swimming and diving of birds

The energetic costs of swimming at the surface (swimming) and swimming underwater (diving) are compared in tufted ducks (Aythya fuligula) and three species of penguins, the gentoo (Pygoscelis papua), the king (Aptenodytes patagonicus), and the emperor (Aythya forsteri). Ducks swim on the surface and use their webbed feet as paddles, whereas penguins tend to swim just below the surface and use their flippers as hydrofoils, the latter being much more efficient. Penguins are more streamlined in shape. Thus, the amount of energy required to transport a given mass of bird a given distance (known as the cost of transport) is some two to three times greater in ducks than in penguins. Ducks are also very buoyant, and overcoming the force of buoyancy accounts for 60% and 85% of the cost of descent and remaining on the bottom, respectively, in these birds. The energy cost of a tufted duck diving to about 1.7 m is similar to that when it is swimming at its maximum sustainable speed at the surface (i.e., approximately 3.5 times the value when resting on water). Nonetheless, because of the relatively short duration of its dives, the tufted duck dives well within its calculated aerobic dive limit (cADL, usable O(2) stores per rate of O(2) usage when underwater). However, these three species of penguins have maximum dive durations ranging from 5 min to almost 16 min and maximum dive depths from 155 to 530 m. When these birds dive, they have to metabolise at no more than when resting in water in order for cADL to encompass the duration of most of their natural dives. In gentoo and king penguins, there is a fall in abdominal temperature during bouts of diving; this may reduce the oxygen requirements in the abdominal region, thus enabling dive duration to be extended further than would otherwise be the case.     

Fibre types in primary ‘flight’ muscles of the African Penguin (Spheniscus demersus)

The African penguin (Spheniscus demersus) is an endangered seabird that resides on the temperate southern coast of Africa. Like all penguins it is flightless, instead using its specialized wings for underwater locomotion termed ‘aquatic flight’. While musculature and locomotion of the large Antarctic penguins have been well studied, smaller penguins show different biochemical and behavioural adaptations to their habitats. We used histochemical and immunohistochemical methods to characterize fibre type composition of the African penguin primary flight muscles, the pectoralis and supracoracoideus. We hypothesized the pectoralis would contain predominantly fast oxidative–glycolytic (FOG) fibres, with mainly aerobic subtypes. As the supracoracoideus and pectoralis both power thrust, we further hypothesized these muscles would have a similar fibre type complement. Our results supported these hypotheses, also showing an unexpected slow fibre population in the deep parts of pectoralis and supracoracoideus. The latissimus dorsi was also examined as it may contribute to thrust generation during aquatic flight, and in other avian species typically contains definitive fibre types. Unique among birds studied to date, the African penguin anterior latissimus dorsi was found to consist mainly of fast fibres. This study shows the African penguin has specialized flight musculature distinct from other birds, including large Antarctic penguins.     

Estimating the rate of oxygen consumption during submersion from the heart rate of diving animals

How animals manage their oxygen stores during diving and other breath-hold activities has been a topic of debate among physiologists for decades. Specifically, while the behavior of free-ranging diving animals suggests that metabolism during submersion must be primarily aerobic in nature, no studies have been able to determine their rate of oxygen consumption during submersion (Vo(2)d) and hence prove that this is the case. In the present study, we combine two previously used techniques and develop a new model to estimate Vo(2)d accurately and plausibly in a free-ranging animal and apply it to data for macaroni penguins (Eudyptes chrysolophus) as an example. For macaroni penguins at least, Vo(2)d can be predicted by measuring heart rate during the dive cycle and the subsequent surface interval duration. Including maximum depth of the dive improves the accuracy of these predictions. This suggests that energetically demanding locomotion events within the dive combine with the differing buoyancy and locomotion costs associated with traveling to depth to influence its cost in terms of oxygen use. This will in turn effect the duration of the dive and the duration of the subsequent recovery period. In the present study, Vo(2)d ranged from 4 to 28 ml.min(-1).kg(-1), indicating that, at least as far as aerobic metabolism was concerned, macaroni penguins were often hypometabolic, with rates of oxygen consumption usually below that for this species resting in water (25.6 ml.min(-1).kg(-1)) and occasionally lower than that while resting in air (10.3 ml.min(-1).kg(-1)).     

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.     

Effects of air and water temperatures on resting metabolism of auklets and other diving birds

For small aquatic endotherms, heat loss while floating on water can be a dominant energy cost, and requires accurate estimation in energetics models for different species. We measured resting metabolic rate (RMR) in air and on water for a small diving bird, the Cassin's auklet (Ptychoramphus aleuticus), and compared these results to published data for other diving birds of diverse taxa and sizes. For 8 Cassin's auklets (~165 g), the lower critical temperature was higher on water (21 °C) than in air (16 °C). Lowest values of RMR (W kg?1) averaged 19% higher on water (12.14 ± 3.14 SD) than in air (10.22 ± 1.43). At lower temperatures, RMR averaged 25% higher on water than in air, increasing with similar slope. RMR was higher on water than in air for alcids, cormorants, and small penguins but not for diving ducks, which appear exceptionally resistant to heat loss in water. Changes in RMR (W) with body mass either in air or on water were mostly linear over the 5- to 20-fold body mass ranges of alcids, diving ducks, and penguins, while cormorants showed no relationship of RMR with mass. The often large energetic effects of time spent floating on water can differ substantially among major taxa of diving birds, so that relevant estimates are critical to understanding their patterns of daily energy use.     

Individual repeatability in laying behaviour does not support the migratory carry‐over effect hypothesis of egg‐size dimorphism in Eudyptes penguins

Penguins of the genus Eudyptes are unique among birds in that their first‐laid A‐egg is 54–85% the mass of their second‐laid B‐egg. Although the degree of intra‐clutch egg‐size dimorphism varies greatly among the seven species of the genus, obligate brood reduction is typical of each, with most fledged chicks resulting from the larger B‐egg. Many authors have speculated upon why Eudyptes penguins have evolved and maintained a highly dimorphic 2‐egg clutch, and why it is the first‐laid egg that is so much smaller than the second, but only recently has a testable, proximate mechanism been proposed. In most species of Eudyptes penguins females appear to initiate egg‐formation at sea during return migration to breeding colonies. In macaroni penguins E. chrysolophus, females with a shorter pre‐laying interval ashore (and thus presumably greater overlap between migration and egg‐formation) lay more dimorphic eggs, suggesting a physiological conflict may constrain growth of the earlier‐initiated A‐egg. This migratory carry‐over effect hypothesis (MCEH) was tested in eastern rockhopper penguins E. chrysocome filholi on Campbell Island, New Zealand, by recording the arrival and lay dates, body sizes, and egg masses of transponder‐tagged females over two years. Females with longer pre‐laying intervals laid less dimorphic clutches, as predicted by the MCEH. However, repeated measures of individual females revealed that within‐individual variation in egg‐size dimorphism between years was unrelated to within‐individual variation in pre‐laying interval. Egg masses, and to a lesser extent egg‐size dimorphism, were highly repeatable traits related to body size and body mass. These results and a detailed consideration of the MCEH suggest that egg‐size dimorphism in Eudyptes penguins is unlikely to be caused by a migratory carry‐over effect.     

The early bear gets the goose: climate change,polar bears and lesser snow geese in western Hudson Bay

As climate change advances the date of spring breakup in Hudson Bay, polar bears are coming ashore earlier. Since they would have lost some of their opportunities to hunt ringed seals from a sea ice platform, they may be deficient in energy. Subadult polar bears appear to come ashore before more mature individuals and the earliest subadults are beginning to overlap the nesting period of the large colony of snow geese also occupying the Cape Churchill Peninsula. The eggs these bears are known to eat could make up some of their energy shortfall. The earlier these eggs are consumed during the snow goose nesting period, the greater would be the energy that is available. Recent studies have shown that the annual survival rate for subadult bears declined in contrast to that of prime aged individuals. If this reduction in survival is related to an increasing energy deficit, as suggested by some, the consumption of goose eggs may reverse the trend and help stabilize the population, at least for some period of time. The total number of polar bears that could benefit from this resource will depend on the increasing temporal overlap with the nesting period and on the foraging behaviors of individuals eating the eggs. It is likely that other food sources will also have to play a role if the polar bears are to persist.     

The impact of locomotor energetics on mammalian foraging

The ecological impact of energy expended on an activity stems from its effect on foraging requirements. For locomotion, the effect of moving each additional unit distance probably depends on the proportional increase in energy expenditure. Other common measures of the cost of locomotion do not reflect the impact of energy expenditure on foraging requirements. In terrestrial mammals, both the effect of body mass and the unit cost itself are very small: moving one kilometre requires less than 2% of all other energy expenditures combined. Total locomotor energy expenditure ranges from 1/2% of daily metabolism for a 10 g mammal to 6% for an elephant. Potential sources of bias in the estimation of these costs include systematic bias in estimates of distance traversed and extra energy required for non-linear locomotion. Because larger mammals can readily locomote at greater speeds, the primary locomotor advantage of large size may not be conservation of energy but of time, which can mean greater safety and more or better food.     

The diet of the King Penguin Aptenodytes patagonicus at Macquarie Island

The diet of King Penguins Aptenodytes patagonicus at Macquarie Island was studied between November 1984 and November 1985 based on stomach flushed samples (obtaining 93% of the total stomach content) from ten birds each month. The mean stomach content mass of the 118 samples was 923 0 g. Percentage by number, percentage by weight and dietary coefficient analysis all showed the main prey of the penguins to be myctophid lantern fish of the species Electrona carlsbergi and Krefftichthys anderssoni. Juvenile fish of both species were eaten from December to July, and adults in August and September. Cephalopods were relatively unimportant in contrast to previous indications. The amount of food brought ashore and the composition of the diet varied over the year, with K. anderssoni the dominant food in all but the winter months when E. carlsbergi replaced it as the principal food item.     

Interannual study of Chinstrap penguin’s diet and reproductive success at Laurie Island, South Orkney Islands, Antarctica

Inter-annual variability in the diet of Chinstrap penguins (Pygoscelis antarctica) at Laurie Island, South Orkney Islands was examined based on stomach contents of adults coming ashore during the 1997/1998–2001/2002 breeding seasons. Krill (Euphausia superba) dominated the diet either as frequency of occurrence (in 100% of samples), number (>99%), and percentage contribution in weight (>99.5%). Other prey items were minor but did vary between years. The contribution in weight of fish, amphipods and cephalopods ranged between 0.01–0.5, <0.01–0.14 and 0–0.03, respectively. Although minor components varied slightly along the years, the weight of stomach contents was significantly different. It was found that for a given weight the maximum observed percentage of undigested krill resulted negatively correlated with the stomach contents total weight. The proportion of whole krill observed in individual penguins, expressed as a fraction of the maximum corresponding to its weight was used to characterize the prevailing conditions in each season.