Integrative assessment of immunity, health-state, growth and survival of Magellanic penguin chicks in a colony exposed to ecotourism.

Accumulating reports of negative impacts of tourist activities on wildlife emphasize the importance of closely monitoring focal populations. Although some effects are readily noticed, more subtle ones such as changes in physiological functions of individuals might go overlooked. Based on evidence of altered physiology associated with ecotourism on Magellanic penguins Spheniscus magellanicus, here we performed an integrated assessment using a diverse physiological toolkit together with more traditional fitness-related measures to better understand mechanisms and potential consequences. Chicks exposed to tourism showed altered immune parameters and elevated flea prevalence, reinforcing previous findings. Tourism-exposed female, but not male, chicks also showed relatively lower hematocrit and plasma protein levels, providing evidence consistent with a sex-specific response to tourist visitation. Physiological alterations detected in tourism-exposed young chicks (week 1-2) were maintained and the effect on flea infestation increased during the study period (week 4-5 of post-hatch). Despite the effects on physiology, these did not seem to translate into immediate fitness costs. No detectable tourism effects were found on brood sex ratios, chick growth and body condition, and survival until week 5-6 post-hatch. We detected no effects on reproductive output and only a marginal effect on nest survival during incubation despite previous reports of tourism-associated alterations in stress indices of adults. This disconnection could result if the physiological changes are not strong enough to impact fitness, if effects balance each other out, or if changes are part of a copying strategy. Alternatively, the physiological alterations might only show impacts later in the brooding cycle or even after chick emancipation from their parents. Our results suggest that integrative monitoring of potential anthropogenic impacts on wildlife should include evaluation of physiological mechanisms and individual-level responses in populations exposed to human activities.

Sex-specific spatial use of the winter foraging areas by Magellanic penguins and assessment of potential conflicts with fisheries during winter dispersal.

Magellanic penguins (Spheniscus magellanicus) disperse widely during winter and are a major consumer of marine resources over the Patagonian Shelf. Magellanic penguins were equipped with geolocators at Martillo Island in late February- early March 2017 and recaptured at the beginning of the next breeding season to recover the devices and to collect blood samples for stable carbon (δ13C) and nitrogen (δ15N) isotope analysis. We evaluated their whole winter dispersal and their trophic niche by sex during the last month of the winter dispersal. Also, we evaluated their spatial overlap with bottom trawl and shrimp fisheries using data from satellite fisheries monitoring. Penguins dispersed northwards up to 42°S and showed latitudinal spatial segregation between sexes during May to August (females were located further north than males). In contrast, during the last month of the winter dispersal females were located more southerly and showed lower trophic position than males. Also, females did not dive as deep as males during winter. We found high overlap between both fisheries and penguin's spatial use in regions with documented interaction. However, no sex-specific statistical differences with fisheries overlap were found. Our results highlight the importance of understanding the spatial domains of each sex and assessment of their potential conflicts with bottom trawl fishery and shrimp fishery during the winter period.

A global population assessment of the Chinstrap penguin (Pygoscelis antarctica).

Using satellite imagery, drone imagery, and ground counts, we have assembled the first comprehensive global population assessment of Chinstrap penguins (Pygoscelis antarctica) at 3.42 (95th-percentile CI: [2.98, 4.00]) million breeding pairs across 375 extant colonies. Twenty-three previously known Chinstrap penguin colonies are found to be absent or extirpated. We identify five new colonies, and 21 additional colonies previously unreported and likely missed by previous surveys. Limited or imprecise historical data prohibit our assessment of population change at 35% of all Chinstrap penguin colonies. Of colonies for which a comparison can be made to historical counts in the 1980s, 45% have probably or certainly declined and 18% have probably or certainly increased. Several large colonies in the South Sandwich Islands, where conditions apparently remain favorable for Chinstrap penguins, cannot be assessed against a historical benchmark. Our population assessment provides a detailed baseline for quantifying future changes in Chinstrap penguin abundance, sheds new light on the environmental drivers of Chinstrap penguin population dynamics in Antarctica, and contributes to ongoing monitoring and conservation efforts at a time of climate change and concerns over declining krill abundance in the Southern Ocean.

The metabolic cost of subcutaneous and abdominal rewarming in king penguins after long-term immersion in cold water.

Marine endotherms in the polar regions face a formidable thermal challenge when swimming in cold water. Hence, they use morphological (fat, blubber) adjustment and peripheral vasoconstriction to reduce demands for heat production in water. The animals then regain normothermia when resting ashore. In the king penguin (Aptenodytes patagonicus) metabolic rate is lower in fed than in fasted individuals during subsequent rewarming on land. This has been suggested to be a consequence of diversion of blood flow to the splanchnic region in fed birds, which reduces peripheral temperatures. However, peripheral temperatures during recovery have never been investigated in birds with different nutritional status. The aim of this study was, therefore, to measure subcutaneous and abdominal temperatures during the rewarming phase on land in fasted and fed king penguins, and investigate to which extent any different rewarming were reflected in recovery metabolic rate (MRR) after long term immersion in cold water. We hypothesized that fed individuals would have a slower increase of subcutaneous temperatures compared to fasted penguins, and a correspondingly lower MRR. Subcutaneous tissues reached normothermia after 24.15 (back) and 21.36 min (flank), which was twice as fast as in the abdomen (46.82 min). However, recovery time was not affected by nutritional condition. MRR during global rewarming (4.56 ± 0.42 W kg-1) was twice as high as resting metabolic rate (RMR; 2.16 ± 0.59 W kg-1). However, MRR was not dependent on feeding status and was significantly elevated above RMR only until subcutaneous temperature had recovered. Contrary to our prediction, fed individuals did not reduce the subcutaneous circulation compared to fasted penguins and did not show any changes in MRR during subsequent recovery. It seems likely that lower metabolic rate in fed king penguins on land reported in other studies might not have been caused primarily by increased circulation to the visceral organs.

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

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.

High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins.

Flight is a key adaptive trait. Despite its advantages, flight has been lost in several groups of birds, notably among seabirds, where flightlessness has evolved independently in at least five lineages. One hypothesis for the loss of flight among seabirds is that animals moving between different media face tradeoffs between maximizing function in one medium relative to the other. In particular, biomechanical models of energy costs during flying and diving suggest that a wing designed for optimal diving performance should lead to enormous energy costs when flying in air. Costs of flying and diving have been measured in free-living animals that use their wings to fly or to propel their dives, but not both. Animals that both fly and dive might approach the functional boundary between flight and nonflight. We show that flight costs for thick-billed murres (Uria lomvia), which are wing-propelled divers, and pelagic cormorants (Phalacrocorax pelagicus) (foot-propelled divers), are the highest recorded for vertebrates. Dive costs are high for cormorants and low for murres, but the latter are still higher than for flightless wing-propelled diving birds (penguins). For murres, flight costs were higher than predicted from biomechanical modeling, and the oxygen consumption rate during dives decreased with depth at a faster rate than estimated biomechanical costs. These results strongly support the hypothesis that function constrains form in diving birds, and that optimizing wing shape and form for wing-propelled diving leads to such high flight costs that flying ceases to be an option in larger wing-propelled diving seabirds, including penguins.

How much is too much? Assessment of prey consumption by Magellanic penguins in Patagonian colonies.

Penguins are major consumers in the southern oceans although quantification of this has been problematic. One suggestion proposes the use of points of inflection in diving profiles ('wiggles') for this, a method that has been validated for the estimation of prey consumption by Magellanic penguins (Spheniscus magellanicus) by Simeone and Wilson (2003). Following them, we used wiggles from 31 depth logger-equipped Magellanic penguins foraging from four Patagonian colonies; Punta Norte (PN), Bahía Bustamente (BB), Puerto Deseado (PD) and Puerto San Julián (PSJ), all located in Argentina between 42-49° S, to estimate the prey captured and calculate the catch per unit time (CPUT) for birds foraging during the early chick-rearing period. Numbers of prey caught and CPUT were significantly different between colonies. Birds from PD caught the highest number of prey per foraging trip, with CPUT values of 68±19 prey per hour underwater (almost two times greater than for the three remaining colonies). We modeled consumption from these data and calculate that the world Magellanic penguin population consumes about 2 million tons of prey per year. Possible errors in this calculation are discussed. Despite this, the analysis of wiggles seems a powerful and simple tool to begin to quantify prey consumption by Magellanic penguins, allowing comparison between different breeding sites. The total number of wiggles and/or CPUT do not reflect, by themselves, the availability of food for each colony, as the number of prey consumed by foraging trip is strongly associated with the energy content and wet mass of each colony-specific 'prey type'. Individuals consuming more profitable prey could be optimizing the time spent underwater, thereby optimizing the energy expenditure associated with the dives.

Activity time budget during foraging trips of emperor penguins.

We developed an automated method using depth and one axis of body acceleration data recorded by animal-borne data loggers to identify activities of penguins over long-term deployments. Using this technique, we evaluated the activity time budget of emperor penguins (n = 10) both in water and on sea ice during foraging trips in chick-rearing season. During the foraging trips, emperor penguins alternated dive bouts (4.8 ± 4.5 h) and rest periods on sea ice (2.5 ± 2.3 h). After recorder deployment and release near the colony, the birds spent 17.9 ± 8.4% of their time traveling until they reached the ice edge. Once at the ice edge, they stayed there more than 4 hours before the first dive. After the first dive, the mean proportions of time spent on the ice and in water were 30.8 ± 7.4% and 69.2 ± 7.4%, respectively. When in the water, they spent 67.9 ± 3.1% of time making dives deeper than 5 m. Dive activity had no typical diurnal pattern for individual birds. While in the water between dives, the birds had short resting periods (1.2 ± 1.7 min) and periods of swimming at depths shallower than 5 m (0.25 ± 0.38 min). When the birds were on the ice, they primarily used time for resting (90.3 ± 4.1% of time) and spent only 9.7 ± 4.1% of time traveling. Thus, it appears that, during foraging trips at sea, emperor penguins traveled during dives >5 m depth, and that sea ice was primarily used for resting. Sea ice probably provides refuge from natural predators such as leopard seals. We also suggest that 24 hours of sunlight and the cycling of dive bouts with short rest periods on sea ice allow emperor penguins to dive continuously throughout the day during foraging trips to sea.

Spatially integrated assessment reveals widespread changes in penguin populations on the Antarctic Peninsula.

As important marine mesopredators and sensitive indicators of Antarctic ecosystem change, penguins have been a major focus of long-term biological research in the Antarctic. However, the vast majority of such studies have been constrained by logistics and relate mostly to the temporal dynamics of individual breeding populations from which regional trends have been inferred, often without regard for the complex spatial heterogeneity of population processes and the underlying environmental conditions. Integrating diverse census data from 70 breeding sites across 31 years in a robust, hierarchical analysis, we find that trends from intensely studied populations may poorly reflect regional dynamics and confuse interpretation of environmental drivers. Results from integrated analyses confirm that Pygoscelis adeliae (Adélie Penguins) are decreasing at almost all locations on the Antarctic Peninsula. Results also resolve previously contradictory studies and unambiguously establish that P. antarctica (Chinstrap Penguins), thought to benefit from decreasing sea ice, are instead declining regionally. In contrast, another open-water species, P. papua (Gentoo Penguin), is increasing in abundance and expanding southward. These disparate population trends accord with recent mechanistic hypotheses of biological change in the Southern Ocean and highlight limitations of the influential but oversimplified "sea ice" hypothesis. Aggregating population data at the regional scale also allows us to quantify rates of regional population change in a way not previously possible.

Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector?

Dynamic body acceleration (DBA) has been used as a proxy for energy expenditure in logger-equipped animals, with researchers summing the acceleration (overall dynamic body acceleration--ODBA) from the three orthogonal axes of devices. The vector of the dynamic body acceleration (VeDBA) may be a better proxy so this study compared ODBA and VeDBA as proxies for rate of oxygen consumption using humans and 6 other species. Twenty-one humans on a treadmill ran at different speeds while equipped with two loggers, one in a straight orientation and the other skewed, while rate of oxygen consumption (VO2) was recorded. Similar data were obtained from animals but using only one (straight) logger. In humans, both ODBA and VeDBA were good proxies for VO2 with all r(2) values exceeding 0.88, although ODBA accounted for slightly but significantly more of the variation in VO2 than did VeDBA (P<0.03). There were no significant differences between ODBA and VeDBA in terms of the change in VO2 estimated by the acceleration data in a simulated situation of the logger being mounted straight but then becoming skewed (P = 0.744). In the animal study, ODBA and VeDBA were again good proxies for VO2 with all r(2) values exceeding 0.70 although, again, ODBA accounted for slightly, but significantly, more of the variation in VO2 than did VeDBA (P<0.03). The simultaneous contraction of muscles, inserted variously for limb stability, may produce muscle oxygen use that at least partially equates with summing components to derive DBA. Thus, a vectorial summation to derive DBA cannot be assumed to be the more 'correct' calculation. However, although within the limitations of our simple study, ODBA appears a marginally better proxy for VO2. In the unusual situation where researchers are unable to guarantee at least reasonably consistent device orientation, they should use VeDBA as a proxy for VO2.

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.

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.

Yolk androgen deposition without an energetic cost for female rockhopper penguins: a compensatory strategy to accelerate brood reduction?

Whether androgen deposition in eggs is physiologically costly for female birds has remained a crucial but unsolved question, despite a broad use of this assumption in functional studies. We tested whether females depositing high androgen concentrations experienced higher mass losses than females depositing low androgen concentrations. Analysing female body mass change during egg formation in rockhopper penguins (Eudyptes chrysocome chrysocome), we observed no energetic cost to androgen deposition. Nevertheless, lighter females laid eggs with higher yolk androgen concentrations. This relationship existed only for the second-laid egg (B-egg), but not for the first-laid egg (A-egg). Since the B-egg is usually the first to hatch and the only one to produce a fledging chick, we hypothesize that differential yolk androgen deposition may be an adaptive strategy for females to affect brood reduction.

Scaling of swim speed and stroke frequency in geometrically similar penguins: they swim optimally to minimize cost of transport.

It has been predicted that geometrically similar animals would swim at the same speed with stroke frequency scaling with mass(-1/3). In the present study, morphological and behavioural data obtained from free-ranging penguins (seven species) were compared. Morphological measurements support the geometrical similarity. However, cruising speeds of 1.8-2.3 m s(-1) were significantly related to mass(0.08) and stroke frequencies were proportional to mass(-0.29). These scaling relationships do not agree with the previous predictions for geometrically similar animals. We propose a theoretical model, considering metabolic cost, work against mechanical forces (drag and buoyancy), pitch angle and dive depth. This new model predicts that: (i) the optimal swim speed, which minimizes the energy cost of transport, is proportional to (basal metabolic rate/drag)(1/3) independent of buoyancy, pitch angle and dive depth; (ii) the optimal speed is related to mass(0.05); and (iii) stroke frequency is proportional to mass(-0.28). The observed scaling relationships of penguins support these predictions, which suggest that breath-hold divers swam optimally to minimize the cost of transport, including mechanical and metabolic energy during dive.

Heart rate as a predictor of energy expenditure in undisturbed fasting and incubating penguins.

Heart rate (f(H)) measurement offers the possibility to monitor energy expenditure (EE) in wild animals if the EE/f(H) relationship for the species, physiological stages and activities of interest is known. This relationship has been extensively studied using oxygen consumption rate ( ) measurement in captive, repeatedly handled king penguins (Aptenodytes patagonicus). Unfortunately, the potential effects of stress on the observed relationships resulting from handling and confinement were not considered. This study is the first involving undisturbed animals, and determines the EE/f(H) relationship in naturally fasting and freely incubating or captivity-acclimatized male and female king penguins. EE determination was based on (1) the measurement of body mass loss during periods of phase II fasting, and (2) the calculation of its energy equivalent from changes in body composition, i.e. 23.9 kJ g(-1). f(H) levels in freely incubating and captivity-acclimatized birds were found to be 50-70% lower than those previously reported for resting king penguins during measurements. Significant EE/f(H) relationships were found in freely incubating and captive males and females (R(2)=0.59 to 0.84), with no difference observed between genders. The best overall relationship was obtained by including fasting duration (t, days) in the model: EE=818+43.7xf(H)+36.3t-1.4txf(H) (R(2)=0.91). This equation yielded EE estimates approximately 26% higher than the previously reported 'best' predictive equation in king penguins, and even more so when f(H) was low. This result suggests that stress induces a disproportionate increase of f(H) vs O(2) consumption, and that the use of EE/f(H) relationships obtained in stressed birds could lead to underestimated EE values.

An improved model of heat transfer through penguin feathers and down.

Penguins, mostly live in the extremely cold Antarctic, are known to have feathers and down, which are light weight, compact and extremely efficient in preventing heat loss. Nevertheless, the mechanisms of heat transfer through the penguin feathers and down, and how the unique characteristics of penguin feathers and down make them such good thermal insulators are not fully understood. In this paper, an integrated model of heat transfer through the penguin feathers and down is developed and computed using finite volume method, with the geometrical structure of the barbules being considered. Monte-Carlo method is adopted to determine the radiative absorption and emission constant in the integrated model. The effective thermal conductance of penguin feathers and down computed from our model compared well with the experimentally measured value reported in the literature. Three models (penguin model, random fibre model (fibre radius=3microm) and random fibre model (fibre radius=10microm)) are further simulated and compared. Results showed that the relative small radius of the barbules of penguin feather and their geometrical structure are responsible for the reduction of heat loss in cold environment.

Improving the precision and accuracy for estimating energy expenditure using the heart rate method.

The "heart rate technique" is commonly used to estimate the rate of oxygen consumption (a proxy for energy expenditure) of free-ranging animals. However, a major limitation of this technique is that interindividual variability in the relationship between heart rate (f(H)) and rate of oxygen consumption (Vo2) generates large errors of estimation when the technique is applied to individual free-ranging animals. In this study, we present a new analysis technique that takes advantage of the observation that the f(H) or Vo2 relationships between individuals are frequently parallel and differ only in elevation. This technique offers superior accuracy and precision of Vo2 estimates, reducing the coefficient of variability from 18% to 9% for individual animals in an example application in macaroni penguins. This approach enables application of the heart rate technique to deduce the energetic strategies of individual animals.

Antennae on transmitters on penguins: balancing energy budgets on the high wire.

The effect of externally mounted antennae on the energetics of penguins was studied by mounting various antennae on a transducer fixed to a model Magellanic penguin Spheniscus magellanicus to determine drag, run at speeds of up to 2 m s(-1) in a swim canal. For rigid antennae set perpendicular to the water flow, measured drag increased with increasing swim speed. Increasing antenna length (for lengths between 100 and 200 mm) or diameter (for diameters between 1 and 4 mm) resulted in accelerating increased drag as a function of both antenna length and diameter. Where antennae were positioned at acute angles to the water flow, drag was markedly reduced, as was drag at higher speeds in flexible antennae. These results were incorporated in a model on the foraging energetics of free-living Magellanic penguins using data (on swim speeds, intervals between prey encounters, amount ingested per patch and dive durations) derived from previously published work and from a field study conducted on birds from a colony at Punta Norte, Argentina, using data loggers. The field work indicated that free-living birds have a foraging efficiency (net energy gain/net energy loss) of about 2.5. The model predicted that birds equipped with the largest rigid external antennae tested (200 mm x 3 mm diameter), set perpendicular to water flow, increased energy expenditure at normal swim speeds of 1.77 m s(-1) by 79% and at prey capture speeds of 2.25 m s(-1) by 147%, and ultimately led to a foraging efficiency that was about 5 times less than that of unequipped birds. Highly flexible antennae were shown to reduce this effect considerably. Deleterious antenna-induced effects are predicted to be particularly critical in penguins that have to travel fast to capture prey. Possible measures taken by the birds to increase foraging efficiency could include reduced travelling speed and selection of smaller prey types. Suggestions are made as to how antenna-induced drag might be minimized for future studies on marine diving animals.