Long-term monitoring reveals widespread and severe declines of understory birds in a protected Neotropical forest.

Long-term studies on the population dynamics of tropical resident birds are few, and it remains poorly understood how their populations have fared in recent decades. Here, we analyzed a 44-y population study of a Neotropical understory bird assemblage from a protected forest reserve in central Panama to determine if and how populations have changed from 1977 to 2020. Using the number of birds captured in mist nets as an index of local abundance, we estimated trends over time for a diverse suite of 57 resident species that comprised a broad range of ecological and behavioral traits. Estimated abundances of 40 (∼70%) species declined over the sampling period, whereas only 2 increased. Furthermore, declines were severe: 35 of the 40 declining species exhibited large proportional losses in estimated abundance, amounting to ≥50% of their initial estimated abundances. Declines were largely independent of ecology (i.e., body mass, foraging guild, or initial abundance) or phylogenetic affiliation. These widespread, severe declines are particularly alarming, given that they occurred in a relatively large (∼22,000-ha) forested area in the absence of local fragmentation or recent land-use change. Our findings provide robust evidence of tropical bird declines in intact forests and bolster a large body of literature from temperate regions suggesting that bird populations may be declining at a global scale. Identifying the ecological mechanisms underlying these declines should be an urgent conservation priority.

Parental benefits and offspring costs reflect parent-offspring conflict over the age of fledging among songbirds.

Parent-offspring conflict has explained a variety of ecological phenomena across animal taxa, but its role in mediating when songbirds fledge remains controversial. Specifically, ecologists have long debated the influence of songbird parents on the age of fledging: Do parents manipulate offspring into fledging to optimize their own fitness or do offspring choose when to leave? To provide greater insight into parent-offspring conflict over fledging age in songbirds, we compared nesting and postfledging survival rates across 18 species from eight studies in the continental United States. For 12 species (67%), we found that fledging transitions offspring from comparatively safe nesting environments to more dangerous postfledging ones, resulting in a postfledging bottleneck. This raises an important question: as past research shows that offspring would benefit-improve postfledging survival-by staying in the nest longer: Why then do they fledge so early? Our findings suggest that parents manipulate offspring into fledging early for their own benefit, but at the cost of survival for each individual offspring, reflecting parent-offspring conflict. Early fledging incurred, on average, a 13.6% postfledging survival cost for each individual offspring, but parents benefitted through a 14.0% increase in the likelihood of raising at least one offspring to independence. These parental benefits were uneven across species-driven by an interaction between nest mortality risk and brood size-and predicted the age of fledging among species. Collectively, our results suggest that parent-offspring conflict and associated parental benefits explain variation in fledging age among songbird species and why postfledging bottlenecks occur.

Plasmodium prevalence across avian host species is positively associated with exposure to mosquito vectors.

The prevalence of vector-borne parasites varies greatly across host species, and this heterogeneity has been used to relate infectious disease susceptibility to host species traits. However, a few empirical studies have directly associated vector-borne parasite prevalence with exposure to vectors across hosts. Here, we use DNA sequencing of blood meals to estimate utilization of different avian host species by Culex mosquitoes, and relate utilization by these malaria vectors to avian Plasmodium prevalence. We found that avian host species that are highly utilized as hosts by avian malaria vectors are significantly more likely to have Plasmodium infections. However, the effect was not consistent among individual Plasmodium taxa. Exposure to vector bites may therefore influence the relative number of all avian Plasmodium infections among host species, while other processes, such as parasite competition and host-parasite coevolution, delimit the host distributions of individual Plasmodium species. We demonstrate that links between avian malaria susceptibility and host traits can be conditioned by patterns of exposure to vectors. Linking vector utilization rates to host traits may be a key area of future research to understand mechanisms that produce variation in the prevalence of vector-borne pathogens among host species.

Identification of Avian and Hemoparasite DNA in Blood-Engorged Abdomens of Culex pipiens (Diptera; Culicidae) from a West Nile Virus Epidemic region in Suburban Chicago, Illinois.

Multiple mosquito-borne parasites cocirculate in nature and potentially interact. To understand the community of parasites cocirculating with West Nile virus (WNV), we screened the bloodmeal content of Culex pipiens L. mosquitoes for three common types of hemoparasites. Blood-fed Cx. pipiens were collected from a WNV-epidemic area in suburban Chicago, IL, from May to September 2005 through 2010. DNA was extracted from dissected abdomens and subject to PCR and direct sequencing to identify the vertebrate host. RNA was extracted from the head or thorax and screened for WNV using quantitative reverse transcriptase PCR. Seventy-nine engorged females with avian host origin were screened using PCR and amplicon sequencing for filarioid nematodes, Haemosporida, and trypanosomatids. Filarioid nematodes were identified in 3.8% of the blooded abdomens, Plasmodium sp. in 8.9%, Haemoproteus in 31.6%, and Trypanosoma sp. in 6.3%. The sequences from these hemoparasite lineages were highly similar to sequences from birds in prior studies in suburban Chicago. Overall, 50.6% of blood-fed Culex pipiens contained hemoparasite DNA in their abdomen, presumably from current or prior bloodmeals. Additionally, we detected hemoparasite DNA in the blooded abdomen of three of 10 Cx. pipiens infected with WNV.

Host group formation decreases exposure to vector-borne disease: a field experiment in a 'hotspot' of West Nile virus transmission.

Animals can decrease their individual risk of predation by forming groups. The encounter-dilution hypothesis extends the potential benefits of gregariousness to biting insects and vector-borne disease by predicting that the per capita number of insect bites should decrease within larger host groups. Although vector-borne diseases are common and can exert strong selective pressures on hosts, there have been few tests of the encounter-dilution effect in natural systems. We conducted an experimental test of the encounter-dilution hypothesis using the American robin (Turdus migratorius), a common host species for the West Nile virus (WNV), a mosquito-borne pathogen. By using sentinel hosts (house sparrows, Passer domesticus) caged in naturally occurring communal roosts in the suburbs of Chicago, we assessed sentinel host risk of WNV exposure inside and outside of roosts. We also estimated per capita host exposure to infected vectors inside roosts and outside of roosts. Sentinel birds caged inside roosts seroconverted to WNV more slowly than those outside of roosts, suggesting that social groups decrease per capita exposure to infected mosquitoes. These results therefore support the encounter-dilution hypothesis in a vector-borne disease system. Our results suggest that disease-related selective pressures on sociality may depend on the mode of disease transmission.

Equivocal support for the climate variability hypothesis within a Neotropical bird assemblage.

The climate variability hypothesis posits that an organism's exposure to temperature variability determines the breadth of its thermal tolerance and has become an important framework for understanding variation in species' susceptibilities to climate change. For example, ectotherms from more thermally stable environments tend to have narrower thermal tolerances and greater sensitivity to projected climate warming. Among endotherms, however, the relationship between climate variability and thermal physiology is less clear, particularly with regard to microclimate variation-small-scale differences within or between habitats. To address this gap, we explored associations between two sources of temperature variation (habitat type and vertical forest stratum) and (1) thermal physiological traits and (2) temperature sensitivity metrics within a diverse assemblage of Neotropical birds (n = 89 species). We used long-term temperature data to establish that daily temperature regimes in open habitats and forest canopy were both hotter and more variable than those in the forest interior and forest understory, respectively. Despite these differences in temperature regime, however, we found little evidence that species' thermal physiological traits or temperature sensitivity varied in association with either habitat type or vertical stratum. Our findings provide two novel and important insights. First, and in contrast to the supporting empirical evidence from ectotherms, the thermal physiology of birds at our study site appears to be largely decoupled from local temperature variation, providing equivocal support for the climate variability hypothesis in endotherms. Second, we found no evidence that the thermal physiology of understory forest birds differed from that of canopy or open-habitat species-an oft-invoked, yet previously untested, mechanism for why these species are so vulnerable to environmental change.

Ongoing introgression of a secondary sexual plumage trait in a stable avian hybrid zone.

Hybrid zones are dynamic systems where natural selection, sexual selection, and other evolutionary forces can act on reshuffled combinations of distinct genomes. The movement of hybrid zones, individual traits, or both are of particular interest for understanding the interplay between selective processes. In a hybrid zone involving two lek-breeding birds, secondary sexual plumage traits of Manacus vitellinus, including bright yellow collar and olive belly color, have introgressed asymmetrically ~50 km across the genomic center of the zone into populations more genetically similar to Manacus candei. Males with yellow collars are preferred by females and are more aggressive than parental M. candei, suggesting that sexual selection was responsible for the introgression of male traits. We assessed the spatial and temporal dynamics of this hybrid zone using historical (1989 - 1994) and contemporary (2017 - 2020) transect samples to survey both morphological and genetic variation. Genome-wide SNP data and several male phenotypic traits show that the genomic center of the zone has remained spatially stable, whereas the olive belly color of male M. vitellinus has continued to introgress over this time period. Our data suggest that sexual selection can continue to shape phenotypes dynamically, independent of a stable genomic transition between species.

Widespread Torpor Use in Hummingbirds from the Thermally Stable Lowland Tropics.

AbstractTorpor, the temporary reduction of metabolic rate and body temperature, is a common energy-saving strategy in endotherms. Because of their small body size and energetically demanding life histories, hummingbirds have proven useful for understanding when and why endotherms use torpor. Previous studies of torpor in hummingbirds have been largely limited to tropical montane species or long-distance migrants that regularly experience challenging thermal conditions. Comparatively little is known, however, about the use of torpor in hummingbirds of the lowland tropics, where relatively high and stable year-round temperatures may at least partially negate the need for torpor. To fill this knowledge gap, we tested for the occurrence of torpor in tropical lowland hummingbirds (n=37 individuals of six species) from central Panama. In controlled experimental conditions simulating the local temperature regime, all six species used torpor to varying degrees and entered torpor at high ambient temperatures (i.e., ≥28°C), indicating that hummingbirds from the thermally stable lowland tropics regularly use torpor. Torpor reduced overnight mass loss, with individuals that spent more time in torpor losing less body mass during temperature experiments. Body mass was the best predictor of torpor depth and duration among and within species-smaller species and individuals tended to use torpor more frequently and enter deeper torpor. Average mass loss in our experiments (∼8%-10%) was greater than that reported in studies of hummingbirds from higher elevation sites (∼4%). We therefore posit that the energetic benefits accrued from torpor may be limited by relatively high nighttime temperatures in the lowland tropics, although further studies are needed to test this hypothesis.

Multi-Year Comparison of Community- and Species-Level West Nile Virus Antibody Prevalence in Birds from Atlanta, Georgia and Chicago, Illinois, 2005-2016.

West Nile virus (WNV) is prevalent in the United States but shows considerable variation in transmission intensity. The purpose of this study was to compare patterns of WNV seroprevalence in avian communities sampled in Atlanta, Georgia and Chicago, Illinois during a 12-year period (Atlanta 2010-2016; Chicago 2005-2012) to reveal regional patterns of zoonotic activity of WNV. WNV antibodies were measured in wild bird sera using ELISA and serum neutralization methods, and seroprevalence among species, year, and location of sampling within each city were compared using binomial-distributed generalized linear mixed-effects models. Seroprevalence was highest in year-round and summer-resident species compared with migrants regardless of region; species explained more variance in seroprevalence within each city. Northern cardinals were the species most likely to test positive for WNV in each city, whereas all other species, on average, tested positive for WNV in proportion to their sample size. Despite similar patterns of seroprevalence among species, overall seroprevalence was higher in Atlanta (13.7%) than in Chicago (5%). Location and year of sampling had minor effects, with location explaining more variation in Atlanta and year explaining more variation in Chicago. Our findings highlight the nature and magnitude of regional differences in WNV urban ecology.

Wild birds and urban ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005-2010.

Bird-facilitated introduction of ticks and associated pathogens is postulated to promote invasion of tick-borne zoonotic diseases into urban areas. Results of a longitudinal study conducted in suburban Chicago, Illinois, USA, during 2005-2010 show that 1.6% of 6,180 wild birds captured in mist nets harbored ticks. Tick species in order of abundance were Haemaphysalis leporispalustris, Ixodes dentatus, and I. scapularis, but 2 neotropical tick species of the genus Amblyomma were sampled during the spring migration. I. scapularis ticks were absent at the beginning of the study but constituted the majority of ticks by study end and were found predominantly on birds captured in areas designated as urban green spaces. Of 120 ticks, 5 were infected with Borrelia burgdorferi, spanning 3 ribotypes, but none were infected with Anaplasma phagocytophilum. Results allow inferences about propagule pressure for introduction of tick-borne diseases and emphasize the large sample sizes required to estimate this pressure.

Pre-reproductive survival in a tropical bird and its implications for avian life histories.

The factors that affect survival until reproduction are essential to understanding the organization of life histories within and among species. Theory predicts, for example, that survival until reproduction influences the optimum level of reproductive investment by parents, which might partly explain prolonged parental care in species with high first-year survival. Tests and refinements of life-history theory have been hampered, however, by a lack of field-based estimates of pre-reproductive survival, especially for tropical species, which have been the subject of many comparative analyses. Tropical species are predicted to have higher first-year survival and delayed reproduction compared to Northern Hemisphere species. We estimated survival until reproduction, age at first reproduction, and sources of variation in juvenile survival in a Neotropical passerine, the Western Slaty-Antshrike (Thamnophilus atrinucha), in central Panama. We observed that fledged antshrikes had 76% survival through the dependent period and 48% survival to the age of 1 year; survival rate was lowest during the first week after leaving the nest. Timing of fledging within the breeding season, fledgling mass, and age at dispersal influenced survival, while sex of offspring and year did not. Individuals did not breed until two years of age, and post-fledging pre-reproductive survival was 41% of annual adult survival. High survival until reproduction in antshrikes balanced their low annual productivity, resulting in a stable population. Survival during the post-fledging period of dependence and the first year of independence in the Western Slaty-Antshrike exceeded estimates for Northern Hemisphere species. This difference appears to be associated with the extended post-fledging parental care, delayed dispersal, low costs of dispersal, and the less seasonal environment of antshrikes.

Early-life patterns of growth are linked to levels of phenotypic trait covariance and postfledging mortality across avian species.

Life history studies have established that trade-offs between growth and survival are common both within and among species. Identifying the factor(s) that mediate this trade-off has proven difficult, however, especially at the among-species level. In this study, we examined a series of potentially interrelated traits in a community of temperate-zone passerine birds to help understand the putative causes and consequences of variation in early-life growth among species. First, we examined whether nest predation risk (a proven driver of interspecific variation in growth and development rates) was correlated with species-level patterns of incubation duration and nestling period length. We then assessed whether proxies for growth rate covaried with mean trait covariance strength (i.e., phenotypic correlations ( rp), which can be a marker of early-life stress) among body mass, tarsus length, and wing length at fledging. Finally, we examined whether trait covariance strength at fledging was related to postfledging survival. We found that higher nest predation risk was correlated with faster skeletal growth and that our proxies for growth corresponded with increased trait covariance strength ( rp), which subsequently, correlated with higher mortality in the next life stage (postfledging period). These results provide an indication that extrinsic pressures (nest predation) impact rates of growth, and that there are costs of rapid growth across species, expressed as higher mean rp and elevated postfledging mortality. The link between higher levels of trait covariance at fledging and increased mortality is unclear, but increased trait covariance strength may reflect reduced phenotypic flexibility (i.e., phenotypic canalization), which may limit an organism's capacity for coping with environmental or ecological variability.

Cost-Reducing Traits for Agonistic Head Collisions: A Case for Neurophysiology.

Many animal species have evolved extreme behaviors requiring them to engage in repeated high-impact collisions. These behaviors include mating displays like headbutting in sheep and drumming in woodpeckers. To our knowledge, these taxa do not experience any notable acute head trauma, even though the deceleration forces would cause traumatic brain injury in most animals. Previous research has focused on skeletomuscular morphology, biomechanics, and material properties in an attempt to explain how animals moderate these high-impact forces. However, many of these behaviors are understudied, and most morphological or computational studies make assumptions about the behavior without accounting for the physiology of an organism. Studying neurophysiological and immune adaptations that covary with these behaviors can highlight unique or synergistic solutions to seemingly deleterious behavioral displays. Here, we argue that selection for repeated, high-impact head collisions may rely on a suite of coadaptations in intracranial physiology as a cost-reducing mechanism. We propose that there are three physiological systems that could mitigate the effects of repeated head trauma: (1) the innate neuroimmune response; (2) the glymphatic system, and (3) the choroid plexus. These systems are interconnected yet can evolve in an independent manner. We then briefly describe the function of these systems, their role in head trauma, and research that has examined how these systems may evolve to help reduce the cost of repeated, forceful head impacts. Ultimately, we note that little is known about cost-reducing intracranial mechanisms making it a novel field of comparative study that is ripe for exploration.

Corticosterone, testosterone and life-history strategies of birds.

Steroid hormones have similar functions across vertebrates, but circulating concentrations can vary dramatically among species. We examined the hypothesis that variation in titres of corticosterone (Cort) and testosterone (T) is related to life-history traits of avian species. We predicted that Cort would reach higher levels under stress in species with higher annual adult survival rates since Cort is thought to promote physiological and behavioural responses that reduce risk to the individual. Conversely, we predicted that peak T during the breeding season would be higher in short-lived species with high mating effort as this hormone is known to promote male fecundity traits. We quantified circulating hormone concentrations and key life-history traits (annual adult survival rate, breeding season length, body mass) in males of free-living bird species during the breeding season at a temperate site (northern USA) and a tropical site (central Panama). We analysed our original data by themselves, and also combined with published data on passerine birds to enhance sample size. In both approaches, variation in baseline Cort (Cort0) among species was inversely related to breeding season length and body mass. Stress-induced corticosterone (MaxCort) also varied inversely with body mass and, as predicted, also varied positively with annual adult survival rates. Furthermore, species from drier and colder environments exhibited lower MaxCort than mesic and tropical species; T was lowest in species from tropical environments. These findings suggest that Cort0, MaxCort and T modulate key vertebrate life-history responses to the environment, with Cort0 supporting energetically demanding processes, MaxCort promoting survival and T being related to mating success.

Linking snake behavior to nest predation in a Midwestern bird community.

Nest predators can adversely affect the viability of songbird populations, and their impact is exacerbated in fragmented habitats. Despite substantial research on this predator-prey interaction, however, almost all of the focus has been on the birds rather than their nest predators, thereby limiting our understanding of the factors that bring predators and nests into contact. We used radiotelemetry to document the activity of two snake species (rat snakes, Elaphe obsoleta; racers, Coluber constrictor) known to prey on nests in Midwestern bird communities and simultaneously monitored 300 songbird nests and tested the hypothesis that predation risk should increase for nests when snakes were more active and in edge habitat preferred by both snake species. Predation risk increased when rat snakes were more active, for all nests combined and for two of the six bird species for which we had sufficient nests to allow separate analyses. This result is consistent with rat snakes being more important nest predators than racers. We found no evidence, however, that nests closer to forest edges were at greater risk. These results are generally consistent with the one previous study that investigated rat snakes and nest predation simultaneously. The seemingly paradoxical failure to find higher predation risk in the snakes' preferred habitat (i.e., edge) might be explained by the snakes using edges at least in part for non-foraging activities. We propose that higher nest predation in fragmented habitats (at least that attributable to snakes) results indirectly from edges promoting larger snake populations, rather than from edges directly increasing the risk of nest predation by snakes. If so, the notion of edges per se functioning as ecological "traps" merits further study.

Hygric Niches for Tropical Endotherms.

Biotic selective pressures dominate explanations for the evolutionary ecology of tropical endotherms. Yet, abiotic factors, principally precipitation regimes, shape biogeographical and phenological patterns in tropical regions. Despite its importance, we lack a framework for understanding when, why, and how rain affects endotherms. Here, we review how tropical birds and mammals respond to rain at individual, population, and community levels, and propose a conceptual framework to interpret divergent responses. Diverse direct and indirect mechanisms underlie responses to rainfall, including physiological, top-down, and food-related drivers. Our framework constitutes a roadmap for the empirical studies required to understand the consequences of rainfall variability. Identifying the patterns and mechanisms underpinning responses to temporal variation in precipitation is crucial to anticipate consequences of anthropogenic climate change.

Avian host community structure and prevalence of West Nile virus in Chicago, Illinois.

Vertebrate host diversity has been postulated to mediate prevalence of zoonotic, vector-borne diseases, such that as diversity increases, transmission dampens. This "dilution effect" is thought to be caused by distribution of infective bites to incompetent reservoir hosts. We quantified avian species richness, avian seroprevalence for antibodies to West Nile virus (WNV), and infection of WNV in Culex mosquitoes, in the Chicago metropolitan area, Illinois, USA, a region of historically high WNV activity. Results indicated high overall avian seroprevalence and variation in seroprevalence across host species; however, there was no negative correlation between avian richness and Culex infection rate or between richness and infection status in individual birds. Bird species with high seroprevalence, especially northern cardinals and mourning doves, may be important sentinels for WNV in Chicago, since they were common and widespread among all study sites. Overall, our results suggest no net effect of increasing species richness to West Nile virus transmission in Chicago. Other intrinsic and extrinsic factors, such as variation in mosquito host preference, reservoir host competence, temperature, and precipitation, may be more important than host diversity for driving interannual variation in WNV transmission. These results from a fine-scale study call into question the generality of a dilution effect for WNV at coarser spatial scales.

Haemosporidian Parasite Infections In the Dickcissel ( Spiza americana): Prevalence and Costs.

Haemosporidian parasites are widespread in birds and are commonly used to evaluate ecological, evolutionary, and behavioral consequences of pathogen infection. While haemosporidian parasites may be important agents of selection, information on the incidence and outcomes of infection in many wild birds remains incomplete and warrants further inquiry. We examined the prevalence and costs of haemosporidian parasites in a wild population of dickcissels ( Spiza americana; n = 170) breeding in central Illinois. Over 2 breeding seasons, prevalence of haemosporidian parasites was 41% and was similar between sexes and years. Within each sex, there was no association between proxies of fitness (body condition and number of fledglings produced) and infection status. While we found no evidence that haemosporidian parasites have a direct, negative impact on dickcissels, we discuss how extra-pair paternity and changes across the life cycle of dickcissels and haemosporidian parasites may have masked or prevented detection of negative effects in our study. Ultimately our findings contribute to a growing literature providing improved clarity on how and when parasite infections can negatively impact wild host organisms and can aid in guiding future work examining such associations.

Interspecific associations between circulating antioxidant levels and life-history variation in birds.

Antioxidants play an important role in protecting tissues against aging-associated oxidative damage and are thus prime candidates for relating physiological mechanisms to variation in life histories. We measured total antioxidant capacity, antioxidant response to stress, and levels of uric acid, vitamin E, and four carotenoids in 95 avian species, mostly passerines from Michigan or Panama. We compared antioxidant measures to seven variables related to life histories (clutch size, survival rate, incubation period, nestling period, basal metabolic rate, body mass, and whether the species lived in a tropical or temperate climate). Life-history-related traits varied over at least three statistically independent axes. Higher antioxidant levels were generally characteristic of more rapid development, lower survival rate, smaller body size, larger clutch size, and higher mass-adjusted metabolic rate, but the relationships of particular antioxidants with individual life-history traits showed considerable complexity. Antioxidant-life history associations differed between tropical and temperate species and varied with respect to taxonomic sampling. Vitamin E showed few relationships with life-history traits. Overall, our results partly support the hypothesis that antioxidant levels evolve to mirror free radical production. Clearly, however, the complex patterns of physiological diversification observed here result from the interplay of many factors, likely including not just investment in somatic maintenance but also phylogenetic constraint, diet, and other aspects of ecology.