Rare edges and abundant cores: range-wide variation in abundance in North American birds.

Understanding how the abundance of species varies across geographical ranges is central to ecology; however, few studies test hypotheses using detailed abundance estimates across the full ranges of species on a continental scale. Here, we use unprecedented, detailed estimates of breeding abundance for North American birds (eBird) to test two hypotheses for how abundance varies across species' ranges. We find widespread support for the rare-edge hypothesis-where the abundance of species declines near the range edge-reflecting both reduced occurrence and lower local abundance near range edges. By contrast, we find mixed support for the abundant-centre hypothesis-where the abundance of species peaks in the centre of the range and declines towards the edges-with limited support in conservative tests within species, but general support in among-species tests that control for unbalanced sampling and consider a broader definition of the range centre. Overall, results are consistent with a gradual decline in suitable conditions and increase in challenge towards the range edge that eventually limit the ability of populations to persist.

Urban tolerance does not protect against population decline in North American birds.

Population declines of organisms are widespread and severe, but some species' populations have remained stable, or even increased. The reasons some species are less vulnerable to population decline than others are not well understood. Species that tolerate urban environments often have a broader environmental tolerance, which, along with their ability to tolerate one of the most human-modified habitats (i.e. cities), might allow them to persist in the face of diverse anthropogenic challenges. Here, we examined the relationship between urban tolerance and annual population trajectories for 397 North American bird species. Surprisingly, we found that urban tolerance was unrelated to species' population trajectories. The lack of a relationship between urban tolerance and population trajectories may reflect other factors driving population declines independent of urban tolerance, challenges that are amplified in cities (e.g. climate warming, disease), and other human impacts (e.g. conservation efforts, broad-scale land-use changes) that have benefitted some urban-avoidant species. Overall, our results illustrate that urban tolerance does not protect species against population decline.

Among-species variation in hormone concentrations is associated with urban tolerance in birds.

As cities expand across the globe, understanding factors that underlie variation in urban tolerance is vital for predicting changes in patterns of biodiversity. Endocrine traits, like circulating hormone concentrations and regulation of endocrine responses, might contribute to variation in species' ability to cope with urban challenges. For example, variation in glucocorticoid and androgen concentrations has been linked to life-history and behavioural traits that are associated with urban tolerance. However, we lack an understanding of the degree to which evolved differences in endocrine traits predict variation in urban tolerance across species. We analysed 1391 estimates of circulating baseline corticosterone, stress-induced corticosterone, and testosterone concentrations paired with citizen-science-derived urban occurrence scores in a broad comparative analysis of endocrine phenotypes across 71 bird species that differ in their occurrence in urban habitats. Our results reveal context-dependent links between baseline corticosterone and urban tolerance, as well as testosterone and urban tolerance. Stress-induced corticosterone was not related to urban tolerance. These findings suggest that some endocrine phenotypes contribute to a species' tolerance of urban habitats, but also indicate that other aspects of the endocrine phenotype, such as the ability to appropriately attenuate responses to urban challenges, might be important for success in cities.

Experimental reduction of haemosporidian infection affects maternal reproductive investment, parental behaviour and offspring condition.

When hosts have a long coevolutionary history with their parasites, fitness costs of chronic infection have often been assumed to be negligible. Yet, experimental manipulation of infections sometimes reveals effects of parasites on their hosts, particularly during reproduction. Whether these effects translate into fitness costs remains unclear. Here, we present the results of an experimental study conducted in a free-ranging population of red-winged blackbirds (Agelaius phoeniceus) naturally experiencing a high prevalence of haemosporidian infections, with more than 95% of breeding adults infected with parasites from one or more haemosporidian genus. To assess effects of infection during reproduction, we manipulated adult red-winged blackbird females' parasite burden by administering an anti-haemosporidian medication before onset of egg-laying. Experimental reduction of infection resulted in significant benefits to mothers and their offspring. Medicated females laid heavier clutches, invested more in incubation and provisioning behaviour, and produced more fledglings than control females. Nestlings of medicated females had higher haematocrit, higher blood glucose, and lower reactive oxygen metabolites than nestlings of control females. Overall, our results provide evidence that, even in a species with high prevalence of infection, parasites can lead to decreased maternal investment and offspring quality, substantially reducing fitness.

Plasticity versus Evolutionary Divergence: What Causes Habitat Partitioning in Urban-Adapted Birds?

AbstractHabitat partitioning can facilitate the coexistence of closely related species and often results from competitive interference inducing plastic shifts of subordinate species in response to aggressive, dominant species (plasticity) or the evolution of ecological differences in subordinate species that reduce their ability to occupy habitats where the dominant species occurs (evolutionary divergence). Evidence consistent with both plasticity and evolutionary divergence exist, but the relative contributions of each to habitat partitioning have been difficult to discern. Here we use a global data set on the breeding occurrence of birds in cities to test predictions of these alternative hypotheses to explain previously described habitat partitioning associated with competitive interference. Consistent with plasticity, the presence of behaviorally dominant congeners in a city was associated with a 65% reduction in the occurrence of subordinate species, but only when the dominant was a widespread breeder in urban habitats. Consistent with evolutionary divergence, increased range-wide overlap with dominant congeners was associated with a 56% reduction in the occurrence of subordinates in cities, even when the dominant was absent from the city. Overall, our results suggest that both plasticity and evolutionary divergence play important, concurrent roles in habitat partitioning among closely related species in urban environments.

Cytonuclear discordance in the crowned-sparrows, Zonotrichia atricapilla and Zonotrichia leucophrys.

The golden-crowned (Zonotrichia atricapilla) and white-crowned (Z. leucophrys) sparrows have been presented as a compelling case for rapid speciation. They display divergence in song and plumage with overlap in their breeding ranges implying reproductive isolation, but have almost identical mitochondrial genomes. Previous research proposed hybridization and subsequent mitochondrial introgression as an alternate explanation, but lacked robust nuclear gene trees to distinguish between introgression and incomplete lineage sorting. We test for signatures of these processes between Z. atricapilla and Z. leucophrys, and investigate the relationships among Z. leucophrys subspecies, using mitochondrial sequencing and a reduced representation nuclear genomic dataset. Contrary to the paraphyly evident in mitochondrial gene trees, we confirmed the reciprocal monophyly of Z. atricapilla and Z. leucophrys using large panels of single nucleotide polymorphisms (SNPs). The pattern of cytonuclear discordance is consistent with limited, historical hybridization and mitochondrial introgression, rather than a recent origin and incomplete lineage sorting between recent sister species. We found evidence of nuclear phylogeographic structure within Z. leucophrys with two distinct clades. Altogether, our results indicate deeper divergences between Z. atricapilla and Z. leucophrys than inferred using mitochondrial markers. Our results demonstrate the limitations of relying solely on mitochondrial DNA for taxonomy, and raise questions about the possibility of selection on the mitochondrial genome during temperature oscillations (e.g. during the Pleistocene). Historical mitochondrial introgression facilitated by past environmental changes could cause erroneous dating of lineage splitting in other taxa when based on mitochondrial DNA alone.

Species interactions limit the occurrence of urban-adapted birds in cities.

Urbanization represents an extreme transformation of more natural systems. Populations of most species decline or disappear with urbanization, and yet some species persist and even thrive in cities. What determines which species persist or thrive in urban habitats? Direct competitive interactions among species can influence their distributions and resource use, particularly along gradients of environmental challenge. Given the challenges of urbanization, similar interactions may be important for determining which species persist or thrive in cities; however, their role remains poorly understood. Here, we use a global dataset to test among three alternative hypotheses for how direct competitive interactions and behavioral dominance may influence the breeding occurrence of birds in cities. We find evidence to support the competitive interference hypothesis: behaviorally dominant species were more widespread in urban habitats than closely related subordinate species, but only in taxa that thrive in urban environments (hereafter, urban adapted), and only when dominant and subordinate species overlapped their geographic ranges. This result was evident across diverse phylogenetic groups but varied significantly with a country's level of economic development. Urban-adapted, dominant species were more widespread than closely related subordinate species in cities in developed, but not developing, countries; countries in economic transition showed an intermediate pattern. Our results provide evidence that competitive interactions broadly influence species responses to urbanization, and that these interactions have asymmetric effects on subordinate species that otherwise could be widespread in urban environments. Results further suggest that economic development might accentuate the consequences of competitive interactions, thereby reducing local diversity in cities.

Population decline in tree swallows (Tachycineta bicolor) linked to climate change and inclement weather on the breeding ground.

Population decline and the threat of extinction are realities currently facing many species. Yet, in most cases, the detailed demographic data necessary to identify causes of population decline are unavailable. Using 43 years (1975-2017) of data from a box-nesting population of tree swallows (Tachycineta bicolor), we identified reduced survival of offspring as a probable demographic cause of population decline. Poor fledging success was associated with increased predation and poor weather conditions during early nestling development. Low juvenile survival and subsequent recruitment was linked to poor weather conditions during the post-fledging period and may also be linked to conditions on the wintering grounds. Regional weather conditions during critical stages of breeding (early nestling and post-fledging) have become progressively worse over the 43-year study period. None of the other factors linked to offspring survival have similarly deteriorated. Overall, our results suggest tree swallows should be added to the growing list of species challenged by climate change, and that other species of aerial insect specialists may face similar impacts of climate change.

Rainy springs linked to poor nestling growth in a declining avian aerial insectivore ( Tachycineta bicolor).

As species shift their ranges and phenology to cope with climate change, many are left without a ready supply of their preferred food source during critical life stages. Food shortages are often assumed to be driven by reduced total food abundance, but here we propose that climate change may cause short-term food shortages for foraging specialists without affecting overall food availability. We frame this hypothesis around the special case of birds that forage on flying insects for whom effects mediated by their shared food resource have been proposed to cause avian aerial insectivores' decline worldwide. Flying insects are inactive during cold, wet or windy conditions, effectively reducing food availability to zero even if insect abundance remains otherwise unchanged. Using long-term monitoring data from a declining population of tree swallows ( Tachycineta bicolor), we show that nestlings' body mass declined substantially from 1977 to 2017. In 2017, nestlings had lower body mass if it rained during the preceding 3 days, though females increased provisioning rates, potentially in an attempt to compensate. Adult body mass, particularly that of the males, has also declined over the long-term study. Mean rainfall during the nestling period has increased by 9.3 ± 0.3 mm decade-1, potentially explaining declining nestling body mass and population declines. Therefore, we suggest that reduced food availability, distinct from food abundance, may be an important and previously overlooked consequence of climate change, which could be affecting populations of species that specialize on foraging on flying insects.

Exogenous glucocorticoids amplify the costs of infection by reducing resistance and tolerance, but effects are mitigated by co-infection.

Individual variation in parasite defences, such as resistance and tolerance, can underlie heterogeneity in fitness and could influence disease transmission dynamics. Glucocorticoid hormone concentrations often change in response to fluctuating environmental conditions and mediate changes in immune function, resource allocation and tissue repair. Thus, changes in glucocorticoid hormone concentrations might mediate individual variation in investment in resistance versus tolerance. In this study, we experimentally increased glucocorticoid concentrations in red-winged blackbirds ( Agelaius phoeniceus) that were naturally infected with haemosporidian parasites, and assessed changes in resistance and tolerance of infection. Glucocorticoid treatment increased burdens of Plasmodium, the parasite causing avian malaria, but only in the absence of co-infection with another Haemosporidian, Haemoproteus. Thus, glucocorticoids might reduce resistance to infection, but co-infection can mitigate the negative consequences of increased hormone concentrations. Glucocorticoid treatment also decreased tolerance of infection. We found no evidence that the inflammatory immune response or rate of red blood cell production underlie the effects of glucocorticoids on resistance and tolerance. Our findings suggest that exogenous glucocorticoids can increase the costs of haemosporidian infections by both increasing parasite numbers and reducing an individual's ability to cope with infection. These effects could scale up to impact populations of both host and parasite.

Higher plasma corticosterone is associated with reduced costs of infection in red-winged blackbirds.

Glucocorticoid hormones allow individuals to rapidly adjust their physiology and behavior to meet the challenges of a variable environment. An individual's baseline concentration of glucocorticoids can reflect shifts in life history stage and resource demands while mediating a suite of physiological and behavioral changes that include immune modulation and resource allocation. Thus, glucocorticoids could facilitate a response to parasites that is optimized for an individual's specific challenges and life history stage. We investigated the relationship between endogenous circulating glucocorticoids and measures of resistance and tolerance to Haemosporidian parasites (including those that cause avian malaria) in red-winged blackbirds (Agelaius phoeniceus). We found that higher endogenous concentrations of circulating glucocorticoids were associated with reduced costs of parasite infection, which is indicative of higher tolerance, but were unrelated to parasite burden in free ranging, breeding male birds. Post-breeding, both males and females with higher glucocorticoid concentrations had higher measures of tolerance to Haemosporidian infection. Our findings suggest a potentially adaptive role for glucocorticoids in shifting the response to parasites to align with an individual's current physiological state and the challenges they face.

Red-winged blackbirds (Agelaius phoeniceus) with higher baseline glucocorticoids also invest less in incubation and clutch mass.

Glucocorticoid hormones facilitate responses to environmental challenges by mediating diverse physiological and behavioral changes, including resource mobilization and altered reproductive effort. Elevated glucocorticoids might indicate that an individual is facing high levels of environmental challenges and thus, elevated concentrations might be associated with reduced fitness (CORT-fitness hypothesis). Alternatively, the energetic demands of reproduction might be a challenge that requires elevated glucocorticoids to mobilize resources to support reproductive effort, ultimately increasing reproductive investment and fitness (CORT-adaptation hypothesis). Investigations of glucocorticoid-fitness relationships have yielded mixed results. Variation in the direction of this relationship could be caused in part by differences in the contexts in which the relationship was assessed. Incorporating context, such as life history stage, could be key to understanding the role of glucocorticoids in influencing fitness outcomes. We investigated the relationship between corticosterone and reproductive effort and success within a single life history stage: incubation of eggs. In an observational study, we measured baseline corticosterone in incubating female red-winged blackbirds (Agelaius phoeniceus), monitored incubation behavior, and determined hatching success for each nest. Incubating birds with higher baseline corticosterone concentrations had more frequent, shorter incubation bouts and spent less time overall incubating their clutches of eggs than birds with lower corticosterone concentrations. Elevated corticosterone was also associated with lower clutch mass, but neither corticosterone nor incubation effort were correlated with hatching success. Although experimental tests are needed to establish causation, these results suggest that during the incubation period, corticosterone might shift resource investment towards self-maintenance, and away from current reproductive effort.

Male song sparrows have elevated testosterone in response to neighbors versus strangers.

Upon hearing a conspecific signal, animals must assess their relationship with the signaller and respond appropriately. Territorial animals usually respond more aggressively to strangers than neighbors in a phenomenon known as the "dear enemy effect". This phenomenon likely evolved because strangers represent a threat to an animal's territory tenure and parentage, whereas neighbors only represent a threat to an animal's parentage because they already possess a territory (providing territory boundaries are established and stable). Although the dear enemy effect has been widely documented using behavioral response variables, little research has been conducted on the physiological responses of animals to neighbors versus strangers. We sought to investigate whether the dear enemy effect is observed physiologically by exposing territorial male song sparrows (Melospiza melodia) to playback simulating a neighbor or a stranger, and then collecting blood samples to measure plasma testosterone levels. We predicted that song sparrows would exhibit increased testosterone levels after exposure to stranger playback compared to neighbor playback, due to the role testosterone plays in regulating aggression. Contrary to our prediction, we found that song sparrows had higher testosterone levels after exposure to neighbor playback compared to stranger playback. We discuss several explanations for our result, notably that corticosterone may regulate the dear enemy effect in male song sparrows and this may inhibit plasma testosterone. Future studies will benefit from examining corticosterone in addition to testosterone, to better understand the hormonal underpinnings of the dear enemy effect.

An experimental test of the physiological consequences of avian malaria infection.

Chronic, low-intensity parasite infections can reduce host fitness through negative impacts on reproduction and survival, even if they produce few overt symptoms. As a result, these parasites can influence the evolution of host morphology, behaviour and physiology. The physiological consequences of chronic infection can provide insight into the processes underlying parasite-driven natural selection. Here, we evaluate the physiological consequences of natural, low-intensity infection in an avian host-parasite system: adult male red-winged blackbirds (Agelaius phoeniceus) infected with haemosporidian parasites. Chronic haemosporidian infection has previously been shown to reduce both reproductive success and survival in several avian species. We used antimalarial medications to experimentally reduce haemosporidian parasitaemia (the proportion of blood cells infected with haemosporidian parasites) and measured the effect of treatment on body condition, haematology, immune function, physiological stress and oxidative state. Treatment with an antimalarial medication reduced parasitaemia for the most prevalent haemosporidian parasites from the genus Plasmodium. Treatment also increased haemoglobin and haematocrit, and decreased red blood cell production rates. We detected no effect of treatment on body condition, immune metrics, plasma corticosterone concentrations, total antioxidant capacity or reactive oxygen metabolites. Our results suggest that the damage and replacement of red blood cells during infection could be important costs of chronic haemosporidian infection. Strong links between parasitaemia and the physiological consequences of infection indicate that even for relatively low-intensity infections, measuring parasitaemia rather than only presence/absence could be important when evaluating the role of infection in influencing hosts' behaviour, physiology or fitness.

How can we estimate natural selection on endocrine traits? Lessons from evolutionary biology.

An evolutionary perspective can enrich almost any endeavour in biology, providing a deeper understanding of the variation we see in nature. To this end, evolutionary endocrinologists seek to describe the fitness consequences of variation in endocrine traits. Much of the recent work in our field, however, follows a flawed approach to the study of how selection shapes endocrine traits. Briefly, this approach relies on among-individual correlations between endocrine phenotypes (often circulating hormone levels) and fitness metrics to estimate selection on those endocrine traits. Adaptive plasticity in both endocrine and fitness-related traits can drive these correlations, generating patterns that do not accurately reflect natural selection. We illustrate why this approach to studying selection on endocrine traits is problematic, referring to work from evolutionary biologists who, decades ago, described this problem as it relates to a variety of other plastic traits. We extend these arguments to evolutionary endocrinology, where the likelihood that this flaw generates bias in estimates of selection is unusually high due to the exceptional responsiveness of hormones to environmental conditions, and their function to induce adaptive life-history responses to environmental variation. We end with a review of productive approaches for investigating the fitness consequences of variation in endocrine traits that we expect will generate exciting advances in our understanding of endocrine system evolution.

Extrapair paternity rates vary with latitude and elevation in emberizid sparrows.

Mating systems can vary among species and populations and thus influence evolutionary trajectories, ecological traits, and population demography. The siring of offspring by an extrapair male, or extrapair paternity (EPP), is a widespread and varied phenomenon in all vertebrate classes. However, we do not understand all of the factors associated with variation in EPP rates. The breeding synchrony hypothesis suggests that EPP rates should increase with latitude and elevation, whereas the paternal care hypothesis predicts that EPP rates should decrease with elevation. To address these hypotheses, we investigated how population EPP rates vary over elevation and latitude in emberizid sparrows. In comparative analyses including the effects of phylogeny, the relationship between EPP rates and elevation depended on latitude. EPP rates were greater in higher-latitude populations. But within higher-latitude populations, EPP rates decreased with increasing elevation. These findings provide support for both the breeding synchrony and paternal care hypotheses, suggesting that in lower-latitude, higher-elevation populations, the need for male parental care does not outweigh the benefits of seeking extrapair fertilizations in populations with relatively synchronous breeding. In contrast, at higher-latitude, higher-elevation sites, the need for male parental care is greater and might drive lower rates of extrapair mating despite highly synchronous breeding.

Future directions in urban endocrinology - The effects of endocrine plasticity on urban tolerance.

After twenty years of studies of endocrine traits in animals living in cities, the field of urban endocrinology has built a robust literature including numerous studies looking for signatures of the effects of urban living, usually in mean circulating hormone concentrations. The findings of this past research have primarily demonstrated the absence of any generalizable endocrine responses to city life. In this opinion paper, I suggest that a strong route forward would include investigations of the role of variation in endocrine plasticity in determining the degree to which organisms tolerate urban challenges (i.e., urban tolerance). Achieving this research aim will require creative experimental and comparative studies, consideration of alternative study systems, and teasing apart of sources of variation in plastic phenotypes (plasticity, sorting, and contemporary evolution). Insight into the role of endocrine plasticity in influencing urban tolerance could help us better understand and predict impacts of expanding urbanization on biodiversity across the globe.

Hormones in the city: endocrine ecology of urban birds.

Urbanization dramatically changes the landscape, presenting organisms with novel challenges and often leading to reduced species diversity. Urban ecologists have documented numerous biotic and abiotic consequences of urbanization, such as altered climate, species interactions, and community composition, but we lack an understanding of the mechanisms underlying organisms' responses to urbanization. Here, I review findings from the nascent field of study of the endocrine ecology of urban birds. Thus far, no clear or consistent patterns have been revealed, but we do have evidence that urban habitat can shape endocrine traits, and that those traits might contribute to adaptation to the urban environment. I suggest strong approaches for future work addressing exciting questions about the role of endocrine traits in mediating responses to urbanization within species across the globe.

Estimates of species-level tolerance of urban habitat in North American birds.

Species vary in their responses to urban habitat; most species avoid these environments, whereas others tolerate or even thrive in them. To better characterize the extent to which species vary in their responses to urban habitat (from this point forwards "urban tolerance"), we used several methods to quantify these responses at a continental scale across all birds. Using open access community science-derived data from the eBird Status and Trends Products and two different types of high-resolution geospatial data that quantify urbanization of landscapes, we calculated urban tolerance for 432 species with breeding ranges that overlap large cities in Canada or the USA. We developed six different calculations to characterize species-level urban tolerance, allowing us to assess how each species' relative abundance across their breeding range varied with estimates of urban habitat use and intensity. We assessed correlations among these six indices, then compressed the two best-performing indices into a single principal component (multivariate urban tolerance index) that captured variation in urban tolerance among species. We assessed the accuracy of our single and multivariate urban tolerance indices using 24 test species that have been well characterized for their tolerance or avoidance of the urban habitat, as well as with previously published, independent urban tolerance estimates. Here, we provide this new dataset of species-level urban tolerance estimates that improves upon previous metrics by incorporating continental-scale, continuous estimates that better differentiate species' tolerance of urban habitat compared with existing, categorical methods. These refined metrics can be used to test hypotheses that link ecological, life history, and behavioral traits to avian urban tolerance. The dataset is licensed as CC-By Attribution 4.0 International. Users must appropriately cite the data paper and dataset if used in publications and scientific presentations.

Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence.

In addition to the observed high diversity of species in the tropics, divergence among populations of the same species exists over short geographic distances in both phenotypic traits and neutral genetic markers. Divergence among populations suggests great potential for the evolution of reproductive isolation and eventual speciation. In birds, song can evolve quickly through cultural transmission and result in regional dialects, which can be a critical component of reproductive isolation through variation in female preference. We examined female and male behavioral responses to local and nonlocal dialects in two allopatric populations of rufous-collared sparrows (Zonotrichia capensis) in the Andes Mountains of Ecuador. Here we show that female sparrows prefer their natal song dialect to the dialect of an allopatric population that is just 25 km away and separated by an unsuitable higher-elevation habitat (pass of 4,200 m), thus providing evidence of prezygotic reproductive isolation among populations. Males showed similar territorial responses to all conspecific dialects with no consistent difference with respect to distance, making male territoriality uninformative for estimating reproductive isolation. This study provides novel evidence for culturally based prezygotic isolation over very short distances in a tropical bird.