Caroline R. Van Hemert

Epizootic of BEak DEformitiEs among WilD BirDs in alaska: an EmErging DisEasE in north amErica?

ABSTRACT. The sudden appearance of a large cluster of animals with gross abnormalities may signal a significant change in an ecosystem. We describe an unusual concentration of beak deformities that appear to have arisen rapidly within Alaska and now extend southward along the Pacific Coast. In Alaska we have documented 2,160 Black-capped Chickadees (Poecile atricapillus) and 435 individuals of 29 other species of birds, primarily during the past decade, with grossly overgrown and often crossed beaks. The annual prevalence of beak abnormalities among adult Black-capped Chickadees in south-central Alaska varied from 3.6% to 9.7% and averaged 6.5 ± 0.5% between 1999 and 2008. Only 0.05 ± 0.05% of nestlings and 0.3 ± 0.2% of juveniles <6 months old had abnormal beaks, which suggests that this is either a latent developmental or an acquired condition. We documented 80 cases in which a Black-capped Chickadee captured with an apparently normal beak was subsequently recaptured with a beak abnormality and 8 cases in which a beak deformity was no longer detectable upon recapture. Necropsy and histopathology of a sample of affected individuals provided no conclusive evidence of the etiology of this condition. Deformities appear to affect primarily the keratin layer of the beak and may result from abnormally rapid growth of the rhamphotheca. Some affected birds also exhibited lesions in other keratinized tissues of the skin, legs, feet, claws, and feathers, which may represent a systemic disorder or secondary conditions. Additional studies are currently underway to determine diagnostic signs and the underlying cause of this avian keratin disorder.

Beak Deformities in Northwestern Crows: Evidence of a Multispecies Epizootic

ABSTRACT. Beak abnormalities are rare among adult birds and, typically, are not widespread in a given population, within a region, or across multiple species. A high concentration of beak deformities was recently documented in Black-capped Chickadees (Poecile atricapillus) and other resident avian species in Alaska. We describe a parallel condition in Northwestern Crows (Corvus caurinus) that signals the emergence of a multispecies epizootic. On the basis of 186 Northwestern Crows captured at six sites in Alaska during 2007 and 2008, we estimated the prevalence of beak deformities in adults to be 16.9 ± 5.3%, the highest rate of gross deformities ever recorded in a wild bird population. Prevalence varied among sites and was as high as 36% on the Kenai Peninsula, which suggests possible epizootic clusters. We also documented beak abnormalities in an additional 148 Northwestern Crows in south-central and southeastern Alaska and in 64 crows near Vancouver, British Columbia, and Puget Sound, Washington, a region where both Northwestern Crows and American Crows (C. brachyrhynchos) occur. The increase in frequency and distribution of crows observed with abnormal beaks throughout the Pacific Northwest since the late 1990s indicates a geographic expansion of this problem. Affected crows exhibited elongated and often crossed beaks that were morphologically similar to deformities documented in Black-capped Chickadees and other species in Alaska over approximately the same period. Additional research is needed to determine the etiology and potential adverse effects on bird populations affected by this disorder.

Wildlife health in a rapidly changing North: focus on avian disease

Climate‐related environmental changes have increasingly been linked to emerging infectious diseases in wildlife. The Arctic is facing a major ecological transition that is expected to substantially affect animal and human health. Changes in phenology or environmental conditions that result from climate warming may promote novel species assemblages as host and pathogen ranges expand to previously unoccupied areas. Recent evidence from the Arctic and subarctic suggests an increase in the spread and prevalence of some wildlife diseases, but baseline data necessary to detect and verify such changes are still lacking. Wild birds are undergoing rapid shifts in distribution and have been implicated in the spread of wildlife and zoonotic diseases. Here, we review evidence of current and projected changes in the abundance and distribution of avian diseases and outline strategies for future research. We discuss relevant climatic and environmental factors, emerging host–pathogen contact zones, the relationship between host condition and immune function, and potential wildlife and human health outcomes in northern regions.

Evidence of accelerated beak growth associated with avian keratin disorder in black-capped chickadees (Poecile atricapillus)

We recently documented an epizootic of beak deformities in more than 2,000 Black-capped Chickadees (Poecile atricapillus) and other wild bird species in North America. This emerging avian disease, which has been termed avian keratin disorder, results in gross overgrowth of the rhamphotheca, the outer, keratinized layer of the beak. To test the hypothesis that the beak deformities characteristic of this disorder are associated with accelerated keratin production, we measured rates of beak growth and wear in affected Black-capped Chickadees (n=16) and a control sample of unaffected chickadees (n=14) collected from south-central (61°09′–61°38′N, 149°11′–149°48′W) and interior Alaska (64°51′–64°53′N, 147°49′–147°59′W). Rates of absolute growth were 50–100% higher in affected birds than they were in control birds and exceeded records from other passerine species. These results suggest that abnormally rapid epidermal growth is the primary physical mechanism by which beak deformities develop and are maintained in affected chickadees. Although beak overgrowth typically worsened over time, differential patterns of wear influenced the severity and morphology of deformities. In some cases, the effects of accelerated keratin growth were partially mitigated by frequent breakage of rhamphothecal tips. However, mortalities occurred in 9 of 16 birds (56%) with beak deformities during the study, suggesting that avian keratin disorder results in severe health consequences for affected birds. Additional study of factors that control beak keratin production is needed to understand the pathogenesis of this debilitating disease in wild birds.

Microanatomy of Passerine Hard-Cornified Tissues: Beak and Claw Structure of the Black-capped Chickadee (Poecile atricapillus)

The microanatomy of healthy beaks and claws in passerine birds has not been well described in the literature, despite the importance of these structures in avian life. Histological processing of hard‐cornified tissues is notoriously challenging and only a few reports on effective techniques have been published. An emerging epizootic of beak deformities among wild birds in Alaska and the Pacific Northwest region of North America recently highlighted the need for additional baseline information about avian hard‐cornified structures. In this study, we examine the beak and claw of the Black‐capped Chickadee (Poecile atricapillus), a common North American passerine that is affected by what has been described as “avian keratin disorder.” We use light and scanning electron microscopy and high‐magnification radiography to document the healthy microanatomy of these tissues and identify features of functional importance. We also describe detailed methods for histological processing of avian hard‐cornified structures and discuss the utility of special stains. Results from this study will assist in future research on the functional anatomy and pathology of hard‐cornified structures and will provide a necessary reference for ongoing investigations of avian keratin disorder in Black‐capped Chickadees and other wild passerine species.

Microbial Infections Are Associated with Embryo Mortality in Arctic-Nesting Geese

ABSTRACT To address the role of bacterial infection in hatching failure of wild geese, we monitored embryo development in a breeding population of Greater white-fronted geese (Anser albifrons) on the Arctic Coastal Plain of Alaska. During 2013, we observed mortality of normally developing embryos and collected 36 addled eggs for analysis. We also collected 17 infertile eggs for comparison. Using standard culture methods and gene sequencing to identify bacteria within collected eggs, we identified a potentially novel species of Neisseria in 33 eggs, Macrococcus caseolyticus in 6 eggs, and Streptococcus uberis and Rothia nasimurium in 4 eggs each. We detected seven other bacterial species at lower frequencies. Sequences of the 16S rRNA genes from the Neisseria isolates most closely matched sequences from N. animaloris and N. canis (96 to 97% identity), but phylogenetic analysis suggested substantial genetic differentiation between egg isolates and known Neisseria species. Although definitive sources of the bacteria remain unknown, we detected Neisseria DNA from swabs of eggshells, nest contents, and cloacae of nesting females. To assess the pathogenicity of bacteria identified in contents of addled eggs, we inoculated isolates of Neisseria, Macrococcus, Streptococcus, and Rothia at various concentrations into developing chicken eggs. Seven-day mortality rates varied from 70 to 100%, depending on the bacterial species and inoculation dose. Our results suggest that bacterial infections are a source of embryo mortality in wild geese in the Arctic.

Novel Picornavirus Associated with Avian Keratin Disorder in Alaskan Birds

ABSTRACT Avian keratin disorder (AKD), characterized by debilitating overgrowth of the avian beak, was first documented in black-capped chickadees (Poecile atricapillus) in Alaska. Subsequently, similar deformities have appeared in numerous species across continents. Despite the widespread distribution of this emerging pathology, the cause of AKD remains elusive. As a result, it is unknown whether suspected cases of AKD in the afflicted species are causally linked, and the impacts of this pathology at the population and community levels are difficult to evaluate. We applied unbiased, metagenomic next-generation sequencing to search for candidate pathogens in birds affected with AKD. We identified and sequenced the complete coding region of a novel picornavirus, which we are calling poecivirus. Subsequent screening of 19 AKD-affected black-capped chickadees and 9 control individuals for the presence of poecivirus revealed that 19/19 (100%) AKD-affected individuals were positive, while only 2/9 (22%) control individuals were infected with poecivirus. Two northwestern crows (Corvus caurinus) and two red-breasted nuthatches (Sitta canadensis) with AKD-consistent pathology also tested positive for poecivirus. We suggest that poecivirus is a candidate etiological agent of AKD. IMPORTANCE Avian keratin disorder (AKD) is an increasingly common disease of wild birds. This disease, characterized by beak overgrowth, was first described in the late 1990s and has been spreading rapidly both geographically and in terms of host species affected. AKD decreases host fitness and can be fatal. However, the cause of the disease has remained elusive, and its impact on host populations is poorly understood. We found a novel and divergent picornavirus in 19/19 AKD-affected black-capped chickadees that we examined but in only 2/9 control cases. We also found this virus in 4 individuals of 2 other passerine species that exhibited symptoms consistent with AKD. Our data suggest that this novel picornavirus warrants further investigation as the causative agent of AKD. Avian keratin disorder (AKD) is an increasingly common disease of wild birds. This disease, characterized by beak overgrowth, was first described in the late 1990s and has been spreading rapidly both geographically and in terms of host species affected. AKD decreases host fitness and can be fatal. However, the cause of the disease has remained elusive, and its impact on host populations is poorly understood. We found a novel and divergent picornavirus in 19/19 AKD-affected black-capped chickadees that we examined but in only 2/9 control cases. We also found this virus in 4 individuals of 2 other passerine species that exhibited symptoms consistent with AKD. Our data suggest that this novel picornavirus warrants further investigation as the causative agent of AKD.

Stable Isotopes Identify Dietary Changes Associated with Beak Deformities in Black-Capped Chickadees (Poecile atricapillus)

ABSTRACT. A large number of beak deformities of unknown etiology have recently been reported in Black-capped Chickadees (Poecile atricapillus) and other resident avian species in Alaska. We investigated the potential association between diet and beak deformities. We analyzed carbon (&dgr;13C) and nitrogen (&dgr;15N) isotopes in whole blood of Black-capped Chickadees captured at three semiurban sites in south-central Alaska. For dietary analysis, we included natural foods (arthropods, seeds, and berries) and anthropogenic items commonly provided in bird feeders (sunflower seeds, peanut butter, and suet). Blood samples from individuals with beak deformities exhibited lower &dgr;15N values and more variable &dgr;13C values than birds with normal beaks. Isotopic values of blood also differed by location for both carbon and nitrogen, but we did not detect a difference in natural dietary items across the three sites. Contributions of individual diet items differed between birds with and without beak deformities, a pattern that likely reflected reduced function of the beak. Affected birds generally consumed fewer arthropods and sunflower seeds and more peanut butter and natural seeds and berries. Although some individuals with beak deformities relied heavily on feeder foods, we did not find evidence of an anthropogenic food source shared by all affected birds. In addition, dietary differences were most pronounced for moderately to severely affected birds, which suggests that these differences are more likely to be a consequence than a cause of deformities.

Avian malaria in a boreal resident species: long-term temporal variability, and increased prevalence in birds with avian keratin disorder

The prevalence of vector-borne parasitic diseases is widely influenced by biological and ecological factors. Environmental conditions such as temperature and precipitation can have a marked effect on haemosporidian parasites (Plasmodium spp.) that cause malaria and those that cause other malaria-like diseases in birds. However, there have been few long-term studies monitoring haemosporidian infections in birds in northern latitudes, where weather conditions can be highly variable and the effects of climate change are becoming more pronounced. We used molecular methods to screen more than 2,000 blood samples collected from black-capped chickadees (Poecile atricapillus), a resident passerine bird. Samples were collected over a 10 year period, mostly during the non-breeding season, at seven sites in Alaska, USA. We tested for associations between Plasmodium prevalence and local environmental conditions including temperature, precipitation, site, year and season. We also evaluated the relationship between parasite prevalence and individual host factors of age, sex and presence or absence of avian keratin disorder. This disease, which causes accelerated keratin growth in the beak, provided a natural study system in which to test the interaction between disease state and malaria prevalence. Prevalence of Plasmodium infection varied by year, site, age and individual disease status but there was no support for an effect of sex or seasonal period. Significantly, birds with avian keratin disorder were 2.6 times more likely to be infected by Plasmodium than birds without the disorder. Interannual variation in the prevalence of Plasmodium infection at different sites was positively correlated with summer temperatures at the local but not statewide scale. Sequence analysis of the parasite cytochrome b gene revealed a single Plasmodium spp. lineage, P43. Our results demonstrate associations between prevalence of avian malaria and a variety of biological and ecological factors. These results also provide important baseline data that will be informative for predicting future changes in Plasmodium prevalence in the subarctic.

A Natural Experiment on the Condition-Dependence of Achromatic Plumage Reflectance in Black-Capped Chickadees

Honest advertisement models posit that only individuals in good health can produce and/or maintain ornamental traits. Even though disease has profound effects on condition, few studies have experimentally tested its effects on trait expression and even fewer have identified a mechanistic basis for these effects. Recent evidence suggests that black and white, but not grey, plumage colors of black-capped chickadees (Poecile atricapillus) are sexually selected. We therefore hypothesized that birds afflicted with avian keratin disorder, a condition that affects the beak and other keratinized tissues, would show reduced expression of black and white, but not grey, color. UV-vis spectrometry of black-capped chickadees affected and unaffected by avian keratin disorder revealed spectral differences between them consistent with this hypothesis. To elucidate the mechanistic bases of these differences, we used scanning electron microscopy (SEM), electron-dispersive x-ray spectroscopy (EDX) and a feather cleaning experiment. SEM showed extreme feather soiling in affected birds, and EDX revealed that this was most likely from external sources. Experimentally cleaning the feathers increased color expression of ornamental feathers of affected, but not unaffected, birds. These data provide strong evidence that black and white color is an honest indicator in chickadees, and that variation in feather dirtiness, likely due to differences in preening behavior is a mechanism for this association.