Wild Songbirds Research Articles

Response of wild songbirds to songs synthesized with a low-dimensional model.

In this work, we used a dynamical system derived from an avian vocal production model to generate synthetic songs that mimic the Zonotrichia capensis songs. We confirmed that these synthetic renditions elicited behavioral responses similar to those evoked by real songs in wild songbirds of the same species. Specifically, we observed an increase in the singing rate of individual birds when a playback device was introduced into their territories. The success of our approach instills confidence in the hypotheses underpinning the model and provides a valuable tool for investigating a wide range of biological questions.

Short-time exposure to light at night affects incubation patterns and correlates with subsequent body weight in great tits (Parus major).

Artificial light at night (ALAN) widely affects wildlife by blurring light-dark differences, including transitions such as sunrise and sunset, thereby affecting regulation of diel rhythms. As a result, activity onsets in many wild diurnal songbirds advance under ALAN. From chronobiological studies, it is known that the direction and strength of the response to light depends on when during the night exposure takes place. However, these experiments are mostly done under continuous light conditions, when animals have free-running rhythms. It remains unclear whether phase-dependence also holds in entrained, wild songbirds; i.e., does the effect of ALAN on activity patterns differ between exposure in the morning compared to the evening? This information is essential to assess the effects of mitigation measures by limiting ALAN to selected times of the night. We exposed incubating great tits (Parus major) inside the nest-box to 4 h of dim light, of which 1 h overlapped with dawn before sunrise or dusk after sunset. We found a small advancing effect of morning-light on activity onset and of evening-light on offset compared to dark controls but not vice versa. Breeding success and chick condition were unaffected by the light treatments. However, light-treated females had lower weights 9-18 days after the end of the treatment compared to the controls, independent of whether ALAN occurred in the morning or the evening, indicating possible costs of ALAN. Despite the weak behavioral response, ALAN might have affected the females' circadian clock or physiology resulting in lower body condition.

Human Salmonellosis Outbreak Linked to Salmonella Typhimurium Epidemic in Wild Songbirds, United States, 2020-2021.

Human Salmonellosis Outbreak Linked to Salmonella Typhimurium Epidemic in Wild Songbirds, United States, 2020-2021.

Screening H3 Histone Acetylation in a Wild Bird, the House Sparrow (Passer Domesticus).

Epigenetic mechanisms are increasingly understood to have major impacts across ecology. However, one molecular epigenetic mechanism, DNA methylation, currently dominates the literature. A second mechanism, histone modification, is likely important to ecologically relevant phenotypes and thus warrants investigation, especially because molecular interplay between methylation and histone acetylation can strongly affect gene expression. There are a limited number of histone acetylation studies on non-model organisms, yet those that exist show that it can impact gene expression and phenotypic plasticity. Wild birds provide an excellent system to investigate histone acetylation, as free-living individuals must rapidly adjust to environmental change. Here, we screen histone acetylation in the house sparrow (Passer domesticus); we studied this species because DNA methylation was important in the spread of this bird globally. This species has one of the broadest geographic distributions in the world, and part of this success is related to the way that it uses methylation to regulate its gene expression. Here, we verify that a commercially available assay that was developed for mammals can be used in house sparrows. We detected high variance in histone acetylation among individuals in both liver and spleen tissue. Further, house sparrows with higher epigenetic potential in the Toll Like Receptor-4 (TLR-4) promoter (i.e., CpG content) had higher histone acetylation in liver. Also, there was a negative correlation between histone acetylation in spleen and TLR-4 expression. In addition to validating a method for measuring histone acetylation in wild songbirds, this study also shows that histone acetylation is related to epigenetic potential and gene expression, adding a new study option for ecological epigenetics.

Human Salmonellosis Outbreak Linked to Salmonella Typhimurium Epidemic in Wild Songbirds, United States, 2020-2021.

Salmonella infection causes epidemic death in wild songbirds, with potential to spread to humans. In February 2021, public health officials in Oregon and Washington, USA, isolated a strain of Salmonella enterica serovar Typhimurium from humans and a wild songbird. Investigation by public health partners ultimately identified 30 illnesses in 12 states linked to an epidemic of Salmonella Typhimurium in songbirds. We report a multistate outbreak of human salmonellosis associated with songbirds, resulting from direct handling of sick and dead birds or indirect contact with contaminated birdfeeders. Companion animals might have contributed to the spread of Salmonella between songbirds and patients; the outbreak strain was detected in 1 ill dog, and a cat became ill after contact with a wild bird. This outbreak highlights a One Health issue where actions like regular cleaning of birdfeeders might reduce the health risk to wildlife, companion animals, and humans.

Variation in local population size predicts social network structure in wild songbirds.

The structure of animal societies is a key determinant of many ecological and evolutionary processes. Yet, we know relatively little about the factors and mechanisms that underpin detailed social structure. Among other factors, social structure can be influenced by habitat configuration. By shaping animal movement decisions, heterogeneity in habitat features, such as vegetation and the availability of resources, can influence the spatiotemporal distribution of individuals and subsequently key socioecological properties such as the local population size and density. Differences in local population size and density can impact opportunities for social associations and may thus drive substantial variation in local social structure. Here, we investigated spatiotemporal variation in population size at 65 distinct locations in a small songbird, the great tit (Parus major) and its effect on social network structure. We first explored the within-location consistency of population size from weekly samples and whether the observed variation in local population size was predicted by the underlying habitat configuration. Next, we created social networks from the birds' foraging associations at each location for each week and examined if local population size affected social structure. We show that population size is highly repeatable within locations across weeks and years and that some of the observed variation in local population size was predicted by the underlying habitat, with locations closer to the forest edge having on average larger population sizes. Furthermore, we show that local population size affected social structure inferred by four global network metrics. Using simple simulations, we then reveal that much of the observed social structure is shaped by social processes. Across different population sizes, the birds' social structure was largely explained by their preference to forage in flocks. In addition, over and above effects of social foraging, social preferences between birds (i.e. social relationships) shaped certain network features such as the extent of realized social connections. Our findings thus suggest that individual social decisions substantially contribute to shaping certain social network features over and above effects of population size alone.

Evidence of site-specific and male-biased germline mutation rate in a wild songbird.

Germline mutations are the ultimate source of genetic variation and the raw material for organismal evolution. Despite their significance, the frequency and genomic locations of mutations, as well as potential sex bias, are yet to be widely investigated in most species. To address these gaps, we conducted whole-genome sequencing of 12 great reed warblers (Acrocephalus arundinaceus) in a pedigree spanning three generations to identify single-nucleotide de novo mutations (DNMs) and estimate the germline mutation rate. We detected 82 DNMs within the pedigree, primarily enriched at CpG sites, but otherwise randomly located along the chromosomes. Furthermore, we observed a pronounced sex bias in DNM occurrence, with male warblers exhibiting three times more mutations than females. After correction for false negatives and adjusting for callable sites, we obtained a mutation rate of 7.16 × 10-9 mutations per site per generation (m/s/g) for the autosomes, and 5.10 × 10-9 m/s/g for the Z chromosome. To demonstrate the utility of species-specific mutation rates, we applied our autosomal mutation rate in models reconstructing the demographic history of the great reed warbler. We uncovered signs of drastic population size reductions pre-dating the last glacial period (LGP), and reduced gene flow between western and eastern populations during the LGP. In conclusion, our results provide one of the few direct estimates of the mutation rate in wild songbirds and evidence for male-driven mutations in accordance with theoretical expectations.

Active Warming of Open Cup Nests Reveals Contrasting Effects of Temperature on Development and Size in Wild Songbirds

Active Warming of Open Cup Nests Reveals Contrasting Effects of Temperature on Development and Size in Wild Songbirds

Drivers of passive leadership in wild songbirds: species-level differences and spatio-temporally dependent intraspecific effects

Collective behaviors are typical for many social species and can have fitness benefits for participating individuals. To maximize the benefits obtained from group living, individuals must coordinate their behaviors to some extent. What are the mechanisms that make certain individuals more likely to initiate collective behaviors, for example, by taking a risk to initially access a resource (i.e., to act as “leaders”)? Here, we examine leading behavior in a natural population of great tits and blue tits. We use automated feeding stations to monitor the feeder visits of tagged individuals within mixed-species flocks, with a small cost (waiting < 2 s) associated with the initial unlocking of the feeder. We find that great tits, males, and individuals with high activity levels were more likely to be leading in each of their feeder visits. Using a null model approach, we demonstrate that the effects of sex and activity on passive leading behavior can be explained by patterns of spatial and temporal occurrence. In other words, these effects can be explained by the times and locations of when individuals visit rather than the actual order of arrival. Hence, an analysis of the causes of leading behavior is needed to separate the effects of different processes. We highlight the importance of understanding the mechanisms behind leading behavior and discuss directions for future experimental work to gain a better understanding of the causes of leadership in natural populations.Significance statementMany species are social and engage in collective behaviors. To benefit from group actions, individuals need to fulfill different roles. Here, we examine leading behavior during feeding events; who feeds first when birds arrive at a resource? In mixed-species flocks of passerines, great tits (the larger and more dominant species), males, and individuals with higher levels of activity lead more often than blue tits, females, and individuals with lower levels of activity. While the species effect remains even when we control for the locations and dates of individual feeder visits, the effects of sex and activity are dependent on when and where birds choose to feed.

Ineffective humoral anti-tick IgY-response in birds: reaction against pathogen constituents?

Background: Variation in parasite burdens among hosts is typically related to differences in adaptive immunity. Comprehension of underlying mechanisms is hence necessary to gain better insights into endemic transmission cycles. Here we investigate whether wild songbirds that have never been exposed to ticks develop adaptive humoral immunity against endemic Ixodes ricinus ticks. Methods: Blue tits were exposed three times in succession to wild Ixodes ricinus ticks. For each infestation, serum samples were obtained. An enzyme-linked immunosorbent assay was developed, using tick salivary antigens, in order to quantify the bird's IgY response against ticks. In addition, at every sampling occasion the birds' body weight (corrected for body size) and haematocrit level was determined. Results: Individual IgY levels against the ticks' salivary proteins increased over three consecutive tick infestations, and large among-individual variation was observed. The responses were specifically directed against I. ricinus; cross-reactivity against the congeneric tree-hole tick Ixodes arboricola was negligibly low. IgY responses did not impinge on tick feeding success (engorgement weight and attachment success). Yet, those birds with the highest immune responses were more capable to reduce the acute harm (blood depletions) by compensating erythrocyte loss. Furthermore, at the end of the experiment, these birds had gained more body weight than birds with lower IgY levels. Conclusions: Latter observations can be considered as an effect of host quality and/or tolerance mechanisms. Birds anticipate the (future) costs of the activation of the immune system by ticks and/or ongoing tick-borne pathogen infections. Furthermore, although unsuccessful against tick feeding, the IgY responses may indirectly protect birds against tick-borne disease by acting against salivary protein secretions on which pathogens rely for transmission.

Ineffective humoral anti-tick IgY-response in birds: reaction against pathogen constituents?

Background:Variation in parasite burdens among hosts is typically related to differences in adaptive immunity. Comprehension of underlying mechanisms is hence necessary to gain better insights into endemic transmission cycles. Here we investigate whether wild songbirds that have never been exposed to ticks develop adaptive humoral immunity against endemicIxodes ricinusticks.Methods: Blue tits were exposed three times in succession to wildIxodes ricinusticks. For each infestation, serum samples were obtained. An enzyme-linked immunosorbent assay was developed, using tick salivary antigens, in order to quantify the bird’s IgY response against ticks. In addition, at every sampling occasion the birds’ body weight (corrected for body size) and haematocrit level was determined.Results:Individual IgY levels against the ticks’ salivary proteins increased over three consecutive tick infestations, and large among-individual variation was observed. The responses were specifically directed againstI. ricinus; cross-reactivity against the congeneric tree-hole tickIxodes arboricolawas negligibly low. IgY responses did not impinge on tick feeding success (engorgement weight and attachment success). Yet, those birds with the highest immune responses were more capable to reduce the acute harm (blood depletions) by compensating erythrocyte loss. Furthermore, at the end of the experiment, these birds had gained more body weight than birds with lower IgY levels.Conclusions:Latter observations can be considered as an effect of host quality and/or tolerance mechanisms. Birds anticipate the (future) costs of the activation of the immune system by ticks and/or ongoing tick-borne pathogen infections. Furthermore, although unsuccessful against tick feeding, the IgY responses may indirectly protect birds against tick-borne disease by acting against salivary protein secretions on which pathogens rely for transmission.

Feathers accurately reflect blood mercury at time of feather growth in a songbird

Methylmercury (MeHg) is a globally distributed pollutant that can negatively affect wildlife. Bird feathers are often used as a monitoring tool of contaminant exposure, but variability in total mercury (THg) content in flight feathers has raised concerns over their utility. The objective of this study was to quantify blood and feather THg depuration through the progression of primary feather molt in order to clarify the relationship between blood and feather mercury concentration, and test the reliability of feather THg measurements as a monitoring tool in wild songbirds. Song sparrows (Melospiza melodia) were experimentally exposed to dietary MeHg and their blood and primary feather THg concentrations were measured during exposure and post-exposure periods of three months each. A rapid decrease in feather and blood THg concentration through molt progression was observed. Primary feather THg content was higher in feathers grown during the MeHg exposure period compared to those grown during the post-exposure period. Primary feather THg concentration was highly correlated with blood THg measured at the time of feather growth (R = 0.98), indicating that, although THg concentration is variable among flight feathers, this reflects temporally sequential molting patterns and declining blood concentration during depuration. Primary flight feathers thus provide an accurate and useful tool for estimating the mercury burden of birds at the time a chosen feather was grown, and have the potential to be an effective and reliable biomonitoring tool for species with well-characterized molt patterns.

Physiological and genetic convergence supports hypoxia resistance in high-altitude songbirds.

Skeletal muscle plays a central role in regulating glucose uptake and body metabolism; however, highland hypoxia is a severe challenge to aerobic metabolism in small endotherms. Therefore, understanding the physiological and genetic convergence of muscle hypoxia tolerance has a potential broad range of medical implications. Here we report and experimentally validate a common physiological mechanism across multiple high-altitude songbirds that improvement in insulin sensitivity contributes to glucose homeostasis, low oxygen consumption, and relative activity, and thus increases body weight. By contrast, low-altitude songbirds exhibit muscle loss, glucose intolerance, and increase energy expenditures under hypoxia. This adaptive mechanism is attributable to convergent missense mutations in the BNIP3L gene, and METTL8 gene that activates MEF2C expression in highlanders, which in turn increases hypoxia tolerance. Together, our findings from wild high-altitude songbirds suggest convergent physiological and genetic mechanisms of skeletal muscle in hypoxia resistance, which highlights the potentially medical implications of hypoxia-related metabolic diseases.

Information use in foraging flocks of songbirds: no evidence for social transmission of patch quality

Animals use behavioural cues from others to make decisions in a variety of contexts. There is growing evidence, from a range of taxa, that information about the locations of food patches can spread through a population via social connections. However, it is not known whether information about their quality transmits similarly. We studied foraging behaviour in a population of wild songbirds with known social associations and tested whether flock members use social information about the profitability of patches to inform their foraging decisions. We provided artificial patches (ephemeral bird feeders) that appeared identical but were either profitable (contained food) or unprofitable (contained no food). If information about patch profitability spreads via social associations, we predicted that empty feeders would only be sampled by individuals that are less connected to each other than expected by chance. In contrast, we found that individuals recorded at empty feeders were more closely associated with each other than predicted by a null model simulating random arrival of individuals, mirroring a pattern of increased connectedness among individuals recorded at full feeders. We then simulated arrival under network-based diffusion of information and found that the observed pattern at both full and empty feeders matched predictions derived from this post hoc model. Our results suggest that foraging songbirds use social cues only about the location of potential food sources, but not their profitability. These findings agree with the hypothesis that individuals balance the relative economic costs of using different information, where the costs of personally sampling a patch upon arrival is low relative to the cost of searching for patches. This study extends previous work on information spread through animal social networks, by suggesting important links between how individuals use information at different stages of the acquisition process and the emerging patterns of patch use at the level of the population.

Eavesdropping on adult vocal interactions does not enhance juvenile song learning: an experiment with wild songbirds

Animals often live within close proximity of multiple conspecific individuals, allowing them to eavesdrop on other animals' signalling interactions to guide their own social behaviours. For a young animal that is learning to vocalize, eavesdropping on vocal interactions between adults may provide a rich source of information: young animals might preferentially learn vocalizations that are commonly heard in interactions between adults or that are heard to be effective for attracting mates or defending resources. We used a multispeaker playback experiment with wild Savannah sparrows, Passerculus sandwichensis , to test the hypothesis that vocal learning is guided by eavesdropping. Over a 6-year period, we tutored young Savannah sparrows with experimental tutor songs; half of the tutor songs were broadcast in simulated vocal interactions between two tutors, and the other half were broadcast as noninteractive, stand-alone solo performances. If eavesdropping plays an important role in guiding vocal learning, we predicted that young birds would preferentially learn the vocalizations heard during interactions between tutors. In contrast to our prediction, young Savannah sparrows did not preferentially learn interactive tutor songs; birds were similarly likely to learn songs heard in an interactive context ( N = 13) and in a noninteractive context ( N = 17). Analysis of live adult tutors' reactions to the loudspeakers showed that they responded with similar vocal behaviour during interactive and noninteractive treatments, and therefore their vocal behaviour did not compromise the playback simulation. We conclude that eavesdropping on vocal interactions between tutors does not appear to be essential for vocal learning of wild Savannah sparrows. • Animals that learn vocalizations may eavesdrop on interactions between tutors. • We used playback to study learning through eavesdropping in wild Savannah sparrows. • Birds learned songs at similar rates from interactive and noninteractive tutors. • Live tutors did not sing differently with interactive versus noninteractive tutors. • We found no evidence that eavesdropping guides vocal learning in Savannah sparrows.

Mercury Exposure and Altered Parental Nesting Behavior in a Wild Songbird.

Methylmercury is a neurotoxin and endocrine disruptor and may impair avian reproduction directly through embryotoxicity or by altering parental care behaviors. We studied mercury exposure and incubation behavior of free-living tree swallows ( Tachycineta bicolor) nesting in artificial nest boxes. Using small temperature dataloggers, we measured incubation constancy (the proportion of each day the female spent incubating eggs), the number of incubation recesses taken per day, and the duration of incubation recesses. We also assessed maternal mercury exposure by measuring mercury concentrations in both blood and eggs. Females with higher mercury concentrations exhibited lower incubation constancy, took more frequent and shorter incubation recesses, and were more likely to take incubation recesses that caused nest temperature decreases that were likely to slow embryonic development. Overall, females that laid eggs with the highest observed mercury concentration (0.53 μg/g fww) spent an average of 12% less time incubating their eggs over the 14-day incubation period than females that laid eggs with the lowest mercury concentration (0.07 μg/g fww). Because less time spent incubating can lower egg temperatures, slow embryonic development, and potentially lengthen the incubation period, these results suggest that environmentally relevant mercury concentrations may negatively influence reproduction by altering parental nesting behaviors of wild songbirds.

Diurnal variation in the production of vocal information about food supports a model of social adjustment in wild songbirds.

Wintering songbirds have been widely shown to make economic foraging decisions to manage the changing balance of risks from predation and starvation over the course of the day. In this study, we ask whether the communication and use of information about food availability differ throughout the day. First, we assessed temporal variation in food-related vocal information produced in foraging flocks of tits (Paridae) using audio recordings at radio-frequency identification-equipped feeding stations. Vocal activity was highest in the morning and decreased into the afternoon. This pattern was not explained by there being fewer birds present, as we found that group sizes increased over the course of the day. Next, we experimentally tested the underlying causes for this diurnal calling pattern. We set up bird feeders with or without playback of calls from tits, either in the morning or in the afternoon, and compared latency to feeder discovery, accumulation of flock members, and total number of birds visiting the feeder. Irrespective of time of day, playbacks had a strong effect on all three response measures when compared to silent control trials, demonstrating that tits will readily use vocal information to improve food detection throughout the day. Thus, the diurnal pattern of foraging behaviour did not appear to affect use and production of food-related vocalizations. Instead, we suggest that, as the day progresses and foraging group sizes increase, the costs of producing calls at the food source (e.g. competition and attraction of predators) outweigh the benefits of recruiting group members (i.e. adding individuals to large groups only marginally increases safety in numbers), causing the observed decrease in vocal activity into the afternoon. Our findings imply that individuals make economic social adjustments based on conditions of their social environment when deciding to vocally recruit group members.

Programmable Automated System for Songbird Ecobehavioral Research (PASSER): Using flexible computer-integrated feeders to conduct high resolution studies of environment-behavior dynamics in songbirds.

Field studies seeking to identify interactions between the environment and behaviors of wild songbirds are often restricted by time, labor, and accessibility of the site; hampering the collection of long‐term, high‐resolution data. Here, we describe the development, utilization, and initial results of a long‐term field study of wild songbird feeding patterns using data collected through an inexpensive microcomputer‐controlled automated feeder. Our studies indicate the “smart feeder” is capable of reliable and accurate data collection on feeding and behavioral metrics over long durations with relation to a wide range of environmental conditions. This enables detailed analysis of songbird's environment–behavior interactions. Our results have identified trends in environment–behavior interactions, microhabitat variations, species‐specific feeding profiles, and differences in the frequency and involvement of displacement events. Computerized feeders enabled us to address environment–behavior interactions, resulting in more detailed data than traditional observational methods. This reinforces conclusions from previous work regarding the potential for automated data collection to be adapted for a wide variety of research studies across the field of ethology.

GUT PARASITE LEVELS ARE ASSOCIATED WITH SEVERITY OF RESPONSE TO IMMUNE CHALLENGE IN A WILD SONGBIRD.

Life history trade-offs have been posited to shape wild animals' immune responses against microparasites (e.g., bacteria, viruses). However, coinfection with gut helminths may bias immune phenotypes away from inflammatory responses and could be another mechanism underlying variation in immune responses. We examined how the magnitude of a common and costly response to microparasites, the acute phase response (APR), varied with helminth coinfection at both the individual and the population levels in Song Sparrows ( Melospiza melodia). The APR includes fever and sickness behaviors, like lethargy and anorexia, and provides a whole-organism metric of immune activation. We combined data on fever and lethargy in response to an immune challenge (lipopolysaccharide) with postmortem data assessing helminth burdens and data on malarial parasite infection from blood samples in sparrows from two populations: southern California and western Washington, US. We predicted that birds with higher helminth burdens would express less severe APRs, at both the individual and population levels. Furthermore, we predicted that these reduced immune responses would diminish resistance against malarial parasites and would thus be associated with higher prevalences of such parasites. Previously, Song Sparrows from Washington have been shown to mount less severe APRs than those from California. In our study, Washington birds also exhibited higher helminth burdens and a higher prevalence of one type of avian malarial parasite. Because of low variation in helminth burdens in California (median=0, range=0-3), we tested within-population relationships only in birds from Washington, where the severity of fever and lethargy correlated negatively with helminth burden. These results suggested that helminth coinfection could help mediate immune responsiveness in wild songbirds.

Evaluating the role of wild songbirds or rodents in spreading avian influenza virus across an agricultural landscape.

BackgroundAvian influenza virus (AIV) infections occur naturally in wild bird populations and can cross the wildlife-domestic animal interface, often with devastating impacts on commercial poultry. Migratory waterfowl and shorebirds are natural AIV reservoirs and can carry the virus along migratory pathways, often without exhibiting clinical signs. However, these species rarely inhabit poultry farms, so transmission into domestic birds likely occurs through other means. In many cases, human activities are thought to spread the virus into domestic populations. Consequently, biosecurity measures have been implemented to limit human-facilitated outbreaks. The 2015 avian influenza outbreak in the United States, which occurred among poultry operations with strict biosecurity controls, suggests that alternative routes of virus infiltration may exist, including bridge hosts: wild animals that transfer virus from areas of high waterfowl and shorebird densities.MethodsHere, we examined small, wild birds (songbirds, woodpeckers, etc.) and mammals in Iowa, one of the regions hit hardest by the 2015 avian influenza epizootic, to determine whether these animals carry AIV. To assess whether influenza A virus was present in other species in Iowa during our sampling period, we also present results from surveillance of waterfowl by the Iowa Department of Natural Resources and Unites Stated Department of Agriculture.ResultsCapturing animals at wetlands and near poultry facilities, we swabbed 449 individuals, internally and externally, for the presence of influenza A virus and no samples tested positive by qPCR. Similarly, serology from 402 animals showed no antibodies against influenza A. Although several species were captured at both wetland and poultry sites, the overall community structure of wild species differed significantly between these types of sites. In contrast, 83 out of 527 sampled waterfowl tested positive for influenza A via qPCR.DiscussionThese results suggest that even though influenza A viruses were present on the Iowa landscape at the time of our sampling, small, wild birds and rodents were unlikely to be frequent bridge hosts.