Lesley P. Bulluck

Factors Influencing Golden-Winged Warbler (Vermivora Chrysoptera) Nest-Site Selection and Nest Survival in the Cumberland Mountains of Tennessee

Abstract Studies of reproduction and habitat use are essential for any species assessment, especially for species with declining populations. We compared habitat in nest sites and randomly selected sites within Golden-winged Warbler (Vermivora chrysoptera) territories. We also modeled the effects of temporal and biotic factors on daily nest survival in relation to the constant-survival model. The percent cover of herbaceous vegetation was greater at nest sites, and that of woody vegetation was greater at non-nest sites. There was support for models with annual variation and a decline in nest survival throughout the nesting season, but the constant-survival model performed equally well. One parameter performed marginally better than the constant-survival model: nests with a woody stem in the substrate had lower nest-survival rates. We conclude that nest-site selection was nonrandom, such that females use specific criteria to select nest sites. However, habitat characteristics did not appear to significantly affect daily nest survival or, therefore, predation rates. Until factors that affect predation rates are better understood, conservation strategies that increase breeding habitat with specific nest-site features may be more successful than attempts to directly control nest survival.

Age-specific responses to spring temperature in a migratory songbird: older females attempt more broods in warmer springs

Increasing global temperature has led to an interest in plasticity in the timing of annual events; however, little is known about the demographic consequences of changing phenology. Annual reproductive success varies significantly among individuals within a population, and some of that variation has to do with the number of broods attempted by reproducing adults. In birds, female age and the timing of reproduction are often predictors of multiple breeding. We hypothesize that double brooding rates may be affected by spring temperature and that the response may vary with female age. We used a long-term reproductive data set for a migratory songbird, the prothonotary warbler (Protonotaria citrea) to assess which factors influence (a) an individual females probability of double brooding and (b) the annual variation in population-level double brooding rates. We found that older and earlier nesting birds are more likely to double brood, and that there is no evidence for senescence with regard to this trait such that the oldest females were most likely to double brood. Previous experience with double brooding (i.e., whether the female double brooded in the previous year) significantly increased the probability of doing so again. When assessing annual variation in the double brooding rate, we found an interaction between spring temperature and the proportion of older females in the population. Specifically, older females are more likely to double brood in years with warmer springs, but this relationship was not seen for younger females. Previous studies have shown that warmer temperatures lead to earlier and narrower peaks in resources and we hypothesize that these peaks are more available to older and earlier arriving females, enabling them to successfully raise more than one brood in a season. Understanding how different age classes respond to changing environmental conditions will be imperative to managing declining species.

Extensive Rangewide Mitochondrial Introgression Indicates Substantial Cryptic Hybridization in the Golden-winged Warbler ( Vermivora chrysoptera)

Widespread population declines of the Golden-winged Warbler (Vermivora chrysoptera) are thought to be due in part to hybridization with the expanding Blue-winged Warbler (V. pinus), which predictably replaces Golden-winged Warblers at breeding sites in which the two species come into contact. However, the mechanism by which this replacement occurs remains unresolved. Recent genetic work has indicated that, even in areas where the two species have been in contact for a short period, introgression of Blue-winged mitochondrial (mtDNA) and nuclear genes into Golden-winged individuals is common. To explore this process on a broader scale, we screened more than 750 individuals from nine U.S. states and three provinces to examine geographic patterns of mtDNA introgression. The only population in which all phenotypic Golden-winged Warblers had Golden-winged mtDNA haplotypes, and in which there are no breeding Blue-winged or hybrid individuals, was in the province of Manitoba, near the northwestern edge of the species’ breeding distribution. The near ubiquity of mitochondrial introgression suggests that there are far fewer genetically pure populations of Goldenwinged Warblers than previously believed, a finding with important implications for this threatened species. RÉSUMÉ. On pense que le déclin à grande échelle des populations de Paruline à ailes dorées (Vermivora chrysoptera) est en partie attribuable à son hybridation avec la Paruline à ailes bleues (V. pinus), laquelle est en expansion et remplace, comme on peut s’y attendre, la Paruline à ailes dorées aux sites de nidification où les deux espèces entrent en contact. Toutefois, le processus par lequel survient ce remplacement demeure inconnu. Des études génétiques récentes ont montré que, même aux endroits où les deux espèces n’ont été en contact que sur une courte période, l’introgression des gènes mitochondriaux (ADNmt) et nucléaires de la Paruline à ailes bleues chez les individus de Paruline à ailes dorées est commune. Pour explorer ce processus à plus grande échelle, nous avons procédé au criblage de plus de 750 individus provenant de neufs États des États-Unis et de trois provinces afin d’examiner les variations géographiques de l’introgression mitochondriale. La seule population dans laquelle toutes les Parulines à ailes dorées phénotypiques présentaient des haplotypes d’ADNmt de Paruline à ailes dorées, et dans laquelle il n’y avait pas d’individus nicheurs de Paruline à ailes bleues ni d’hybrides, se trouvait au Manitoba, près de la limite nord-ouest de l’aire de reproduction de l’espèce. La quasiomniprésence de l’introgression mitochondriale permet de croire qu’il y a beaucoup moins de populations génétiquement pures de Paruline à ailes dorées que ce qu’on pensait, une découverte significative pour cette espèce menacée.

Nesting Bird “Host Funnel” Increases Mosquito-Bird Contact Rate

ABSTRACT Increases in vector-host contact rates can enhance arbovirus transmission intensity. We investigated weekly fluctuations in contact rates between mosquitoes and nesting birds using the recently described Nest Mosquito Trap (NMT). The number of mosquitoes per nestling increased from <1 mosquito per trap night to 36.2 in the final 2 wk of the nesting season. Our evidence suggests the coincidence of the end of the avian nesting season and increasing mosquito abundances may have caused a “host funnel,” concentrating host-seeking mosquitoes to the few remaining nestlings. The relative abundance of mosquitoes collected by the NMT suggests that significantly more Aedes albopictus (Skuse) and Culex pipiens (L.) /restuans (Theobald) sought nesting bird bloodmeals than were predicted by their relative abundances in CO2-baited Centers for Disease Control and Prevention light and gravid traps. Culex salinarius (Coquillett) and Culex erraticus Dyar and Knab were collected in NMTs in proportion to their relative abundances in the generic traps. Temporal host funnels and nesting bird host specificity may enhance arbovirus amplification and explain observed West Nile virus and St. Louis encephalitis virus amplification periods.

Biotransport of Algal Toxins to Riparian Food Webs

The occurrence of harmful algal blooms has resulted in growing worldwide concern about threats to aquatic life and human health. Microcystin (MC), a cyanotoxin, is the most widely reported algal toxin in freshwaters. Prior studies have documented its presence in aquatic food webs including commercially important fish and shellfish. In this paper we present the first evidence that algal toxins propagate into riparian food webs. We show that MC is present in emerging aquatic insects (Hexagenia mayflies) from the James River Estuary and their consumers (Tetragnathidae spiders and Prothonotary Warblers, Protonotaria citrea). MC levels in Prothonotary Warblers varied by age class, with nestlings having the highest levels. At the site where nestlings received a higher proportion of aquatic prey (i.e., mayflies) in their diet, we observed higher MC concentrations in liver tissue and fecal matter. Warbler body condition and growth rate were not related to liver MC levels, suggesting that aquatic prey may provide dietary benefits that offset potential deleterious effects of the toxin. This study provides evidence that threats posed by algal toxins extend beyond the aquatic environments in which blooms occur.

Prothonotary warbler nestling growth and condition in response to variation in aquatic and terrestrial prey availability

Abstract Aquatic prey subsidies entering terrestrial habitats are well documented, but little is known about the degree to which these resources provide fitness benefits to riparian consumers. Riparian species take advantage of seasonal pulses of both terrestrial and aquatic prey, although aquatic resources are often overlooked in studies of how diet influences the reproductive ecology of these organisms. Ideally, the timing of resource pulses should occur at the time of highest reproductive demand. This study investigates the availability of aquatic (mayfly) and terrestrial (caterpillar) prey resources as well as the nestling diet of the prothonotary warbler (Protonotaria citrea) at two sites along the lower James River in Virginia during the 2014 breeding season. We found large differences in availability of prey items between the two sites, with one having significantly higher mayfly availability. Nestling diet was generally reflective of prey availability, and nestlings had faster mean growth rates at the site with higher aquatic prey availability. Terrestrial prey were fed more readily at the site with lower aquatic prey availability, and at this site, nestlings fed mayflies had higher mean growth rates than nestlings fed only terrestrial prey. Our results suggest that aquatic subsidies are an important resource for nestling birds and are crucial to understanding the breeding ecology of riparian species.

Nest Mosquito Trap quantifies contact rates between nesting birds and mosquitoes.

ABSTRACT: Accurate estimates of host-vector contact rates are required for precise determination of arbovirus transmission intensity. We designed and tested a novel mosquito collection device, the Nest Mosquito Trap (NMT), to collect mosquitoes as they attempt to feed on unrestrained nesting birds in artificial nest boxes. In the laboratory, the NMT collected nearly onethird of the mosquitoes introduced to the nest boxes. We then used these laboratory data to estimate our capture efficiency of field-collected bird-seeking mosquitoes collected over 66 trap nights. We estimated that 7.5 mosquitoes per trap night attempted to feed on nesting birds in artificial nest boxes. Presence of the NMT did not have a negative effect on avian nest success when compared to occupied nest boxes that were not sampled with the trap. Future studies using the NMT may elucidate the role of nestlings in arbovirus transmission and further refine estimates of nesting bird and vector contact rates.

Opportunistic conspecific brood parasitism in a box-nesting population of Prothonotary Warblers (Protonotaria citrea)

ABSTRACT Conspecific brood parasitism (CBP), although prevalent in some avian taxa, is easily overlooked when it occurs in low frequencies, and therefore the ecology of this behavior has only occasionally been described in passerines. We describe the occurrence of CBP in a population of Prothonotary Warblers (Protonotaria citrea) breeding in nest boxes, demonstrate associated fitness costs, and investigate parasite strategy. We genotyped individuals at 6 microsatellite loci and used Cervus software to determine log-likelihood of maternity (LOD scores) for offspring and social mothers. We set critical cutoff LOD scores at 95% confidence for exclusion of the social mother and assignment of a parasite mother from the breeding population. Of 805 nestlings (233 family groups during 2009–2013), we found that 12.7% had genotypes that were incompatible with their social mother. Females with unrelated nestlings (hosts) fledged fewer biological offspring within the host year than nonhost females despite fledging more total offspring, but being a host was not significantly associated with total reproductive success over 5 yr of breeding. We were able to identify only ∼30% of parasite females, which suggests that the majority of parasites may be floaters (i.e. non-nesters) in the population or nesting in nearby natural cavities. We found no evidence of host selection based on host age, arrival at the breeding site, or nest-box productivity in the previous year. This opportunistic behavior is likely facilitated by the nesting ecology of this population, in that nest sites are limited, conspicuous, and relatively dense. Future studies investigating CBP in populations using natural cavities can help elucidate the drivers of this behavior.

Vector Contact Rates on Eastern Bluebird Nestlings Do Not Indicate West Nile Virus Transmission in Henrico County, Virginia, USA

Sensitive indicators of spatial and temporal variation in vector-host contact rates are critical to understanding the transmission and eventual prevention of arboviruses such as West Nile virus (WNV). Monitoring vector contact rates on particularly susceptible and perhaps more exposed avian nestlings may provide an advanced indication of local WNV amplification. To test this hypothesis we monitored WNV infection and vector contact rates among nestlings occupying nest boxes (primarily Eastern bluebirds; Sialia sialis, Turdidae) across Henrico County, Virginia, USA, from May to August 2012. Observed host-seeking rates were temporally variable and associated with absolute vector and host abundances. Despite substantial effort to monitor WNV among nestlings and mosquitoes, we did not detect the presence of WNV in these populations. Generally low vector-nestling host contact rates combined with the negative WNV infection data suggest that monitoring transmission parameters among nestling Eastern bluebirds in Henrico County, Virginia, USA may not be a sensitive indicator of WNV activity.

Population trends in Vermivora warblers are linked to strong migratory connectivity

Significance Identifying drivers of population trends in migratory animals is difficult due to their reliance on different geographic regions throughout the annual cycle. Populations of Nearctic–Neotropical migratory birds are often thought to be limited by spatial variation in factors affecting reproduction and survival during the breeding season. We tracked individual songbirds from a two-species complex of New World warblers and discovered unequivocal evidence of a system in which strong associations between breeding areas and nonbreeding areas (i.e., migratory connectivity) is concordant with breeding population trends. The strong migratory connectivity we documented is associated with differential rates of land-use change in population-specific nonbreeding areas. Our results suggest that other migratory species with similar population trends may also exhibit strong migratory connectivity. Migratory species can experience limiting factors at different locations and during different periods of their annual cycle. In migratory birds, these factors may even occur in different hemispheres. Therefore, identifying the distribution of populations throughout their annual cycle (i.e., migratory connectivity) can reveal the complex ecological and evolutionary relationships that link species and ecosystems across the globe and illuminate where and how limiting factors influence population trends. A growing body of literature continues to identify species that exhibit weak connectivity wherein individuals from distinct breeding areas co-occur during the nonbreeding period. A detailed account of a broadly distributed species exhibiting strong migratory connectivity in which nonbreeding isolation of populations is associated with differential population trends remains undescribed. Here, we present a range-wide assessment of the nonbreeding distribution and migratory connectivity of two broadly dispersed Nearctic-Neotropical migratory songbirds. We used geolocators to track the movements of 70 Vermivora warblers from sites spanning their breeding distribution in eastern North America and identified links between breeding populations and nonbreeding areas. Unlike blue-winged warblers (Vermivora cyanoptera), breeding populations of golden-winged warblers (Vermivora chrysoptera) exhibited strong migratory connectivity, which was associated with historical trends in breeding populations: stable for populations that winter in Central America and declining for those that winter in northern South America.