Plasma metabolites reflect seasonally changing metabolic processes in a long-distance migrant shorebird (Calidris canutus)

Migrant birds have tightly scheduled annual cycles consisting of several distinct life cycle (sub-)stages such as reproduction, migration, moult and overwintering, each of which have specific metabolic requirements (e.g., fattening during migration, protein build-up during moult). This study examines changes in fat and protein metabolism during the annual cycle of body mass and moult over 1.5 years in a captive flock of an arctic-breeding shorebird, the red knot Calidris canutus islandica. 2–5 h after food withdrawal, plasma uric acid levels were still decreasing and β-hydroxy-butyrate levels were low, indicating prolonged catabolism of dietary protein, probably linked with a conversion into lipids. Such a late-resorptive state is achieved much earlier in passerines, but only after several days in penguins and, thus, seems to depend on meal size or mass-specific metabolic rate. Substages of body mass gain and high body mass were characterized by increased plasma triglyceride levels reflecting increased turnover of lipids, and low levels of the ketone body β-hydroxy-butyrate, indicating that the bird is not short of glucose. The high uric acid levels during these substages indicated an increased breakdown of nutritional protein. During moult, plasma triglyceride levels were low, suggesting that lipids were less available than at other times of the year. It is concluded that plasma metabolite levels indicate the metabolic processes related to migratory fuelling and moult and the influence of exogeneous factors.

Oxidative stress in endurance flight: an unconsidered factor in bird migration

Migrating birds perform extraordinary endurance flights, up to 200 h non-stop, at a very high metabolic rate and while fasting. Such an intense and prolonged physical activity is normally associated with an increased production of reactive oxygen and nitrogen species (RONS) and thus increased risk of oxidative stress. However, up to now it was unknown whether endurance flight evokes oxidative stress. We measured a marker of oxidative damage (protein carbonyls, PCs) and a marker of enzymatic antioxidant capacity (glutathione peroxidase, GPx) in the European robin (Erithacus rubecula), a nocturnal migrant, on its way to the non-breeding grounds. Both markers were significantly higher in European robins caught out of their nocturnal flight than in conspecifics caught during the day while resting. Independently of time of day, both markers showed higher concentrations in individuals with reduced flight muscles. Adults had higher GPx concentrations than first-year birds on their first migration. These results show for the first time that free-flying migrants experience oxidative stress during endurance flight and up-regulate one component of antioxidant capacity. We discuss that avoiding oxidative stress may be an overlooked factor shaping bird migration strategies, e.g. by disfavouring long non-stop flights and an extensive catabolism of the flight muscles

Physiological Aeroecology: Anatomical and Physiological Adaptations for Flight

Flight has evolved independently in birds, bats, and insects and was present in the Mesozoic pterosaurians that have disappeared. Of the roughly one million living animal species, more than three-quarters are flying insects. Flying is an extremely successful way of locomotion. At first glance, this seems surprising because leaving the ground and moving in the air is energetically expensive. We will therefore start with the question: why do some animals spend a substantial proportion of their life in the air? To generate lift, a few key features are required, and yet, animals show incredible diversity in their flight mechanics. We will review constraints imposed by body size including anatomical adaptations of the skeleton, muscles, and organs necessary to stay airborne with a special focus on the wings. Ecology of the aerial organism, such as diet or migration, has diversified flight styles and the physiological adaptations required to optimize performance. For example, animals are exposed to low temperatures and low oxygen pressure at high altitude, whereas overheating can pose a problem at low altitudes. Moreover, aerial prey can be particularly apparent to aerial predators resulting in selection on flight speed and maneuverability of predators and prey. Flight is energetically costly, much more costly than walking, with the majority of the cost dictated by body mass. Hence, adding weight load to fuel flight also adds to the cost of flight. We review energy supply for flight, and special adaptations for long-term flights. Aeroecology has resulted in extraordinary visual and aural sensory systems of predators, which in coordination with the locomotor system are under strong selection to detect and intercept prey in flight

Supplemental Information 1: Raw data: Plasma metabolite concentrations, moult stage, and timing of capture for young common snipe migrating through central Poland

Moult of feathers entails considerable physiological and energetic costs to an avian organism. Even under favourable feeding conditions, endogenous body stores and energy reserves of moulting birds are usually severely depleted. Thus, most species of birds separate moult from other energy-demanding activities, such as migration or reproduction. Common snipe Gallinago gallinago is an exception, as during the first autumn migration many young snipe initiate the post-juvenile moult, which includes replacement of body feathers, lesser and median wing coverts, tertials, and rectrices. Here, we evaluated moult-related changes in blood plasma biochemistry of the common snipe during a period of serious trade-off in energy allocation between moult and migration. For this purpose, concentrations of basic metabolites in plasma were evaluated in more than 500 young snipe migrating through Central Europe. We found significant changes in the plasma concentrations of total protein, triglyceride and glucose over the course of moult, while the concentrations of uric acid and albumin did not change. Total protein concentration increased significantly in the initial stage of moult, probably as a result of increased production of keratin, but it decreased to the pre-moult level at the advanced stage of moult. Plasma triglyceride concentration decreased during the period of tertial and rectrice moult, which reflected depletion of endogenous fat reserves. By contrast, glucose concentration increased steadily during the course of moult, which could be caused by increased catabolism of triglycerides (via gluconeogenesis) or, alternatively, due to increased glucocorticoids as a stress response. Our results suggest that physiological changes associated with moult may be considered important determinants of the low pace of migration typical of the common snipe

Variation in feather corticosterone levels in Alpine swift nestlings provides support for the hypo-responsive hypothesis

Acknowledgements: The authors would like to thank the numerous students who helped collecting data in the field and the city council of Solothurn for access the Bieltor tower. SJE would like to thank Benedetta Catitti for producing the figures and Lukas Jenni for valuable comments on the manuscript. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.Peer reviewedPostprintPublisher PD

Why Do Migratory Birds Sing on Their Tropical Wintering Grounds?

Many long-distance migratory birds sing extensively on their tropical African wintering grounds, but the function of this costly behavior remains unknown. In this study, we carry out a first empirical test of three competing hypotheses, combining a field study of great reed warblers (Acrocephalus arundinaceus) wintering in Africa with a comparative analysis across Palearctic-African migratory songbird species. We asked whether winter song (i) functions to defend nonbreeding territories, (ii) functions as practice to improve complex songs for subsequent breeding, or (iii) is a nonadaptive consequence of elevated testosterone carryover. We found support for neither the long-assumed territory-defense hypothesis (great reed warblers had widely overlapping home ranges and showed no conspecific aggression) nor the testosterone-carryover hypothesis (winter singing in great reed warblers was unrelated to plasma testosterone concentration). Instead, we found strongest support for the song-improvement hypothesis, since great reed warblers sang a mate attraction song type rather than a territorial song type in Africa, and species that sing most intensely in Africa were those in which sexual selection acts most strongly on song characteristics; they had more complex songs and were more likely to be sexually monochromatic. This study underlines how sexual selection can have far-reaching effects on animal ecology throughout the annual cycle.MCS was funded by the Gates Cambridge Trust and the Natural Sciences and Engineering Research Council of Canada. CNS was supported by a Royal Society Dorothy Hodgkin Fellowship, a BBSRC David Phillips Fellowship, and the DST-NRF Centre of Excellence at the Percy FitzPatrick Institute.This is the author accepted manuscript. The final version is available from the University of Chicago Press via http://dx.doi.org/10.1086/68468

Eye region surface temperature dynamics during acute stress relate to baseline glucocorticoids independently of environmental conditions

Reactions to acute stressors are critical for survival. Yet, the challenges of assessing underlying physiological processes in the field limit our understanding of how variation in the acute stress response relates to fitness in free-living animals. Glucocorticoid secretion during acute stress can be measured from blood plasma concentrations, but each blood sample can only provide information for one point in time. Also, the number of samples that can be extracted from an individual in the field is usually limited to avoid compromising welfare. This restricts capacity for repeated assessment, and therefore temporal resolution of findings within- and between-acute stress responses - both of which are important for determining links between acute stress and fitness. Acute stress induces additional body surface temperature changes that can be measured non-invasively, and at high frequencies using thermal imaging, offering opportunities to overcome these limitations. But, this method's usefulness in the field depends on the extent that environmental conditions affect the body surface temperature response, which remains poorly understood. We assessed the relative importance of individual physiology (baseline glucocorticoid concentrations) and environmental conditions (air temperature and relative humidity) in determining the eye region surface temperature (Teye) response to acute stress, in wild blue tits (Cyanistes caeruleus) during trapping, handling and blood sampling. When controlling for between-individual baseline variation, Teye initially dropped rapidly below, and then recovered above baseline, before declining more slowly until the end of the test, 160 s after trap closure. One measure of the amplitude of this response – the size of the initial drop in Teye – was dependent on environmental conditions, but not baseline corticosterone. Whereas, two properties defining response dynamics – the timing of the initial drop, and the slope of the subsequent recovery – were related to baseline corticosterone concentrations, independently of environmental conditions. This suggests inferring the acute stress response using thermal imaging of Teye will be practical under fluctuating environmental conditions in the field

A rare study from the wintering grounds provides insight into the costs of malaria infection for migratory birds

Malaria parasites can have strong effects on the population dynamics and evolution of migratory bird species. In many species, parasite transmission occurs on the wintering grounds, but studies to determine the consequences of infection have taken place during the breeding season, when malaria parasites circulate at chronic levels. We examined the predictors of malarial infections for great reed warblers during the northern winter in Africa, where active parasite transmission is thought to occur and naïve individuals experience acute infections. Counter to expectations, we found that winter infection intensities were lower than those encountered on the breeding grounds. One potential explanation is that reduced immune function during breeding allows parasites to persist at higher chronic intensities. We found no relationships between the incidence or intensity of infection on condition (as measured by scaled mass index, plasma metabolites, and feather corticosterone), spring migration departure dates, or home range sizes. We also tested a prediction of the Hamilton–Zuk hypothesis and found that male ornament (song) quality was unrelated to parasitic infection status. Overall, our results provide the first evidence that long-distance migrants captured on their wintering grounds are in the chronic stage of infection, and suggest that winter studies may fare no better than breeding studies at determining the costs of acute malarial infection for great reed warblers.This is the final version of the article. It first appeared from Wiley via http://dx.doi.org/10.1111/jav.0087

A rare study from the wintering grounds provides insight into the costs of malaria infection for migratory birds

Malaria parasites can have strong effects on the population dynamics and evolution of migratory bird species. In many species, parasite transmission occurs on the wintering grounds, but studies to determine the consequences of infection have taken place during the breeding season, when malaria parasites circulate at chronic levels. We examined the predictors of malarial infections for great reed warblers during the northern winter in Africa, where active parasite transmission is thought to occur and naïve individuals experience acute infections. Counter to expectations, we found that winter infection intensities were lower than those encountered on the breeding grounds. One potential explanation is that reduced immune function during breeding allows parasites to persist at higher chronic intensities. We found no relationships between the incidence or intensity of infection on condition (as measured by scaled mass index, plasma metabolites, and feather corticosterone), spring migration departure dates, or home range sizes. We also tested a prediction of the Hamilton–Zuk hypothesis and found that male ornament (song) quality was unrelated to parasitic infection status. Overall, our results provide the first evidence that long‐distance migrants captured on their wintering grounds are in the chronic stage of infection, and suggest that winter studies may fare no better than breeding studies at determining the costs of acute malarial infection for great reed warblers.This is the final version of the article. It first appeared from Wiley via http://dx.doi.org/10.1111/jav.0087

Eye region surface temperature reflects both energy reserves and circulating glucocorticoids in a wild bird

Body temperature of endotherms shows substantial within- and between-individual variation, but the sources of this variation are not fully understood in wild animals. Variation in body temperature can indicate how individuals cope with their environment via metabolic or stress-induced effects, both of which may relate to depletion of energy reserves. Body condition can reflect heat production through changes to metabolic rate made to protect energy reserves. Additionally, changes in metabolic processes may be mediated by stress-related glucocorticoid secretion, which is associated with altered blood-flow patterns that affect regional body temperatures. Accordingly, both body condition and glucocorticoid secretion should relate to body temperature. We used thermal imaging, a novel non-invasive method of temperature measurement, to investigate relationships between body condition, glucocorticoid secretion and body surface temperature in wild blue tits (Cyanistes caeruleus). Individuals with lower body condition had lower eye-region surface temperature in both non-breeding and breeding seasons. Eye-region surface temperature was also negatively correlated with baseline circulating glucocorticoid levels in non-breeding birds. Our results demonstrate that body surface temperature can integrate multiple aspects of physiological state. Consequently, remotely-measured body surface temperature could be used to assess such aspects of physiological state non-invasively in free-living animals at multiple life history stages