Developmental programming of the adrenocortical stress response by yolk testosterone depends on sex and life history stage.

Developmental exposure of embryos to maternal hormones such as testosterone in the avian egg influences the expression of multiple traits, with certain effects being sex specific and lasting into adulthood. This pleiotropy, sex dependency and persistency may be the consequence of developmental programming of basic systemic processes such as adrenocortical activity or metabolic rate. We investigated whether experimentally increased in ovo exposure to testosterone influenced hypothalamus-pituitary-adrenal function, i.e. baseline and stress-induced corticosterone secretion, and resting metabolic rate (RMR) of adult male and female house sparrows (Passer domesticus). In previous experiments with this passerine bird we demonstrated effects of embryonic testosterone exposure on adult agonistic and sexual behavior and survival. Here we report that baseline corticosterone levels and the stress secretion profile of corticosterone are modified by in ovo testosterone in a sex-specific and life history stage-dependent manner. Compared with controls, males from testosterone-treated eggs had higher baseline corticosterone levels, whereas females from testosterone-treated eggs showed prolonged stress-induced corticosterone secretion during the reproductive but not the non-reproductive phase. Adult RMR was unaffected by in ovo testosterone treatment but correlated with integrated corticosterone stress secretion levels. We conclude that exposure of the embryo to testosterone programs the hypothalamus-pituitary-adrenal axis in a sex-specific manner that in females depends, in expression, on reproductive state. The modified baseline corticosterone levels in males and stress-induced corticosterone levels in females may explain some of the long-lasting effects of maternal testosterone in the egg on behavior and could be linked to previously observed reduced mortality of testosterone-treated females.

Animal tracking meets migration genomics: transcriptomic analysis of a partially migratory bird species.

Seasonal migration is a widespread phenomenon, which is found in many different lineages of animals. This spectacular behaviour allows animals to avoid seasonally adverse environmental conditions to exploit more favourable habitats. Migration has been intensively studied in birds, which display astonishing variation in migration strategies, thus providing a powerful system for studying the ecological and evolutionary processes that shape migratory behaviour. Despite intensive research, the genetic basis of migration remains largely unknown. Here, we used state-of-the-art radio-tracking technology to characterize the migratory behaviour of a partially migratory population of European blackbirds (Turdus merula) in southern Germany. We compared gene expression of resident and migrant individuals using high-throughput transcriptomics in blood samples. Analyses of sequence variation revealed a nonsignificant genetic structure between blackbirds differing by their migratory phenotype. We detected only four differentially expressed genes between migrants and residents, which might be associated with hyperphagia, moulting and enhanced DNA replication and transcription. The most pronounced changes in gene expression occurred between migratory birds depending on when, in relation to their date of departure, blood was collected. Overall, the differentially expressed genes detected in this analysis may play crucial roles in determining the decision to migrate, or in controlling the physiological processes required for the onset of migration. These results provide new insights into, and testable hypotheses for, the molecular mechanisms controlling the migratory phenotype and its underlying physiological mechanisms in blackbirds and other migratory bird species.

Artificial light at night desynchronizes strictly seasonal reproduction in a wild mammal.

Change in day length is an important cue for reproductive activation in seasonally breeding animals to ensure that the timing of greatest maternal investment (e.g. lactation in mammals) coincides with favourable environmental conditions (e.g. peak productivity). However, artificial light at night has the potential to interfere with the perception of such natural cues. Following a 5-year study on two populations of wild marsupial mammals exposed to different night-time levels of anthropogenic light, we show that light pollution in urban environments masks seasonal changes in ambient light cues, suppressing melatonin levels and delaying births in the tammar wallaby. These results highlight a previously unappreciated relationship linking artificial light at night with induced changes in mammalian reproductive physiology, and the potential for larger-scale impacts at the population level.

Repeated stressors in adulthood increase the rate of biological ageing.

BACKGROUND: Individuals of the same age can differ substantially in the degree to which they have accumulated tissue damage, akin to bodily wear and tear, from past experiences. This accumulated tissue damage reflects the individual's biological age and may better predict physiological and behavioural performance than the individual's chronological age. However, at present it remains unclear how to reliably assess biological age in individual wild vertebrates. METHODS: We exposed hand-raised adult Eurasian blackbirds (Turdus merula) to a combination of repeated immune and disturbance stressors for over one year to determine the effects of chronic stress on potential biomarkers of biological ageing including telomere shortening, oxidative stress load, and glucocorticoid hormones. We also assessed general measures of individual condition including body mass and locomotor activity. RESULTS: By the end of the experiment, stress-exposed birds showed greater decreases in telomere lengths. Stress-exposed birds also maintained higher circulating levels of oxidative damage compared with control birds. Other potential biomarkers such as concentrations of antioxidants and glucocorticoid hormone traits showed greater resilience and did not differ significantly between treatment groups. CONCLUSIONS: The current data demonstrate that repeated exposure to experimental stressors affects the rate of biological ageing in adult Eurasian blackbirds. Both telomeres and oxidative damage were affected by repeated stress exposure and thus can serve as blood-derived biomarkers of biological ageing.

Does urban life change blood oxidative status in birds?

Cities may expose wild animals to new types of selection pressures, potentially leading to differentiation among urban and rural populations. One cellular mechanism likely important in determining the viability of vertebrate populations is resistance to oxidative stress, as tissue degradation resulting from oxidative stress may decrease reproductive performance and survival. We hypothesized that city-thriving Eurasian blackbirds (Turdus merula) would be more resistant to oxidative stress when exposed to stressful conditions than rural conspecifics. Hand-raised city and rural blackbirds kept under common garden conditions indeed differed in blood oxidative status when exposed to chronic stress: city birds had lower oxidative damage during stressful conditions compared with rural birds, but also tended to generally maintain lower levels of non-enzymatic and enzymatic antioxidants than rural birds. These findings show that individuals from urban and rural areas differ intrinsically in their blood oxidative status physiology, possibly as an adaptation to city life.

Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds.

The growing interest in the effects of light pollution on daily and seasonal cycles of animals has led to a boost of research in recent years. In birds, it has been hypothesized that artificial light at night can affect daily aspects of behaviour, but one caveat is the lack of knowledge about the light intensity that wild animals, such as birds, are exposed to during the night. Organisms have naturally evolved daily rhythms to adapt to the 24-h cycle of day and night, thus, it is important to investigate the potential shifts in daily cycles due to global anthropogenic processes such as urbanization. We captured adult male European blackbirds (Turdus merula) in one rural forest and two urban sites differing in the degree of anthropogenic disturbance. We tagged these birds with light loggers and simultaneously recorded changes in activity status (active/non-active) through an automated telemetry system. We first analysed the relationship between light at night, weather conditions and date with daily activity onset and end. We then compared activity, light at night exposure and noise levels between weekdays and weekends. Onset of daily activity was significantly advanced in both urban sites compared to the rural population, while end of daily activity did not vary either among sites. Birds exposed to higher amounts of light in the late night showed earlier onset of activity in the morning, but light at night did not influence end of daily activity. Light exposure at night and onset/end of daily activity timing was not different between weekdays and weekends, but all noise variables were. A strong seasonal effect was detected in both urban and rural populations, such as birds tended to be active earlier in the morning and later in the evening (relative to civil twilight) in the early breeding season than at later stages. Our results point at artificial light at night as a major driver of change in timing of daily activity. Future research should focus on the costs and benefits of altered daily rhythmicity in birds thriving in urban areas.

Migratory lifestyle carries no added overall energy cost in a partial migratory songbird.

Seasonal bird migration may provide energy benefits associated with moving to areas with less physiologically challenging climates or increased food availability, but migratory movements themselves may carry high costs. However, time-dynamic energy profiles of free-living migrants-especially small-bodied songbirds-are challenging to measure. Here we quantify energy output and thermoregulatory costs in partially migratory common blackbirds using implanted heart rate and temperature loggers paired with automated radio telemetry and energetic modelling. Our results show that blackbirds save considerable energy in preparation for migration by decreasing heart rate and body temperature 28 days before departure, potentially dwarfing the energy costs of migratory flights. Yet, in warmer wintering areas, migrants do not appear to decrease total daily energy expenditure despite a substantially reduced cost of thermoregulation. These findings indicate differential metabolic programmes across different wintering strategies despite equivalent overall energy expenditure, suggesting that the maintenance of migration is associated with differences in energy allocation rather than with total energy expenditure.

Artificial light at night advances avian reproductive physiology.

Artificial light at night is a rapidly increasing phenomenon and it is presumed to have global implications. Light at night has been associated with health problems in humans as a consequence of altered biological rhythms. Effects on wild animals have been less investigated, but light at night has often been assumed to affect seasonal cycles of urban dwellers. Using light loggers attached to free-living European blackbirds (Turdus merula), we first measured light intensity at night which forest and city birds are subjected to in the wild. Then we used these measurements to test for the effect of light at night on timing of reproductive physiology. Captive city and forest blackbirds were exposed to either dark nights or very low light intensities at night (0.3 lux). Birds exposed to light at night developed their reproductive system up to one month earlier, and also moulted earlier, than birds kept under dark nights. Furthermore, city birds responded differently than forest individuals to the light at night treatment, suggesting that urbanization can alter the physiological phenotype of songbirds. Our results emphasize the impact of human-induced lighting on the ecology of millions of animals living in cities and call for an understanding of the fitness consequences of light pollution.

Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities.

When animals live in cities, they have to adjust their behaviour and life histories to novel environments. Noise pollution puts a severe constraint on vocal communication by interfering with the detection of acoustic signals. Recent studies show that city birds sing higher-frequency songs than their conspecifics in non-urban habitats. This has been interpreted as an adaptation to counteract masking by traffic noise. However, this notion is debated, for the observed frequency shifts seem to be less efficient at mitigating noise than singing louder, and it has been suggested that city birds might use particularly high-frequency song elements because they can be produced at higher amplitudes. Here, we present the first phonetogram for a songbird, which shows that frequency and amplitude are strongly positively correlated in the common blackbird (Turdus merula), a successful urban colonizer. Moreover, city blackbirds preferentially sang higher-frequency elements that can be produced at higher intensities and, at the same time, happen to be less masked in low-frequency traffic noise.

Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds.

INTRODUCTION: Artificial light-at-night is known to affect a broad array of behaviours and physiological processes. In urbanized bird species, light-at-night advances important biological rhythms such as daily cycles of activity/rest and timing of reproduction, but our knowledge of the underlying physiological mechanisms is limited. Given its role as chronobiological signal, melatonin is a strong candidate for mediating the effects of light-at-night. RESULTS: We exposed urban and rural European blackbirds (Turdus merula) to two light treatments equal in photoperiod but with different light intensities at night. The control group was exposed to 0.0001 lux (almost darkness), while the experimental group was exposed to 0.3 lux at night, simulating conditions recorded previously on free-living urban blackbirds. We obtained diel profiles of plasma melatonin for all birds in summer (July) and winter (January), while simultaneously recording locomotor activity. Daily patterns of melatonin concentrations were clearly affected by light-at-night in both seasons. In winter, melatonin concentrations of light-at-night birds were lower in the early and late night than in those of birds kept in darkness. In summer, melatonin concentrations of the light-at-night birds were lower through all night compared to birds kept in darkness. Locomotor activity in light-at-night birds was overall higher than in control individuals, both during the day and at night, and it increased sharply before dawn. In winter, the amount of activity before dawn in the light-at-night group correlated with changes in melatonin from midnight to late night: the greater the decrease in melatonin, the greater the amount of pre-dawn activity. Urban and rural birds responded similarly to light-at-night with respect to melatonin, but differed in their behaviour, with rural birds showing more locomotor activity than urban counterparts. CONCLUSIONS: This study points to reduced melatonin release at night as a potential physiological mechanism underlying the advanced onset of morning activity of urbanized birds. Based on the pattern of melatonin secretion, we suggest that birds responded to light-at-night as if they were exposed to a longer day than birds kept under dark nights.

Female-biased obligate strategies in a partially migratory population.

Partial migration occurs when a breeding population consists of seasonal migrants and year-round residents. Although it is common among birds, the basis of individual movement decisions within partially migratory populations is still unresolved. Over 4 years, we used state of the art tracking techniques, a combination of geolocators and radio transmitters, to follow individual European blackbirds Turdus merula year round from a partially migratory population to determine individual strategies and departure and arrival dates. The individual-based tracking combined with measures of energetic and hormonal (corticosterone) state enabled us to distinguish between obligate and facultative migration and to test several classical hypotheses of partial migration: the 'Arrival Time'-, 'Dominance'- and 'Thermal Tolerance'-hypotheses. Two distinct periods of departures from the breeding grounds were observed during the study; one in early autumn, and another during the midst of winter. Although blackbirds that migrated in autumn were never observed overwintering within 300 km of the study site, four individuals that departed in the winter were observed within 40 km. Females were significantly more likely to migrate in autumn than males but there was no difference in the age or body size of migrants and non migrants in autumn. Just prior to autumn migration, migrants had higher fat scores than non migrants and tended to have higher concentrations of baseline corticosterone, but similar concentrations of triglycerides. Unlike autumn migrants, we found no difference between the tendencies of males versus females to depart in winter, nor did we find any difference in body size or age of individuals that departed in the winter. Autumn migration was sex biased and resembled obligate migration. Our results provide strong support for the 'Arrival Time' hypothesis for partial migration in the autumn. We found no clear support for the 'Dominance' or 'Thermal Tolerance' hypotheses. By tracking individuals year round, we were able to identify a second period of departures. Overall, these results suggest the co-occurrence of obligate autumn migrants, winter movements and sedentary individuals within a single population.

A multi-species evaluation of digital wildlife monitoring using the Sigfox IoT network.

Bio-telemetry from small tags attached to animals is one of the principal methods for studying the ecology and behaviour of wildlife. The field has constantly evolved over the last 80 years as technological improvement enabled a diversity of sensors to be integrated into the tags (e.g., GPS, accelerometers, etc.). However, retrieving data from tags on free-ranging animals remains a challenge since satellite and GSM networks are relatively expensive and or power hungry. Recently a new class of low-power communication networks have been developed and deployed worldwide to connect the internet of things (IoT). Here, we evaluated one of these, the Sigfox IoT network, for the potential as a real-time multi-sensor data retrieval and tag commanding system for studying fauna across a diversity of species and ecosystems. We tracked 312 individuals across 30 species (from 25 g bats to 3 t elephants) with seven different device concepts, resulting in more than 177,742 successful transmissions. We found a maximum line of sight communication distance of 280 km (on a flying cape vulture [Gyps coprotheres]), which sets a new documented record for animal-borne digital data transmission using terrestrial infrastructure. The average transmission success rate amounted to 68.3% (SD 22.1) on flying species and 54.1% (SD 27.4) on terrestrial species. In addition to GPS data, we also collected and transmitted data products from accelerometers, barometers, and thermometers. Further, we assessed the performance of Sigfox Atlas Native, a low-power method for positional estimates based on radio signal strengths and found a median accuracy of 12.89 km (MAD 5.17) on animals. We found that robust real-time communication (median message delay of 1.49 s), the extremely small size of the tags (starting at 1.28 g without GPS), and the low power demands (as low as 5.8 µAh per transmitted byte) unlock new possibilities for ecological data collection and global animal observation.

New frontiers in bird migration research.

Bird migrations are impressive behavioral phenomena, representing complex spatiotemporal strategies to balance costs of living while maximizing fitness. The field of bird migration research has made great strides over the past decades, yet fundamental gaps remain. Technologies have sparked a transformation in the study of bird migration research by revealing remarkable insights into the underlying behavioral, cognitive, physiological and evolutionary mechanisms of these diverse journeys. Here, we aim to encourage broad discussions and promote future studies by highlighting research fields that are characterized by major knowledge gaps or conflicting evidence, namely the fields of navigation, social learning, individual development, energetics and conservation. We approach each topic by summarizing the current state of knowledge and provide a future outlook of ideas and state-of-the-art methods to further advance the field. Integrating knowledge across these disciplines will allow us to understand the adaptive abilities of different species and to develop effective conservation strategies in a rapidly changing world.

A songbird adjusts its heart rate and body temperature in response to season and fluctuating daily conditions.

In a seasonal world, organisms are continuously adjusting physiological processes relative to local environmental conditions. Owing to their limited heat and fat storage capacities, small animals, such as songbirds, must rapidly modulate their metabolism in response to weather extremes and changing seasons to ensure survival. As a consequence of previous technical limitations, most of our existing knowledge about how animals respond to changing environmental conditions comes from laboratory studies or field studies over short temporal scales. Here, we expanded beyond previous studies by outfitting 71 free-ranging Eurasian blackbirds (Turdus merula) with novel heart rate and body temperature loggers coupled with radio transmitters, and followed individuals in the wild from autumn to spring. Across seasons, blackbirds thermoconformed at night, i.e. their body temperature decreased with decreasing ambient temperature, but not so during daytime. By contrast, during all seasons blackbirds increased their heart rate when ambient temperatures became colder. However, the temperature setpoint at which heart rate was increased differed between seasons and between day and night. In our study, blackbirds showed an overall seasonal reduction in mean heart rate of 108 beats min-1 (21%) as well as a 1.2°C decrease in nighttime body temperature. Episodes of hypometabolism during cold periods likely allow the birds to save energy and, thus, help offset the increased energetic costs during the winter when also confronted with lower resource availability. Our data highlight that, similar to larger non-hibernating mammals and birds, small passerine birds such as Eurasian blackbirds not only adjust their heart rate and body temperature on daily timescales, but also exhibit pronounced seasonal changes in both that are modulated by local environmental conditions such as temperature. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

A partial migrant relies upon a range-wide cue set but uses population-specific weighting for migratory timing.

BACKGROUND: Many birds species range over vast geographic regions and migrate seasonally between their breeding and overwintering sites. Deciding when to depart for migration is one of the most consequential life-history decisions an individual may make. However, it is still not fully understood which environmental cues are used to time the onset of migration and to what extent their relative importance differs across a range of migratory strategies. We focus on departure decisions of a songbird, the Eurasian blackbird Turdus merula, in which selected Russian and Polish populations are full migrants which travel relatively long-distances, whereas Finnish and German populations exhibit partial migration with shorter migration distances. METHODS: We used telemetry data from the four populations (610 individuals) to determine which environmental cues individuals from each population use to initiate their autumn migration. RESULTS: When departing, individuals in all populations selected nights with high atmospheric pressure and minimal cloud cover. Fully migratory populations departed earlier in autumn, at longer day length, at higher ambient temperatures, and during nights with higher relative atmospheric pressure and more supportive winds than partial migrants; however, they did not depart in higher synchrony. Thus, while all studied populations used the same environmental cues, they used population-specific and locally tuned thresholds to determine the day of departure. CONCLUSIONS: Our data support the idea that migratory timing is controlled by general, species-wide mechanisms, but fine-tuned thresholds in response to local conditions.

Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds.

Wildlife inhabiting urban environments exhibit drastic changes in morphology, physiology, and behavior. It has often been argued that these phenotypic responses could be the result of micro-evolutionary changes following the urbanization process. However, other mechanisms such as phenotypic plasticity, maternal effects, and developmental plasticity could be involved as well. To address maternal effects as potential mechanisms, we compared maternal hormone and antibody concentrations in eggs between city and forest populations of European blackbirds (Turdus merula), a widely distributed species for which previous research demonstrated differences in behavioral and physiological traits. We measured egg and yolk mass, yolk concentrations of androgens (androstenedione [A4], testosterone [T], 5α-dihydrotestosterone [5α-DHT], and immunoglobulins [IgY]) and related them to population, clutch size, laying order, embryo sex, and progress of breeding season. We show (a) earlier onset of laying in the city than forest population, but similar egg and clutch size; (b) higher overall yolk androgen concentrations in the forest than the city population (sex-dependent for T); (c) greater among-female variation of yolk T and 5α-DHT concentrations in the forest than city population, but similar within-clutch variation; (d) similar IgY concentrations with a seasonal decline in both populations; and (e) population-specific positive (city) or negative (forest) association of yolk A4 and T with IgY concentrations. Our results are consistent with the hypotheses that hormone-mediated maternal effects contribute to differences in behavioral and physiological traits between city and forest individuals and that yolk androgen and immunoglobulin levels can exhibit population-specific relationships rather than trade-off against each other.

Independent colonization of multiple urban centres by a formerly forest specialist bird species.

Urban areas are expanding rapidly, but a few native species have successfully colonized them. The processes underlying such colonization events are poorly understood. Using the blackbird Turdus merula, a former forest specialist that is now one of the most common urban birds in its range, we provide the first assessment of two contrasting urban colonization models. First, that urbanization occurred independently. Second, that following initial urbanization, urban-adapted individuals colonized other urban areas in a leapfrog manner. Previous analyses of spatial patterns in the timing of blackbird urbanization, and experimental introductions of urban and rural blackbirds to uncolonized cities, suggest that the leapfrog model is likely to apply. We found that, across the western Palaearctic, urban blackbird populations contain less genetic diversity than rural ones, urban populations are more strongly differentiated from each other than from rural populations and assignment tests support a rural source population for most urban individuals. In combination, these results provide much stronger support for the independent urbanization model than the leapfrog one. If the former model predominates, colonization of multiple urban centres will be particularly difficult when urbanization requires genetic adaptations, having implications for urban species diversity.

Increased sedentariness in European Blackbirds following urbanization: a consequence of local adaptation?

Urbanization changes local environmental conditions and may lead to altered selection regimes for life history traits of organisms thriving in cities. Previous studies have reported changes in breeding phenology and even trends toward increased sedentariness in migratory bird species colonizing urban areas. However, does the change in migratory propensity simply represent a phenotypic adjustment to local urban environment, or is it genetically based and hence the result of local adaptation? To test this, we hand-raised European Blackbirds (Turdus merula) from urban and forest populations, quantified their nocturnal activity and fat deposition covering two complete migratory cycles and examined the consequences of a reduced migratory propensity for the timing of gonadal development (a physiological measure of the seasonal timing of reproduction). Although nocturnal activities differed strikingly between fall and spring seasons, with low activities during the fall and high activities during the spring seasons, our data confirm, even in birds kept from early life under common-garden conditions, a change toward reduced migratoriness in urban blackbirds. The first score of a principal component analysis including amount of nocturnal activity and fat deposition, defined as migratory disposition, was lower in urban than in forest males particularly during their first year, whereas females did not differ. The results suggest that the intrinsic but male-biased difference is genetically determined, although early developmental effects cannot be excluded. Moreover, individuals with low migratory disposition developed their gonads earlier, resulting in longer reproductive seasons. Since urban conditions facilitate earlier breeding, intrinsic shifts to sedentariness thus seem to be adaptive in urban habitats. These results corroborate the idea that urbanization has evolutionary consequences for life history traits such as migratory behavior.

Migration confers winter survival benefits in a partially migratory songbird.

To evolve and to be maintained, seasonal migration, despite its risks, has to yield fitness benefits compared with year-round residency. Empirical data supporting this prediction have remained elusive in the bird literature. To test fitness related benefits of migration, we studied a partial migratory population of European blackbirds (Turdus merula) over 7 years. Using a combination of capture-mark-recapture and radio telemetry, we compared survival probabilities between migrants and residents estimated by multi-event survival models, showing that migrant blackbirds had 16% higher probability to survive the winter compared to residents. A subsequent modelling exercise revealed that residents should have 61.25% higher breeding success than migrants, to outweigh the survival costs of residency. Our results support theoretical models that migration should confer survival benefits to evolve, and thus provide empirical evidence to understand the evolution and maintenance of migration.

Stress and the city: urbanization and its effects on the stress physiology in European blackbirds.

Animals colonizing cities are exposed to many novel and potentially stressful situations. There is evidence that chronic stress can cause deleterious effects. Hence, wild animals would suffer from city life unless they adjusted their stress response to the conditions in a city. Here we show that European Blackbirds born in a city have a lower stress response than their forest conspecifics. We hand-raised urban and forest-living individuals of that species under identical conditions and tested their corticosterone stress response at an age of 5, 8, and 11 months. The results suggest that the difference is genetically determined, although early developmental effects cannot be excluded. Either way, the results support the idea that urbanization creates a shift in coping styles by changing the stress physiology of animals. The reduced stress response could be ubiquitous and, presumably, necessary for all animals that thrive in ecosystems exposed to frequent anthropogenic disturbances, such as those in urban areas.