Applying science to pressing conservation needs for penguins.

More than half of the world's 18 penguin species are declining. We, the Steering Committee of the International Union for Conservation of Nature Species Survival Commission Penguin Specialist Group, determined that the penguin species in most critical need of conservation action are African penguin (Spheniscus demersus), Galápagos penguin (Spheniscus mendiculus), and Yellow-eyed penguin (Megadyptes antipodes). Due to small or rapidly declining populations, these species require immediate scientific collaboration and policy intervention. We also used a pairwise-ranking approach to prioritize research and conservation needs for all penguins. Among the 12 cross-taxa research areas we identified, we ranked quantifying population trends, estimating demographic rates, forecasting environmental patterns of change, and improving the knowledge of fisheries interactions as the highest priorities. The highest ranked conservation needs were to enhance marine spatial planning, improve stakeholder engagement, and develop disaster-management and species-specific action plans. We concurred that, to improve the translation of science into effective conservation for penguins, the scientific community and funding bodies must recognize the importance of and support long-term research; research on and conservation of penguins must expand its focus to include the nonbreeding season and juvenile stage; marine reserves must be designed at ecologically appropriate spatial and temporal scales; and communication between scientists and decision makers must be improved with the help of individual scientists and interdisciplinary working groups.

Aplicación de Ciencia en las Necesidades de Conservación Urgentes para los Pingüinos. Resumen Más de la mitad de las 18 especies de pingüinos del mundo están disminuyendo. Nosotros, el Comité Directivo de la Unión Internacional para la Conservación de la Naturaleza, Grupo de Especialistas en Pingüinos, determinamos que las especies de pingüinos con necesidades críticas de conservación son el pingüino africano (Spheniscus demersus), el pingüino de las Galápagos (Spheniscus mendiculus) y el pingüino de ojos amarillos (Megadyptes antipodes). Debido a que sus poblaciones son pequeñas o están declinando rápidamente, estos pingüinos requieren colaboración científica e intervención política inmediatas. También utilizamos un método de clasificación por pares para priorizar las necesidades de investigación y conservación para todas las especies de pingüinos. Entre las 12 áreas de investigación que identificamos, las más prioritarias fueron: cuantificación de las tendencias poblacionales, estimación de las tasas demográficas, predicción de las patrones de cambio ambiental y mejora del conocimiento de las interacciones con pesquerías. Las mayores necesidades de conservación fueron: optimizar la planificación marina espacial, mejorar la colaboración de las partes interesadas y desarrollar planes de manejo de desastres y de acción para cada especie. Coincidimos en que, para mejorar la traducción de la ciencia en la conservación efectiva de los pingüinos, la comunidad científica y los organismos financiadores deben reconocer la importancia de la investigación a largo plazo y apoyarla; la investigación sobre pingüinos y su conservación debe expandir su enfoque para incluir la época no reproductiva y la etapa juvenil; las reservas marinas deben ser diseñadas a escalas espaciotemporales ecológicamente apropiadas; y la comunicación entre científicos y tomadores de decisiones debe mejorar con la ayuda de científicos individuales y grupos de trabajo interdisciplinario.

Exploration during early life: distribution, habitat and orientation preferences in juvenile king penguins.

BACKGROUND: The early life of marine apex predators is poorly known, particularly for diving species. The orientation and foraging skills are presumably less developed in juveniles than in adults, especially during their first year at sea when juveniles might disperse further than adults. METHODS: Over two years of monitoring, we tracked the movements of 17 juvenile king penguins (Aptenodytes patagonicus, ~ 1 year old) using satellite relay tags from Crozet Archipelago (Southern Indian Ocean), starting when birds left their natal colony for the first time. For comparison we also tagged 6 non-breeding adults, which at that stage, similar to juveniles, are unhampered by reproductive constraints and might roam further than breeders. We used a combination of cluster analysis and habitat modelling to investigate and compare the movement patterns and habitat use of experienced (non-breeding adults) and non-experienced (juveniles) individuals. RESULTS: While juvenile penguins and non-breeding adults followed similar routes, the movements by adults started later in the season and ranged over a considerably smaller area than juveniles. Net squared displacement analysis revealed that both groups did not move to a specific wintering area. Changes in direction of juveniles in respect to their departure island were similar and synchronous for both years. Habitat models revealed that foraging behaviour was affected by environmental variables such as wind or current speeds, sea surface temperature, or oceanic productivity, for both stages. Analysis of tracks revealed that birds moved predominately perpendicular or against the main direction of the Antarctic Circumpolar Current and the prevailing wind during austral summer (juveniles only) and autumn (juveniles and non-breeding adults). However, both juveniles and adults were more likely to move against the prevailing winds if productivity increased along their trajectories. CONCLUSIONS: The exceptional duration of our tracking study provided unprecedented insights into the distribution, habitat preferences and orientation of two poorly known life history stages of an expert avian diver. Our study suggests that juveniles might use both innate and learnt skills to reach profitable foraging areas during their first year at sea, which is critical in long-lived species.

Where do penguins go during the inter-breeding period? Using geolocation to track the winter dispersion of the macaroni penguin.

Although penguins are key marine predators from the Southern Ocean, their migratory behaviour during the inter-nesting period remains widely unknown. Here, we report for the first time, to our knowledge, the winter foraging movements and feeding habits of a penguin species by using geolocation sensors fitted on penguins with a new attachment method. We focused on the macaroni penguin Eudyptes chrysolophus at Kerguelen, the single largest consumer of marine prey among all seabirds. Overall, macaroni penguins performed very long winter trips, remaining at sea during approximately six months within the limits of the Southern Ocean. They departed from Kerguelen in an eastward direction and distributed widely, over more than 3.10(6) km(2). The penguins spent most of their time in a previously unrecognized foraging area, i.e. a narrow latitudinal band (47-49 degrees S) within the central Indian Ocean (70-110 degrees E), corresponding oceanographically to the Polar Frontal Zone. There, their blood isotopic niche indicated that macaroni penguins preyed mainly upon crustaceans, but not on Antarctic krill Euphausia superba, which does not occur at these northern latitudes. Such winter information is a crucial step for a better integrative approach for the conservation of this species whose world population is known to be declining.

Modeling the marine resources consumed in raising a king penguin chick: an energetics approach.

Accurate estimates of penguin energetics would represent an important contribution to our understanding of the trophodynamics of the Southern Ocean ecosystem and our ability to predict effects of environmental change on these species. We used the heart rate-rate of oxygen consumption technique to estimate rate of energy expenditure in adult king penguins raising a chick, in combination with data from the literature on changes in adult mass, chick energy requirements, and prey energy density. Our model estimated a variety of energetic costs and quantities of prey consumption related to raising a king penguin chick during the austral summer. The total energy requirements of a king penguin chick at the Crozet Archipelago from hatching until reaching a mass of 8 kg 90 d later is 271 MJ, representing the consumption of 38.4 kg of myctophid fish. A successfully breeding male requires 0.78 kg d(-1) of fish during the entirety of the incubation period and 1.14 kg d(-1) during the subsequent 90 d of chick rearing. Assuming the same energy requirements for females, the estimated 580,000 pairs of king penguins that breed successfully at Crozet each year, together with their chicks, consume a total of around 190,000 tons of fish during the incubation and summer rearing periods combined. If, due to depletion of fish stocks, the diet of breeders and chicks during the summer becomes identical to the typical diet of adults during the austral winter, the mass of prey required by both adults and chicks combined (where the chick still reaches 8 kg after 90 d) would increase by more than 25%.

Southern Ocean frontal structure and sea-ice formation rates revealed by elephant seals.

Polar regions are particularly sensitive to climate change, with the potential for significant feedbacks between ocean circulation, sea ice, and the ocean carbon cycle. However, the difficulty in obtaining in situ data means that our ability to detect and interpret change is very limited, especially in the Southern Ocean, where the ocean beneath the sea ice remains almost entirely unobserved and the rate of sea-ice formation is poorly known. Here, we show that southern elephant seals (Mirounga leonina) equipped with oceanographic sensors can measure ocean structure and water mass changes in regions and seasons rarely observed with traditional oceanographic platforms. In particular, seals provided a 30-fold increase in hydrographic profiles from the sea-ice zone, allowing the major fronts to be mapped south of 60 degrees S and sea-ice formation rates to be inferred from changes in upper ocean salinity. Sea-ice production rates peaked in early winter (April-May) during the rapid northward expansion of the pack ice and declined by a factor of 2 to 3 between May and August, in agreement with a three-dimensional coupled ocean-sea-ice model. By measuring the high-latitude ocean during winter, elephant seals fill a "blind spot" in our sampling coverage, enabling the establishment of a truly global ocean-observing system.

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.

Buoyancy and maximal diving depth in penguins: do they control inhaling air volume?

Using a newly developed data logger to measure acceleration, we demonstrate that free-ranging king and Adélie penguins only beat their flippers substantially during the first part of descent or when they were presumed to be chasing prey at the bottom of dives. Flipper beating stopped during the latter part of ascent: at 29+/-9 % (mean +/- S.D.) of dive depth (mean dive depth=136.8+/-145.1 m, N=425 dives) in king penguins, and at 52+/-20 % of dive depth (mean dive depth=72.9+/-70.5 m, N=664 dives) in Adélie penguins. Propulsive swim speeds of both species were approximately 2 m s(-1) during dives; however, a marked increase in speed, up to approximately 2.9 m s(-1), sometimes occurred in king penguins during the passive ascending periods. During the prolonged ascending, oblique ascent angle and slowdown near the surface may represent one way to avoid the potential risk of decompression sickness. Biomechanical calculations for data from free-ranging king and Adélie penguins indicate that the air volume of the birds (respiratory system and plumage) can provide enough buoyancy for the passive ascent. When comparing the passive ascents for shallow and deep dives, there is a positive correlation between air volume and the depth of the dive. This suggests that penguins regulate their air volume to optimize the costs and benefits of buoyancy.

Feeding behaviour of free-ranging penguins determined by oesophageal temperature.

Sea birds play a major role in marine food webs, and it is important to determine when and how much they feed at sea. A major advance has been made by using the drop in stomach temperature after ingestion of ectothermic prey. This method is less sensitive when birds eat small prey or when the stomach is full. Moreover, in diving birds, independently of food ingestion, there are fluctuations in the lower abdominal temperature during the dives. Using oesophageal temperature, we present here a new method for detecting the timing of prey ingestion in free-ranging sea birds, and, to our knowledge, report the first data obtained on king penguins (Aptenodytes patagonicus). In birds ashore, which were hand-fed 2-15 g pieces of fish, all meal ingestions were detected with a sensor in the upper oesophagus. Detection was poorer with sensors at increasing distances from the beak. At sea, slow temperature drops in the upper oesophagus and stomach characterized a diving effect per se. For the upper oesophagus only, abrupt temperature variations were superimposed, therefore indicating prey ingestions. We determined the depths at which these occurred. Combining the changes in oesophageal temperatures of marine predators with their diving pattern opens new perspectives for understanding their foraging strategy, and, after validation with concurrent applications of classical techniques of prey survey, for assessing the distribution of their prey.

Impact of externally attached loggers on the diving behaviour of the king penguin.

The impact of relatively small externally attached time series recorders on some foraging parameters of seabirds was investigated during the austral summer of 1995 by monitoring the diving behaviour of 10 free-ranging king penguins (Aptenodytes patagonicus) over one foraging trip. Time-depth recorders were implanted in the abdominal cavities of the birds, and half of the animals also had dummy loggers attached on their backs. Although most of the diving behaviour was not significantly affected by the external loggers (P>0.05), the birds with externally attached loggers performed almost twice as many shallow dives, between 0 and 10 m depth, as the birds without external loggers. These shallow dives interrupted more frequently the deep-diving sequences in the case of birds with external loggers (percentage of deep dives followed by deep dives: 46% for birds with implants only vs. 26% for birds with an external attachment). Finally, the distribution pattern of the postdive durations plotted against the hour of the day was more heterogeneous for the birds with an external package. In addition, these penguins had extended surfacing times between two deep dives compared to birds without external attachments (P<0.0001). These results suggest the existence of an extra energy cost induced by externally attached loggers.

Seabirds as monitors of upper-ocean thermal structure. King penguins at the Antarctic polar front, east of Kerguelen sector.

The main objective of this work was to assess the potential of diving birds to monitor the hydrographic features near the Antarctic polar front. We compared the temperature/depth profiles recorded by instrumented King penguins Aptenodytes patagonicus at Kerguelen Islands (South Indian Ocean) with the oceanographic and remote sensing (satellite) data available for the same area during the same season. The birds were equipped with time/depth/temperature recorders or Argos transmitters. In addition, two birds were instrumented (of which one successfully) both with a time/depth/temperature recorder and an Argos transmitter. King penguins foraged as far as 400 km from the coast, in water masses with a vertical temperature structure characteristic of the region just south of the polar front. The temperature/depth profiles recorded throughout the dives (up to 270 m) revealed a pronounced thermocline. A three-dimensional distribution of water temperature was reconstructed. Comparison with previous hydrographic data shows a high correlation. Instrumented predators may therefore usefully and cheaply complement the database provided by conventional hydrographic surveys and remote sensing, especially in distant and rough areas such as the Southern Ocean.

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.

Diving energetics in king penguins (Aptenodytes patagonicus).

Dive duration in wild king penguins and the energetic cost of swimming in a 30m long swim channel were determined at Ile de la Possession, Crozet Archipelago, using external data loggers and respirometry, respectively. Calibrated electronic data loggers equipped with a pressure sensor were used to determine dive durations: 95% of dives were less than 6 min long and 66% of dives were less than 4 min long. Dive patterns show that king penguins may intersperse long dive durations (4-6.3 min) with short ones (1.5-3 min) and make surface pauses of variable duration between them (0.5-3.5 min), or dive regularly (for up to 5 h) with long dive durations (5 min) and constant interdive surface intervals (1.5 min). The latter indicates that the aerobic dive limits (ADL) of this species could be higher and oxygen consumption lower than previously reported. Assuming that king penguins dive within their aerobic limit, different approaches to the analysis of the data obtained in the swim channel are discussed to derive the ADL. Swimming speeds observed in the channel ranged from 0.9 to 3.4 m s-1. Transport costs were lowest between 1.8 and 2.2 m s-1. Although at 2.2 m s-1 king penguins used only 10.3 Wkg-1 over a dive+surface cycle (minimal transport costs of 4.7 J kg-1 m-1), we speculate that tisse oxygen consumption during submergence may be as low as 0.23 ml O2 kg-1 s-1 (2.1 times standard metabolic rate, SMR) or perhaps lower (which gives an ADL of 4.2 min). During surface phases, oxygen uptake would be increased to at least 1 ml O2kg-1 s-1 (9.3 times SMR). This implies that at least 70% of all dives are aerobic. Potential physiological mechanisms allowing king penguins to partition O2 consumption between submergence and surface periods remain, however, unclear.