Valerie A. O'Brien

An enzootic vector-borne virus is amplified at epizootic levels by an invasive avian host

Determining the effect of an invasive species on enzootic pathogen dynamics is critical for understanding both human epidemics and wildlife epizootics. Theoretical models suggest that when a naive species enters an established host–parasite system, the new host may either reduce (‘dilute’) or increase (‘spillback’) pathogen transmission to native hosts. There are few empirical data to evaluate these possibilities, especially for animal pathogens. Buggy Creek virus (BCRV) is an arthropod-borne alphavirus that is enzootically transmitted by the swallow bug (Oeciacus vicarius) to colonially nesting cliff swallows (Petrochelidon pyrrhonota). In western Nebraska, introduced house sparrows (Passer domesticus) invaded cliff swallow colonies approximately 40 years ago and were exposed to BCRV. We evaluated how the addition of house sparrows to this host–parasite system affected the prevalence and amplification of a bird-associated BCRV lineage. The infection prevalence in house sparrows was eight times that of cliff swallows. Nestling house sparrows in mixed-species colonies were significantly less likely to be infected than sparrows in single-species colonies. Infected house sparrows circulated BCRV at higher viraemia titres than cliff swallows. BCRV detected in bug vectors at a site was positively associated with virus prevalence in house sparrows but not with virus prevalence in cliff swallows. The addition of a highly susceptible invasive host species has led to perennial BCRV epizootics at cliff swallow colony sites. The native cliff swallow host confers a dilution advantage to invasive sparrow hosts in mixed colonies, while at the same sites house sparrows may increase the likelihood that swallows become infected.

Prevalence and Pathology of West Nile Virus in Naturally Infected House Sparrows, Western Nebraska, 2008

Nestling birds are rarely sampled in the field for most arboviruses, yet they may be important in arbovirus amplification cycles. We sampled both nestling and adult house sparrows (Passer domesticus) in western Nebraska for West Nile virus (WNV) or WNV-specific antibodies throughout the summer of 2008 and describe pathology in naturally infected nestlings. Across the summer, 4% of nestling house sparrows were WNV-positive; for the month of August alone, 12.3% were positive. Two WNV-positive nestlings exhibited encephalitis, splenomegaly, hepatic necrosis, nephrosis, and myocarditis. One nestling sparrow had large mural thrombi in the atria and ventricle and immunohistochemical staining of WNV antigen in multiple organs including the wall of the aorta and pulmonary artery; cardiac insufficiency thus may have been a cause of death. Adult house sparrows showed an overall seroprevalence of 13.8% that did not change significantly across the summer months. The WNV-positive nestlings and the majority of seropositive adults were detected within separate spatial clusters. Nestling birds, especially those reared late in the summer when WNV activity is typically greatest, may be important in virus amplification.

Phylogeographical structure and evolutionary history of two Buggy Creek virus lineages in the western Great Plains of North America

Buggy Creek virus (BCRV) is an unusual arbovirus within the western equine encephalitis complex of alphaviruses. Associated with cimicid swallow bugs (Oeciacus vicarius) as its vector and the cliff swallow (Petrochelidon pyrrhonota) and house sparrow (Passer domesticus) as its amplifying hosts, this virus is found primarily in the western Great Plains of North America at spatially discrete swallow nesting colonies. For 342 isolates collected in Oklahoma, Nebraska, Colorado and North Dakota, from 1974 to 2007, we sequenced a 2076 bp region of the 26S subgenomic RNA structural glycoprotein coding region, and analysed phylogenetic relationships, rates of evolution, demographical histories and temporal genetic structure of the two BCRV lineages found in the Great Plains. The two lineages showed distinct phylogeographical structure: one lineage was found in the southern Great Plains and the other in the northern Great Plains, and both occurred in Nebraska and Colorado. Within each lineage, there was additional latitudinal division into three distinct sublineages. One lineage is showing a long-term population decline. In comparing sequences taken from the same sites 8-30 years apart, in one case one lineage had been replaced by the other, and in the other cases there was little evidence of the same haplotypes persisting over time. The evolutionary rate of BCRV is in the order of 1.6-3.6x10(-4) substitutions per site per year, similar to that estimated for other temperate-latitude alphaviruses. The phylogeography and evolution of BCRV could be better understood once we determine the nature of the ecological differences between the lineages.

PATHOLOGY AND VIRUS DETECTION IN TISSUES OF NESTLING HOUSE SPARROWS NATURALLY INFECTED WITH BUGGY CREEK VIRUS (TOGAVIRIDAE)

Alphaviruses (Togaviridae) infect wild birds, but clinical illness and death attributable to virus in naturally infected birds is rarely reported, particularly for small passerine species or nestlings. Buggy Creek virus is a unique alphavirus in the Western equine encephalomyelitis virus (WEEV) complex that is vectored by the cimicid swallow bug (Oeciacus vicarius), an ectoparasite of the colonially nesting Cliff Swallow (Petrochelidon pyrrhonota) and the introduced House Sparrow (Passer domesticus). While sampling birds for Buggy Creek virus (BCRV) during the summers of 2007 and 2008, we discovered large numbers of clinically ill or dead House Sparrow nestlings. Ill nestlings exhibited ataxia, torticollis, paresis, and lethargy. Histologic examination revealed that encephalitis was the most common finding, followed by myositis, myocarditis, and hepatic changes, but pathology was highly variable. We isolated BCRV from brain tissue in most of the ill or dead nestlings, and from blood, liver, kidney, spleen, lung, feather pulp, and skin in some birds. To our knowledge, this is the first report of clinical illness, gross pathology, and histopathology for a WEEV-complex alphavirus in a field-collected passerine species.

Ecological divergence of two sympatric lineages of Buggy Creek virus, an arbovirus associated with birds

Most arthropod-borne viruses (arboviruses) show distinct serological subtypes or evolutionary lineages, with the evolution of different strains often assumed to reflect differences in ecological selection pressures. Buggy Creek virus (BCRV) is an unusual RNA virus (Togaviridae, Alphavirus) that is associated primarily with a cimicid swallow bug (Oeciacus vicarius) as its vector and the Cliff Swallow (Petrochelidon pyrrhonota) and the introduced House Sparrow (Passer domesticus) as its amplifying hosts. There are two sympatric lineages of BCRV (lineages A and B) that differ from each other by > 6% at the nucleotide level. Analysis of 385 BCRV isolates all collected from bug vectors at a study site in southwestern Nebraska, USA, showed that the lineages differed in their peak times of seasonal occurrence within a summer. Lineage A was more likely to be found at recently established colonies, at those in culverts (rather than on highway bridges), and at those with invasive House Sparrows, and in bugs on the outsides of nests. Genetic diversity of lineage A increased with bird colony size and at sites with House Sparrows, while that of lineage B decreased with colony size and was unaffected by House Sparrows. Lineage A was more cytopathic on mammalian cells than was lineage B. These two lineages have apparently diverged in their transmission dynamics, with lineage A possibly more dependent on birds and lineage B perhaps more a bug virus. The long-standing association between Cliff Swallows and BCRV may have selected for immunological resistance to the virus by swallows and thus promoted the evolution of the more bug-adapted lineage B. In contrast, the recent arrival of the introduced House Sparrow and its high competence as a BCRV amplifying host may be favoring the more bird-dependent lineage A.

Are Wild Birds Important in the Transport of Arthropod-borne Viruses?

Abstract.— The encephalitic arthropod-borne viruses (arboviruses) can cause a variety of serious human and wildlife diseases, including eastern equine encephalomyelitis, western equine encephalomyelitis, St. Louis encephalitis, Japanese encephalitis, and West Nile neuroinvasive disease. Understanding how these pathogens are dispersed through the environment is important both in managing their health-related impact and in interpreting patterns of their genetic variability over wide areas. Because many arboviruses infect wild birds and can be amplified to a level that makes birds infectious to insect vectors, numerous workers have suggested that the movements of migratory birds represent a major way that these viruses can be transported on a local, continental, and intercontinental scale. Virus transport by birds can, in theory, explain the colonization of new geographic regions by arboviruses, why some arboviruses in widely separated areas are genetically similar, and how arboviruses annually recur in temp...

Host-Seeking Mosquito Distribution in Habitat Mosaics of Southern Great Plains Cross-Timbers

ABSTRACT Landscape fragmentation often increases contact between humans, wildlife, and potential disease vectors. We examined how adult host-seeking mosquitoes respond to small-scale habitat differences within southern Great Plains cross-timber habitat mosaics in northern Oklahoma consisting of eastern red cedar (Juniperus virginianus L.) woodlands, mixed-deciduous woodlands, and adjacent grasslands. Mosquitoes responded most markedly to an overall grassland-woodland habitat gradient, with species separating by habitat based largely on tree density. Differences in abundance of host-seeking females occurred at fine spatial scales, sometimes varying dramatically over distances as little as 200 m when tree density changed abruptly. Tree type was not as important as tree density, although the West Nile virus vector Culex tarsalis Coquillett showed a greater affinity for areas containing eastern red cedar than for deciduous woodlands. The invasive Aedes albopictus Skuse showed equal affinity for both tree types. Conversion of grassland habitats in the Great Plains to more vegetated environments associated with humans (towns and homesteads) and the invasion of grasslands by eastern red cedar may change the species composition of mosquito, bird, and mammal assemblages and potentially alter arbovirus exposure for humans.

No Evidence for Spring Re-introduction of an Arbovirus by Cliff Swallows

Abstract We sampled 100 Cliff Swallows (Petrochelidon pyrrhonota), just after arrival in Nebraska breeding areas, to ascertain if migrating birds re-introduce Buggy Creek virus (BCRV; Togaviridae) to north-temperate localities in spring. Most birds sampled were previously banded and were known to have used parasite-free nesting colonies in past summers and/or were seronegative to BCRV; thus, they were unlikely to have been previously exposed to the virus in their breeding areas. None of the birds had evidence of viral RNA in blood, as measured by RT-PCR. These results are consistent with other studies that have shown little evidence that migratory birds re-introduce arboviruses to temperate localities between years.

Fluctuating survival selection explains variation in avian group size

Significance A characteristic feature of animal groups is extensive variation in size. Biologists have recognized that group size can often have profound effects on the fitness of individuals, and often certain group sizes afford greater short-term benefits than others. When individuals in some group sizes are less successful, what maintains pervasive variation in group sizes in nature remains a fundamental problem in behavioral biology. In colonial cliff swallows, survival advantages regularly fluctuate among group sizes over time. This study shows that changes in the direction and form of natural selection on colony size serve to maintain a wide range of group sizes and represents the first case, to our knowledge, in which the advantages and disadvantages of different group sizes regularly fluctuate in a natural vertebrate population. Most animal groups vary extensively in size. Because individuals in certain sizes of groups often have higher apparent fitness than those in other groups, why wide group size variation persists in most populations remains unexplained. We used a 30-y mark–recapture study of colonially breeding cliff swallows (Petrochelidon pyrrhonota) to show that the survival advantages of different colony sizes fluctuated among years. Colony size was under both stabilizing and directional selection in different years, and reversals in the sign of directional selection regularly occurred. Directional selection was predicted in part by drought conditions: birds in larger colonies tended to be favored in cooler and wetter years, and birds in smaller colonies in hotter and drier years. Oscillating selection on colony size likely reflected annual differences in food availability and the consequent importance of information transfer, and/or the level of ectoparasitism, with the net benefit of sociality varying under these different conditions. Averaged across years, there was no net directional change in selection on colony size. The wide range in cliff swallow group size is probably maintained by fluctuating survival selection and represents the first case, to our knowledge, in which fitness advantages of different group sizes regularly oscillate over time in a natural vertebrate population.

Group Size and Nest Spacing Affect Buggy Creek Virus (Togaviridae: Alphavirus) Infection in Nestling House Sparrows

The transmission of parasites and pathogens among vertebrates often depends on host population size, host species diversity, and the extent of crowding among potential hosts, but little is known about how these variables apply to most vector-borne pathogens such as the arboviruses (arthropod-borne viruses). Buggy Creek virus (BCRV; Togaviridae: Alphavirus) is an RNA arbovirus transmitted by the swallow bug (Oeciacus vicarius) to the cliff swallow (Petrochelidon pyrrhonota) and the introduced house sparrow (Passer domesticus) that has recently invaded swallow nesting colonies. The virus has little impact on cliff swallows, but house sparrows are seriously affected by BCRV. For house sparrows occupying swallow nesting colonies in western Nebraska, USA, the prevalence of BCRV in nestling sparrows increased with sparrow colony size at a site but decreased with the number of cliff swallows present. If one nestling in a nest was infected with the virus, there was a greater likelihood that one or more of its nest-mates would also be infected than nestlings chosen at random. The closer a nest was to another nest containing infected nestlings, the greater the likelihood that some of the nestlings in the focal nest would be BCRV-positive. These results illustrate that BCRV represents a cost of coloniality for a vertebrate host (the house sparrow), perhaps the first such demonstration for an arbovirus, and that virus infection is spatially clustered within nests and within colonies. The decreased incidence of BCRV in sparrows as cliff swallows at a site increased reflects the “dilution effect,” in which virus transmission is reduced when a vector switches to feeding on a less competent vertebrate host.