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.

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.

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.

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.

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.

Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity.

Once-abundant aerial insectivores, such as the Tree Swallow (Tachycineta bicolor), have declined steadily in the past several decades, making it imperative to understand all aspects of their ecology. Aerial insectivores forage on a mixture of aquatic and terrestrial insects that differ in fatty acid composition, specifically long-chain omega-3 polyunsaturated fatty acid (LCPUFA) content. Aquatic insects contain high levels of both LCPUFA and their precursor omega-3 PUFA, alpha-linolenic acid (ALA), whereas terrestrial insects contain much lower levels of both. We manipulated both the quantity and quality of food for Tree Swallow chicks in a full factorial design. Diets were either high-LCPUFA or low in LCPUFA but high in ALA, allowing us to separate the effects of direct LCPUFA in diet from the ability of Tree Swallows to convert their precursor, ALA, into LCPUFA. We found that fatty acid composition was more important for Tree Swallow chick performance than food quantity. On high-LCPUFA diets, chicks grew faster, were in better condition, and had greater immunocompetence and lower basal metabolic rates compared with chicks on both low LCPUFA diets. Increasing the quantity of high-LCPUFA diets resulted in improvements to all metrics of performance while increasing the quantity of low-LCPUFA diets only resulted in greater immunocompetence and lower metabolic rates. Chicks preferentially retained LCPUFA in brain and muscle when both food quantity and LCPUFA were limited. Our work suggests that fatty acid composition is an important dimension of aerial insectivore nutritional ecology and reinforces the importance of high-quality aquatic habitat for these declining birds.

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.

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.

Integrated population models reveal local weather conditions are the key drivers of population dynamics in an aerial insectivore.

Changes to weather patterns under a warming climate are complex: while warmer temperatures are expected virtually worldwide, decreased mean precipitation is expected at mid-latitudes. Migratory birds depend on broad-scale weather patterns to inform timing of movements, but may be more susceptible to local weather patterns during sedentary periods. We constructed Bayesian integrated population models (IPMs) to assess whether continental or local weather effects best explained population dynamics in an environmentally sensitive aerial insectivorous bird, the tree swallow (Tachycineta bicolor), along a transcontinental gradient from British Columbia to Saskatchewan to New York, and tested whether population dynamics were synchronous among sites. Little consistency existed among sites in the demographic rates most affecting population growth rate or in correlations among rates. Juvenile apparent survival at all sites was stable over time and greatest in New York, whereas adult apparent survival was more variable among years and sites, and greatest in British Columbia and Saskatchewan. Fledging success was greatest in Saskatchewan. Local weather conditions explained significant variation in adult survival in Saskatchewan and fledging success in New York, corroborating the hypothesis that local more than continental weather drives the population dynamics of this species and, therefore, demographic synchrony measured at three sites was limited. Nonetheless, multi-population IPMs can be a powerful tool for identifying correlated population trajectories caused by synchronous demographic rates, and can pinpoint the scale at which environmental drivers are responsible for changes. We caution against applying uniform conservation actions for populations where synchrony does not occur or is not fully understood.

Understanding spatial distributions: negative density-dependence in prey causes predators to trade-off prey quantity with quality.

Negative density-dependence is generally studied within a single trophic level, thereby neglecting its effect on higher trophic levels. The 'functional response' couples a predator's intake rate to prey density. Most widespread is a type II functional response, where intake rate increases asymptotically with prey density; this predicts the highest predator densities at the highest prey densities. In one of the most stringent tests of this generality to date, we measured density and quality of bivalve prey (edible cockles Cerastoderma edule) across 50 km² of mudflat, and simultaneously, with a novel time-of-arrival methodology, tracked their avian predators (red knots Calidris canutus). Because of negative density-dependence in the individual quality of cockles, the predicted energy intake rates of red knots declined at high prey densities (a type IV, rather than a type II functional response). Resource-selection modelling revealed that red knots indeed selected areas of intermediate cockle densities where energy intake rates were maximized given their phenotype-specific digestive constraints (as indicated by gizzard mass). Because negative density-dependence is common, we question the current consensus and suggest that predators commonly maximize their energy intake rates at intermediate prey densities. Prey density alone may thus poorly predict intake rates, carrying capacity and spatial distributions of predators.

Optimizing identification of clinically relevant Gram-positive organisms by use of the Bruker Biotyper matrix-assisted laser desorption ionization-time of flight mass spectrometry system.

Matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) can be used as a method for the rapid identification of microorganisms. This study evaluated the Bruker Biotyper (MALDI-TOF MS) system for the identification of clinically relevant Gram-positive organisms. We tested 239 aerobic Gram-positive organisms isolated from clinical specimens. We evaluated 4 direct-smear methods, including "heavy" (H) and "light" (L) smears, with and without a 1-µl direct formic acid (FA) overlay. The quality measure assigned to a MALDI-TOF MS identification is a numerical value or "score." We found that a heavy smear with a formic acid overlay (H+FA) produced optimal MALDI-TOF MS identification scores and the highest percentage of correctly identified organisms. Using a score of ≥2.0, we identified 183 of the 239 isolates (76.6%) to the genus level, and of the 181 isolates resolved to the species level, 141 isolates (77.9%) were correctly identified. To maximize the number of correct identifications while minimizing misidentifications, the data were analyzed using a score of ≥1.7 for genus- and species-level identification. Using this score, 220 of the 239 isolates (92.1%) were identified to the genus level, and of the 181 isolates resolved to the species level, 167 isolates (92.2%) could be assigned an accurate species identification. We also evaluated a subset of isolates for preanalytic factors that might influence MALDI-TOF MS identification. Frequent subcultures increased the number of unidentified isolates. Incubation temperatures and subcultures of the media did not alter the rate of identification. These data define the ideal bacterial preparation, identification score, and medium conditions for optimal identification of Gram-positive bacteria by use of MALDI-TOF MS.

Temperature effects on food supply and chick mortality in tree swallows (Tachycineta bicolor).

Tree swallow (Tachycineta bicolor) breeding success in Ithaca, NY, USA, over the past quarter century has shown generally healthy fledgling production punctuated by years of high nestling mortality. This study tested the potential effects that temperature may have on the food supply and breeding success of swallows. Data from 17 years of daily insect samples were used to relate flying insect abundances to daily maximum temperatures and to define "cold snaps" as strings of consecutive days when the maximum temperatures did not exceed critical temperatures. The distributions of cold snaps and chick mortality events were investigated both through detailed reconstructions of the fates and fate dates of individual chicks, focused on the three breeding seasons of lowest fledging success, and with less detailed brood-level analyses of a larger 11-year dataset including years of more moderate mortality. Mark-recapture analyses of daily brood survival rate (DSR) reveal very strong support for the effects of cold temperatures on brood survival rates, and all the top models agree on a critical temperature of 18.5 °C for insect flight activity in Ithaca. The individual-level analyses, focused on years of higher mortality, favored a 3-day cold snap definition as the most predictive of DSR effects, whereas the larger-scale brood-level analyses revealed 1- and 2-day cold snaps as having the most significant effects on DSR. Regardless, all analyses reveal that, in an age of generally warmer climates, the largest effect of weather on swallow fledgling production is from cold temperatures.

Ancestry and evolution of seasonal migration in the Parulidae.

Seasonal migration in birds is known to be highly labile and subject to rapid change in response to selection, such that researchers have hypothesized that phylogenetic relationships should neither predict nor constrain the migratory behaviour of a species. Many theories on the evolution of bird migration assume a framework that extant migratory species have evolved repeatedly and relatively recently from sedentary tropical or subtropical ancestors. We performed ancestral state reconstructions of migratory behaviour using a comprehensive, well-supported phylogeny of the Parulidae (the 'wood-warblers'), a large family of Neotropical and Nearctic migratory and sedentary songbirds, and examined the rates of gain and loss of migration throughout the Parulidae. Counter to traditional hypotheses, our results suggest that the ancestral wood-warbler was migratory and that losses of migration have been at least as prevalent as gains throughout the history of Parulidae. Therefore, extant sedentary tropical radiations in the Parulidae represent losses of latitudinal migration and colonization of the tropics from temperate regions. We also tested for phylogenetic signal in migratory behaviour, and our results indicate that although migratory behaviour is variable within some wood-warbler species and clades, phylogeny significantly predicts the migratory distance of species in the Parulidae.

Phylogeny of the Tachycineta genus of New World swallows: insights from complete mitochondrial genomes.

The Tachycineta genus of swallows is comprised of nine species that range from Alaska to southern Chile. We sequenced the entire mitochondrial genome of each member of Tachycineta and generated a completely resolved phylogenetic hypothesis for the corresponding mitochondrial gene tree. Our analyses confirm the presence of two sub-clades within Tachycineta that are associated with geography: a North American/Caribbean clade and a South/Central American clade. We found considerable variation among regions of the mitochondrial genome in both substitution rates and the level of information that each region supplied for phylogenetic reconstruction. We found no evidence of positive directional selection within mitochondrial coding regions, but we identified numerous sites under purifying selection. This finding suggests that, despite differences in life history traits and distributions, mitochondrial genes in Tachycineta are predominantly under purifying selection for conserved function.

Species trees for the tree swallows (Genus Tachycineta): an alternative phylogenetic hypothesis to the mitochondrial gene tree.

The New World swallow genus Tachycineta comprises nine species that collectively have a wide geographic distribution and remarkable variation both within- and among-species in ecologically important traits. Existing phylogenetic hypotheses for Tachycineta are based on mitochondrial DNA sequences, thus they provide estimates of a single gene tree. In this study we sequenced multiple individuals from each species at 16 nuclear intron loci. We used gene concatenated approaches (Bayesian and maximum likelihood) as well as coalescent-based species tree inference to reconstruct phylogenetic relationships of the genus. We examined the concordance and conflict between the nuclear and mitochondrial trees and between concatenated and coalescent-based inferences. Our results provide an alternative phylogenetic hypothesis to the existing mitochondrial DNA estimate of phylogeny. This new hypothesis provides a more accurate framework in which to explore trait evolution and examine the evolution of the mitochondrial genome in this group.

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.

A test of the mismatch hypothesis: How is timing of reproduction related to food abundance in an aerial insectivore?

In seasonal environments, vertebrates are generally thought to time their reproduction so offspring are raised during the peak of food abundance. The mismatch hypothesis predicts that reproductive success is maximized when animals synchronize their reproduction with the food supply. Understanding the mechanisms influencing the timing of reproduction has taken on new urgency as climate change is altering environmental conditions during reproduction, and there is concern that species will not be able to synchronize their reproduction with changing food supplies. Using data from five sites over 24 years (37 site-years), we tested the assumptions of the mismatch hypothesis in the Tree Swallow (Tachycineta bicolor), a widespread aerial insectivore, whose timing of egg-laying has shifted earlier by nine days since the 1950s. Contrary to the mismatch hypothesis, the start of egg-laying was strongly related to food abundance (flying insect biomass) during the laying period and not to timing of the seasonal peak in food supply. In fact, food abundance generally continued to increase throughout the breeding season, and there was no evidence of selection based on the mistiming of laying with the seasonal peak of food abundance. In contrast, there was selection for laying earlier, because birds that lay earlier generally have larger clutches and fledge more young. Overall, initial reproductive decisions in this insectivore appear to be based on the food supply during egg formation and not the nestling period. Thus, the mismatch hypothesis may not apply in environments with relatively constant or abundant food throughout the breeding season. Although climate change is often associated with earlier reproduction, our results caution that it is not necessarily driven by selection for synchronized reproduction.