Combined use of two supervised learning algorithms to model sea turtle behaviours from tri-axial acceleration data.

Accelerometers are becoming ever more important sensors in animal-attached technology, providing data that allow determination of body posture and movement and thereby helping to elucidate behaviour in animals that are difficult to observe. We sought to validate the identification of sea turtle behaviours from accelerometer signals by deploying tags on the carapace of a juvenile loggerhead (Caretta caretta), an adult hawksbill (Eretmochelys imbricata) and an adult green turtle (Chelonia mydas) at Aquarium La Rochelle, France. We recorded tri-axial acceleration at 50 Hz for each species for a full day while two fixed cameras recorded their behaviours. We identified behaviours from the acceleration data using two different supervised learning algorithms, Random Forest and Classification And Regression Tree (CART), treating the data from the adult animals as separate from the juvenile data. We achieved a global accuracy of 81.30% for the adult hawksbill and green turtle CART model and 71.63% for the juvenile loggerhead, identifying 10 and 12 different behaviours, respectively. Equivalent figures were 86.96% for the adult hawksbill and green turtle Random Forest model and 79.49% for the juvenile loggerhead, for the same behaviours. The use of Random Forest combined with CART algorithms allowed us to understand the decision rules implicated in behaviour discrimination, and thus remove or group together some 'confused' or under--represented behaviours in order to get the most accurate models. This study is the first to validate accelerometer data to identify turtle behaviours and the approach can now be tested on other captive sea turtle species.

Emperor penguin body surfaces cool below air temperature.

Emperor penguins Aptenodytes forsteri are able to survive the harsh Antarctic climate because of specialized anatomical, physiological and behavioural adaptations for minimizing heat loss. Heat transfer theory predicts that metabolic heat loss in this species will mostly depend on radiative and convective cooling. To examine this, thermal imaging of emperor penguins was undertaken at the breeding colony of Pointe Géologie in Terre Adélie (66°40' S 140° 01' E), Antarctica in June 2008. During clear sky conditions, most outer surfaces of the body were colder than surrounding sub-zero air owing to radiative cooling. In these conditions, the feather surface will paradoxically gain heat by convection from surrounding air. However, owing to the low thermal conductivity of plumage any heat transfer to the skin surface will be negligible. Future thermal imaging studies are likely to yield further insights into the adaptations of this species to the Antarctic climate.

Influence of weather conditions on the flight of migrating black storks.

This study tested the potential influence of meteorological parameters (temperature, humidity, wind direction, thermal convection) on different migration characteristics (namely flight speed, altitude and direction and daily distance) in 16 black storks (Ciconia nigra). The birds were tracked by satellite during their entire autumnal and spring migration, from 1998 to 2006. Our data reveal that during their 27-day-long migration between Europe and Africa (mean distance of 4100 km), the periods of maximum flight activity corresponded to periods of maximum thermal energy, underlining the importance of atmospheric thermal convection in the migratory flight of the black stork. In some cases, tailwind was recorded at the same altitude and position as the birds, and was associated with a significant rise in flight speed, but wind often produced a side azimuth along the birds' migratory route. Whatever the season, the distance travelled daily was on average shorter in Europe than in Africa, with values of 200 and 270 km d(-1), respectively. The fastest instantaneous flight speeds of up to 112 km h(-1) were also observed above Africa. This observation confirms the hypothesis of thermal-dependant flight behaviour, and also reveals differences in flight costs between Europe and Africa. Furthermore, differences in food availability, a crucial factor for black storks during their flight between Europe and Africa, may also contribute to the above-mentioned shift in daily flight speeds.

Ecophysiological response of Adelie penguins facing an experimental increase in breeding constraints.

Foraging strategies play a key role in breeding effort. Little is known, however, about their connection with hormonal and nutritional states, especially when breeding constraints vary. Here, we experimentally increased foraging costs and thus breeding constraints by handicapping Adélie penguins (Pygoscelis adeliae) with dummy devices representing 3-4% of the penguins' cross-sectional area. We examined food-related stress (via plasma corticosterone concentration) and nutritional state (via metabolite levels). Concurrently, we investigated the use of ecological niches via the isotopic signature of red blood cells indicating the trophic position (delta(15)N) and the spatial distribution (delta(13)C) of penguins. Handicapped birds performed approximately 70% longer foraging trips and lost approximately 60% more body mass than controls and their partners. However, corticosterone levels and the nutritional state were unchanged. The isotopic signature revealed that males and females differed in their foraging behaviour: upper trophic levels contributed more in the males' diet, who foraged in more pelagic areas. Handicapped and partner birds adopted the same strategy at sea: a shift towards higher delta(13)C values suggested that they foraged in more coastal areas than controls. This change in foraging decisions may optimize feeding time by decreasing travelling time. This may partly compensate for the presumed lower foraging efficiency of handicapped birds and for the energetic debt of their partners who had to fast approximately 70% longer on the nest. We propose that this flexible use of ecological niches may allow birds facing increased breeding constraints to avoid chronic stress and to minimize the impact on their body condition.

Heart rate and energetics of free-ranging king penguins (Aptenodytes patagonicus).

The main objective of this study was to determine heart rate (fh) and the energetic costs of specific behaviours of king penguins while ashore and while foraging at sea during their breeding period. In particular, an estimate was made of the energetic cost of diving in order to determine the proportion of dives that may exceed the calculated aerobic dive limit (cADL; estimated usable O2 stores/estimated rate of oxygen consumption during diving). An implanted data logger enabled fh and diving behaviour to be monitored from 10 free-ranging king penguins during their breeding period. Using previously determined calibration equations, it was possible to estimate rate of oxygen consumption (VO2) when the birds were ashore and during various phases of their foraging trips. Diving behaviour showed a clear diurnal pattern, with a mixture of deep (>40 m), long (>3 min) and shallow (<40 m), short (<3 min) dives from dawn to dusk and shallow, short dives at night. Heart rate during dive bouts and dive cycles (dive + post-dive interval) was 42% greater than that when the birds were ashore. During diving, fh was similar to the 'ashore' value (87+/-4 beats min(-1)), but it did decline to 76% of the value recorded from king penguins resting in water. During the first hour after a diving bout, fh was significantly higher than the average value during diving (101+/-4 beats min(-1)) and for the remainder of the dive bout. Rates of oxygen consumption estimated from these (and other) values of fh indicate that when at sea, metabolic rate (MR) was 83% greater than that when the birds were ashore [3.15 W kg(-1) (-0.71, +0.93), where the values in parentheses are the computed standard errors of the estimate], while during diving bouts and dive cycles, it was 73% greater than the 'ashore' value. Although estimated MR during the total period between dive bouts was not significantly different from that during dive bouts [5.44 W kg(-1) (-0.30, +0.32)], MR during the first hour following a dive bout was 52% greater than that during a diving bout. It is suggested that this large increase following diving (foraging) activity is, at least in part, the result of rewarming the body, which occurs at the end of a diving bout. From the measured behaviour and estimated values of VO2, it was evident that approximately 35% of the dives were in excess of the cADL. Even if VO2 during diving was assumed to be the same as when the birds were resting on water, approximately 20% of dives would exceed the cADL. As VO2 during diving is, in fact, that estimated for a complete dive cycle, it is quite feasible that VO2 during diving itself is less than that measured for birds resting in water. It is suggested that the regional hypothermia that has been recorded in this species during diving bouts may be at least a contributing factor to such hypometabolism.

Adjustments of gastric pH, motility and temperature during long-term preservation of stomach contents in free-ranging incubating king penguins.

Male king penguins are able to store undigested food in their stomach for up to 3 weeks during their incubation fast, which evidently implies some modification of their digestive process. Using small electronic recorders, we studied the change in gastric pH, motility and temperature during the first week of food storage. The pH could be maintained at values as high as 6 throughout the incubation fast, a pH that is unfavourable for avian gastric proteinase activity. Gastric motility was never completely inhibited but could be markedly reduced. Stomach temperature was maintained at around 38 degrees C. The fact that stomach temperature of incubating birds did not show a daily rhythmic fluctuation as seen in non-breeding birds could be due to temperature constraints on embryo development. Thus the present study demonstrates substantial adjustments of pH and gastric motility in incubating king penguins, which may contribute to the inhibition of digestive gastric processes.

Effects of fasting and refeeding on jejunal morphology and cellular activity in rats in relation to depletion of body stores.

BACKGROUND: Intestinal mucosa atrophy following a period of starvation characterized by the mobilization of fat stores for energy expenditure (phase II) worsen after a long fast marked by an increase in protein catabolism (phase III). However, the morphology of the jejunum is completely restored after 3 days of refeeding. The aim of this study was to determine the mechanisms involved in the rapid jejunal restoration following the critical phase III. METHODS: Jejunal structure was observed through conventional and environmental scanning electron microscopy, whilst cellular dynamics were studied using classical optic microscopy tools and immunohistochemistry. RESULTS: Mucosal structural atrophy during fasting proved to worsen over the two phases. During phase II, apoptosis is still present at the tip of the villi, the number of mitosis in crypts showed a 30% decrease and a transient drop in cell migration is observed. During phase III, however, an 85% rise in mitosis was noticed along with an increase in cell migration and the disappearance of apoptotic cells at the villus tips. This increased cell renewal continues after food ingestion. CONCLUSIONS: Starved rats appeared to be in a phase of energy sparing in phase II, with depressed cellular events in the intestinal mucosa. In phase III, however, the preservation of functional cells and the early increase in crypt cell proliferation should prepare the mucosa to refeeding and could explain why jejunal repairs are complete after 3 days of refeeding following either phase II or phase III.

Long-term effects of flipper bands on penguins.

Changes in seabird populations, and particularly of penguins, offer a unique opportunity for investigating the impact of fisheries and climatic variations on marine resources. Such investigations often require large-scale banding to identify individual birds, but the significance of the data relies on the assumption that no bias is introduced in this type of long-term monitoring. After 5 years of using an automated system of identification of king penguins implanted with electronic tags (100 adult king penguins were implanted with a transponder tag, 50 of which were also flipper banded), we can report that banding results in later arrival at the colony for courtship in some years, lower breeding probability and lower chick production. We also found that the survival rate of unbanded, electronically tagged king penguin chicks after 2-3 years is approximately twice as large as that reported in the literature for banded chicks.

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.

Are non-migrant white storks (Ciconia ciconia) able to survive a cold-induced fast?

Northwestern European populations of White Storks (Ciconia ciconia) have been restored by settling young birds which, after having been maintained captive for 3 years, do not migrate when released. Since they are still supplied with food, the question we address here is how settled White Storks would cope with a fast resulting from a cold spell if food were no longer available. We therefore measured daily body mass loss, nitrogen excretion and daily energy expenditure under natural photoperiod and climatic conditions in six captive White Storks exposed to 5 days of food deprivation during winter. Daily ambient temperature ranged between -10 and 17 degrees C. After an initial decrease in both daily body mass loss and nitrogen excretion during the first day of fasting, these two parameters stabilized at low values. Lipids were the main fuel energy source (91%) and body proteins accounted for the remainder (9%). The rate of CO(2) production, measured with the doubly labeled water method, decreased significantly (P<0.001) during fasting when compared to the ad libitum value. Our data show that the metabolic adjustments of White Storks facing starvation are similar to those found in birds well-adapted to long-term fasting. From the determination of lipid and protein stores and of lipid and protein depletion rates, we conclude that White Storks would be able to survive at least during 4 weeks, a period of time twice as long as the duration of cold spells usually occurring in the Alsace region.

Restoration of the jejunal mucosa in rats refed after prolonged fasting.

To investigate the importance of body fuel depletion on gut rehabilitation after food deprivation, we compared the kinetics of jejunal mucosa alteration and restoration in rats that were refed after reaching different stages in body fuel depletion. Rats (P2) were refed while still in the so-called phase II, where body protein utilization is minimized, whereas rats (P3) were refed when they had reached the stage of increasing protein utilization (phase III). There was a significant decrease in total mass of intestine (P2, -30%; P3, -40%) and jejunal mucosa (P2, -52%; P3, -60%), as well in the size of the crypts (P2, -15%; P3, -36%) and villi (P2, -37%; P3, -55%). Structural changes of the mucosa included disappearance of some villi and a reduction in the size and number of crypts. Despite the larger morphological alterations in P3, the restoration of mucosa was as fast and complete after only 3 days of refeeding for both P2 and P3 rats. The respective roles of the mitosis pressure and of the lamina propria dynamics were studied. The rapid reversibility of the gut mucosal alterations due to fasting might constitute an integrative process.

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.

A new technique for monitoring the behaviour of free-ranging Adélie penguins.

Measurement of the time allocation of penguins at sea has been a major goal of researchers in recent years. Until now, however, no equipment has been available that would allow measurement of the aquatic and terrestrial behaviour of an Antarctic penguin while it is commuting between the colony and the foraging grounds. A new motion detector, based on the measurement of acceleration, has been used here in addition to current methods of inferring behaviour using data loggers that monitor depth and speed. We present data on the time allocation of Adélie penguins (Pygoscelis adeliae) according to the different types of behaviours they display during their foraging trips: walking, tobogganing, standing on land, lying on land, resting at the water surface, porpoising and diving. To illustrate the potential of this new technique, we compared the behaviour of Adélie penguins during the chick-rearing period in a fast sea-ice region and an ice-free region. The proportion of time spent standing, lying on land and walking during foraging trips was greater for penguins in the sea-ice region (37.6+/-13.3% standing, 21.6+/-15.6% lying and 5.9+/-6.3% walking) than for those in the ice-free region (12.0+/-15.8 % standing, 0.38+/-0.60% lying and 0 % walking), whereas the proportion of time spent resting at the water surface and porpoising was greater for birds in the ice-free region (38.1+/-6.4% resting and 1.1+/-1.1% porpoising) than for those in the sea-ice region (3.0+/-2.3% resting and 0% porpoising; means +/- s.d., N=7 for the sea-ice region, N=4 for the ice-free region). Using this new approach, further studies combining the monitoring of marine resources in different Antarctic sites and the measurement of the energy expenditure of foraging penguins, e.g. using heart rates, will constitute a powerful tool for investigating the effects of environmental conditions on their foraging strategy. This technique will expand our ability to monitor many animals in the field.

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.

Determining body fuels of wintering mallards.

Measuring body lipids and proteins of wild animals such as mallards is essential to determine the impact of the environment on their body condition. A major difficulty, however, is that biochemical analysis of carcass is tedious and therefore cannot be applied at a large scale. The main objective of this study was therefore to find out if simple measurements can be used as indices of total body lipids and proteins. Four classes of lipid and protein indices, derived on a 'source' group, were defined according to their complexity and condition of application (field or laboratory). Accuracy of the indices was evaluated on an independent group, of which the body composition calculated from indices was compared to carcass analysis. In live birds, body mass was an accurate and convenient predictor for both lipid and protein masses. If carcasses are available, extensive analysis provides a higher accuracy for body lipids only. This can be simply obtained through multiple regressions using abdominal fat mass and/or dry body mass.

Precise monitoring of porpoising behaviour of Adélie penguins determined using acceleration data loggers.

A new method using acceleration data loggers enabled us to measure the porpoising behaviour of Adélie penguins (Pygoscelis adeliae), defined as a continuous rapid swimming with rhythmic serial leaps. Previous hydrodynamic models suggested that leaping would be energetically cheaper when an animal swims continuously at depths of less than three maximum body diameters below the water surface. In the present study, free-ranging Adélie penguins leapt at a mean speed of 2.8 m s(-)(1) above the predicted threshold speed (0.18-1. 88 m s(-)(1)). Wild penguins reduced drag by swimming deeper (0.91 m) and did not swim continuously within the high-drag layer while submerged. This indicates that previous calculations may be incomplete. Moreover, leaps represented an average of only 3.8 % of the total distance travelled during the porpoising cycle, which would make energy savings marginal. Among the six penguins used in our study, two did not porpoise and three porpoised for less than 7 min, also indicating that this behaviour was not important during travel to and from foraging sites, as has been previously suggested. Birds mainly porpoised at the start and end of a trip. One explanation of porpoising might be an escape behaviour from predators.

Intersexual differences in the diving behaviour of foraging subantarctic cormorant (Phalacrocorax albiventer) and Japanese cormorant (P. filamentosus).

Cormorants feed by feet-propelled diving. How cormorants optimize foraging is of a particular interest in relation to the understanding of the feeding strategies of diving birds, as well as within the debate about cormorants' impact on sustainable resources. Using microdata loggers that recorded diving depth, we investigated the foraging strategy of males and females of subantarctic cormorants, which inhabit cold regions, and of Japanese cormorants, which live in the northern temperate zone. For both species, males and females daily spent the same amount of time submerged, and apparently captured the same amount of fish. However, males dived deeper and longer, which could be explained by their 15-20% larger body mass and may minimize potential competition for food.

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.