Search

The position of the Moon in relation to the Earth and the Sun gives rise to several predictable cycles, and natural changes in nighttime light intensity are known to cause alterations to physiological processes and behaviors in many animals. The limited research undertaken to date on the physiological responses of animals to the lunar illumination has exclusively focused on the synodic lunar cycle (full moon to full moon, or moon phase) but the moon's orbit—its distance from the Earth—may also be relevant. Every month, the moon moves from apogee, its most distant point from Earth—and then to perigee, its closest point to Earth. Here, we studied wild barnacle geese (Branta leucopsis) to investigate the influence of multiple interacting lunar cycles on the physiology of diurnally active animals. Our study, which uses biologging technology to continually monitor body temperature and heart rate for an entire annual cycle, asks whether there is evidence for a physiological response to natural cycles in lunar brightness in wild birds, particularly “supermoon” phenomena, where perigee coincides with a full moon. There was a three‐way interaction between lunar phase, lunar distance, and cloud cover as predictors of nighttime mean body temperature, such that body temperature was highest on clear nights when the full moon coincided with perigee moon. Our study is the first to report the physiological responses of wild birds to “supermoon” events; the wild geese responded to the combination of two independent lunar cycles, by significantly increasing their body temperature at night. That wild birds respond to natural fluctuations in nighttime ambient light levels support the documented responses of many species to anthropogenic sources of artificial light, that birds seem unable to override. As most biological systems are arguably organized foremost by light, this suggests that any interactions between lunar cycles and local weather conditions could have significant impacts on the energy budgets of birds.

Many different physiological changes have been observed in wild waterfowl during the flightless stage of wing moult, including a loss of body mass. Previously we established that captive barnacle geese (Branta leucopsis) underwent this characteristic decrease in body mass during their wing moult, even though they had unlimited and unrestricted access to food. In the present study we aimed to determine if this body mass loss during moult comprised mainly a reduction in fat stores, and to ascertain if the captive geese undergo pre-migratory and pre-winter fattening over a similar temporal scale to their wild conspecifics. The non-destructive technique of deuterium oxide isotope dilution was employed to provide repeated measurements of estimated fat deposition from a captive flock of fourteen barnacle geese. Birds were injected with deuterium oxide at 7 distinct intervals for one annual cycle. During the flightless period of the moult, body fat decreased by approximately 40% from the pre-moult value. During late-September and early October, body fat reached its highest point in the annual cycle, both as an absolute value and as a percentage of total body mass. We propose that while the energetic cost of wing moult is not the ultimate cause of fat loss in moulting barnacle geese, the approximate 212 g of fat catabolised during moult would provide sufficient energy to cover the cost of the replacement of the flight feathers, estimated to be 6384 kJ, over an approximate 42 day period. We conclude that the previously recorded increase in metabolism during moult in the geese, led to the use of endogenous fat reserves because the birds reduced rather than increased their food intake rates owing to the increased risk of predation when flightless. We also conclude that captive barnacle geese do undergo pre-winter and pre-migratory fattening, providing further evidence of the innate nature of these fat deposition cycles.

Feathers act as aerodynamic cantilevers, and to withstand the prolonged cyclical loading that occurs during flight, feathers must be stiff, lightweight and strong. We experimentally tested the differences in feather structure, primarily stiffness and size, between (a) wild and captive Barnacle GeeseBranta leucopsis,and (b) primary feathers dropped during the annual flight feather moult, and those feathers freshly regrown during the moult process. We found that, despite having undergone a 5,000km round-trip migration, flight feathers dropped during moult in the wild geese were stiffer than those measured in the captive geese, both for those dropped during moult and those re-grown. We propose that this may be related to diet or stress in the captive geese.

Dominant individuals within animal groups will frequently place themselves in the most beneficial position for maximal protection against predation. Higher perches are generally associated with reduced predation risk in birds, so we predicted that dominant birds will preferentially place themselves on higher perches. We tested this by determining the dominance hierarchy in two populations of captive birds (Homing Pigeons Columba livia and Great Cormorants Phalacrocorax carbo), and relating rank within the dominance hierarchy to observed perch height preferences. We found that perch choice was significantly repeatable in pigeons, and that more dominant individuals of both species selected higher perches. As well as facilitating early detection of and escape from potential predators, higher perches are also likely to facilitate the display of aggression to other group members.

Birds migrating through extreme environments can experience a range of challenges while meeting the demands of flight, including highly variable ambient temperatures, humidity and oxygen levels. However, there has been limited research into avian thermoregulation during migration in extreme environments. This study aimed to investigate the effect of flight performance and high altitude on body temperature (Tb) of free-flying bar-headed geese (Anser indicus), a species that completes a high-altitude trans-Himalayan migration through very cold, hypoxic environments. We measured abdominal Tb, along with altitude (via changes in barometric pressure), heart rate and body acceleration of bar-headed geese during their migration across the Tibetan Plateau. Bar-headed geese vary the circadian rhythm of Tb in response to migration, with peak daily Tb during daytime hours outside of migration but early in the morning or overnight during migration, reflecting changes in body acceleration. However, during flight, changes in Tb were not consistent with changes in flight performance (as measured by heart rate or rate of ascent) or altitude. Overall, our results suggest that bar-headed geese are able to thermoregulate during high-altitude migration, maintaining Tb within a relatively narrow range despite appreciable variation in flight intensity and environmental conditions.

© 2019 The Authors. Functional Ecology © 2018 British Ecological Society Animals are expected to be judicious in the use of the energy they gain due to the costs and limits associated with its intake. The management of energy expenditure (EE) exhibited by animals has previously been considered in terms of three patterns: the constrained, independent and performance patterns of energy management. These patterns can be interpreted by regressing daily EE against maintenance EE measured over extended periods. From the multiple studies on this topic, there is equivocal evidence about the existence of universal patterns in certain aspects of energy management. The implicit assumption that animals exhibit specifically one of three discrete energy management patterns, and without variation, seems simplistic. We suggest that animals can exhibit gradations of different energy management patterns and that the exact pattern will fluctuate as their environmental context changes. To investigate these ideas, and for possible large-scale patterns in energy management, we analysed long-term heart rate data—a strong proxy for EE—across and within individuals in 16 species of birds, mammals and fish. Our analyses of 292 individuals representing 46,539 observation-days suggest that vertebrates typically exhibit predominantly the independent or performance energy patterns at the across-individual level, and that the pattern does not associate with taxonomic group. Within individuals, however, animals generally exhibit some degree of energy constraint. Together, these findings indicate that across diverse species, some individuals supply more energy to all aspects of their life than do others, however all individuals must trade-off deployment of their available energy between competing functions. This demonstrates that within-individual analyses are essential for the interpretation of energy management patterns. We also found that species do not necessarily exhibit a fixed energy management pattern but rather temporal variation in their energy management over the year. Animals’ energy management exhibited stronger energy constraint during periods of higher EE, which typically coincided with clear and key life cycle events such as reproduction, suggesting an adaptive plasticity to respond to fluctuating energy demands. A plain language summary is available for this article.

Waterfowl undergo an annual simultaneous flight-feather moult that renders them flightless for the duration of the regrowth of the flight feathers. In the wild, this period of flightlessness could restrict the capacity of moulting birds to forage and escape predation. Selection might therefore favour a short moult, but feather growth is constrained and presumably energetically demanding. We therefore tested the hypothesis that for birds that undergo a simultaneous flight-feather moult, this would be the period in the annual cycle with the highest minimum daily heart rates, reflecting these increased energetic demands. Implantable heart rate data loggers were used to record year-round heart rate in six wild barnacle geese ( Branta leucopsis ), a species that undergoes a simultaneous flight-feather moult. The mean minimum daily heart rate was calculated for each individual bird over an 11-month period, and the annual cycle was divided into seasons based on the life-history of the birds. Mean minimum daily heart rate varied significantly between seasons and was significantly elevated during wing moult, to 200 ± 32 beats min −1 , compared to all other seasons of the annual cycle, including both the spring and autumn migrations. The increase in minimum daily heart rate during moult is likely due to feather synthesis, thermoregulation and the reallocation of minerals and protein.

Energy management models provide theories and predictions for how animals manage their energy budgets within their energetic constraints, in terms of their resting metabolic rate (RMR) and daily energy expenditure (DEE). Thus, uncovering what associations exist between DEE and RMR is key to testing these models. Accordingly, there is considerable interest in the relationship between DEE and RMR at both inter- and intraspecific levels. Interpretation of the evidence for particular energy management models is enhanced by also considering the energy spent specifically on costly activities (activity energy expenditure [AEE] = DEE - RMR). However, to date there have been few intraspecific studies investigating such patterns. Our aim was to determine whether there is a generality of intraspecific relationships among RMR, DEE, and AEE using long-term data sets for bird and mammal species. For mammals, we use minimum heart rate (fH), mean fH, and activity fH as qualitative proxies for RMR, DEE, and AEE, respectively. For the birds, we take advantage of calibration equations to convert fH into rate of oxygen consumption in order to provide quantitative proxies for RMR, DEE, and AEE. For all 11 species, the DEE proxy was significantly positively correlated with the RMR proxy. There was also evidence of a significant positive correlation between AEE and RMR in all four mammal species but only in some of the bird species. Our results indicate there is no universal rule for birds and mammals governing the relationships among RMR, AEE, and DEE. Furthermore, they suggest that birds tend to have a different strategy for managing their energy budgets from those of mammals and that there are also differences in strategy between bird species. Future work in laboratory settings or highly controlled field settings can tease out the environmental and physiological processes contributing to variation in energy management strategies exhibited by different species.

In leghorn chickens (Gallus gallus domesticus) of standard breed (large) and bantam (small) varieties, artificial selection has led to females being permanently gravid and sexual selection has led to male-biased size dimorphism. Using respirometry, videography and morphological measurements, sex and variety differences in metabolic cost of locomotion, gait utilisation and maximum sustainable speed (Umax) were investigated during treadmill locomotion. Males were capable of greater Umax than females and used a grounded running gait at high speeds, which was only observed in a few bantam females and no standard breed females. Body mass accounted for variation in the incremental increase in metabolic power with speed between the varieties, but not the sexes. For the first time in an avian species, a greater mass-specific incremental cost of locomotion, and minimum measured cost of transport (CoTmin) were found in males than in females. Furthermore, in both varieties, the female CoTmin was lower than predicted from interspecific allometry. Even when compared at equivalent speeds (using Froude number), CoT decreased more rapidly in females than in males. These trends were common to both varieties despite a more upright limb in females than in males in the standard breed, and a lack of dimorphism in posture in the bantam variety. Females may possess compensatory adaptations for metabolic efficiency during gravidity (e.g. in muscle specialization/posture/kinematics). Furthermore, the elevated power at faster speeds in males may be linked to their muscle properties being suited to inter-male aggressive combat.

Exercise at high altitude is extremely challenging, largely due to hypobaric hypoxia (low oxygen levels brought about by low air pressure). In humans, the maximal rate of oxygen consumption decreases with increasing altitude, supporting progressively poorer performance. Bar-headed geese (Anser indicus) are renowned high altitude migrants and, although they appear to minimize altitude during migration where possible, they must fly over the Tibetan Plateau (mean altitude 4800 m) for much of their annual migration. This requires considerable cardiovascular effort, but no study has assessed the extent to which bar-headed geese may train prior to migration for long distances, or for high altitudes. Using implanted loggers that recorded heart rate, acceleration, pressure, and temperature, we found no evidence of training for migration in bar-headed geese. Geese showed no significant change in summed activity per day or maximal activity per day. There was also no significant change in maximum heart rate per day or minimum resting heart rate, which may be evidence of an increase in cardiac stroke volume if all other variables were to remain the same. We discuss the strategies used by bar-headed geese in the context of training undertaken by human mountaineers when preparing for high altitude, noting the differences between their respective cardiovascular physiology. published

For many polar species, climate change is likely to result in range contractions and negative population trends. For those species whose distribution is limited by sea ice and cold water, however, polar warming could result in population increases and range expansion. Population increases of great cormorants Phalacrocorax carbo in Greenland are associated with warmer sea surface temperatures, but the actual impact of environmental change on cormorant spatial ecology remains unclear. In the present study, we investigate how Arctic warming is likely to influence the distribution of cormorants in Greenland. Using geolocation data, we show that many individuals that breed above the Arctic Circle migrate south and winter at lower latitude. We then couple estimates of migratory flight costs with a model that predicts daily energy expenditure during winter on the basis of water temperature, ambient illumination during diving, dive depth and day length. This model shows that the most energy efficient strategy predicted for any breeding location is to migrate as far south as possible, and that, for a given wintering location, it is more energetically expensive to breed at high latitude. We argue that cormorants currently undertake a winter migration to escape the polar night and reduce winter energy costs and that their wintering grounds in Greenland will remain largely unchanged under Arctic warming. This is because low levels of ambient illumination during the polar night will continue to restrict foraging opportunities at high latitude during winter. Northward expansion of the breeding range will result in increased energy expenditure associated with long migratory flights, and the cost of such flights may ultimately limit the breeding range of cormorants. Such limitations are likely to represent a general constraint on the capacity of visually guided predators to respond to climate warming, and may limit the predicted poleward range shifts of these species.

While some migratory birds perform non-stop flights of over 11 000 km, many species only spend around 15% of the day in flight during migration, posing a question as to why flight times for many species are so short. Here, we test the idea that hyperthermia might constrain flight duration (FD) in a short-distance migrant using remote biologging technology to measure heart rate, hydrostatic pressure and body temperature in 19 migrating eider ducks (Somateria mollissima), a short-distance migrant. Our results reveal a stop-and-go migration strategy where migratory flights were frequent (14 flights day−1) and short (15.7 min), together with the fact that body temperature increases by 1°C, on average, during such flights, which equates to a rate of heat storage index (HSI) of 4°C h−1. Furthermore, we could not find any evidence that short flights were limited by heart rate, together with the fact that the numerous stops could not be explained by the need to feed, as the frequency of dives and the time spent feeding were comparatively small during the migratory period. We thus conclude that hyperthermia appears to be the predominant determinant of the observed migration strategy, and suggest that such a physiological limitation to FD may also occur in other species.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.

Summary1. Bird migration is often seen as the summit of animal performance. Because higher foragingeffort associated with fuelling and increased flight activity should generate maximum level ofenergy turnover, we expect the migratory process to be constrained by energy, whether it isenergy expenditure or energy intake.2. We used implanted data loggers to continuously monitor foraging effort, flight activity andheart rate (as a proxy for rate of energy expenditure), in a wild migratory sea duck before andafter moult migration to test the energy budget limitation hypothesis.3. We show that despite the fact that departing birds forage at three times the level observedduring post-migration, daily energy expenditure (DEE) remains the same when periods beforeand after migration are compared.4. In an attempt to determine how the birds achieve such a feat, we compared heart rate whenactive (feeding and flying) for the periods before and after migration and found no significantdifference for feeding and flight heart rate. However, heart rate during periods of inactivity wassignificantly lower during fuelling which together with a reduced time spent flying completelycounteracted the observed high energy costs of foraging.5. The time spent active represented a tiny proportion (8–20%) of the 24-h time budget suggest-ing that energy minimization and an optimization process may be at work here, confounding anyapparent support for the energy budget limitation hypothesis. We thus concluded that similarDEE before and after migration could be owing to the bird’s inability to increase energy expendi-tureoveracertainlimitortothesurvivalcostsassociatedwithacertainlevel ofphysicalexertion.Nevertheless, our results indicate that behavioural, and possibly physiological, compensationmay beusedasamechanismtoreduce theoverallenergycostoffuellingin migratingbirds.Key-words: activity budget, daily energy expenditure, foraging effort, heart rate method,migration, oxidative stress, Somateria mollissimaIntroduction

Many species of waterfowl undergo a post-breeding simultaneous flight feather moult (wing moult) which renders them flightless and vulnerable to predation for up to 4 weeks. Here we present an analysis of the correlations between individual time-budgets and body mass states in 13 captive Barnacle Geese Branta leucopsis throughout an entire wing moult. The daily percentage of time spent resting was positively correlated with initial body mass at the start of wing moult. Behaviour of individual birds during wing moult is dependent on initial physiological state, which may in turn be dependent on foraging ability; the storage of energy before the start of wing moult will help birds to reduce exposure to the dangers of predation.

Bone is continually undergoing cycles of apposition and resorption referred to as adaptive remodelling. We tested the hypothesis that captive moulting Barnacle Geese (Branta leucopsis) would show adaptive bone mineralisation during the flightless period of their annual flight feather moult, despite having never flown. The three leg bones showed selective changes in mineralisation in terms of mass and mineral content, while the wing bones did not change in mass or mineral content. The tibia/fibula was the only bone to also undergo significant changes in mass, increasing as moult progressed then decreasing significantly towards the end of moult. This was not a response to changing body mass. Instead, we propose that this is a response to the requirement for increased strength brought about by the significant increase in the force producing muscles that attach to the tibia. The femur and tarsometarsus showed the opposite trend, with mineral content decreasing significantly during mid-moult before increasing again at the end. These changes were also independent of changing body mass, suggesting instead that the calcium, or rather calcium derivatives, were mobilised for feather regrowth. This study demonstrates significant and selective adaptive natural changes in bone mass and mineralization that have not been previously demonstrated. That they should also occur in captive birds which show a decrease in locomotion during the wing moult period, suggests a high endogenous capacity for these changes.

Arctic seas have warmed and sea ice has retreated. This has resulted in range contraction and population declines in some species, but it could potentially be a boon for others. Great Cormorants Phalacrocorax carbo have a partially wettable plumage and seem poorly suited to foraging in Arctic waters. We show that rates of population change of Cormorant colonies around Disko Bay, Greenland, are positively correlated with sea surface temperature, suggesting that they may benefit from a warming Arctic. However, although Cormorant populations may increase in response to Arctic warming, the extent of expansion of their winter range may ultimately be limited by other factors, such as sensory constraints on foraging behaviour during long Arctic nights.

Virulent outbreaks of highly pathogenic avian influenza (HPAI) since 2005 have raised the question about the roles of migratory and wild birds in the transmission of HPAI. Despite increased monitoring, the role of wild waterfowl as the primary source of the highly pathogenic H5N1 has not been clearly established. The impact of outbreaks of HPAI among species of wild birds which are already endangered can nevertheless have devastating consequences for the local and non-local ecology where migratory species are established. Understanding the entangled dynamics of migration and the disease dynamics will be key to prevention and control measures for humans, migratory birds and poultry. Here, we present a spatial dynamic model of seasonal migration derived from first principles and linking the local dynamics during migratory stopovers to the larger scale migratory routes. We discuss the effect of repeated epizootic at specific migratory stopovers for bar-headed geese ( Anser indicus ). We find that repeated deadly outbreaks of H5N1 on stopovers during the autumn migration of bar-headed geese could lead to a larger reduction in the size of the equilibrium bird population compared with that obtained after repeated outbreaks during the spring migration. However, the opposite is true during the first few years of transition to such an equilibrium. The age-maturation process of juvenile birds which are more susceptible to H5N1 reinforces this result.

Up to half the world's population of bar-headed geese (Anser indicus) migrate between central Asia and India and fly between 5000 m and 9000 m above sea level as they cross the Himalayas. The partial pressures of oxygen at these altitudes are, respectively, about 50% and 30% those at sea level. Flapping flight is energetically expensive, so how are bar-headed geese able to migrate at such altitudes? The haemoglobin of bar-headed geese has a greater affinity for oxygen than those of lowland birds, and birds are able to hyperventilate to a greater extent than mammals during severe hypoxia. Together, these mean that the concentration of oxygen in the arterial blood at a given altitude is greater in bar-headed geese than in lowland birds and mammals. The low partial pressure of CO(2) in arterial blood (hypocapnia) that accompanies hyperventilation does not cause reduction of cerebral blood flow in birds as it does in mammals, thus there is greater oxygen delivery to the brain in hypoxic birds, including bar-headed geese, than in mammals. Captive bar headed geese could not maintain elevated aerobic metabolism during exercise at a simulated altitude of 8500 m and their cardiac stroke volume was much lower than that during exercise at sea level. This suggests that if some individuals of this species of geese do really manage to fly over Mt Everest, they may only do so if they receive assistance from vertical air movements, for example from lee waves downwind from the mountains.

Abdominally implanted data-loggers have been used to study the behaviour and physiology of birds, with no detectable negative effects. This technique has great potential for smaller and streamlined species, since these animals tend to be more prone to the negative effects that may be associated with externally attached devices. We conducted the first assessment of the impacts of abdominally implanted heart-rate data-loggers on a smaller species, the Little Penguin (Eudyptula minor), which weighs ~1.1 kg. The number and duration of trips to sea were recorded in male penguins implanted with a device (n = 10) and compared with a control group not implanted with a device (n = 10). Trips were recorded for the entire duration of the Penguins’ winter non-breeding period, which for this species is the time of year when their energy budgets are most delicately balanced. The heart-rate data-loggers appeared to have no effect on percentage of time spent at sea, and the number and duration of overnight trips of 2–5 days or 6–26 days. Implanted Penguins undertook fewer trips of

Seabirds that forage by plunge diving dive less frequently than those that dive from the water surface, and spend less time in flight than more generalist foragers. We hypothesised that this is due to foraging by plunge diving entailing a high energetic cost, which in turn is due to high energetic costs of take-off and flight. Using heart rate as a proxy for metabolic rate, we evaluated the energetic costs of foraging by plunge diving in the Australasian gannet Morus serrator. As expected, flight entailed a high energetic cost, and energy expenditure during foraging was equivalent to that during flight and significantly higher than that when animals were resting during foraging trips or were inactive on land. These values represent the highest costs of foraging yet recorded in a seabird, and the low frequency of plunge diving can be attributed to these high costs. On average, Australasian gannets perform 2.6 dives h�1when foraging, with a mean dive duration of 3.4 s. As a result, they spend

SUMMARY Quantifying a relationship between heart rate ( f H ) and rate of oxygen consumption ( V O 2 ) allows the estimation of V O 2 from f H recordings in free-ranging birds. It has been proposed that this relationship may vary throughout an animal9s annual cycle, due to changes in physiological status. Barnacle geese, Branta leucopsis , provide an ideal model to test this hypothesis, as they exhibit significant intra-annual variability in body mass, body composition and abdominal temperature, even in captivity. Heart rate data loggers were implanted in 14 captive barnacle geese, and at six points in the year the relationship between f H and V O 2 was determined. The f H / V O 2 relationship was also determined in seven moulting wild barnacle geese to examine whether relationships from captive animals might be applicable to wild animals. In captive barnacle geese, the f H / V O 2 relationship was significantly different only between two out of the six periods when the relationship was determined (late September–early October and November). Accounting for changes in physiological parameters such as body mass, body composition and abdominal temperature did not eliminate this difference. The relationship between f H and V O 2 obtained from wild geese was significantly different from all of the relationships derived from the captive geese, suggesting that it is not possible to apply calibrations from captive birds to wild geese. However, the similarity of the f H and V O 2 relationship derived during moult in the captive geese to those during the remainder of the annual cycle implies it is not unreasonable to assume that the relationship between f H / V O 2 during moult in the wild geese is indicative of the relationship throughout the remainder of the annual cycle.

We measured daily energy expenditure (DEE) continuously for a whole year in a free ranging bird, the macaroni penguin Eudyptes chrysolophus. We combined these measurements with concurrently recorded foraging behaviour, and literature information on body mass and dietary factors to estimate prey consumption rates and foraging success. DEE was at a maximum during late chick-rearing but was equally high during all other active phases of the breeding season. DEE was approximately 4xresting metabolic rate, which accords with established theory and suggests a common 'energetic ceiling' throughout the summer period. However, whether this represents a maximum in physiological capacity, or a rate which optimises fitness is still unclear. Rates of prey consumption and foraging success followed different patterns from daily energy expenditure. Daily prey consumption was high as the penguins prepared for long fasts associated with moulting and incubation but relatively low during chick-rearing, when foraging areas were restricted and foraging success lower. It appears that the energy intake of macaroni penguins is subject to extrinisic or environmental constraints rather than to intrinsic physiological limits.

Pinnipeds are major consumers in marine ecosystems, and understanding their energy budgets is essential to determining their role in food webs, particularly where there is competition with fisheries. Food consumption and energy expenditure have been evaluated in pinnipeds using different methods, but the use of heart rate to estimate energy expenditure is potentially a very powerful tool suited to the life history of these animals. We tested a procedure for the subcutaneous implantation of heart rate data loggers to determine whether heart rate could be recorded for ≥1 year in free-ranging pinnipeds, as it has been in birds. We implanted 3 captive California sea lions (Zalophus californianus) and 3 captive northern elephant seals (Mirounga angustirostris) with heart rate data loggers and monitored their recovery and behavior in a controlled environment. In both species, the implantation site allowed for excellent detection of the electrocardiogram, and we observed heart rate signatures characteristic of behaviors such as resting and diving. Although all 3 sea lions recovered well from the implantation surgery, all 3 elephant seals showed a substantial inflammatory response for unknown reasons, and we removed the implanted data loggers. Subcutaneous implantation of data loggers is a powerful technique to study physiology, energetics, and behavior in California sea lions, but more work is required to realize the potential of this technique in northern elephant seals.

The movement of marine vertebrates has been tracked using a variety of techniques, all of which depend on the external attachment of a transmitting or recording device. However, these devices can have negative effects on the subject animals, limiting both the quantity and quality of data collected. We present a new method for monitoring large-scale movement of marine vertebrates that uses behavioural data stored on a surgically implanted data logger. The technique (‘behavioural geolocation’) relies on the principles of light-based geolocation but rather than measuring ambient light levels, changes in diving behaviour associated with sunrise and sunset are used to infer daylength and time of local sunrise, and hence location. We present data from a trial, post-hoc, analysis of diving data collected from macaroni penguins Eudyptes chrysolophus during long foraging trips associated with incubation and preparation for moult. Our results showed that the penguins usually travelled to the polar frontal zone to the north of their breeding colony at South Georgia, an area broadly consistent with previously measured behaviour and the availability of preferred prey at this period of the annual cycle.

Diving is indicative of foraging in cormorants (Phalacrocoracidae). We have investigated a range of parameters associated with diving in Great Cormorants Phalacrocorax carbo to provide insight into the bases of cormorant predatory strategies. We hypothesize that if vision is important in cormorant foraging behaviour, and if they are not constrained by the position of their prey in the water column, then diving behaviour will be modulated primarily in response to the diel variation in ambient light levels. Specifically, we propose that cormorants forage at shallower depths when light levels are low, and more deeply when light levels are high. We provide evidence that this is the case. We recorded the occurrence of cormorant diving behaviour using implanted data loggers and recorded ambient light levels and water temperature using leg-mounted loggers in a sample of free-living Great Cormorants in Greenland. Our results show that dives are shallower at the beginning and end of each day when light levels are lower. We suggest that these data support the hypothesis that cormorant foraging is visually-guided even though recent evidence has shown that their underwater visual acuity is poor.

Maximum aerobic metabolic rate, measured in terms of rate of oxygen consumption during exercise ( ), is well known to scale to body mass (M) with an exponent greater than the value of 0·75 predicted by models based on the geometry of systems that supply nutrients. # 2. Recently, the observed scaling for (∝M0·872) has been hypothesized to arise because of the temperature dependence of biological processes, and because large species show a greater increase in muscle temperature when exercising than do small species. # 3. Based on this hypothesis, we predicted that will be positively related to ambient temperature, because heat loss is restricted at high temperatures and body temperature is likely to be elevated to a greater extent than during exercise in the cold. # 4. This prediction was tested using a comparative phylogenetic generalized least-squares (PGLS) approach, and 34 measurements of six species of rodent (20·5–939 g) maximally exercising at temperatures from –16 to 30 °C. # 5. is unrelated to testing temperature, but is negatively related to acclimation temperature. We conclude that prolonged cold exposure increases exercise-induced by acting as a form of aerobic training in mammals, and that elevated muscle temperatures of large species do not explain the scaling of across taxa.

The use of allometric scaling to estimate drug doses, regimes, and clearance rates (metabolic dosing) is based on the principle that the amount of drug to be administered is more closely related to daily energy use than to body mass (kg). Thus, by using the allometric estimations of minimal energy consumption (MEC) in kcal day-1 based on the formula MEC=kM bb, where b=3, it is thought to be possible to extrapolate appropriate drug dosage regimens to species for which direct MEC data are unavailable. However, the allometric equations for respiratory variables in birds were developed 30 years ago, and were based on a very small sample size, while the appropriate scaling exponent for the allometry of energy use is a matter of considerable debate. Hence, we revisit the issue of the scaling of therapeutic regimes in birds using the most current expanded database available (resting metabolic rate data for 296 species across 17 bird orders), taking account of the non-independence of species in this process using a phylogenetically independent approach. We show that the use of caloric values to estimate daily energy consumption introduces significant error into the formula, as there are a number of assumptions that are made when converting rate of oxygen consumption to a caloric value. We also show that there are significant differences in the proportionality or Hainsworth coefficients k across taxa when the data are examined in a phylogenetic context, although the allometric scaling exponent does not vary. We therefore recommend the use of only data based on oxygen consumption values, and not caloric values, and a multi-order phylogenetic model when calculating the appropriate drug dosage regime. © 2008 The Authors.

Predatory diving birds, such as cormorants (Phalacrocoracidae), have been generally regarded as visually guided pursuit foragers. However, due to their poor visual resolution underwater, it has recently been hypothesized that Great Cormorants do not in fact employ a pursuit-dive foraging technique. They appear capable of detecting typical prey only at short distances, and primarily use a foraging technique in which prey may be detected only at close quarters or flushed from a substratum or hiding place. In birds, visual field parameters, such as the position and extent of the region of binocular vision, and how these are altered by eye movements, appear to be determined primarily by feeding ecology. Therefore, to understand further the feeding technique of Great Cormorants we have determined retinal visual fields and eye movement amplitudes using an ophthalmoscopic reflex technique. We show that visual fields and eye movements in cormorants exhibit close similarity with those of other birds, such as herons (Ardeidae) and hornbills (Bucerotidae), which forage terrestrially typically using a close-quarter prey detection or flushing technique and/or which need to examine items held in the bill before ingestion. We argue that this visual field topography and associated eye movements is a general characteristic of birds whose foraging requires the detection of nearby mobile prey items from within a wide arc around the head, accurate capture of that prey using the bill, and visual examination of the caught prey held in the bill. This supports the idea that cormorants, although visually guided predators, are not primarily pursuit predators, and that their visual fields exhibit convergence towards a set of characteristics that meet the perceptual challenges of close-quarter prey detection or flush foraging in both aquatic and terrestrial environments.

Although the replacement of feathers apparently represents the major event of somatic production in the annual cycle of wild birds, knowledge about the energetics of molt has always been hampered by logistical and technical difficulties, which are exacerbated by the fact that birds are able to compensate behaviorally to buffer any variation in energy demand. During wing molt, sea ducks (Mergini) and other diving birds lose all of their wing feathers at once, leading to a period of temporary flightlessness of variable duration, a condition that considerably restricts their movements and increases the probability of predation. In the present study, we present the first results aimed at quantifying the duration of flightlessness, energy expenditure, and foraging effort during molt of a wing-propelled diving bird, the Common Eider (Somateria mollissima). Data loggers were implanted in the body cavity of 13 females to record heart rate and hydrostatic pressure (depth) every two seconds for a period of 220 days. Flight frequency and duration were assessed from elevated and constant heart rate, and the absence of flight was used to quantify the duration of flightlessness, which lasted, on average, 36 +/- 8 days (mean +/- SD). Using a period of four weeks before and four weeks after the flightless period, we found that dive depth (ranging from 1 to 2 m, on average) and daily diving time did not vary during the course of the study. Daily metabolic rate increased by 9%, and resting metabolic rate by 12% from the pre-molt period to the flightless period and remained high during the post-molt period. This study indicates that the energetic costs of replacing flight remiges in female eiders are substantial, although this is not associated with any change in foraging effort, which suggests that female Common Eiders lose mass during wing molt. Finally, estimates of energy savings associated with the total absence of flights during wing molt represent 6% of daily metabolic rate or 14% of resting metabolic rate. This finding contrasts with the classical view that little or no benefit is associated with a flightless condition. We suggest that such energy savings may have favored the evolution of temporary flightlessness in diving birds.

Foraging behaviour and energy expenditure were measured continuously throughout the chick-rearing period of free-ranging macaroni penguins Eudyptes chrysolophus. These data were integrated with values obtained from the literature on body mass, assimilation efficiency, body reserve consumption and deposition rates, chick growth and energy expenditure and energy content of food in a new type of algorithm to predict (with 95% confidence limits (CL)) foraging success and daily changes in body mass. A successfully breeding pair of macaroni penguins will capture 111.7 kg (95% CL: 79.4 to 158.0 kg) of prey during the chick-rearing period. The crucial phase of the chick rearing period was around the time that chicks creche, when prey consumption rates more than dou- bled as the male assisted in foraging and recovered from a long fast. Female macaroni penguins extracted 2.28 (1.60 to 3.26) and males extracted 2.84 (2.02 to 3.99) g of prey from their environment for every minute spent submerged during foraging. Only 15.3 (14.7 to 15.6)% of all prey consumed was fed to chicks. While food capture rates increase in the middle of the breeding season, this may be more a function of greater food availability than a response to demands from their chick. Male and female macaroni penguins have differing breeding strategies with the male showing the characteris- tics of a capital then income breeder while the female has a strategy that shows characteristics of both capital and income strategies simultaneously. The high synchronicity and precise timing of the mac- aroni penguin breeding season and timing of the increase in prey capture rates suggest an influx of prey to their foraging area during the middle of the breeding season. A depletion of prey resources in the foraging area used during the breeding season could affect foraging success and have pro- found effects on the body condition and composition of this species and its ability to raise chicks suc- cessfully.

International audience; Penguins are known to have high pedestrian locomotory costs in comparison to other cursorial birds, but the ecological consequences of this difference have received limited attention. Here we present a method for the accurate estimation of onshore energetics based on measurements of body mass, simple morphometrics and distance moved. The method is shown to be similarly accurate to other field-based estimates of energy expenditure, but has the advantage of logistical simplicity. King penguins spend 30-50% of their time ashore and may walk distances of several kilometres to and from their breeding colonies. However, in such cases the total energetic cost of pedestrian locomotion is estimated to be only 1.0% of the energy expended whilst ashore. Thus, despite a high instantaneous cost, pedestrian locomotion is a small and possibly negligible component of total energy turnover in king penguins.

Complex physiological traits, such as routine aerobic metabolic rate or exercise performance, are indicators of the functional integrity of fish that can reveal sub-lethal toxicological effects of aquatic pollutants. These traits have proved valuable in laboratory investigations of the sub-lethal effects of heavy metals, ammonia and various xenobiotics. It is not known, however, whether they can also function as biomarkers of the complex potential range of effects upon overall functional integrity caused by exposure to mixtures of chemicals in polluted natural environments. The current study used portable swimming respirometers to compare exercise performance and respiratory metabolism of fish exposed in cages for three weeks to either clean or polluted sites on three urban European river systems: the river Lambro, Milan, Italy; the rivers Blythe, Cole and Tame, Birmingham, UK; and the river Amstel, Amsterdam, The Netherlands. The UK and Italian rivers were variously polluted with high levels of both bioavailable heavy metals and organics, and the Amstel by mixtures of bioavailable organics at high concentrations. In both the UK and Italy, indigenous chub (Leuciscus cephalus) exposed to clean or polluted sites swam equally well in an initial performance test, but the chub from polluted sites could not repeat this performance after a brief recovery interval. These animals were unable to raise the metabolic rate and allocate oxygen towards exercise in the second trial, an effect confirmed in successive campaigns in Italy. Swimming performance was therefore a biomarker indicator of pollutant exposure in chub exposed at these sites. Exposure to polluted sites on the river Amstel did not affect the repeat swimming performance of cultured cloned carp (Cyprinus carpio), indicating either a species-specific tolerance or relative absence of heavy metals. However, measurements of oxygen uptake during swimming revealed increased rates of routine aerobic metabolism in both chub and carp at polluted sites in all of the rivers studied, indicating a sub-lethal metabolic loading effect. Therefore, the physiological traits of exercise performance and metabolic rate have potential as biomarkers of the overall sub-lethal toxic effects of exposure to complex mixtures of pollutants in rivers, and may also provide insight into why fish do not colonize some polluted environments.

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 ˙ O 2 ) 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 ˙ O 2 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 ˙ O 2 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 ˙ O 2 from published, field fH data. The major conclusions from the present study are: (1) in contrast to that for walking, the f H – V ˙ O 2 relationship for swimming king penguins is not affected by body mass; (2) prediction equation (1), log ( V ˙ O 2 ) = - 0.279 + 1.24 log ( f H ) + 0.0237 t - 0.0157 log ( f H ) t , derived in a previous study, is the most suitable equation presently available for estimating V ˙ O 2 in king penguins for all locomotory and nutritional states. A number of possible problems associated with producing an f H – V ˙ O 2 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 ˙ O 2 prediction equations, is explained.

SUMMARY Many different physiological changes have been observed in wild waterfowl during the flightless stage of wing moult, including a loss of body mass. We aimed to determine whether captive barnacle geese (Branta leucopsis)would show the characteristic decrease in body mass during their wing moult,even though they had unlimited and unrestricted access to food. Fourteen captive geese were weighed at 1–2-week intervals for two complete years. During the flightless period of the moult, body mass decreased by approximately 25% from the pre-moult value. To understand the basis of this change, the rate of oxygen consumption was measured during daytime and nighttime at six points in the second year, and at three points (before,during and after wing moult) behavioural observations were made. Measurements of the rate of oxygen consumption showed an 80% increase above that of the nonmoulting periods of the year. We propose that metabolism was increased during moult because of the cost of feather synthesis. Although food was available, the captive birds chose not to forage and instead increased the proportion of time spent resting. It is likely that this behaviour in response to wing moult is a strategy to avoid predation in the wild. Thus, the innate nature of this behaviour has potential survival value for wild birds of this species. We conclude that the increase in metabolism led to the use of endogenous energy reserves because the birds reduced rather than increased their food intake rates, and as a result, the barnacle geese lost body mass during wing moult.

Population connectivity is an important consideration in studies of disease transmission and biological conservation, especially with regard to migratory species. Determining how and when different subpopulations intermingle during different phases of the annual cycle can help identify important geographical regions or features as targets for conservation efforts and can help inform our understanding of continental-scale disease transmission. In this study, stable isotopes of hydrogen and carbon in contour feathers were used to assess the degree of molt-site fidelity among Bar-headed Geese (Anser indicus) captured in north-central Mongolia. Samples were collected from actively molting Bar-headed Geese (n = 61), and some individual samples included both a newly grown feather (still in sheath) and an old, worn feather from the bird's previous molt (n = 21). Although there was no difference in mean hydrogen isotope ratios for the old and new feathers, the isotopic variance in old feathers was approximately three times higher than that of the new feathers, which suggests that these birds use different and geographically distant molting locations from year to year. To further test this conclusion, online data and modeling tools from the isoMAP website were used to generate probability landscapes for the origin of each feather. Likely molting locations were much more widespread for old feathers than for new feathers, which supports the prospect of low molt-site fidelity. This finding indicates that population connectivity would be greater than expected based on data from a single annual cycle, and that disease spread can be rapid even in areas like Mongolia where Bar-headed Geese generally breed in small isolated groups.

Bar-headed geese cross the Himalayas on one of the most iconic high-altitude migrations in the world. Heart rates and metabolic costs of flight increase with elevation and can be near maximal during steep climbs. Their ability to sustain the high oxygen demands of flight in air that is exceedingly oxygen-thin depends on the unique cardiorespiratory physiology of birds in general along with several evolved specializations across the O2transport cascade.

Geese need to hug the land to fly high Animal migrations provide numerous examples of astonishing feats. Impressive even among these is the migration of bar-headed geese across the Himalayan Mountains, which reach heights of thousands of meters. Bishop et al. remotely monitored birds' heart rates, movement, and body temperature during migration. The geese “hug” the landforms, taking advantage of drafting and wind patterns. This unexpected strategy conserves energy, even though it means the geese repeatedly lose, and must then regain, altitude. Science , this issue p. 250

This review discusses the advancements in our understanding of the physiology and behaviour of avian diving that have been underpinned by optimal foraging theory and the testing of optimal models. To maximise their foraging efficiency during foraging periods, diving birds must balance numerous factors that are directly or indirectly related to the replenishment of the oxygen stores and the removal of excess carbon dioxide. These include (1) the time spent underwater (which diminishes the oxygen supply, increases carbon dioxide levels and may even include a build up of lactate due to anaerobic metabolism), (2) the time spent at the surface recovering from the previous dive and preparing for the next (including reloading their oxygen supply, decreasing their carbon dioxide levels and possibly also metabolising lactate) and (3) the trade-off between maximising oxygen reserves for consumption underwater by taking in more air to the respiratory system, and minimising the energy costs of positive buoyancy caused by this air, to maximise the time available underwater to forage. Due to its importance in avian diving, replenishment of the oxygen stores has become integral to models of optimal diving, which predict the time budgeting of animals foraging underwater. While many of these models have been examined qualitatively, such tests of predictive trends appear fallible and only quantifiable support affords strong evidence of their predictive value. This review describes how the quantification of certain optimal diving models, using tufted ducks, indeed demonstrates some predictive success. This suggests that replenishment of the oxygen stores and removal of excess carbon dioxide have significant influences on the duration of the surface period between dives. Nevertheless, present models are too simplistic to be robust predictors of diving behaviour for individual animals and it is proposed that they require refinement through the incorporation of other variables that also influence diving behaviour such as, perhaps, prey density and predator avoidance.

Fish have a central respiratory pattern generator (CRPG) in the brain stem that initiates activity in a series of cranial nerves innervating respiratory muscles. These nerves burst sequentially in the order of their rostrocaudal distribution in the central nervous system. When respiratory drive is high, this activity spreads caudally to occipital and anterior spinal neurons that project via the hypobranchial nerves to stimulate hypaxial muscles, causing active jaw abduction. The CRPG may also recruit the heart. Fish, like mammals, show respiratory components in the intrinsic variability of heart rate (HRV). Cardiorespiratory synchrony in the dogfish is driven by bursting activity in the cardiac branches of the vagus nerve, which emanates from preganglionic neurons in the dorsal vagal motor nucleus. A respiratory component in HRV is difficult to discriminate in other species, requiring the use of power spectral analysis and the subsequent elimination of aliased components.

1. We use a large interspecific data set on diving variables for birds and mammals, and statistical techniques to control for the effects of phylogenetic non-independence, to assess evolutionary associations among different elements of diving behaviour across a broad and diverse range of diving species. Our aim is to assess whether the diving ability of homeothermic vertebrates is influenced by factors other than the physiology of the species. 2. Body mass is related to dive duration even when dive depth is controlled for and thus for a given dive depth, larger species dive for longer. This implies that larger species have a greater capacity for diving than is expressed in their dive depth. Larger animals that dive shallowly, probably for ecological reasons such as water depth, make use of the physiological advantage that their size confers by diving for longer. 3. Dive duration correlates with dive depth more strongly than with body mass. This confirms that some animals are poor divers for their body mass, either because of a lower physiological capacity or because their behaviour limits their diving. 4. Surface duration relates not only to dive duration but also to dive depth, as well as to both independently. This indicates a relationship between dive depth and surface duration controlling for dive duration, which suggests that deeper dives are energetically more expensive than shallow dives of the same duration. 5. Taxonomic class does not improve any of the dive variable models in the present study. There is thus an unsuspected consistency in the broad responses of different groups to the effects on diving of the environment, which are therefore general features of diving evolution. © 2006 The Authors.

1. Time and energy are key currencies in animal ecology, and judicious management of these is a primary focus for natural selection. At present, however, there are only two main methods for estimation of rate of energy expenditure in the field, heart rate and doubly labelled water, both of which have been used with success; but both also have their limitations. 2. The deployment of data loggers that measure acceleration is emerging as a powerful tool for quantifying the behaviour of free-living animals. Given that animal movement requires the use of energy, the accelerometry technique potentially has application in the quantification of rate of energy expenditure during activity. 3. In the present study, we test the hypothesis that acceleration can serve as a proxy for rate of energy expenditure in free-living animals. We measured rate of energy expenditure as rates of O2 consumption (VO2) and CO2 production (VCO2) in great cormorants (Phalacrocorax carbo) at rest and during pedestrian exercise. VO2 and VCO2 were then related to overall dynamic body acceleration (ODBA) measured with an externally attached three-axis accelerometer. 4. Both VO2 and VCO2 were significantly positively associated with ODBA in great cormorants. This suggests that accelerometric measurements of ODBA can be used to estimate VO2 and VCO2 and, with some additional assumptions regarding metabolic substrate use and the energy equivalence of O2 and CO2, that ODBA can be used to estimate the activity specific rate of energy expenditure of free-living cormorants. 5. To verify that the approach identifies expected trends in from situations with variable power requirements, we measured ODBA in free-living imperial cormorants (Phalacrocorax atriceps) during foraging trips. We compared ODBA during return and outward foraging flights, when birds are expected to be laden and not laden with captured fish, respectively. We also examined changes in ODBA during the descent phase of diving, when power requirements are predicted to decrease with depth due to changes in buoyancy associated with compression of plumage and respiratory air. 6. In free-living imperial cormorants, ODBA, and hence estimated VO2, was higher during the return flight of a foraging bout, and decreased with depth during the descent phase of a dive, supporting the use of accelerometry for the determination of activity-specific rate of energy expenditure.

1. Measurements of the rate of oxygen consumption (Vo 2 ) in the field are usually impractical, so several studies of endotherms have utilized heart rate (f H ) as a correlate of Vo 2 because of the tight relationship that often exists between the two variables. There have been several reports, however, where the relationship between f H and Vo 2 changes or disassociates under different physiological or psychological circumstances. This may be further confounded in ectothermic vertebrates, which experience relatively large fluctuations in body temperature (T b ). 2. The aim of the present study was to characterize in Rosenberg's Goanna (Varanus rosenbergi) the relationship that exists between T b , f H and Vo 2 at rest and at different levels of exercise, during periods of heating and cooling, and following ingestion of a meal. 3. The combinations of T b and f H were accurate at predicting Vo 2 of animals at different levels of exercise and recovery, and during the postprandial period. 4. Predictions of Vo 2 became less reliable during periods of relatively rapid heating when f H and blood flow increase for thermoregulatory purposes with no associated increase in Vo 2 . To counter this, f H was excluded from the prediction equation when the rate of heating exceeded 20% of the predicted mass-dependent maximum attainable rate, and Vo 2 was predicted using T b alone. 5. The resultant Vo 2 prediction equation was used to estimate Vo 2 of seven animals that were allowed to thermoregulate behaviourally, and the mean predicted Vo 2 (Vo 2pred ) was not significantly different from the mean measured Vo 2 (Vo 2meas ) for fasting or postprandial lizards.

6 PAGES; International audience; We describe a method that allows prediction of resting metabolic rate (RMR, ml O2 Æ min1) in adult male and female king penguins on shore by measuring body mass (Mb) and the length of the foot, flipper and beak. This method is accurate, underestimating measured RMR (n=114) by 4% in a data set consisting of 44 birds (33 males and 11 females). Measurement error was unbiased with respect to fasting duration and can therefore estimate RMR during any stage of fasting. This new method provides significant cost and logistical savings when estimating RMR during fieldwork, allowing RMR of a large number of birds to be measured quickly. These findings suggest the possibility that the use of Mb and morphometrics will allow development of general and specific equations to estimate RMR in other species.