A hard fruit to swallow.

Foraging niches become more specialized toward bird range limits.

The effects of humidity on thermoregulatory physiology of a small songbird.

Scholander-Irving curves describe the relationship between ambient temperature and metabolic rate and are fundamental to understanding the energetic demands of homeothermy. However, Scholander-Irving curves are typically measured in dry air, which is not representative of the humidity many organisms experience in nature. Consequently, it is unclear (1) whether Scholander-Irving curves (especially below thermoneutrality) are altered by humidity, given the effects of humidity on thermal properties of air, and (2) whether physiological responses associated with Scholander-Irving curves in the lab reflect organismal performance in humid field conditions. We used laboratory experiments and biophysical models to test the effects of humidity on the thermoregulatory physiology of tree swallows (Tachycineta bicolor). We also tested whether physiological responses measured under lab conditions were correlated with field body temperatures and nestling provisioning rates. We found that humidity reduced rates of evaporative water loss but did not have large effects on body temperature or metabolic rate, suggesting that swallows can decouple evaporative cooling, body temperature and metabolic rate. Although the effect of humidity on metabolic rate in the lab was small, our biophysical models indicated that energetic costs of thermoregulation were ∼8% greater in simulations that used metabolic rates from birds in humid compared with dry conditions. Finally, we found mixed evidence that physiological responses measured in the lab under humid or dry conditions were associated with body temperature and nest provisioning rates in the field. Our results help clarify the effect of humidity on endotherm thermoregulation, which may help forecast organismal responses to environmental change.

Developmental stage-dependent effects of perceived predation risk on nestling tree swallows (Tachycineta bicolor).

The risk of predation directly affects the physiology, behavior, and fitness of wild birds. Strong social connections with conspecifics could help individuals recover from a stressful experience such as a predation event; however, competitive interactions also have the potential to exacerbate stress. Few studies have investigated the interaction between environmental stressors and the social landscape in wild bird populations. In 2 years of field studies, we experimentally simulated predation attempts on breeding female tree swallows (Tachicyneta bicolor). At the same time, we manipulated female breast plumage color, a key social signal. Simulated predation events on tree swallows early in the nestling period reduced young nestlings' mass by approximately 20% and shortened telomere lengths. Ultimately, only 31% of nestlings in the predation group fledged compared with 70% of control nestlings. However, the effects of experimental manipulations were timing dependent: the following year when we swapped the order of the experimental manipulations and simulated predation during incubation, there were no significant effects of predation on nestling condition or fledging success. Contrary to our expectations, manipulation of the social environment did not affect the response of tree swallows to simulated predation. However, manipulating female plumage during the nestling period did reduce nestling skeletal size and mass, although the effects depended on original plumage brightness. Our data demonstrate that transient stressors on female birds can have carry-over effects on their nestlings if they occur during critical periods in the breeding season.

Experimentally elevated corticosterone does not affect bacteria killing ability of breeding female tree swallows (Tachycineta bicolor).

The immune system can be modulated when organisms are exposed to acute or chronic stressors. Glucocorticoids (GCs), the primary hormonal mediators of the physiological stress response, are suspected to play a crucial role in immune modulation. However, most evidence of stress-associated immunomodulation does not separate the effects of glucocorticoid-dependent pathways from those of glucocorticoid-independent mechanisms on immune function. In this study, we experimentally elevated circulating corticosterone, the main avian glucocorticoid, in free-living female tree swallows (Tachycineta bicolor) for one to two weeks to test its effects on immune modulation. Natural variation in bacteria killing ability (BKA), a measure of innate constitutive immunity, was predicted by the interaction between timing of breeding and corticosterone levels. However, experimental elevation of corticosterone had no effect on BKA. Therefore, even when BKA is correlated with natural variation in glucocorticoid levels, this relationship may not be causal. Experiments are necessary to uncover the causal mechanisms of immunomodulation and the consequences of acute and chronic stress on disease vulnerability. Findings in other species indicate that acute increases in GCs can suppress BKA; but our results support the hypothesis that this effect does not persist over longer timescales, during chronic elevations in GCs. Direct comparisons of the effects of acute vs. chronic elevation of GCs on BKA will be important for testing this hypothesis.

Social signal manipulation and environmental challenges have independent effects on physiology, internal microbiome, and reproductive performance in tree swallows (Tachycineta bicolor).

The social environment that individuals experience appears to be a particularly salient mediator of stress resilience, as the nature and valence of social interactions are often related to subsequent health, physiology, microbiota, and overall stress resilience. Relatively few studies have simultaneously manipulated the social environment and ecological challenges under natural conditions. Here, we report the results of experiments in wild tree swallows (Tachycineta bicolor) in which we manipulated both ecological challenges (predator encounters and flight efficiency reduction) and social interactions (by experimental dulling of a social signal). In two experiments conducted in separate years, we reversed the order of these treatments so that females experienced either an altered social signal followed by a challenge or vice-versa. Before, during, and after treatments were applied, we tracked breeding success, morphology and physiology (mass, corticosterone, and glucose), nest box visits via an RFID sensor network, cloacal microbiome diversity, and fledging success. Overall, we found that predator exposure during the nestling period reduced the likelihood of fledging and that signal manipulation sometimes altered nest box visitation patterns, but little evidence that the two categories of treatment interacted with each other. We discuss the implications of our results for understanding what types of challenges and what conditions are most likely to result in interactions between the social environment and ecological challenges.

Females with Increased Costs Maintain Reproductive Output: A Field Experiment in a Common Songbird.

Reproduction and self-maintenance are energetically costly activities involved in classic life history trade-offs. However, few studies have measured the responses of wild organisms to simultaneous changes in reproductive and self-maintenance costs, which may have interactive effects. In free-living female Barn Swallows (Hirundo rustica), we simultaneously manipulated reproductive costs (by adding or removing two nestlings) and self-maintenance costs (by attaching a ∼1 g weight in the form of a GPS tag to half of our study birds) and measured mass, immune status, blood glucose, feather growth, and reproductive output (likelihood of a second clutch, number of eggs, and time between clutches). GPS tags allowed us to analyze how movement range size affected response to brood size manipulation. Tagging altered females' immune function as evidenced by an elevated heterophil to lymphocyte (H:L) ratio, but all females were equally likely to lay more eggs. There was no evidence of interactive effects of the tagging and brood size treatment. Range size was highly variable, and birds with large ranges grew feathers more slowly, but analyzing the effect of brood size manipulation while accounting for variation in range size did not result in any physiological response. Our results support the theoretical prediction that short-lived vertebrates do face a trade-off between reproduction and self-maintenance and, when faced with increased costs, tend to preserve investment in reproduction at the expense of parental condition. This experiment also helps us to understand how movement patterns may be relevant to life history trade-offs in wild birds.

Experimental manipulation of sexual traits in barn swallow populations-No evidence for divergent sexual selection.

Safran et al. (2016a) manipulated two sexual traits (ventral plumage coloration and tail streamer length) in male barn swallows (Hirundo rustica) and reported divergent effects on paternity change between two study populations, in Colorado and Israel. They concluded that geographical variation in the two phenotypic traits is maintained by divergent sexual selection. However, the response variable they used, the longitudinal change in paternity from a pre-treatment clutch to a post-treatment clutch, does not reflect an unbiased effect of the treatment. Here, I show that the magnitude of the change in paternity is influenced by variation in the initial paternity score among the treatment groups, which is presumably due to stochastic variation from low sample sizes in the treatment groups. When the bias was accounted for in re-analyses of the Israeli dataset, the statistical significance of one of two treatment effects disappeared. Similar re-analyses of the American population were not possible due to inaccessibility of raw data for individual clutches, but an assessment of the mean scores indicates that the two significant treatment effects in this population were similarly biased in their initial paternity scores. The conclusion of divergent sexual selection on male phenotypic traits between the two populations does not seem to be supported.

Timing of Breeding Reveals a Trade-Off between Immune Investment and Life History in Tree Swallows.

The allocation of limited resources among life history traits creates trade-offs that constrain the range of possible phenotypes of organisms. In animals, the cost of maintaining an effective immune response may reduce the ability to invest in reproduction, resulting in altered susceptibility to disease. However, not all members of a population face identical constraints because differences in an individual's environmental context or physiological state can influence the degree to which traits are negatively associated. Here, we evaluated how variation in timing of breeding, a correlate of fitness, may result in different patterns of trait associations between immunity and reproduction. We measured constitutive immunity in breeding female tree swallows (Tachycineta bicolor) using a bacteria killing assay with blood plasma to assess the relationships between bacteria killing ability (BKA), reproductive effort, and reproductive success. We found that timing of breeding can influence the association between BKA and reproductive effort, but its effects are not homogeneous among all traits. Late-breeding tree swallows with stronger BKA laid smaller clutches, a pattern that was not apparent in early breeders. Regardless of the timing of breeding, birds with stronger BKA fed their nestlings less. Despite a negative association with reproductive effort, we found no association between immunity and reproductive success. We provide evidence that individual tree swallows do not experience some trade-offs equally, and that timing of breeding likely plays a role in how costs of immunity are weighed. To understand how investment in immunity can limit life history traits, we must consider how a variation among individuals influences the relative costs of immunity.

Interacting effects of cold snaps, rain, and agriculture on the fledging success of a declining aerial insectivore.

Climate change predicts the increased frequency, duration, and intensity of inclement weather periods such as unseasonably low temperatures (i.e., cold snaps) and prolonged precipitation. Many migratory species have advanced the phenology of important life history stages and, as a result, are likely to be exposed to these periods of inclement spring weather more often, therefore risking reduced fitness and population growth. For declining avian species, including aerial insectivores, anthropogenic landscape changes such as agricultural intensification are another driver of population declines. These landscape changes may affect the foraging ability of food provisioning parents and reduce the survival of nestlings exposed to inclement weather through, for example, pesticide exposure impairing thermoregulation and punctual anorexia. Breeding in agro-intensive landscapes may therefore exacerbate the negative effects of inclement weather under climate change. We observed that a significant reduction in the availability of insect prey occurred when daily maximum temperatures fell below 18.3°C, and thereby defined any day when the maximum temperature fell below this value as a day witnessing a cold snap. We then combined daily information on the occurrence of cold snaps and measures of precipitation to assess their impact on the fledging success of Tree Swallows (Tachycineta bicolor) occupying a nest box system placed across a gradient of agricultural intensification. Estimated fledging success of this declining aerial insectivore was 36.2% lower for broods experiencing 4 cold-snap days during the 12 days post-hatching period versus broods experiencing none, and this relationship was worsened when facing more precipitation. We further found that the overall negative effects of a brood experiencing periods of inclement weather was exacerbated in more agro-intensive landscapes. Our results indicate that two of the primary hypothesized drivers of many avian population declines may interact to further increase the rate of declines in certain landscape contexts.

High turn-over rates at the upper range limit and elevational source-sink dynamics in a widespread songbird.

The formation of an upper distributional range limit for species breeding along mountain slopes is often based on environmental gradients resulting in changing demographic rates towards high elevations. However, we still lack an empirical understanding of how the interplay of demographic parameters forms the upper range limit in highly mobile species. Here, we study apparent survival and within-study area dispersal over a 700 m elevational gradient in barn swallows (Hirundo rustica) by using 15 years of capture-mark-recapture data. Annual apparent survival of adult breeding birds decreased while breeding dispersal probability of adult females, but not males increased towards the upper range limit. Individuals at high elevations dispersed to farms situated at elevations lower than would be expected by random dispersal. These results suggest higher turn-over rates of breeding individuals at high elevations, an elevational increase in immigration and thus, within-population source-sink dynamics between low and high elevations. The formation of the upper range limit therefore is based on preference for low-elevation breeding sites and immigration to high elevations. Thus, shifts of the upper range limit are not only affected by changes in the quality of high-elevation habitats but also by factors affecting the number of immigrants produced at low elevations.

Chronic noise exposure has context-dependent effects on stress physiology in nestling Tree Swallows (Tachycineta bicolor).

Anthropogenic noise is increasing in intensity and scope, resulting in changes to acoustic landscapes and largely negative effects on a range of species. In birds, noise can mask acoustic signals used in a variety of communication systems, including parent-offspring communication. As a result, nestling birds raised in noise may have challenges soliciting food from parents and avoiding detection by predators. Given that passerine nestlings are confined to a nest and therefore cannot escape these challenges, noise may also act as a chronic stressor during their development. Here, we raised Tree Swallow (Tachycineta bicolor) nestlings with or without continuous, white noise to test whether noise exposure affected baseline and stress-induced plasma, integrated feather corticosterone levels, and immune function. Stress physiology and immune function may also vary with the competitive environment during development, so we also examined whether noise effects varied with brood size and nestling mass. We found that overall, exposure to noise did not alter nestling stress physiology or immune function. However, light nestlings raised in noise exhibited lower baseline plasma and integrated feather corticosterone than heavy nestlings, suggesting alternative physiological responses to anthropogenic stimuli. Furthermore, light nestlings in larger broods had reduced PHA-induced immune responses compared to heavy nestlings, and PHA-induced immune responses were associated with higher levels of baseline plasma and feather CORT. Overall, our findings suggest that noise can alter the stress physiology of developing birds; however, these effects may depend on developmental conditions and the presence of other environmental stressors, such as competition for resources. Our findings may help to explain why populations are not uniformly affected by noise.

Climatic change and extinction risk of two globally threatened Ethiopian endemic bird species.

Climate change is having profound effects on the distributions of species globally. Trait-based assessments predict that specialist and range-restricted species are among those most likely to be at risk of extinction from such changes. Understanding individual species' responses to climate change is therefore critical for informing conservation planning. We use an established Species Distribution Modelling (SDM) protocol to describe the curious range-restriction of the globally threatened White-tailed Swallow (Hirundo megaensis) to a small area in southern Ethiopia. We find that, across a range of modelling approaches, the distribution of this species is well described by two climatic variables, maximum temperature and dry season precipitation. These same two variables have been previously found to limit the distribution of the unrelated but closely sympatric Ethiopian Bush-crow (Zavattariornis stresemanni). We project the future climatic suitability for both species under a range of climate scenarios and modelling approaches. Both species are at severe risk of extinction within the next half century, as the climate in 68-84% (for the swallow) and 90-100% (for the bush-crow) of their current ranges is predicted to become unsuitable. Intensive conservation measures, such as assisted migration and captive-breeding, may be the only options available to safeguard these two species. Their projected disappearance in the wild offers an opportunity to test the reliability of SDMs for predicting the fate of wild species. Monitoring future changes in the distribution and abundance of the bush-crow is particularly tractable because its nests are conspicuous and visible over large distances.

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.

Experimental competition induces immediate and lasting effects on the neurogenome in free-living female birds.

Periods of social instability can elicit adaptive phenotypic plasticity to promote success in future competition. However, the underlying molecular mechanisms have primarily been studied in captive and laboratory-reared animals, leaving uncertainty as to how natural competition among free-living animals affects gene activity. Here, we experimentally generated social competition among wild, cavity-nesting female birds (tree swallows, Tachycineta bicolor). After territorial settlement, we reduced the availability of key breeding resources (i.e., nest boxes), generating heightened competition; within 24 h we reversed the manipulation, causing aggressive interactions to subside. We sampled females during the peak of competition and 48 h after it ended, along with date-matched controls. We measured transcriptomic and epigenomic responses to competition in two socially relevant brain regions (hypothalamus and ventromedial telencephalon). Gene network analyses suggest that processes related to energy mobilization and aggression (e.g., dopamine synthesis) were up-regulated during competition, the latter of which persisted 2 d after competition had ended. Cellular maintenance processes were also down-regulated after competition. Competition additionally altered methylation patterns, particularly in pathways related to hormonal signaling, suggesting those genes were transcriptionally poised to respond to future competition. Thus, experimental competition among free-living animals shifts gene expression in ways that may facilitate the demands of competition at the expense of self-maintenance. Further, some of these effects persisted after competition ended, demonstrating the potential for epigenetic biological embedding of the social environment in ways that may prime individuals for success in future social instability.

Avian mud nest architecture by self-secreted saliva.

Mud nests built by swallows (Hirundinidae) and phoebes (Sayornis) are stable granular piles attached to cliffs, walls, or ceilings. Although these birds have been observed to mix saliva with incohesive mud granules, how such biopolymer solutions provide the nest with sufficient strength to support the weight of the residents as well as its own remains elusive. Here, we elucidate the mechanism of strong granular cohesion by the viscoelastic paste of bird saliva through a combination of theoretical analysis and experimental measurements in both natural and artificial nests. Our mathematical model considering the mechanics of mud nest construction allows us to explain the biological observation that all mud-nesting bird species should be lightweight.

The relative contribution of individual quality and changing climate as drivers of lifetime reproductive success in a short-lived avian species.

Animal populations are influenced strongly by fluctuations in weather conditions, but long-term fitness costs are rarely explored, especially in short-lived avian species. We evaluated the relative contributions of individual characteristics and environmental conditions to lifetime reproductive success (LRS) of female tree swallows (Tachycineta bicolor) from two populations breeding in contrasting environments and geographies, Saskatchewan and British Columbia, Canada. Female swallows achieved higher LRS by breeding early in the season and producing more fledglings. Other measures of female quality had virtually no influence on LRS. Genetic factors did not predict LRS, as there was no correlation between life-history components for sister pairs nor between mothers and their daughters. Instead, climate variability-indexed by spring pond density (i.e., abundance of wetland basins holding water) during years when females bred-had strong positive effects on female LRS in more arid Saskatchewan but only weak positive effects of moisture conditions were detected in wetter British Columbia. Overall, several life history trait correlates of LRS were similar between populations, but local environmental factors experienced by individuals while breeding produced large differences in LRS. Consequently, variable and extreme environmental conditions associated with changing climate are predicted to influence individual fitness of distinct populations within a species' range.

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.

Environmental unpredictability shapes glucocorticoid regulation across populations of tree swallows.

The ability to respond appropriately to challenges is an important contributor to fitness. Variation in the regulation of glucocorticoid hormones, which mediate the phenotypic response to challenges, can therefore influence the ability to persist in a given environment. We compared stress responsiveness in four populations of tree swallows (Tachycineta bicolor) breeding under different environmental conditions to evaluate support for different selective pressures in driving the evolution of glucocorticoid regulation. In accordance with the environmental unpredictability hypothesis, stronger stress responses were seen in more unpredictable environments. Contrary to the reproductive value hypothesis, the stress response was not lower in populations engaging in more valuable reproductive attempts. Populations with stronger stress responses also had stronger negative feedback, which supports a "mitigating" rather than a "magnifying" effect of negative feedback on stress responses. These results suggest that combining a robust stress response with strong negative feedback may be important for persisting in unpredictable or rapidly changing environments.

Divergent sexual signals reflect costs of local parasites.

Many closely related populations are distinguished by variation in sexual signals and this variation is hypothesized to play an important role in reproductive isolation and speciation. Within populations, there is considerable evidence that sexual signals provide information about the incidence and severity of parasite infections, but it remains unclear if variation in parasite communities across space could play a role in initiating or maintaining sexual trait divergence. To test for variation in parasite-associated selection, we compared three barn swallow subspecies with divergent sexual signals. We found that parasite community structure and host tolerance to ecologically similar parasites varied between subspecies. Across subspecies we also found that different parasites were costly in terms of male survival and reproductive success. For each subspecies, the preferred sexual signal(s) were associated with the most costly local parasite(s), indicating that divergent signals are providing relevant information to females about local parasite communities. Across subspecies, the same traits were often associated with different parasites, indicating that parasite-sexual signal links are quite flexible and may evolve relatively quickly. This study provides evidence for (1) variation in parasite communities and (2) different parasite-sexual signal links among three closely related subspecies with divergent sexual signal traits, suggesting that parasites may play an important role in initiating and/or maintaining the divergence of sexual signals among these closely related, yet geographically isolated populations.

Do swallows (Hirundo daurica) use the visual cue of hatchling down-feathers to discriminate parasite alien nestlings?

Egg recognition is a variable but common anti-parasitism defense among different species of birds with brood parasites. In contrast, nestling recognition is rare. Very few studies have found nestling recognition in brood parasite hosts and determined the rejection mechanism behind this behavior. Hosts may use the number of hatchling down-feathers to reject parasite nestlings. We tested whether hatchling down-feathers is a visual cue for the red-rumped swallow, a host that can recognize and reject parasite nestlings. Our results indicated that red-rumped swallows do not recognize foreign nestlings based on hatchling down-feathers. The closed nest structure and hatchling morph may explain the absence of such a mechanism. None of the rejection mechanisms found in previous studies could explain the nestling recognition in swallows. Olfactory cues, tactile cues, or other visual cues, except for single nestling or hatchling down-feathers, may provide nestling recognition in red-rumped swallows. More study is needed to evaluate these possibilities.