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.     

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.     

Predation by ants controls swallow bug (Hemiptera: Cimicidae: Oeciacus vicarius) infestations

The swallow bug (Oeciacus vicarius) is the only known vector for Buggy Creek virus (BCRV), an alphavirus that circulates in cliff swallows (Petrochelidon pyrrhonota) and house sparrows (Passer domesticus) in North America. We discovered ants (Crematogaster lineolata and Formica spp.) preying on swallow bugs at cliff swallow colonies in western Nebraska, U.S.A. Ants reduced the numbers of visible bugs on active swallow nests by 74‐90%, relative to nests in the same colony without ants. Ant predation on bugs had no effect on the reproductive success of cliff swallows inhabiting the nests where ants foraged. Ants represent an effective and presumably benign way of controlling swallow bugs at nests in some colonies. They may constitute an alternative to insecticide use at sites where ecologists wish to remove the effects of swallow bugs on cliff swallows or house sparrows. By reducing bug numbers, ant presence may also lessen BCRV transmission at the spatial foci (bird colony sites) where epizootics occur. The effect of ants on swallow bugs should be accounted for in studying variation among sites in vector abundance.     

Parasites favour intermediate nestling mass and brood size in cliff swallows

A challenge of life‐history theory is to explain why animal body size does not continue to increase, given various advantages of larger size. In birds, body size of nestlings and the number of nestlings produced (brood size) have occasionally been shown to be constrained by higher predation on larger nestlings and those from larger broods. Parasites also are known to have strong effects on life‐history traits in birds, but whether parasitism can be a driver for stabilizing selection on nestling body size or brood size is unknown. We studied patterns of first‐year survival in cliff swallows (Petrochelidon pyrrhonota) in western Nebraska in relation to brood size and nestling body mass in nests under natural conditions and in those in which hematophagous ectoparasites had been removed by fumigation. Birds from parasitized nests showed highest first‐year survival at the most common, intermediate brood‐size and nestling‐mass categories, but cliff swallows from nonparasitized nests had highest survival at the heaviest nestling masses and no relationship with brood size. A survival analysis suggested stabilizing selection on brood size and nestling mass in the presence (but not in the absence) of parasites. Parasites apparently favour intermediate offspring size and number in cliff swallows and produce the observed distributions of these traits, although the mechanisms are unclear. Our results emphasize the importance of parasites in life‐history evolution.     

The incidence of American swallow bugs (Oeciacus vicarius) in barn swallow (Hirundo rustica) colonies in northeast Texas

The American swallow bug (Oeciacus vicarius) is an important ectoparasite of cliff swallows (Petrochelidon pyrrhonota) and is known to harbor several types of arbovirus. A recent study in northeast Texas suggested that O. vicarius might occur in barn swallows (Hirundo rustica) at rates much higher than previously thought. The purpose of this study was to determine the extent to which barn swallows in northeast Texas are parasitized by O. vicarius and how well this parasite is adapting to this novel host. A sample of 498 nests at 54 colonies was inspected for O. vicarius. Forty colonies (74.1%) were infected, while 310 nests (62.2%) were infected. Large colonies were more likely to be infected than small colonies. Colonies that also contained cliff swallows were more likely to be infected than colonies without cliff swallows. Infection levels in barn swallow nests were comparable to those reported for cliff swallows, though age and sex class ratios differed. Demographic changes among swallow species, including range expansions, increased colony sizes, and more frequent interspecific nesting associations have likely facilitated the movement of O. vicarius from the cliff swallow into a novel host, the barn swallow.     

Nest spacing in relation to settlement time in colonial cliff swallows

How colonial animals space their nests in relation to conspecifics may provide clues as to whether coloniality provides net benefits or occurs only because breeding sites are limited. We examined how nearest-neighbour distance varied in relation to settlement time in the highly colonial cliff swallow, Petrochelidon pyrrhonota, comparing observed nearest-neighbour distances to those expected if birds spread out to maximize nest spacing. Cliff swallows generally settled closer to each other than required by the available substrate, and clustered their nests closer in large colonies than in small ones. The first settlers at a colony site spaced themselves further apart than later arrivals but did not maximize nearest-neighbour distances. The first arrivals maintained greater nest spacing throughout the season than did birds that arrived later. Colony size and amount of nesting substrate had no effect on initial settlement distances of the first arrivals, but eventual nearest-neighbour distances declined with colony size. First arrivals may gain less from nesting with conspecifics and thus are less likely to cluster their nests than later arrivals, which may often be young or na?ve birds that gain more from the social benefits of colonial nesting. The results are consistent with the presumed social advantages cliff swallows receive from coloniality and do not support the hypothesis that colonies result from nesting site limitation. Copyright 2000 The Association for the Study of Animal Behaviour.     

Ectoparasites cause increased bilateral asymmetry of naturally selected traits in a colonial bird

Abstract Parasitism has been shown to correlate with levels of bilateral symmetry in some organisms, with more asymmetric individuals often having more parasites. However, few studies have shown experimentally that parasitism directly causes increased asymmetry. By fumigating some cliff swallow (Petrochelidon pyrrhonota) colonies and leaving others untreated, we investigated experimentally whether ectoparasitism by the cimicid swallow bug led to higher levels of asymmetry in length of wings, outer tail feathers, and tarsus among juvenile and adult birds. Juveniles from fumigated colonies measured soon after fledging had significantly less asymmetry in wing and outer tail length than juveniles from nonfumigated colonies; asymmetry in tarsus length was unaffected by parasitism. Adults that had undergone one or more post‐juvenal molts on the wintering grounds showed no differences in asymmetry between those reared in fumigated vs. nonfumigated colonies. These results show that ectoparasitism directly leads to increased feather asymmetry in cliff swallows, probably through parasite‐induced nutritional stress. Because wing and tail asymmetry impair flight performance and reduce foraging efficiency, the increased asymmetry caused by parasites represents a fitness cost to cliff swallows. This is among the few experimental studies to show an effect of parasites on asymmetry of naturally selected characters.     

Phylogenetic analysis of Buggy Creek virus: evidence for multiple clades in the Western Great Plains, United States of America

We present the first detailed phylogenetic analysis of Buggy Creek virus (BCRV), a poorly known alphavirus with transmission cycles involving a cimicid swallow bug (Oeciacus vicarius) vector and cliff swallows (Petrochelidon pyrrhonota) and house sparrows (Passer domesticus) as the principal avian hosts. Nucleotide sequences of a 2,075-bp viral envelope glycoprotein-coding region, covering the entire PE2 gene, were determined for 33 BCRV isolates taken from swallow bugs at cliff swallow colonies in Nebraska and Colorado in the summer of 2001 and were compared with the corresponding region of BCRV isolates collected from Oklahoma in the 1980s. We also analyzed isolates of the closely related Fort Morgan virus (FMV) collected from Colorado in the 1970s. Phylogenetic analysis indicated that BCRV falls into the western equine encephalomyelitis complex of alphaviruses, in agreement with antigenic results and a previous alphavirus phylogeny based on the E1 coding region. We found four distinct BCRV/FMV clades, one each unique to Nebraska, Colorado, and Oklahoma and one containing isolates from both Nebraska and Colorado. BCRV isolates within the two clades from Nebraska showed 5.7 to 6.2% nucleotide divergence and 0.7 to 1.9% amino acid divergence, and within these clades, we found multiple subclades. Nebraska subclades tended to be confined to one or a few cliff swallow colonies that were close to each other in space, although in some cases, near-identical isolates were detected at sites up to 123 km apart. Viral gene flow occurs when cliff swallows move (bugs) between colony sites, and the genetic structure of BCRV may reflect the limited dispersal abilities of its insect vector.     

Arbovirus infection increases with group size

Buggy Creek (BCR) virus is an arthropod-borne alphavirus that is naturally transmitted to its vertebrate host the cliff swallow (Petrochelidon pyrrhonota) by an invertebrate vector, namely the cimicid swallow bug (Oeciacus vicarius). We examined how the prevalence of the virus varied with the group size of both its vector and host. The study was conducted in southwestern Nebraska where cliff swallows breed in colonies ranging from one to 3700 nests and the bug populations at a site vary directly with the cliff swallow colony size. The percentage of cliff swallow nests containing bugs infected with BCR virus increased significantly with colony size at a site in the current year and at the site in the previous year. This result could not be explained by differences in the bug sampling methods, date of sampling, sample size of the bugs, age structure of the bugs or the presence of an alternate host, the house sparrow (Passer domesticus). Colony sites that were reused by cliff swallows showed a positive autocorrelation in the percentage of nests with infected bugs between year t and year t+1, but the spatial autocorrelation broke down for year t+2. The increased prevalence of BCR virus at larger cliff swallow colonies probably reflects the larger bug populations there, which are less likely to decline in size and lead to virus extinction. To the authors' knowledge this is the first demonstration of arbovirus infection increasing with group size and one of the few known predictive ecological relationships between an arbovirus and its vectors/hosts. The results have implications for both understanding the fitness consequences of coloniality for cliff swallows and understanding the temporal and spatial variation in arboviral epidemics.     

Immune Responses of a Native and an Invasive Bird to Buggy Creek Virus (Togaviridae: Alphavirus) and Its Arthropod Vector,the Swallow Bug (Oeciacus vicarius)

Invasive species often display different patterns of parasite burden and virulence compared to their native counterparts. These differences may be the result of variability in host-parasite co-evolutionary relationships, the occurrence of novel host-parasite encounters, or possibly innate differences in physiological responses to infection between invasive and native hosts. Here we examine the adaptive, humoral immune responses of a resistant, native bird and a susceptible, invasive bird to an arbovirus (Buggy Creek virus; Togaviridae: Alphavirus) and its ectoparasitic arthropod vector (the swallow bug; Oeciacus vicarius). Swallow bugs parasitize the native, colonially nesting cliff swallow (Petrochelidon pyrrhonota) and the introduced house sparrow (Passer domesticus) that occupies nests in cliff swallow colonies. We measured levels of BCRV-specific and swallow bug-specific IgY levels before nesting (prior to swallow bug exposure) and after nesting (after swallow bug exposure) in house sparrows and cliff swallows in western Nebraska. Levels of BCRV-specific IgY increased significantly following nesting in the house sparrow but not in the cliff swallow. Additionally, house sparrows displayed consistently higher levels of swallow bug-specific antibodies both before and after nesting compared to cliff swallows. The higher levels of BCRV and swallow bug specific antibodies detected in house sparrows may be reflective of significant differences in both antiviral and anti-ectoparasite immune responses that exist between these two avian species. To our knowledge, this is the first study to compare the macro- and microparasite-specific immune responses of an invasive and a native avian host exposed to the same parasites.     

Phylogenetic Analysis of Buggy Creek Virus: Evidence for Multiple Clades in the Western Great Plains, United States of America

We present the first detailed phylogenetic analysis of Buggy Creek virus (BCRV), a poorly known alphavirus with transmission cycles involving a cimicid swallow bug (Oeciacus vicarius) vector and cliff swallows (Petrochelidon pyrrhonota) and house sparrows (Passer domesticus) as the principal avian hosts. Nucleotide sequences of a 2,075-bp viral envelope glycoprotein-coding region, covering the entire PE2 gene, were determined for 33 BCRV isolates taken from swallow bugs at cliff swallow colonies in Nebraska and Colorado in the summer of 2001 and were compared with the corresponding region of BCRV isolates collected from Oklahoma in the 1980s. We also analyzed isolates of the closely related Fort Morgan virus (FMV) collected from Colorado in the 1970s. Phylogenetic analysis indicated that BCRV falls into the western equine encephalomyelitis complex of alphaviruses, in agreement with antigenic results and a previous alphavirus phylogeny based on the E1 coding region. We found four distinct BCRV/FMV clades, one each unique to Nebraska, Colorado, and Oklahoma and one containing isolates from both Nebraska and Colorado. BCRV isolates within the two clades from Nebraska showed 5.7 to 6.2% nucleotide divergence and 0.7 to 1.9% amino acid divergence, and within these clades, we found multiple subclades. Nebraska subclades tended to be confined to one or a few cliff swallow colonies that were close to each other in space, although in some cases, near-identical isolates were detected at sites up to 123 km apart. Viral gene flow occurs when cliff swallows move (bugs) between colony sites, and the genetic structure of BCRV may reflect the limited dispersal abilities of its insect vector.     

Heritable choice of colony size in cliff swallows: does experience trump genetics in older birds?

The variation in breeding-colony size seen in populations of most colonial birds may reflect heritable choices made by individuals who are phenotypically specialized for particular social environments. Although a few studies have reported evidence for genetically based choice of group sizes in birds, we know relatively little about the extent to which animals potentially rely on experience versus innate preferences in deciding with how many conspecifics to settle at different times of their lives. We conducted a cross-fostering experiment in 1997-1998 on cliff swallows (Petrochelidon pyrrhonota) in southwestern Nebraska, USA, in which some individuals were reared in colonies different in size from those in which they were born. Breeding-colony sizes chosen by this cohort of birds were monitored by mark-recapture throughout their lives. A multistate mark-recapture analysis revealed that birds in their first breeding year chose colony sizes similar to those of their birth, regardless of their rearing environment, confirming a previous analysis. Beyond the first breeding year, however, cliff swallows' colony choice was less dependent on where they were born. Birds born in small colonies and reared in large colonies showed evidence of a delayed rearing effect, with these birds overwhelmingly choosing large colonies in later years. Heritabilities suggested strong genetic effects on first-year colony choice but not in later years. Cliff swallows' genetically based colony-size preferences their first year could be a way to ensure matching of their phenotype to an appropriate social environment as yearlings. In later years, familiarity with particular colony sites and available information on site quality may override innate group-size preferences when birds choose colonies.     

南充金腰燕、家燕繁殖生态比较及易卵易雏实验

2004年3～10月对四川南充地区家燕、金腰燕的繁殖生态进行了观察,比较了其繁殖生态习性及雏鸟的生长特性,进行了家燕、金腰燕之间的易卵易雏实验.结果表明,家燕于2月中旬迁入南充,9月中旬开始迁离;金腰燕迁来较家燕晚,2月底～3月初迁入,9月中旬迁离.家燕于4月初产卵;金腰燕在4月上旬产卵.金腰燕卵的各项量衡度均较家燕的大,出壳时金腰燕雏鸟体重也比家燕雏鸟稍重.金腰燕雏鸟的体长、翅长、尾长、外部器官及体重的增长较家燕的快.而易卵、易雏的金腰燕雏鸟增长曲线则在金腰燕和家燕的雏鸟之间.易卵易雏的实验表明,在孵卵和育雏过程中,金腰燕与家燕之间彼此互换卵可以接受,易换雏鸟也可以接受.     

Testis size increases with colony size in cliff swallows

By using a sample of over 800 male cliff swallows (Petrochelidonpyrrhonota) that died during a rare climatic event in our Nebraskastudy area in 1996, we investigated how testis size was relatedto body size, age, parasite load, a bird's past colony-sizehistory, and spleen size. Testis volume increased with bodysize. After correcting for body size, testis volume was lowestfor birds age 1 and 2 years but did not vary with age for males3 years old or more. Birds occupying parasite-free (fumigated)colonies had significantly larger testes than did birds at nonfumigatedsites. Testis volume increased significantly with the size ofthe breeding colonies a bird had used in the past. Testis volumehad no relationship with spleen volume after correcting forbody size. The results show within a species that larger testesare favored in more social environments, probably reflectinga response to increased rates of extrapair copulation (and thussperm competition) among cliff swallows in large colonies. Thepresence of ectoparasites, by inflating levels of plasma corticosterone,may in turn reduce testis mass. These data provide no supportfor the hypothesis that large testes, perhaps by producing moretestosterone, are immunosuppressive and thus costly for thatreason.     

Nest predation and the evolution of nestling begging calls

Begging by nestling birds can be conspicuous and loud. Such displays are thought to function in signalling nestling condition and securing parental care, but they also may inadvertently attract the attention of predators. We compared the structure of nestling begging calls to the risk of predation among 24 species of birds breeding in a forest community in central Arizona. After controlling for body size and phylogeny, we found that species subject to greater nest predation had calls with higher frequency (pitch) and lower amplitude (loudness) than species subject to lower rates of nest predation. As these acoustic features make it difficult for potential predators to pinpoint the source of a sound, our results suggest that an increased risk of predation has led to the evolution of begging calls that minimize locatability. The relationship between call structure and the risk of predation also supports the hypothesis that attracting predators is a direct cost of begging and that such costs can constrain any evolutionary escalation in the intensity of nestling begging.     

Ecological and phenological covariates of offspring sex ratio in barn swallows

Non-random sex allocation in relation to parental, ecological and phenological factors has been investigated in several correlational studies of birds, mostly based on few breeding seasons and relatively small sample sizes, which have led to different results. We investigated sex ratio of nestling barn swallows (Hirundo rustica) in relation to adult sex ratio, laying date, clutch size, colony size and meteorological conditions in a sample of 553 broods (>2200 nestlings) during 10 years. At the population level, nestling sex ratio varied among years and deviated from parity in two years. Sex ratio among adults did not predict offspring sex ratio in the current or the following year. At the within-family level, the proportion of sons increased with laying date in large clutches, did not vary among clutches of intermediate size, and tended to decline with laying date in small clutches. Large colonies harbored more sons. The proportion of males increased with temperature during laying whereas the effects of temperature during the pre- or post-laying periods and that of rainfall were non-significant. These patterns of variation of offspring sex ratio did not differ between years. Thus, we identified several potential causal sources of variation in barn swallow offspring sex ratio, including temporal, phenological and ecological factors. The observation of an association of offspring sex with temperature during laying is novel for birds and may be mediated by effects on maternal steroid hormones profile. The ecological and evolutionary implications of present findings are discussed in the light of adaptive sex allocation theory.     

Effects of livestock farming on birds of rural areas in Europe

In the last decades, profound modifications of agricultural practices occurred in Europe, including the introduction of modern livestock farming. These modifications negatively affected the fauna of rural areas, as indicated by the large demographic declines suffered by several populations of birds typical of these habitats. The impact of agricultural practices on bird populations has been widely investigated, while the effect of livestock farming has seldom been assessed. To fill this gap, we carried out a quantitative meta-analysis of the existing scientific literature and evaluated the size of the effects of livestock farming on birds of rural areas in Europe. We only found 26 papers on this topic, from which 72 effect sizes could be estimated. The barn swallow (Hirundo rustica) was the species on which most studies focused. Livestock farming positively influenced presence and distribution of barn swallows in breeding habitats, while it did not significantly affect reproduction of this species. Effects on other bird species typical of rural habitats were non-significant. The positive effect on the insectivorous barn swallow might be mediated by the enhanced insect abundance where livestock is reared. In addition, habitat features typical of rural settings where livestock is reared (e.g. cattle-sheds or large hayfields) positively affected barn swallows independently of actual presence of livestock at a setting. Presence of livestock at rural setting therefore seems beneficial to barn swallows, but not significantly to other bird species typical of rural habitats. The effect of livestock farming on birds of rural habitats has been under-investigated to date.     

Barn swallows prefer to nest at sites hidden from neighboring nests within a loose colony

Some loosely colonial species scatter their nests within a colony. Most studies on mechanisms that generate such scattered nests within a colony have primarily focused on the measurement of distance related to the intensity of interactions among conspecific neighbors. However, these interactions can change not only with distance between nests but also with other factors. In particular, whether the nest is hidden from neighbors can strongly affect the intensity of interaction for birds that usually use sight for communication. To show the possible benefit of nesting at sites hidden from neighboring nests, we studied the nest arrangements and settlement patterns within a barn swallow colony. We tested whether the swallows prefer nesting at sites hidden from neighboring nests in cattle barns that are often used as colony sites by the swallows in Japan. We found that the sides of ceiling beams hidden from neighbors were preferred as nesting sites. A randomization test suggested that the rectangular sections occupied by swallows were not spaced out within a colony. The results suggested that the swallows preferred nesting sites hidden from their neighbors and did not space out their nests within a colony. This paper also refutes intraspecific brood parasitism as a plausible function of this behavior.     

Host and vector movement affects genetic diversity and spatial structure of Buggy Creek virus (Togaviridae)

Determining the degree of genetic variability and spatial structure of arthropod-borne viruses (arboviruses) may help in identifying where strains that potentially cause epidemics or epizootics occur. Genetic diversity in arboviruses is assumed to reflect relative mobility of their vertebrate hosts (and invertebrate vectors), with highly mobile hosts such as birds leading to genetic similarity of viruses over large areas. There are no empirical studies that have directly related host or vector movement to virus genetic diversity and spatial structure. Using the entire E2 glycoprotein-coding region of 377 Buggy Creek virus isolates taken from cimicid swallow bugs (Oeciacus vicarius), the principal invertebrate vector for this virus, we show that genetic diversity between sampling sites could be predicted by the extent of movement by transient cliff swallows (Petrochelidon pyrrhonota) between nesting colonies where the virus and vectors occur. Pairwise F(ST) values between colony sites declined significantly with increasing likelihood of a swallow moving between those sites per 2-day interval during the summer nesting season. Sites with more bird movement between them had virus more similar genetically than did pairs of sites with limited or no bird movement. For one virus lineage, Buggy Creek virus showed greater haplotype and nucleotide diversity at sites that had high probabilities of birds moving into or through them during the summer; these sites likely accumulated haplotypes by virtue of frequent virus introductions by birds. Cliff swallows probably move Buggy Creek virus by transporting infected bugs on their feet. The results provide the first empirical demonstration that genetic structure of an arbovirus is strongly associated with host/vector movement, and suggest caution in assuming that bird-dispersed arboviruses always have low genetic differentiation across different sites.