Foraging to obtain food, either for self-maintenance or at presumably elevated rates to provide for offspring, is thought to be an energetically demanding activity but one that is essential for fitness (higher reproductive success and survival). Nevertheless, the physiological mechanisms that allow some individuals to support higher foraging performance, and the mechanisms underlying costs of high workload, remain poorly understood. We experimentally manipulated foraging behaviour in zebra finches () using the technique described by Koetsier and Verhulst (2011) Birds in the 'high foraging effort' (HF) group had to obtain food either while flying/hovering or by making repeated hops or jumps from the ground up to the feeder, behaviour typical of the extremely energetically expensive foraging mode observed in many free-living small passerines. HF birds made significantly more trips to the feeder per 10 min, whereas control birds spent more time (perched) at the feeder. Despite this marked change in foraging behaviour, we documented few short- or long-term effects of 'training' (3 days and 90 days of 'training', respectively) and some of these effects were sex specific. There were no effects of treatment on basal metabolic rate, haematocrit, haemoglobin or plasma glycerol, triglyceride and glucose levels, and masses of kidney, crop, large intestine, small intestine, gizzard and liver. HF females had higher masses of flight muscle, leg muscle, heart and lung compared with controls. In contrast, HF males had lower heart mass than controls and there were no differences for other organs. When both sexes were pooled, there were no effects of treatment on body composition. Finally, birds in the HF treatment group had higher levels of reactive oxygen metabolites (dROMs) and, consequently, although treatment did not affect total anti-oxidant capacity, birds in the HF treatment group had higher oxidative stress.
Many behaviors crucial for survival and reproductive success in free-living animals, including migration, foraging, and escaping from predators, involve elevated levels of physical activity. However, although there has been considerable interest in the physiological and biomechanical mechanisms that underpin individual variation in exercise performance, to date, much work on the physiology of exercise has been conducted in laboratory settings that are often quite removed from the animal's ecology. Here we review current, laboratory-based model systems for exercise (wind or swim tunnels for migration studies in birds and fishes, manipulation of exercise associated with non-migratory activity in birds, locomotion in lizards, and wheel running in rodents) to identify common physiological markers of individual variation in exercise capacity and/or costs of increased activity. Secondly, we consider how physiological responses to exercise might be influenced by (1) the nature of the activity (i.e., voluntary or involuntary, intensity, and duration), and (2) resource acquisition and food availability, in the context of routine activities in free-living animals. Finally, we consider evidence that the physiological effects of experimentally-elevated activity directly affect components of fitness such as reproduction and survival. We suggest that developing more ecologically realistic laboratory systems, incorporating resource-acquisition, functional studies across multiple physiological systems, and a life-history framework, with reproduction and survival end-points, will help reveal the mechanisms underlying the consequences of exercise, and will complement studies in free-living animals taking advantage of new developments in wildlife-tracking.
Aerobic capacity is assumed to be a main predictor of workload ability and haematocrit (Hct) and haemoglobin (Hb) have been suggested as key determinants of aerobic performance. Intraspecific studies have reported increases in Hct and Hb in response to increased workload. Furthermore, Hct and Hb vary markedly among individuals and throughout the annual cycle in free-living birds and it has been suggested that this variation reflects adaptive modulation of these traits to meet seasonal changes in energy demands. We used a comparative dataset of haematological traits, measures of metabolic rate (57 species), and life-history traits (160 species) to test several hypotheses for adaptive variation in haematology in relation to migration and altitude. We then extended these general ideas to test relationships between Hct and basal metabolic rate, daily energy expenditure and activity energy expenditure, using the 57 species that we have metabolic rate information for. We found that at the interspecific level, full migrants have higher Hct and Hb than partial migrants and non-migrants, and that altitude is positively correlated with Hb but not Hct. Hct is positively associated with activity energy expenditure (energy spent specifically on costly activities), suggesting that haematological traits could be adaptively modulated based on life-history traits and that Hct is a potential physiological mediator of energetic constraint.
Despite widely held assumptions that hematocrit (Hct) is a key determinant of aerobic capacity and exercise performance, this relationship has not often been tested rigorously in birds and results to date are mixed. Migration in birds involves high-intensity exercise for long durations at various altitudes. Therefore, it provides a good model system to examine the effect of Hct on flight performance and physiological responses of exercise at high altitude. We treated yellow-rumped warblers (Setophaga coronata) with avian erythropoietin (EPO) and anti-EPO to experimentally manipulate Hct and assessed flight performance at low and high altitudes using a hypobaric wind tunnel. We showed that anti-EPOtreated birds had lower Hct than vehicle-and EPO-treated birds posttreatment. Anti-EPO-treated birds also had marginally lower exercise performance at low altitude, committing a higher number of strikes (mistakes) in the first 30 min of flight. However, anti-EPO-treated birds performed significantly better at high altitude, attaining a higher altitude in a ramped altitude challenge to 3000 m equivalent altitude, and with a longer duration of flight at high altitude. Birds exercising at high altitude showed decreased Hct, increased glucose mobilization and decreased antioxidant capacity, regardless of treatment. In summary, we provide experimental evidence that the relationship between Hct and exercise performance is dependent on altitude. Future studies should investigate whether free-living birds adaptively modulate their Hct, potentially through a combination of erythropoiesis and plasma volume regulation (i.e. hemodilution), based on the altitude they fly at during migratory flight.
Considerable progress has been made in understanding the physiological basis for variation in the life‐history patterns of animals, particularly with regard to the roles of oxidative stress and hormonal regulation. However, an underappreciated and understudied area that could play a role in mediating inter‐ and intraspecific variation of life history is endoplasmic reticulum (ER) stress, and the resulting unfolded protein response (UPRER). ER stress response and the UPRER maintain proteostasis in cells by reducing the intracellular load of secretory proteins and enhancing protein folding capacity or initiating apoptosis in cells that cannot recover. Proper modulation of the ER stress response and execution of the UPRER allow animals to respond to intracellular and extracellular stressors and adapt to constantly changing environments. ER stress responses are heritable and there is considerable individual variation in UPRER phenotype in animals, suggesting that ER stress and UPRER phenotype can be subjected to natural selection. The variation in UPRER phenotype presumably reflects the way animals respond to ER stress and environmental challenges. Most of what we know about ER stress and the UPRER in animals has either come from biomedical studies using cell culture or from experiments involving conventional laboratory or agriculturally important models that exhibit limited genetic diversity. Furthermore, these studies involve the assessment of experimentally induced qualitative changes in gene expression as opposed to the quantitative variations that occur in naturally existing populations. Almost all of these studies were conducted in controlled settings that are often quite different from the conditions animals experience in nature. Herein, we review studies that investigated ER stress and the UPRER in relation to key life‐history traits including growth and development, reproduction, bioenergetics and physical performance, and ageing and senescence. We then ask if these studies can inform us about the role of ER stress and the UPRER in mediating the aforementioned life‐history traits in free‐living animals. We propose that there is a need to conduct experiments pertaining to ER stress and the UPRER in ecologically relevant settings, to characterize variation in ER stress and the UPRER in free‐living animals, and to relate the observed variation to key life‐history traits. We urge others to integrate multiple physiological systems and investigate how interactions between ER stress and oxidative stress shape life‐history trade‐offs in free‐living animals.
Here, we studied the life-long monogamous zebra finch, to examine the relationship between circulating sex steroid profiles and pair-maintenance behavior in pairs of wild-caught zebra finches (paired in the laboratory for >1 month). We used liquid chromatography-tandem mass spectrometry to examine a total of eight androgens and progestins [pregnenolone, progesterone, dehydroepiandrosterone (DHEA), androstenediol, pregnan-3,17-diol-20-one, androsterone, androstanediol, and testosterone]. In the plasma, only pregnenolone, progesterone, DHEA, and testosterone were above the limit of quantification. Sex steroid profiles were similar between males and females, with only circulating progesterone levels significantly different between the sexes (female > male). Circulating pregnenolone levels were high in both sexes, suggesting that pregnenolone might serve as a circulating prohormone for local steroid synthesis in zebra finches. Furthermore, circulating testosterone levels were extremely low in both sexes. Additionally, we found no correlations between circulating steroid levels and pair-maintenance behavior. Taken together, our data raise several interesting questions about the neuroendocrinology of zebra finches.
International audienceMonogamous pair bonds can be transient or long-lasting, which varies across species. The neuroendocrine mechanisms regulating pair maintenance behaviours are largely unknown, yet fundamental to our understanding of monogamy. Furthermore, the expression and regulation of pair maintenance behaviour is likely to be greatly influenced by social and environmental contexts. Our previous research suggested that androgens might regulate long-term pair maintenance behaviour in the monogamous zebra finch, Taeniopygia guttata. Here, we tested the hypothesis that testosterone treatment to males affects long-term pair maintenance behaviour in zebra finches. Established pairs were randomly assigned to one of two groups: control (N = 8) or testosterone (N = 7). Males were given either an empty or a testosterone-filled Silastic implant. Physical and acoustic affiliative behaviours and plasma testosterone levels were examined at three time points: pre-implantation, 30 days post-implant and 60 days post-implant. Importantly, we examined affiliative behaviours under two contexts: in the home cage (baseline) and following a brief chase (post stressor). Male testosterone treatment had no effects on behaviour during the baseline period, but significantly affected behaviours during the post stressor period. Specifically, testosterone-treated males spent less time in close proximity to their partner and sang more. To our knowledge, this is the first report of a context-dependent effect in the neuroendocrine regulation of pair maintenance behaviour, as well as the first report of an inhibitory effect of testosterone on zebra finch pairing behaviours. These results raise interesting questions about the function of affiliative behaviours in established pair bonds
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