Novel insights into symbiont population structure: Globe-trotting avian feather mites contradict the specialist-generalist variation hypothesis.

Researchers often examine symbiont host specificity as a species-level pattern, but it can also be key to understanding processes occurring at the population level, which are not as well understood. The specialist-generalist variation hypothesis (SGVH) attempts to explain how host specificity influences population-level processes, stating that single-host symbionts (specialists) exhibit stronger population genetic structure than multi-host symbionts (generalists) because of fewer opportunities for dispersal and more restricted gene flow between populations. However, this hypothesis has not been tested in systems with highly mobile hosts, in which population connectivity may vary temporally and spatially. To address this gap, we tested the SGVH on proctophyllodid feather mites found on migratory warblers (family Parulidae) with contrasting host specificities, Amerodectes protonotaria (a host specialist of Protonotaria citrea) and A. ischyros (a host generalist of 17 parulid species). We used a pooled-sequencing approach and a novel workflow to analyse genetic variants obtained from whole genome data. Both mite species exhibited fairly weak population structure overall, and contrary to predictions of the SGVH, the generalist was more strongly structured than the specialist. These results may suggest that specialists disperse more freely among conspecifics, whereas generalists sort according to geography. Furthermore, our results may reflect an unexpected period for mite transmission - during the nonbreeding season of migratory hosts - as mite population structure more closely reflects the distributions of hosts during the nonbreeding season. Our findings alter our current understanding of feather mite biology and highlight the potential for studies to explore factors driving symbiont diversification at multiple evolutionary scales.

Evolution of moult-migration is directly linked to aridity of the breeding grounds in North American passerines.

To avoid energy allocation conflicts, birds generally separate breeding, migration and moult during the annual cycle. North American passerines typically moult on the breeding grounds prior to autumn migration. However, some have evolved a moult-migration strategy in which they delay moult until stopping over during autumn migration. Rohwer et al. (2005) proposed the 'push-pull hypothesis' as an explanation for the evolution of this moult strategy, but it has not been empirically tested. Poor conditions on the breeding grounds at the end of the summer would push birds to depart prior to moult, while productive stopover locations would pull them. We tested for a relationship between moult-migration and breeding grounds aridity as measured by the normalized difference vegetation index. Our results strongly support the 'push' aspect of the push-pull hypothesis and indicate that arid breeding grounds, primarily in western North America, would drive species to evolve stopover moult-migration, although this relationship may depend upon migration distance.

Population assignment reveals low migratory connectivity in a weakly structured songbird.

Understanding migratory connectivity is essential for determining the drivers behind population dynamics and for implementing effective conservation strategies for migratory species. Genetic markers provide a means to describe migratory connectivity; however, they can be uninformative for species with weak population genetic structure, which has limited their application. Here, we demonstrated a genomic approach to describing migratory connectivity in the prothonotary warbler, Protonotaria citrea, a Neotropical songbird of conservation concern. Using 26,189 single nucleotide polymorphisms (SNPs), we revealed regional genetic structure between the Mississippi River Valley and the Atlantic Seaboard with overall weak genetic differentiation among populations (FST  = 0.0055; 95% CI: 0.0051-0.0059). Genetic variation had a stronger association with geographic rather than environmental factors, with each explaining 14.5% and 8.2% of genetic variation, respectively. By varying the numbers of genomic markers used in population assignment models with individuals of known provenance, we identified a maximum assignment accuracy (89.7% to site, 94.3% to region) using a subset of 600 highly differentiated SNPs. We then assigned samples from nonbreeding sites to breeding region and found low migratory connectivity. Our results highlight the importance of filtering markers for informative loci in models of population assignment. Quantifying migratory connectivity for weakly structured species will be useful for expanding studies to a wider range of migratory species across taxonomic groups and may contribute to a deeper understanding of the evolution of migratory strategies.

A call for full annual cycle research in animal ecology.

For vertebrates, annual cycles are organized into a series of breeding and non-breeding periods that vary in duration and location but are inextricably linked biologically. Here, we show that our understanding of the fundamental ecology of four vertebrate classes has been limited by a severe breeding season research bias and that studies of individual and population-level responses to natural and anthropogenic change would benefit from a full annual cycle perspective. Recent emergence of new analytical and technological tools for studying individual and population-level animal movement could help reverse this bias. To improve understanding of species biology and reverse the population declines of many vertebrate species, a concerted effort to move beyond single season research is vital.

Experimental and observational studies of seasonal interactions between overlapping life history stages in a migratory bird.

Prior to reproduction, migratory animals are at the juxtaposition of three life history stages in which they must finish the non-breeding stage, initiate and complete migration, and prepare for the onset of breeding. However, how these stages interact with one another is not fully understood. We provide evidence that, for migratory birds that begin breeding development prior to departure from non-breeding sites, the level of breeding preparation can drive migration phenology, a critical behavioral determinant of reproductive success. Specifically, male American redstart (Setophaga ruticilla) plasma androgen levels, which increase in males during the period leading into migration, were positively correlated with energetic condition. We empirically tested the hypothesis that elevated androgen simultaneously supports migratory and breeding preparation in a hormone manipulation field experiment. Males with testosterone implants showed advanced preparation for migration and breeding, and ultimately departed on migration earlier than controls. It is assumed that early departure leads to early arrival at breeding areas, which increases breeding success. Collectively, our observational and experimental results demonstrate how overlapping life history stages can interact to influence important components of an individual's fitness. This highlights the critical need for understanding population processes across the full life cycle of an organism to better understand the ecological and evolutionary origins of complex life history events.

Stress in the city? Coyote hair cortisol varies with intrinsic and extrinsic factors within a heavily urbanized landscape.

Wildlife living in proximity to people are exposed to both natural and anthropogenic factors that may influence cortisol production associated with stress response. While some species, including coyotes (Canis latrans), have become commonplace in developed areas throughout North America, urban individuals still must navigate ever-changing, novel environments and cope with frequent disturbance. Given that coyotes are relatively large predators compared to most other urban wildlife, they face unique pressures such as crossing roadways to use suitable habitat fragments and are at a greater risk of being detected and experiencing negative human interactions. To assess whether urbanization influences hypothalamic-pituitary-adrenal axis activity in free-ranging coyotes, we analyzed cortisol concentration in hair samples from 97 coyotes residing across the urbanization gradient within the Greater Chicago Metropolitan area. As the proportion of developed landcover within coyote home ranges increased, coyotes experienced more stress. Body condition and social status also had strong relationships with stress. Animals in poorer body condition experienced more stress and subordinate coyotes experienced less stress than alphas. We also found some evidence that stress varied seasonally and among different age classes. Understanding how intrinsic and extrinsic factors influence endocrine activity in urban carnivores is vital for predicting how hormone production and related behavioral patterns may change in future populations as more areas become developed.

Convergent remodelling of the gut microbiome is associated with host energetic condition over long-distance migration.

The gut microbiome can be thought of as a virtual organ given its immense metabolic capacity and profound effects on host physiology. Migratory birds are capable of adaptively modulating many aspects of their physiology to facilitate long-distance movements, raising the hypothesis that their microbiome may undergo a parallel remodeling process that helps to meet the energetic demands of migration.To test this hypothesis, we investigated changes in gut microbiome composition and function over the fall migration of the Blackpoll Warbler (Setophaga striata), which exhibits one of the longest known autumnal migratory routes of any songbird and rapidly undergoes extensive physiological remodeling during migration.Overall, our results showed that the Blackpoll Warbler microbiome differed significantly across phases of fall migration. This pattern was driven by a dramatic increase in the relative abundance of Proteobacteria, and more specifically a single 16S rRNA gene amplicon sequence variant belonging to the family Enterobacteriaceae. Further, Blackpoll Warblers exhibited a progressive reduction in microbiome diversity and within-group variance over migration, indicating convergence of microbiome composition among individuals during long-distance migration. Metagenomic analysis revealed that the gut microbiome of staging individuals was enriched in bacterial pathways involved in vitamin, amino acid, and fatty acid biosynthesis, as well as carbohydrate metabolism, and that these pathways were in turn positively associated with host body mass and subcutaneous fat deposits.Together, these results provide evidence that the gut microbiome of migratory birds may undergo adaptive remodeling to meet the physiological and energetic demands of long-distance migration.

Songbirds initiate migratory flights synchronously relative to civil dusk.

BACKGROUND: Each spring and fall billions of songbirds depart on nocturnal migrations across the globe. Theory suggests that songbirds should depart on migration shortly after sunset to maximize their potential for nightly flight duration or to time departure with the emergence of celestial cues needed for orientation and navigation. Although captive studies have found that songbirds depart during a narrow window of time after sunset, observational studies have found that wild birds depart later and more asynchronously relative to sunset than predicted. METHODS: We used coded radio tags and automated radio-telemetry to estimate the time that nearly 400 individuals from nine songbird species departed their breeding or wintering grounds across North America. We also assessed whether each species was most likely beginning long-distance migratory flights at departure or instead first making non-migratory regional flights. We then explored variation in nocturnal departure time by post-departure movement type, species, age, sex, and season. RESULTS: We found that 90% of individuals from species that were likely initiating long-distance migratory flights departed within 69 min of civil dusk, regardless of species, season, age, or sex. By contrast, species that likely first made non-migratory regional movements away from the migratory destination departed later and more asynchronously throughout the night. Regardless of post-departure movement type, 98% of individuals departed after civil dusk but otherwise showed no preference in relation to twilight phase. CONCLUSIONS: Although the presence of celestial orientation cues at civil dusk may set a starting point for departure each night, the fact that species likely beginning long-distance migration departed earlier and more synchronously relative to civil dusk than those first making non-migratory regional movements is consistent with the hypothesis that departing promptly after civil dusk functions to maximize the potential for nightly flight duration and distance. By studying the onset of migration, our study provides baseline information about departure decisions that may enhance our understanding of departure timing throughout migration.

Early elevation of testosterone advances migratory preparation in a songbird.

The timing of events associated with spring migration can be an important determinant of fitness for migratory birds. The need to prepare and maintain physical condition for migration is one demand that must be met for early arrival on breeding areas, and this demand is compounded by the energetic demands of the physiological transition to breeding. Here, we examined whether migratory birds, specifically males, can adequately meet both of these demands by elevating the sex steroid testosterone early during migratory preparation. To test this, we used a captive experiment in which we photostimulated male dark-eyed juncos (Junco hyemalis) and manipulated circulating testosterone. We predicted males with elevated testosterone would prepare to migrate and breed faster than control males or males where the ability of testosterone to bind with receptors, or be converted to estradiol, was inhibited (testosterone inhibited). We measured migratory preparation using mass, food intake, fat deposits and nocturnal activity (Zugunruhe). To estimate breeding preparation, we measured the diameter of the cloacal protuberance (CP). We found that males in the testosterone treatment group began migratory preparation approximately 10 days before controls. There was no difference in the magnitude of peak migratory condition between testosterone-implanted birds and controls. Males implanted with testosterone also reached the onset of breeding preparation faster and had larger peak CP diameter compared with controls. Testosterone-inhibited birds showed no signs of migratory preparation and only a weak increase in CP diameter. These results demonstrate that early elevation of testosterone during migratory preparation could incur benefits for males in terms of the ability to depart earlier from non-breeding areas and arrive in a more advanced breeding condition. This experiment demonstrates that there may be important physiological underpinnings to known winter to breeding season carry-over effects in migratory birds.

Restoration of gallery forest patches improves recruitment of motacú palms (Attalea princeps) while diversifying and increasing wildlife populations.

Globally, forest-savanna mosaic landscapes are of significant conservation importance but have been widely impacted by human land-use. We studied how restoration, through cessation of long-term cattle grazing impacts (i) forest regeneration; (ii) forest understory structure and composition; and (iii) populations and diversity of large mammals and nocturnal birds, within naturally patchy gallery forests in the Beni Savannas of Bolivia. Comparing grazed and restored sites, we assessed the abundance and composition of tree functional types at different life stages (seedlings, saplings and adults), with focus on the region's key palm species Attalea princeps (motacú). Additionally, we surveyed habitat structure and composition in the shrub and ground-layer, and monitored occurrence and encounter rates of large mammals and nocturnal birds along dusk and evening transects. We found evidence of lower recruitment of motacú palms on the grazed site and lower potential for natural motacú regeneration. Principal Components Analysis revealed forests on grazed sites had simpler, more open shrub-layers and altered ground-layer structure and composition including increased bare ground. Mammal species richness was greater on the restored site, and there were more declining, globally threatened and site-unique species. Species richness was similar for nocturnal birds within forests on both the grazed and restored site, but nearly all species tended to be encountered more frequently on the restored site. Our results suggest cattle negatively impact forest regeneration and alter the structure and composition of the shrub and ground layer with potential consequences for the diversity and abundance of wildlife. Our study represents one of only a handful completed in the Beni region of Bolivia to date. The Beni is currently under pressure from widespread, largely unregulated cattle ranching. Our results thus provide vital evidence to support development of restoration and conservation policy, and its integration with rangeland management in this threatened and critically understudied region.

Evolution of winter molting strategies in European and North American migratory passerines.

Molt is critical for birds as it replaces damaged feathers and worn plumage, enhancing flight performance, thermoregulation, and communication. In passerines, molt generally occurs on the breeding grounds during the postbreeding period once a year. However, some species of migrant passerines that breed in the Nearctic and Western Palearctic regions have evolved different molting strategies that involve molting on the overwintering grounds. Some species forego molt on the breeding grounds and instead complete their prebasic molt on the overwintering grounds. Other species molt some or all feathers a second time (prealternate molt) during the overwintering period. Using phylogenetic analyses, we explored the potential drivers of the evolution of winter molts in Nearctic and Western Palearctic breeding passerines. Our results indicate an association between longer photoperiods and the presence of prebasic and prealternate molts on the overwintering grounds for both Nearctic and Western Palearctic species. We also found a relationship between prealternate molt and generalist and water habitats for Western Palearctic species. Finally, the complete prealternate molt in Western Palearctic passerines was linked to longer days on the overwintering grounds and longer migration distance. Longer days may favor the evolution of winter prebasic molt by increasing the time window when birds can absorb essential nutrients for molt. Alternatively, for birds undertaking a prealternate molt at the end of the overwintering period, longer days may increase exposure to feather-degrading ultra-violet radiation, necessitating the replacement of feathers. Our study underlines the importance of the overwintering grounds in the critical process of molt for many passerines that breed in the Nearctic and Western Palearctic regions.

Striving for population-level conservation: integrating physiology across the biological hierarchy.

The field of conservation physiology strives to achieve conservation goals by revealing physiological mechanisms that drive population declines in the face of human-induced rapid environmental change (HIREC) and has informed many successful conservation actions. However, many studies still struggle to explicitly link individual physiological measures to impacts across the biological hierarchy (to population and ecosystem levels) and instead rely on a 'black box' of assumptions to scale up results for conservation implications. Here, we highlight some examples of studies that were successful in scaling beyond the individual level, including two case studies of well-researched species, and using other studies we highlight challenges and future opportunities to increase the impact of research by scaling up the biological hierarchy. We first examine studies that use individual physiological measures to scale up to population-level impacts and discuss several emerging fields that have made significant steps toward addressing the gap between individual-based and demographic studies, such as macrophysiology and landscape physiology. Next, we examine how future studies can scale from population or species-level to community- and ecosystem-level impacts and discuss avenues of research that can lead to conservation implications at the ecosystem level, such as abiotic gradients and interspecific interactions. In the process, we review methods that researchers can use to make links across the biological hierarchy, including crossing disciplinary boundaries, collaboration and data sharing, spatial modelling and incorporating multiple markers (e.g. physiological, behavioural or demographic) into their research. We recommend future studies incorporating tools that consider the diversity of 'landscapes' experienced by animals at higher levels of the biological hierarchy, will make more effective contributions to conservation and management decisions.

Bergmann's rule is followed at multiple stages of postembryonic development in a long-distance migratory songbird.

Bergmann's rule is a well-established, ecogeographical principle that states that body size varies positively with latitude, reflecting the thermoregulatory benefits of larger bodies as temperatures decline. However, this principle does not seem to easily apply to migratory species that are able to avoid the extreme temperatures during winter at higher latitudes. Further, little is known about the ontogeny of this relationship across life stages or how it is influenced by ongoing global climate change. To address these knowledge gaps, we assessed the contemporary relationship between latitude and body size in a long-distance migratory species, the prothonotary warbler (Protonotaria citrea) across life stages (egg to adult) on their breeding grounds. We also measured historic eggs (1865-1961) to assess if the relationship between latitude and size during this life stage has changed over time. In accordance with Bergmann's rule, we found a positive relationship between latitude and body mass during all post-embryonic life stages, from early nestling stage through adulthood. We observed this same predicted pattern with historic eggs, but contemporary eggs exhibited the reverse (negative) relationship. We suggest that these results indicate a genetic component to this pattern and speculate that selection for larger body size in altricial nestlings as latitude increases may possibly drive the pattern in migratory species as even rare extreme cold weather events may cause mortality during early life stages. Furthermore, the opposite relationships observed in eggs, dependent on time period, may be related to the rapidly warming environments of higher latitudes that is associated with climate change. Although it is unclear what mechanism(s) would allow for this recent reversal in eggs (but still allow for its maintenance in later life stages). This evidence of a reversal suggests that anthropogenic climate change may be in the process of altering one of the longest-standing principles in ecology.

Remote estimation of overwintering home ranges in an elusive, migratory nocturnal bird.

Due to a long running research bias toward the breeding season, there are major gaps in knowledge on the basic nonbreeding ecology of many species, preventing a full-annual cycle focus in ecology and conservation. Exacerbating this problem is the fact that many species are extremely difficult to detect outside of breeding. Here, we demonstrate a partial solution to this problem by using archival GPS tags to examine the overwintering ecology of a migratory nocturnal bird, the eastern whip-poor-will (Antrostomus vociferous). We deployed tags on 21 individuals and were able to recover 11 (52%) one year later. Tags collected high precision (approx. 10 m) points throughout the nonbreeding period. With continuous time movement models, we used these data to estimate overwintering home ranges. All individuals exhibited at least one bounded home range during this phase of the annual cycle, three of eleven had two wintering locations, and home range area ranged from 0.50 to 10.85 ha. All overwintering home ranges contained closed-canopy forest land cover (42%-100%), and no other land cover type represented >40% of any home range. We found some evidence, with caveats, that total edge within the landscape surrounding the home range was negatively related to home range area. The prevalence of contiguous closed-canopy forest cover in overwintering home ranges contrasts with apparent breeding habitat preferences, which includes clear-cuts and other, more open, habitats. This study is the first to reveal key aspects of overwintering space use in this species by using archival GPS to overcome both logistical and methodological limitations. Expanded use of such technology is critical to gathering basic ecological and distributional data, necessary for achieving a more complete understanding of full-annual cycles of animal populations.

Color expression in experimentally regrown feathers of an overwintering migratory bird: implications for signaling and seasonal interactions.

Plumage coloration in birds plays a critical role in communication and can be under selection throughout the annual cycle as a sexual and social signal. However, for migratory birds, little is known about the acquisition and maintenance of colorful plumage during the nonbreeding period. Winter habitat could influence the quality of colorful plumage, ultimately carrying over to influence sexual selection and social interactions during the breeding period. In addition to the annual growth of colorful feathers, feather loss from agonistic interactions or predator avoidance could require birds to replace colorful feathers in winter or experience plumage degradation. We hypothesized that conditions on the wintering grounds of migratory birds influence the quality of colorful plumage. We predicted that the quality of American redstart (Setophaga ruticilla) tail feathers regrown after experimental removal in Jamaica, West Indies, would be positively associated with habitat quality, body condition, and testosterone. Both yearling (SY) and adult (ASY) males regrew feathers with lower red chroma, suggesting reduced carotenoid content. While we did not observe a change in hue in ASY males, SY males shifted from yellow to orange plumage resembling experimentally regrown ASY feathers. We did not observe any effects of habitat, testosterone, or mass change. Our results demonstrate that redstarts are limited in their ability to adequately replace colorful plumage, regardless of habitat, in winter. Thus, feather loss on the nonbreeding grounds can affect social signals, potentially negatively carrying over to the breeding period.