Across the deserts and sea: inter-individual variation in migration routes of south-central European barn swallows (Hirundo rustica).

BACKGROUND: The spatiotemporal organization of migratory routes of long-distance migrants results from trade-offs between minimizing the journey length and en route risk of migration-related mortality, which may be reduced by avoiding crossing inhospitable ecological barriers. Despite flourishing avian migration research in recent decades, little is still known about inter-individual variability in migratory routes, as well as the carry-over effects of spatial and temporal features of migration on subsequent migration stages. METHODS: We reconstructed post- and pre-breeding migration routes, barrier crossing behaviour and non-breeding movements of the largest sample (N = 85) analysed to date of individual barn swallows breeding in south-central Europe, which were tracked using light-level geolocators. RESULTS: Most birds spent their non-breeding period in the Congo basin in a single stationary area, but a small fraction of itinerant individuals reaching South Africa was also observed. Birds generally followed a 'clockwise loop migration pattern', moving through the central Mediterranean and the Sahara Desert during post-breeding (north to south) migration yet switching to a more western route, along the Atlantic coast of Africa, Iberia and western Mediterranean during the pre-breeding (south to north) migration. Southward migration was straighter and less variable, while northward migration was significantly faster despite the broader detour along the Atlantic coast and Iberia. These patterns showed limited sex-related variability. The timing of different circannual events was tightly linked with previous migration stages, considerably affecting migration route and speed of subsequent movements. Indeed, individuals departing late from Africa performed straighter and faster pre-breeding migrations, partly compensating for the initial departure delays, but likely at the cost of performing riskier movements across ecological barriers. CONCLUSIONS: Different spatiotemporal migration strategies during post- and pre-breeding migration suggest that conditions en route may differ seasonally and allow for more efficient travelling along different migration corridors in either season. While highlighting patterns of inter-individual variability, our results support increasing evidence for widespread loop migration patterns among Afro-Palearctic avian migrants. Also, they suggest that carry-over effects acting across different phases of the annual cycle of migratory species can have major impacts on evolutionary processes.

Climate change shifts the timing of nutritional flux from aquatic insects.

Climate change can decouple resource supply from consumer demand, with the potential to create phenological mismatches driving negative consequences on fitness. However, the underlying ecological mechanisms of phenological mismatches between consumers and their resources have not been fully explored. Here, we use long-term records of aquatic and terrestrial insect biomass and egg-hatching times of several co-occurring insectivorous species to investigate temporal mismatches between the availability of and demand for nutrients that are essential for offspring development. We found that insects with aquatic larvae reach peak biomass earlier in the season than those with terrestrial larvae and that the relative availability of omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFAs) to consumers is almost entirely dependent on the phenology of aquatic insect emergence. This is due to the 4- to 34-fold greater n-3 LCPUFA concentration difference in insects emerging from aquatic as opposed to terrestrial habitats. From a long-sampled site (25 years) undergoing minimal land use conversion, we found that both aquatic and terrestrial insect phenologies have advanced substantially faster than those of insectivorous birds, shifting the timing of peak availability of n-3 LCPUFAs for birds during reproduction. For species that require n-3 LCPUFAs directly from diet, highly nutritious aquatic insects cannot simply be replaced by terrestrial insects, creating nutritional phenological mismatches. Our research findings reveal and highlight the increasing necessity of specifically investigating how nutritional phenology, rather than only overall resource availability, is changing for consumers in response to climate change.

Turbulence explains the accelerations of an eagle in natural flight.

Turbulent winds and gusts fluctuate on a wide range of timescales from milliseconds to minutes and longer, a range that overlaps the timescales of avian flight behavior, yet the importance of turbulence to avian behavior is unclear. By combining wind speed data with the measured accelerations of a golden eagle (Aquila chrysaetos) flying in the wild, we find evidence in favor of a linear relationship between the eagle's accelerations and atmospheric turbulence for timescales between about 1/2 and 10 s. These timescales are comparable to those of typical eagle behaviors, corresponding to between about 1 and 25 wingbeats, and to those of turbulent gusts both larger than the eagle's wingspan and smaller than large-scale atmospheric phenomena such as convection cells. The eagle's accelerations exhibit power spectra and intermittent activity characteristic of turbulence and increase in proportion to the turbulence intensity. Intermittency results in accelerations that are occasionally several times stronger than gravity, which the eagle works against to stay aloft. These imprints of turbulence on the bird's movements need to be further explored to understand the energetics of birds and other volant life-forms, to improve our own methods of flying through ceaselessly turbulent environments, and to engage airborne wildlife as distributed probes of the changing conditions in the atmosphere.

Rapid adjustments of migration and life history in hemisphere-switching cliff swallows.

Many aspects of bird migration are necessarily innate.1 However, the extent of deterministic genetic control, environmental influence, and individual decision making in the control of migration remains unclear.2-8 Globally, few cases of rapid and dramatic life-history changes resulting in novel migration strategies are known. An example is latitudinal trans-hemispheric breeding colonization, whereby a subpopulation suddenly begins breeding on its non-breeding range.9-13 These life-history reversals demand concomitant changes in the timing of migration, feather molt, and breeding if the population is to remain viable.13 Cliff swallows, Petrochelidon pyrrhonota, are long-distance migrants that breed in North America and spend the non-breeding season mostly in South America.14 However, in 2015, a small population switched hemispheres by breeding successfully in Argentina,9 over 8,000 km from the nearest potential source, after presumably failed attempts.15,16 This provided a unique chance to characterize the early mechanisms of change in migratory behavior and phenology and to assess the possibility of double breeding. We tracked cliff swallows with geolocators following their second and fourth breeding seasons in Argentina, documenting inverted seasonality, three new migratory patterns and non-breeding areas (North America, Mesoamerica, and South America), and a shift of molt phenology by approximately 6 months, all possibly arising within a single generation. These birds did not practice migratory double breeding, although some spent the boreal summer in the traditional breeding range. Our data show that fundamental phenological changes occurred very rapidly during colonization and that phenotypic plasticity can underlie profound changes in the life histories of migratory birds.

Birds advancing lay dates with warming springs face greater risk of chick mortality.

In response to a warming planet with earlier springs, migratory animals are adjusting the timing of essential life stages. Although these adjustments may be essential for keeping pace with resource phenology, they may prove insufficient, as evidenced by population declines in many species. However, even when species can match the tempo of climate change, other consequences may emerge when exposed to novel conditions earlier in the year. Here, using three long-term datasets on bird reproduction, daily insect availability, and weather, we investigated the complex mechanisms affecting reproductive success in an aerial insectivore, the tree swallow (Tachycineta bicolor). By examining breeding records over nearly half a century, we discovered that tree swallows have continuously advanced their egg laying by ∼3 d per decade. However, earlier-hatching offspring are now exposed to inclement weather events twice as often as they were in the 1970s. Our long-term daily insect biomass dataset shows no long-term trends over 25 y but precipitous drops in flying insect numbers on days with low ambient temperatures. Insect availability has a considerable impact on chick survival: Even a single inclement weather event can reduce offspring survival by >50%. Our results highlight the multifaceted threats that climate change poses on migrating species. The decoupling between cold snap occurrence and generally warming spring temperatures can affect reproductive success and threaten long-term persistence of populations. Understanding the exact mechanisms that endanger aerial insectivores is especially timely because this guild is experiencing the steepest and most widespread declines across North America and Europe.

Full lifetime perspectives on the costs and benefits of lay-date variation in tree swallows.

Animals must balance various costs and benefits when deciding when to breed. The costs and benefits of breeding at different times have received much attention, but most studies have been limited to investigating short-term season-to-season fitness effects. However, breeding early, versus late, in a season may influence lifetime fitness over many years, trading off in complex ways across the breeder's lifespan. In this study, we examined the complete life histories of 867 female tree swallows (Tachycineta bicolor) breeding in Ithaca, New York, between 2002 and 2016. Earlier breeders outperformed later breeders in short-term measures of reproductive output and offspring quality. Though there were weak indications that females paid long-term future survival costs for breeding early, lifetime fledgling output was markedly higher overall in early-breeding birds. Importantly, older females breeding later in the season did not experience compensating life history advantages that suggested an alternative equal-fitness breeding strategy. Rather, most or all of the swallows appear to be breeding as early as they can, and differences in lay dates appear to be determined primarily by differences in individual quality or condition. Lay date had a significant repeatability across breeding attempts by the same female, and the first lay date of females fledged in our population was strongly influenced by the first lay date of their mothers, indicating the potential for ongoing selection on lay date. By examining performance over the entire lifespan of a large number of individuals, we were able to clarify the relationship between timing of breeding and fitness and gain new insight into the sources of variability in this important life history trait.

Wandering woodpeckers: foray behavior in a social bird.

In many cooperatively breeding taxa, nonbreeding subordinates, or helpers, use extra-territorial forays to discover dispersal opportunities. Such forays are considered energetically costly and foraying birds face aggression from conspecific members of the territories they visit. In contrast, breeders in cooperatively breeding taxa are expected to foray seldomly. We used novel tracking technologies to follow 62 acorn woodpeckers (Melanerpes formicivorus), a cooperatively breeding bird, to study extra-territorial foray behavior. Both helpers and breeders engaged in extra-territorial forays routinely and often several times per day. Helpers forayed earlier in the day and invested more time when foraying to high-quality territories. Unexpectedly, breeders forayed as often and as far as helpers. Breeders from high-quality territories forayed closer to their home territories than breeders from low-quality territories, reflecting a potential trade-off between foraying and territory defense. Such a routine pattern of extra-territorial forays in both helpers and breeders suggests that the motives behind forays differ by sex and social status and involve more than simply searching for dispersal opportunities.

Developmental temperature predicts the adult response to stressors in a free-living passerine.

Early-life conditions can have substantial effects on the ways animals respond to stressors as adults. In particular, thermal conditions during development affect juveniles' responses to stressors, and there is evidence that these effects may extend into adulthood. However, these effects remain poorly understood, especially in free-living organisms. We test the prediction that ambient temperatures during laying, embryonic development and nestling development affect the hormonal mediators of the response to stressors in adults. To do so, we use a long-term dataset of tree swallows (Tachycineta bicolor) with records from both natal development and adult breeding. We found a strong, negative relationship between ambient temperature during early development (incubation) and an individual's corticosterone (CORT) response to stress later in life (while incubating her own young). Thermal conditions during other stages of natal development also showed a weak relationship with baseline CORT during provisioning. In a post hoc analysis, we found no evidence that ambient temperature during development differentially influenced the survival and recruitment of juveniles with different CORT phenotypes. Our results show that thermal conditions during development can have long-term effects on how individuals respond to stressors.

Differences in perceived predation risk associated with variation in relative size of extra-pair and within-pair offspring.

Extra-pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra-pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra-pair and within-pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer-winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer-winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra-pair and within-pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.

Temperate-Tropical Variation in Breeding Synchrony and Extra-Pair Paternity Among New World Tachycineta Swallows.

Extra-pair paternity rates vary markedly across avian taxa, but patterns of variation in this trait have been obscured by a paucity of data on closely related species, especially those spanning broad environmental gradients. Here we compare variation in extra-pair paternity rates among five species in the widespread swallow genus Tachycineta. Rates of extra-pair paternity vary widely in this group, ranging from 13 to 87% of nests having extra-pair young. The inter-specific variation in extra-pair paternity within this small group of closely related swallows has a range equivalent to that found among all Hirundinidae and is close to the range of variation across all birds. Despite theory that predicts extra-pair paternity rates to be explained by latitudinal variation in breeding synchrony our results show that extra-pair paternity rates in this genus do not closely track a latitudinal gradient, as predicted by studies of other life-history traits, and are not explained by differences in breeding synchrony as previously suggested. The genetic mating systems of birds, described by the rates of extra-pair paternity, are connected to all other life-history traits through a complex network of trade-offs with organismal (phylogenetic) and ecological (environmental) factors. Disentangling each of these interactions to understand latitudinal patterns in any given life-history trait remains a daunting task.

The environmental and genetic determinants of chick telomere length in Tree Swallows (Tachycineta bicolor).

Conditions during early life can have dramatic effects on adult characteristics and fitness. However, we still know little about the mechanisms that mediate these relationships. Telomere shortening is one possibility. Telomeres are long sequences of DNA that protect the ends of chromosomes. They shorten naturally throughout an individual's life, and individuals with short telomeres tend to have poorer health and reduced survival. Given this connection between telomere length (TL) and fitness, natural selection should favor individuals that are able to retain longer telomeres for a greater portion of their lives. However, the ability of natural selection to act on TL depends on the extent to which genetic and environmental factors influence TL. In this study, we experimentally enlarged broods of Tree Swallows (Tachycineta bicolor) to test the effects of demanding early-life conditions on TL, while simultaneously cross-fostering chicks to estimate heritable genetic influences on TL. In addition, we estimated the effects of parental age and chick sex on chick TL. We found that TL is highly heritable in Tree Swallow chicks, and that the maternal genetic basis for TL is stronger than is the paternal genetic basis. In contrast, the experimental manipulation of brood size had only a weak effect on chick TL, suggesting that the role of environmental factors in influencing TL early in life is limited. There was no effect of chick sex or parental age on chick TL. While these results are consistent with those reported in some studies, they are in conflict with others. These disparate conclusions might be attributable to the inherent complexity of telomere dynamics playing out differently in different populations or to study-specific variation in the age at which subjects were measured.

Reconstruction of long-distance bird migration routes using advanced machine learning techniques on geolocator data.

Geolocators are a well-established technology to reconstruct migration routes of animals that are too small to carry satellite tags (e.g. passerine birds). These devices record environmental light-level data that enable the reconstruction of daily positions from the time of twilight. However, all current methods for analysing geolocator data require manual pre-processing of raw records to eliminate twilight events showing unnatural variation in light levels, a step that is time-consuming and must be accomplished by a trained expert. Here, we propose and implement advanced machine learning techniques to automate this procedure and we apply them to 108 migration tracks of barn swallows ( Hirundo rustica). We show that routes reconstructed from the automated pre-processing are comparable to those obtained from manual selection accomplished by a human expert. This raises the possibility of fully automating light-level geolocator data analysis and possibly analysing the large amount of data already collected on several species.

A range-wide domino effect and resetting of the annual cycle in a migratory songbird.

Latitudinal differences in timing of breeding are well documented but how such differences carry over to influence timing of events in the annual cycle of migratory birds is not well understood. We examined geographical variation in timing of events throughout the year using light-level geolocator tracking data from 133 migratory tree swallows ( Tachycineta bicolor) originating from 12 North American breeding populations. A swallow's breeding latitude influenced timing of breeding, which then carried over to affect breeding ground departure. This resulted in subsequent effects on the arrival and departure schedules at autumn stopover locations and timing of arrival at non-breeding locations. This 'domino effect' between timing events was no longer apparent by the time individuals departed for spring migration. Our range-wide analysis demonstrates the lasting impact breeding latitude can have on migration schedules but also highlights how such timing relationships can reset when individuals reside at non-breeding sites for extended periods of time.

Brief Increases in Corticosterone Affect Morphology, Stress Responses, and Telomere Length but Not Postfledging Movements in a Wild Songbird.

Organisms are frequently exposed to challenges during development, such as poor weather and food shortage. Such challenges can initiate the hormonal stress response, which involves secretion of glucocorticoids. Although the hormonal stress response helps organisms deal with challenges, long-term exposure to high levels of glucocorticoids can have morphological, behavioral, and physiological consequences, especially during development. Glucocorticoids are also associated with telomere shortening, and they have a complex relationship with survival. To investigate whether brief, acute exposures to glucocorticoids can also produce these phenotypic effects in free-living birds, we exposed wild tree swallow (Tachycineta bicolor) nestlings to a brief exogenous dose of corticosterone once per day for 5 d and then measured their morphology, baseline and stress-induced corticosterone levels, and telomere length. We also deployed radio tags on a subset of nestlings, which allowed us to determine the age at which tagged nestlings left the nest (fledged) and their pattern of presence and absence at the natal site during the postbreeding period. Corticosterone-treated nestlings had lower mass, higher baseline and stress-induced corticosterone, and reduced telomeres; other metrics of morphology were affected weakly or not at all. Our treatment resulted in no significant effect on survival to fledging, fledge age, or age at first departure from the natal site, and we found no negative effect of corticosterone on interannual return rate. These results show that brief acute corticosterone exposure during development can have measurable effects on phenotype in free-living tree swallows. Corticosterone may therefore mediate correlations between rearing environment and phenotype in developing organisms, even in the absence of prolonged stressors.

Solar-powered radio tags reveal patterns of post-fledging site visitation in adult and juvenile Tree Swallows Tachycineta bicolor.

The availability of small, lightweight tracking devices enhances our ability to study birds during mobile phases of their lives. Tree Swallows Tachycineta bicolor, a model species of wild songbird, are well-studied during their breeding season; but our understanding of their biology at other times of the year, when they are not tied to the fixed location of a nest, is more limited. We developed a lightweight radio tag with no battery (solar nanotag) to study the movements of small animals, and we deployed it to explore the behavior of Tree Swallows after the end of their summer breeding season. We tagged 32 breeding adult swallows and 36 juveniles and monitored their presence and absence at the breeding site during the post-fledging period. Although our observations are based on very small sample sizes, the tags revealed previously unknown patterns in Tree Swallow behavior during the post-breeding season. Some Tree Swallow fledglings continued to visit the site repeatedly in the months following the nesting season, with the latest detection occurring on September 30th; by contrast, all adults had permanently departed by the end of July. These results inform future hypotheses about post-breeding movements in Tree Swallows. But, more generally, the detection of tagged swallows on their distant wintering grounds, seven months after tagging, indicates the potential of studying small passerine movements throughout their entire lifetimes, and suggests a rich array of applications for these "Life Tags" to study the movements of small animals world-wide.

Aquatic insects rich in omega-3 fatty acids drive breeding success in a widespread bird.

Ecologists studying bird foraging ecology have generally focused on food quantity over quality. Emerging work suggests that food quality, in terms of highly unsaturated omega-3 fatty acids (HUFA), can have equally important effects on performance. HUFA, which are present in aquatic primary producers, are all but absent in vascular plants, and HUFA content is also correspondingly higher in aquatic insects. Here, we show that Tree Swallow (Tachycineta bicolor) chicks rapidly accumulate HUFA from food during the nestling period. Using data sampled over 24 years, we also show that Tree Swallow breeding success is positively associated with the availability of HUFA-rich aquatic insects. Variation in aquatic insect biomass during chick development was a strong predictor of fledging success, whereas variation in terrestrial insects had little effect on fledging success. Our results highlight the potential for nutritional mismatches between insectivores and high-quality prey to affect avian reproductive performance.

The lingering impact of stress: brief acute glucocorticoid exposure has sustained, dose-dependent effects on reproduction.

Acutely stressful experiences can have profound and persistent effects on phenotype. Across taxa, individuals differ remarkably in their susceptibility to stress. However, the mechanistic causes of enduring stress effects, and of individual differences in stress susceptibility, are poorly understood. Here, we tested whether brief, acute increases in glucocorticoid hormones have persistent effects on phenotype, and whether effects differ according to the magnitude or duration of elevation. We used a novel method to non-invasively manipulate hormone levels on short time scales: the application of corticosterone gel to a model egg secured in the nest. Free-living female tree swallows (Tachycineta bicolor) exposed to several brief corticosterone increases during incubation showed dose-dependent differences in behaviour throughout the reproductive period. Birds receiving treatments that simulated higher or longer acute stress responses later provisioned larger broods at lower rates; the resulting offspring were smaller in size. Treatment did not influence female body condition, oxidative stress, reproductive success or inter-annual survival, but exposed females maintained higher baseline corticosterone after treatments ceased. Overall, these results indicate that brief, acute elevations in glucocorticoids in adulthood can have long-term consequences. Furthermore, individuals that mount a greater or longer acute stress response may be more likely to experience lingering effects of stress.

Inherent limits of light-level geolocation may lead to over-interpretation.

In their 2015 Current Biology paper, Streby et al.[1] reported that Golden-winged Warblers (Vermivora chrysoptera), which had just migrated to their breeding location in eastern Tennessee, performed a facultative and up to ">1,500 km roundtrip" to the Gulf of Mexico to avoid a severe tornadic storm. From light-level geolocator data, wherein geographical locations are estimated via the timing of sunrise and sunset, Streby et al.[1] concluded that the warblers had evacuated their breeding area approximately 24 hours before the storm and returned about five days later. The authors presented this finding as evidence that migratory birds avoid severe storms by temporarily moving long-distances. However, the tracking method employed by Streby et al.[1] is prone to considerable error and uncertainty. Here, we argue that this interpretation of the data oversteps the limits of the used tracking technique. By calculating the expected geographical error range for the tracked birds, we demonstrate that the hypothesized movements fell well within the geolocators' inherent error range for this species and that such deviations in latitude occur frequently even if individuals remain stationary.

The rate of telomere loss is related to maximum lifespan in birds.

Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

Conversion efficiency of α-linolenic acid to omega-3 highly unsaturated fatty acids in aerial insectivore chicks.

Food availability and quality are both critical for growing young animals. In nature, swallows (Tachycineta bicolor) and other aerial insectivores feed on both aquatic insects, which are rich in omega-3 highly unsaturated fatty acids (HUFAs), and terrestrial insects, which contain considerably lower amounts of omega-3 HUFAs. Carnivorous mammals and fishes must obtain omega-3 HUFAs from their diet, as they have lost the capacity to convert the precursor omega-3 α-linolenic acid (ALA) into omega-3 HUFAs. Thus, the relative value of aquatic versus terrestrial insects depends not only on the fatty acid composition of the prey but also on the capacity of consumers to convert ALA into omega-3 HUFAs. We used a combination of stable-isotope-labeled fatty acid tracers to ask whether, and how efficiently, tree swallows can deposit newly synthesized omega-3 HUFAs into tissue. Our data show for the first time that tree swallows can convert ALA into omega-3 HUFAs deposited in liver and skeletal muscle. However, high tree swallow demand for omega-3 HUFAs combined with low ALA availability in natural terrestrial foods may strain their modest conversion ability. This suggests that while tree swallows can synthesize omega-3 HUFAs de novo, omega-3 HUFAs are ecologically essential nutrients in natural systems. Our findings thus provide mechanistic support for our previous findings and the importance of omega-3 HUFA-rich aquatic insects for tree swallows and most likely other aerial insectivores with similar niches.