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Telomeres are chromosome protectors that shorten during cell replication and in stressful conditions. Developing individuals are susceptible to telomere erosion when their growth is fast and resources limited. This is critical because the rate of telomere attrition in early life is linked to health and life span of adults. The metabolic telomere attrition hypothesis (MeTA) suggests that telomere dynamics can respond to biochemical signals conveying information about the organism’s energetic state. Among these signals are glucocorticoids (hormones that promote catabolic processes, potentially impairing costly telomere maintenance) and nucleotides, which activate anabolic pathways though the cellular enzyme target of rapamycin (TOR) preventing telomere attrition. During the energetically demanding growth phase, the regulation of telomeres in response to two contrasting signals—one promoting telomere maintenance and the other inducing attrition—provides an ideal experimental setting to test MeTa. We studied nestlings of a rapidly developing free-living passerine, the great tit (Parus major), that either received glucocorticoids (Cort-chicks), nucleotides (Nuc-chicks), or a combination of both (NucCort-chicks) all compared with controls (Cnt-chicks). Contrary to Cort-chicks, which showed telomere attrition, NucCort-chicks, did not. NucCort-chicks was the only group showing increased gene expression of telo2 (proxy for TOR activation), of mitochondrial enzymes linked to ATP production (atp5f1a-atp5f1b-cox6a1-cox4) and a higher efficiency in aerobically producing ATP. NucCort-chicks had also a higher expression of telomere maintenance genes (trf2) and of enzymatic antioxidant genes (gpx4-sod1). The findings show that nucleotides availability is crucial for preventing telomere erosion during fast growth in stressful environments.

Migratory passerine birds fly long distances twice a year alternating nocturnal flights with stopovers to rest and replenish energy stores. The duration of each stopover depends on several factors including internal clocks, meteorological conditions, and environmental factors such as availability of food. Foraging entails energetic costs, and if birds need to refuel efficiently, they should modulate their activity in relation to food availability. We investigated how food availability influences locomotor activity in migrating birds of six passerine species at a spring stopover site in the central Mediterranean Sea. We selected birds with low fat scores which we expected to be strongly motivated to refuel. We simulated stopover sites of different quality by providing temporarily caged birds with different amounts of food to simulate scarce to abundant food. We analysed the diurnal locomotory activity as a proxy for food searching effort. Low food availability resulted in an increased diurnal locomotor activity in almost all species, while all birds showed low intensity of nocturnal migratory restlessness. In conclusion, our study shows that food availability in an important determinant of behaviour of migratory birds at stopover sites.

The study of avian migration physiology has advanced substantially in the past few decades, yet despite the key role of migratory stopovers in influencing total migration time, our knowledge on the physiological control of this crucial stage is still scarce. Research in stopover physiology has recently taken new directions and uncovered new mechanisms which help us understand how multiple internal factors, such as body condition or fuelling rate, interact with one another to trigger the rapid metabolic and behavioural switches that underlie stopover decisions. In this paper, we review a series of studies that our group conducted during the last 14 years on the island of Ponza (Italy), an important stopover site for thousands of small passerines migrating from Africa to Europe in spring. Focusing on nocturnally migrating passerines, we first discuss the pivotal role of fuel stores in decision-making processes during stopover. We then present recent research on the effects of food availability and fuel accumulation on behaviour shown by migrants at stopover places. Finally, we summarise recent findings on the hormonal factors that participate in controlling the switch between non-migratory and migratory state. Although the review is focused on our studies, we include recent work by other groups in this field.

Twice a year, billions of birds take on drastic physiological and behavioural changes to migrate between breeding and wintering areas. On migration, most passerine birds regularly stop over along the way to rest and refuel. Endogenous energy stores are not only the indispensable fuel to complete long distance flights, but are also important peripheral signals that once integrated in the brain modulate crucial behavioural decisions, such as the decision to resume migration after a stopover. A network of hormones signals metabolic fuel availability to the brain in vertebrates, including the recently discovered gut-hormone ghrelin. Here, we show that ghrelin takes part in the control of migratory behaviour during spring migration in a wild migratory passerine. We manipulated blood concentrations of ghrelin of 53 yellow-rumped warblers (Setophaga coronata coronata) caught during stopover and automatically radio-tracked their migratory behaviour following release. We found that injections of acylated and unacylated ghrelin rapidly induced movements away from the release site, indicating that the ghrelin system acts centrally to mediate stopover departure decisions. The effects of the hormone manipulation declined within 8 h following release, and did not affect the overall rate of migration. These results provide experimental evidence for a pivotal role of ghrelin in the modulation of behavioural decisions during migration. In addition, this study offers insights into the regulatory functions of metabolic hormones in the dialogue between gut and brain in birds.

Telomeres are DNA structures that protect chromosome ends. However, telomeres shorten during cell replication and at critically low lengths can reduce cell replicative potential, induce cell senescence and decrease fitness. Stress exposure, which elevates glucocorticoid hormone concentrations, can exacerbate telomere attrition. This phenomenon has been attributed to increased oxidative stress generated by glucocorticoids (‘oxidative stress hypothesis’). We recently suggested that glucocorticoids could increase telomere attrition during stressful periods by reducing the resources available for telomere maintenance through changes in the metabolic machinery (‘metabolic telomere attrition hypothesis’). Here we tested whether experimental increases in glucocorticoid levels affected telomere length and mitochondrial function in wild great tit (Parus major) nestlings during the energy-demanding early growth. We monitored resulting corticosterone (Cort) concentrations in plasma, and in red blood cells, telomere lengths and mitochondrial metabolism (metabolic rate, proton leak, oxidative phosphorylation, maximal mitochondrial capacity and mitochondrial inefficiency). We assessed oxidative damage caused by reactive oxygen species (ROS) metabolites as well as the total non-enzymatic antioxidant protection in plasma. Compared with control (Ctrl) nestlings, Cort-nestlings had higher baseline corticosterone, shorter telomeres and higher mitochondrial metabolic rate. Importantly, Cort-nestlings showed increased mitochondrial proton leak, leading to a decreased ATP production efficiency. Treatment groups did not differ in oxidative damage or antioxidants. Hence, glucocorticoid-induced telomere attrition is associated with changes in mitochondrial metabolism, but not with ROS production. These findings support the hypothesis that shortening of telomere length during stressful periods is mediated by glucocorticoids through metabolic rearrangements.

The hormone melatonin, a main component of the avian circadian system, plays an important role in the physiological transitions that accompany the activation of the migratory phenotype in passerine birds. Most small passerines migrate at night when circulating concentrations of melatonin are elevated. Previous work measured nocturnal melatonin levels of migratory birds only in captive animals, because free-living individuals are usually caught at day time. In this study, we compared nocturnal melatonin levels of European robins (Erithacus rubecula) caught during the day and held in cages overnight with those of birds that were caught at night and sampled immediately. We found that circulating melatonin at night was lower in birds held in cages compared to birds that were actively migrating. This result suggests that temporary caging affects the melatonin system and that in nature melatonin levels could be generally higher than those previously described by studies on captive birds.

During migration, birds need to optimize their time and/or energy management, especially during stop-overs. Previous studies with caged birds under controlled condition support the notion that departure decisions are condition-dependent, but they did not take into account the availability or the actual intake of food. In the study reported here we investigated whether food intake interacts with condition in influencing migratory disposition in temporarily caged wild migrants. We conducted the study on Garden Warblers (Sylvia borin) and European Robins (Erithacus rubecula) at a spring stop-over site that is reached after a long non-stop flight over the Mediterranean Sea. The birds were held in cages during the day and the first night following capture, and their locomotor activity, food intake, and body mass change were recorded. In both species, food intake was positively correlated with body mass change. Body condition was positively correlated with migratory restlessness (Zugunruhe) in both species and was also negatively related to diurnal activity in Garden Warblers. Food intake was negatively correlated with diurnal activity in Garden Warblers. When only birds with low fat scores were considered, we found a positive effect of food intake on Zugunruhe in Garden Warblers. In general, European Robins consumed less food than Garden Warblers and no significant effects on Zugunruhe were found. Our results show that food intake interacts with condition in affecting migratory behavior during stop-overs. In particular, food intake may induce Garden Warblers with low fat stores at arrival to leave a stop-over site earlier. The large individual variability in food consumption supports the notion that birds vary in their capacity to refuel soon after arrival at a stop-over site. Overall, our work suggests that the decision to stay at the stop-over site or to resume migration depends on the interaction of condition, refueling capacity and rate, and migratory strategy.

During migration, birds spend more than 80 % of the time at stopover sites to rest and refuel before and after crossing ecological barriers such as deserts or seas. Since stopover has intrinsic costs in terms of energy and time, birds should try to minimize its duration, which is dependent on the combined effects of environmental factors, endogenous programmes, and physiological conditions. Previous studies on long-distance migrants caught after crossing an ecological barrier have indicated that body condition strongly influences the decision whether to prolong stopover or resume migration, with lean birds staying longer than fat birds. In short-distance migrants, evidence is still scarce regarding a determinant role for physiological condition in stopover behaviour after crossing an ecological barrier. Here, we studied whether migratory restlessness (Zugunruhe) at a stopover site is dependent on physiological condition in three European short-distance migratory passerines: black redstarts, European robins, and European stonechats. In all species, an integrated measure of condition based on body mass, amount of subcutaneous fat, and thickness of pectoral muscles predicted the intensity of Zugunruhe. Overall, our results confirmed the importance of energy reserves in determining stopover duration, illustrating similar stopover strategies in short- and long-distance migrants.