Susanne Jenni-Eiermann

FUEL SUPPLY AND METABOLIC CONSTRAINTS IN MIGRATING BIRDS

Energy management for endurance flight critically determines the ecological options in the life history of migrant birds. Apart from the amount of energy stores, the types of fuel used and metabolic constraints determine endurance performance in long-distance migrants. The three main types of fuel (lipids, glycogen, protein) are evaluated regarding (a) costs of transport and maintenance, (b) supply to the muscles during flight, (c) adverse effects during, and (d) after, flight, and (e) refuelling. Lipids are the best fuel type with respect to three of these five criteria, but pose problems regarding the supply from adipose tissues to the muscles and regarding oxidation. Nevertheless, birds can maximize the contribution of energy derived from lipids as a proportion of the total energy expenditure to about 95% during migratory endurance flight. Mechanisms to do so may include enhancing fatty acid transport to the flight muscles, increasing initial fat stores and increasing aerobic capacity. A very low relative contribution of energy derived from protein (RPC) is attained by migrating birds (around 5%), similar to that of long-term fasting birds. RPC values of fasting birds depend on initial fat content and are lower than in fasting mammals. This suggests that in fasting birds the absolute amount of protein catabolism is roughly proportional to metabolic rate. Mechanisms to increase the relative contribution of energy derived from fat are costly. Hence, they are expected to modify the power curve relating energy expenditure to flight speed and predictions derived from it. It is also expected that migrants flying short non-stop distances or risking dehydration will not maximize lipid utilization to the same extent as birds flying long distances non-stop. Hence, the optimal amount and proportions of fat and protein stored and functional organ sizes are expected to depend on the migration strategy, particularly on the duration of non-stop flights and the risk of dehydration.

Plasma Metabolite Levels Predict Individual Body-Mass Changes in a Small Long-Distance Migrant, the Garden Warbler

-Change in body mass is an important measurement in many studies addressing changes in energy stores or condition. Usually, change in body mass is measured in birds caught twice, but this has a number of drawbacks (e.g. low number of retraps, retraps not representative of all first captures, adverse effects of first capture on body-mass development). Therefore, we investigated whether plasma metabolites correlate with body-mass change, and which metabolites could be used to predict body-mass change in birds caught once. In an experiment, 20 Garden Warblers (Sylvia borin) were given different amounts of food to induce stable, increasing, and decreasing body masses. Most of the eight plasma metabolites we examined were significantly correlated with the change in body mass between early morning and midday, the time of blood sampling, but not with body mass or various measures of activity. Metabolites that are known to characterize resorption were elevated in birds gaining body mass and metabolites characteristic of fasting were elevated in birds losing body mass. Triglycerides and ,B-hydroxy-butyrate together explained 61% of the variation in body-mass change (triglycerides alone 44% and ,3-hydroxy-butyrate alone 51%). These metabolites may be used to predict body-mass change in birds caught once, provided that the reliability and sensitivity of this method are checked in field tests. Received 27 September 1993, accepted 30 January 1994. BIRDS MAY FACE DEFICITS in their energy balance during the nonactive period of the day, during periods of several days, or even over a series of weeks. They usually build up energy stores in anticipation of such periods and as an adaptive compromise to different selective pressures (e.g. Lima 1986, Lehikoinen 1987, Moreno 1989, Ekman and Hake 1990, Rogers and Smith 1993). This results in fluctuating energy stores between foraging and nonforaging periods (usually day and night) superimposed on longer periods of net energy storage and net energy expenditure (King 1972). For instance, cold and short winter days, bad weather, incubation, feeding young, and migration may all be associated with decreasing energy stores and preceded by energy storage. Body mass is a crude but widely used estimate of energy stores because it is easy and harmless to measure. If corrected for size, body mass may be used as an indication of condition (e.g. Blem 1990). Changes in body mass may give a fairly accurate picture of the fluctuations in energy stores (e.g. Rogers and Rogers 1990). The measurement of changes in body mass of free-living birds is important in a variety of contexts. For instance, it may allow the assessment of the effects of food availability on energy storage in different habitats, under different weather conditions, and under different degrees of competition or predation (e.g. Bibby et al. 1976, Bibby and Green 1983, Buchanan et al. 1985, Lima 1985, Lindstrom 1990, Moore and Yong 1991). Body-mass changes may indicate periods of constraints and periods of adaptive mass variations during the annual cycle (Moreno 1989). Evaluation of body-mass changes may allow study of the pattern and environmental influences of energy storage during stopovers by migrants (e.g. Bibby et al. 1976, Mehlum 1983a, b, Biebach 1985, Biebach et al. 1986, Alerstam and Lindstrom 1990). In free-living birds, changes in body mass generally are measured in birds caught at least twice, usually at the same place. This, however, has a number of drawbacks: (1) changes in body mass are measured only in the subsample of retraps and this may reduce the sample size drastically, especially when trap shyness is a factor; (2) a certain group of birds may not be recaught and, thus, the sample of retraps may not be representative (e.g. Bibby et al. 1976, Biebach et al. 1986, Veiga 1986, Winker et al. 1992); and (3) first capture may have an adverse

Metabolic responses to flight and fasting in night-migrating passerines

Summary1.Small passerine migrants achieve endurance flight while fasting, together with one of the highest mass-specific energy rates. Metabolic responses to flight and fasting were examined in three species of free-living migrants (Sylvia borin, Ficedula hypoleuca, Erithacus rubecula) by measuring plasma concentrations of glucose, uric acid, triglycerides, glycerol, free fatty acids (FFA), and β-hydroxybutyrate (β-OHB) in three main physiological situations (feeding, overnight fasting, nocturnal flight) and while changing between these situations.2.Overnight-fasted birds showed low triglyceride and uric acid levels. Contrary to mammals, FFA and glycerol levels were not increased in agreement with published data on birds. The transition from feeding to fasting (post-feeding) was distinguished by a temporary rise in FFA and a drop in glucose levels.3.Birds utilize fat during migratory flight, indicated by high levels of FFA, glycerol, and β-OHB. For the first time, high triglyceride levels were found in an exercising vertebrate. The use of protein during flight was demonstrated by high uric acid levels.4.Birds kept inactive after flight showed a more pronounced reduction of the fat and protein utilization and post-exercise ketosis than naturally landed birds.5.Differences among the three species in the metabolic pattern suggest that the garden warbler shows the greatest metabolic adaption to endurance flight, having the highest levels of fat metabolites and the highest body fat reserves.

Spreading free-riding snow sports represent a novel serious threat for wildlife

Stress generated by humans on wildlife by continuous development of outdoor recreational activities is of increasing concern for biodiversity conservation. Human disturbance often adds to other negative impact factors affecting the dynamics of vulnerable populations. It is not known to which extent the rapidly spreading free-riding snow sports actually elicit detrimental stress (allostatic overload) upon wildlife, nor what the potential associated fitness and survival costs are. Using a non-invasive technique, we evaluated the physiological stress response induced by free-riding snow sports on a declining bird species of Alpine ecosystems. The results of a field experiment in which radiomonitored black grouse (Tetrao tetrix) were actively flushed from their snow burrows once a day during four consecutive days showed an increase in the concentration of faecal stress hormone (corticosterone) metabolites after disturbance. A large-scale comparative analysis across the southwestern Swiss Alps indicated that birds had higher levels of these metabolites in human-disturbed versus undisturbed habitats. Disturbance by snow sport free-riders appears to elevate stress, which potentially represents a new serious threat for wildlife. The fitness and survival costs of allostatic adjustments have yet to be estimated.

High Plasma Triglyceride Levels in Small Birds during Migratory Flight: A New Pathway for Fuel Supply during Endurance Locomotion at Very High Mass-Specific Metabolic Rates?

Plasma fat metabolites were measured during the nocturnal migratory flight in three species of small passerines. The birds had higher free fatty acid (FFA) and glycerol levels than resting birds that had been fasted overnight. In contrast to exercising mammals and large birds, they also had elevated levels of triglyceride and the very low density lipoprotein (VLDL) fraction. It is hypothesized that FFA reesterification in the liver and delivery of triglyceride-VLDL to the flight muscles helps to circumvent constraints in energy supply during endurance locomotion in animals with very high mass-specific metabolic rates.

Parental investment and its sensitivity to corticosterone is linked to melanin-based coloration in barn owls

Behavioral and physiological responses to unpredictable changes in environmental conditions are, in part, mediated by glucocorticoids (corticosterone in birds). In polymorphic species, individuals of the same sex and age display different heritable melanin-based color morphs, associated with physiological and reproductive parameters and possibly alternative strategies to cope with variation in environmental conditions. We examined whether the role of corticosterone in resolving the trade-off between self-maintenance and reproductive activities covaries with the size of melanin-based spots displayed on the ventral body side of male barn owls. Administration of corticosterone to simulate physiological stress in males revealed pronounced changes in their food-provisioning rates to nestlings compared to control males. Corticosterone-treated males with small eumelanic spots reduced nestling provisioning rates as compared to controls, and also to a greater degree than did corticosterone-treated males with large spots. Large-spotted males generally exhibited lower parental provisioning and appear insensitive to exogenous corticosterone suggesting that the size of the black spots on the breast feathers predicts the ability to cope with stressful situations. The reduced provisioning rate of corticosterone-treated males caused a temporary reduction in nestling growth rates but, did not affect fledgling success. This suggests that moderately elevated corticosterone levels are not inhibitory to current reproduction but rather trigger behavioral responses to maximize lifetime reproductive success.

Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian kestrels Falco tinnunculus

SUMMARY Environmental conditions affect growth and development and, through developmental plasticity, create phenotypic variation. In suboptimal conditions current survival is traded-off against development. Corticosterone, the main glucocorticoid in birds, may be involved in the reallocation of energy from growth to maintenance, but its effect on growth has rarely been investigated in altricial birds under natural conditions in the wild. In free-living Eurasian kestrel Falco tinnunculus nestlings, we artificially elevated corticosterone to stress-induced levels over 2–3 days in the middle of the nestling stage by implanting biodegradable implants, controlling the treatment with a placebo group. We measured the length of primary feather 8, hand length, tarsus length, body mass and subcutaneous fat stores from day 10 to 25. During corticosterone elevation, primary growth of cort-nestlings was significantly reduced to 71% of placebo-nestlings, hand and tarsus growth were significantly reduced to 14% and 26% of placebo-nestlings, respectively, and body mass increase stopped, while subcutaneous fat-store growth was not affected. Over the following 5 days, primary growth was still significantly suppressed to 84% of placebo-nestlings, while hand, tarsus and body mass growth were back to normal. During the subsequent 4 days, cort-nestlings partly compensated for the lag in body mass by significantly accelerating the body mass increase compared with placebo-nestlings. Before fledging, primary length was 10% shorter, hand and tarsus 5% and 4% shorter and body mass 8.5% lower in cort-nestlings than in placebo-nestlings, while fat score did not differ significantly between the two groups. Thus, we have shown that in free-living, altricial nestlings a few days of elevated plasma corticosterone levels alone, without food restriction, suppressed growth and this could only partly be compensated for afterwards. Feather, bone and body mass growth were reduced to different degrees, indicating that corticosterone had a differential effect on different structures. This demonstrates that corticosterone is probably involved in the control of developmental plasticity.

Effects of corticosterone pellets on baseline and stress-induced corticosterone and corticosteroid-binding-globulin

Exogenous administration of glucocorticoids is a widely used and efficient tool to investigate the effects of elevated concentrations of these hormones in field studies. Because the effects of corticosterone are dose and duration-dependent, the exact course of plasma corticosterone levels after exogenous administration needs to be known. We tested the performance of self-degradable corticosterone pellets (implanted under the skin) in elevating plasma corticosterone levels. We monitored baseline (sampled within 3min after capture) total corticosterone levels and investigated potential interactions with corticosteroid-binding-globulin (CBG) capacity and the endogenous corticosterone response to handling in Eurasian kestrel Falco tinnunculus and barn owl Tyto alba nestlings. Corticosterone pellets designed for a 7-day-release in rodents elevated circulating baseline total corticosterone during only 2-3 days compared to placebo-nestlings. Highest levels occurred 1-2days after implantation and levels decreased strongly thereafter. CBG capacity was also increased, resulting in a smaller, but still significant, increase in baseline free corticosterone levels. The release of endogenous corticosterone as a response to handling was strong in placebo-nestlings, but absent 2 and 8 days after corticosterone pellet implantation. This indicates a potential shut-down of the hypothalamo-pituitary-adrenal axis after the 2-3 days of elevated baseline corticosterone levels. 20 days after pellet implantation, the endogenous corticosterone response to handling of nestlings implanted with corticosterone pellets attained similar levels as in placebo-nestlings. Self-degradable pellets proved to be an efficient tool to artificially elevate circulating baseline corticosterone especially in field studies, requiring only one intervention. The resulting peak-like elevation of circulating corticosterone, the concomitant elevation of CBG capacity, and the absence of an endogenous corticosterone response to an acute stressor have to be taken into account.

Pheomelanin‐Based Coloration and the Ability to Cope with Variation in Food Supply and Parasitism

Although gene by environment interactions may play a key role in the maintenance of genetic polymorphisms, little is known about the ecological factors involved in these interactions. We investigated whether food supply and parasites can mediate covariation between the degree of adult pheomelanin‐based coloration, a heritable trait, and offspring body mass in the tawny owl (Strix aluco). We swapped clutches between nests to allocate genotypes randomly among environments. Three weeks after hatching, we challenged the immune system of 80 unrelated nestlings with either a phytohemagglutinin (PHA) or a lipopolysaccharide, surrogates of alternative parasites, and then fed them ad lib. or food‐restricted them during the following 6 days in the laboratory. Whatever the immune challenge, nestlings fed ad lib. converted food more efficiently into body mass when their biological mother was dark pheomelanic. In contrast, food‐restricted nestlings challenged with PHA lost less body mass when their biological mother was pale pheomelanic. Nestling tawny owls born from differently melanic mothers thus show differing reaction norms relative to food availability and parasitism. This suggests that dark and pale pheomelanic owls reflect alternative adaptations to food availability and parasites, factors known to vary in space and time.

Contributions of endocrinology to the migration life history of birds

Migration is a key life cycle stage in nearly 2000 species of birds and is a greatly appreciated phenomenon in both cultural and academic arenas. Despite a long research tradition concerning many aspects of migration, investigations of hormonal contributions to migratory physiology and behavior are more limited and represent a comparatively young research field. We review advances in our understanding of the hormonal mechanisms of migration with particular emphasis on the sub-stages of the migration life history: development, departure, flight and arrival. These sub-stages vary widely in their behavioral, ecological and physiological contexts and, as such, should be given appropriate individual consideration.