Parasite exchange and hybridisation at a wild-feral-domestic interface.

Interactions between wild, feral, and domestic animals are of economic and conservation significance. The pigeon Columba livia is a synanthropic species in a feral form, but it also includes the rare Rock Dove. Columba livia is an important player at the wild-domestic interface, acting as a carrier of avian diseases, and the feral form threatens Rock Doves with extinction via hybridisation. Despite its abundance, little is known about drivers of disease prevalence in C. livia, or how disease and hybridisation represent synergistic threats to Rock Doves. We focused on infection by the parasite Trichomonas, first collating prevalence estimates in domestic and free-living populations from relevant studies of C. livia. Second, we characterised variation in the diversity and prevalence of Trichomonas among three C. livia populations in the United Kingdom: a feral, a Rock Dove, and a feral-wild hybrid population. Across multiple continents, free-living pigeons had lower Trichomonas infection than captive conspecifics, but the effect was weak. Environmental factors which could impact Trichomonas infection status did not explain variation in infection among populations. Among the British populations, strain diversity varied, and there was lower parasite prevalence in Rock Doves than feral pigeons. Individual infection status was not explained by the available covariates, including hybrid score and site. The drivers of Trichomonas prevalence are unclear, perhaps due to idiosyncratic local-scale drivers. However, given the population-level variation in both infection prevalence and introgressive hybridisation, the potential combined effects could accelerate the extinction of the Rock Dove. Further study of the synergistic effects of multiple types of biotic interactions at the wild-feral-domestic interface is warranted, especially where vagile, globally distributed and superabundant animals are involved.

Bird species with wider geographical ranges have higher blood parasite diversity but not prevalence across the African-Eurasian flyway.

Avian blood parasites, from the genera Plasmodium, Haemoproteus and Leucocytozoon, are predicted to alter their range and prevalence as global temperatures change, and host and vector ranges shift. Understanding large-scale patterns in the prevalence and diversity of avian malaria and malaria-like parasites is important due to an incomplete understanding of their effects in the wild, where studies suggest even light parasitaemia can potentially cause rapid mortality, especially in naïve populations. We conducted phylogenetically controlled analyses to test for differences in prevalence and lineage diversity of haemoparasite infection (for Plasmodium, Haemoproteus and Leucocytozoon) in and between resident and migratory species along the African-Eurasian flyway. To test whether migratory strategy or range size drives differences in parasite prevalence and diversity between resident and migrant species, we included three categories of resident species: Eurasian only (n = 36 species), African only (n = 41), and species resident on both continents (n = 17), alongside intercontinental migrants (n = 64), using a subset of data from the MalAvi database comprising 27,861 individual birds. We found that species resident on both continents had a higher overall parasite diversity than all other categories. Eurasian residents had lower Plasmodium diversity than all other groups, and both migrants and species resident on both continents had higher Haemoproteus diversity than both African and Eurasian residents. Leucocytozoon diversity did not differ between groups. Prevalence patterns were less clear, with marked differences between genera. Both Plasmodium and Leucocytozoon prevalence was higher in species resident on both continents and African residents than in migrants and Eurasian residents. Haemoproteus prevalence was lower in Eurasian residents than species resident on both continents. Our findings contrast with previous findings in the North-South American flyway, where long-distance migrants had higher parasite diversity than residents and short-distance migrants, although we found contrasting patterns for parasite diversity to those seen for parasite prevalence. Crucially, our results suggest that geographic range may be more important than migratory strategy in driving parasite diversity within species along the African-Palaearctic flyway. Our findings differ between the three parasite genera included in our analysis, suggesting that vector ecology may be important in determining these large-scale patterns. Our results add to our understanding of global patterns in parasite diversity and abundance, and highlight the need to better understand the influence of vector ecology to understand the drivers of infection risk and predict responses to environmental change.

Epidemiology of protozoan and helminthic parasites in wild passerine birds of Britain and Ireland.

Avian endoparasites play important roles in conservation, biodiversity and host evolution. Currently, little is known about the epidemiology of intestinal helminths and protozoans infecting wild birds of Britain and Ireland. This study aimed to determine the rates of parasite prevalence, abundance and infection intensity in wild passerines. Fecal samples (n = 755) from 18 bird families were collected from 13 sites across England, Wales and Ireland from March 2020 to June 2021. A conventional sodium nitrate flotation method allowed morphological identification and abundance estimation of eggs/oocysts. Associations with host family and age were examined alongside spatiotemporal and ecological factors using Bayesian phylogenetically controlled models. Parasites were detected in 20.0% of samples, with corvids and finches having the highest prevalences and intensities, respectively. Syngamus (33%) and Isospora (32%) were the most prevalent genera observed. Parasite prevalence and abundance differed amongst avian families and seasons, while infection intensity varied between families and regions. Prevalence was affected by diet diversity, while abundance differed by host age and habitat diversity. Infection intensity was higher in birds using a wider range of habitats, and doubled in areas with feeders present. The elucidation of these patterns will increase the understanding of parasite fauna in British and Irish birds.

Evidence for strain-specific virulence of Trichomonas gallinae in African columbiformes.

Infection by parasites or pathogens can have marked physiological impacts on individuals. In birds, infection may affect moult and feather growth, which is an energetically demanding time in the annual cycle. Previous work has suggested a potential link between clinically visible Trichomonas gallinae infection and wing length in turtle doves Streptopelia turtur arriving on breeding grounds. First, T. gallinae infection was characterized in 149 columbids from 5 species, sampled on turtle dove wintering grounds in Senegal during the moulting period, testing whether infection by T. gallinae is linked to moult. Trichomonas gallinae prevalence was 100%, so rather than testing for differences between infected and uninfected birds, we tested for differences in moult progression between birds infected by different T. gallinae strains. Twelve strains of T. gallinae were characterized at the internal transcribed spacer 1 (ITS1)/5.8S/ITS2 region, of which 6 were newly identified within this study. In turtle doves only, evidence for differences in wing length by strain was found, with birds infected by strain Tcl-1 having wings nearly 6 mm longer than those infected with strain GEO. No evidence was found for an effect of strain identity within species on moult progression, but comparisons between infected and uninfected birds should be further investigated in species where prevalence is lower.

Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur.

Understanding the frequency, spatiotemporal dynamics and impacts of parasite coinfections is fundamental to developing control measures and predicting disease impacts. The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high-throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron-hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%-100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within-host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite-induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations.

Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome.

Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host-microbe interactions.

High prevalence of the neonicotinoid clothianidin in liver and plasma samples collected from gamebirds during autumn sowing.

Since neonicotinoid insecticides were introduced to the agricultural market, evidence of the negative impacts of these systemic compounds on non-target species has accumulated. Birds are one of the largest groups of species to inhabit farmland, but the extent of neonicotinoid exposure in avian communities is poorly understood and very little is known about how any exposure may affect wild birds. Here, free-living gamebirds were used as a model group to measure the extent of avian exposure to the neonicotinoid clothianidin via seed treatment. During a typical sowing period of winter cereals treated with clothianidin, blood and liver samples were collected simultaneously from individual hunted gamebird carcasses, both pre- (n = 18) and post-sowing (n = 57) and were analysed for clothianidin via LC/MS-MS. Body weight, fat score and faecal parasite load were also quantified in the birds to ascertain whether any of these health parameters were associated with clothianidin exposure under field conditions. Clothianidin was detected in 6% of individuals sampled pre-sowing and 89% of individuals sampled post-sowing. The frequency of clothianidin detection in plasma samples and the concentration of clothianidin in liver and plasma samples decreased significantly between the first week and 2-4 weeks post-sowing. Faecal parasite load was positively associated with concentrations of clothianidin in the liver (but not plasma) of partridge species, but there was no association between clothianidin concentration and fat score or body weight, for either sample type. This study provides clear evidence that treated seed is a source of pesticide exposure for gamebirds following autumn sowing. These findings have implications for gamebirds worldwide where seed treatments are in use, and will aid the design of any future avian biomonitoring studies for agrochemical compounds.

From seeds to plasma: Confirmed exposure of multiple farmland bird species to clothianidin during sowing of winter cereals.

Neonicotinoids are the largest group of systemic insecticides worldwide and are most commonly applied as agricultural seed treatments. However, little is known about the extent to which farmland birds are exposed to these compounds during standard agricultural practices. This study uses winter cereal, treated with the neonicotinoid clothianidin, as a test system to examine patterns of exposure in farmland birds during a typical sowing period. The availability of neonicotinoid-treated seed was recorded post-sowing at 39 fields (25 farms), and camera traps were used to monitor seed consumption by wild birds in situ. The concentration of clothianidin in treated seeds and crop seedlings was measured via liquid chromatography-tandem mass spectrometry, and avian blood samples were collected from 11 species of farmland bird from a further six capture sites to quantify the prevalence and level of clothianidin exposure associated with seed treatments. Neonicotinoid-treated seeds were found on the soil surface at all but one of the fields surveyed at an average density of 2.8 seeds/m2. The concentration of clothianidin in seeds varied around the target application rate, whilst crop seedlings contained on average 5.9% of the clothianidin measured in seeds. Exposure was confirmed in 32% of bird species observed in treated fields and 50% of individual birds post-sowing; the median concentration recorded in positive samples was 12 ng/mL. Results here provide clear evidence that a variety of farmland birds are subject to neonicotinoid exposure following normal agricultural sowing of neonicotinoid-treated cereal seed. Furthermore, the widespread availability of seeds at the soil surface was identified as a primary source of exposure. Overall, these data are likely to have global implications for bird species and current agricultural policies where neonicotinoids are in use, and may be pertinent to any future risk assessments for systemic insecticide seed treatments.

Using long-term datasets to assess the impacts of dietary exposure to neonicotinoids on farmland bird populations in England.

Over the last 20 years, a new group of systemic insecticides-the neonicotinoids-has gained prominence in arable systems, and their application globally has risen year on year. Previous modelling studies using long-term data have suggested that neonicotinoid application has had a detrimental impact on bird populations, but these studies were either limited to a single species or neglected to analyse specific exposure pathways in conjunction with observed population trends. Using bird abundance data, neonicotinoid usage records and cropping data for England at a 5x5 km resolution, generalised linear mixed models were used to test for spatio-temporal associations between neonicotinoid use and changes in the populations of 22 farmland bird species between 1994 and 2014, and to determine whether any associations were explained by dietary preferences. We assigned farmland bird species to three categories of dietary exposure to neonicotinoids based on literature data for species diets and neonicotinoid residues present in dietary items. Significant estimates of neonicotinoid-related population change were obtained for 13 of the 22 species (9 positive effects, 4 negative effects). Model estimates for individual species were not collectively explained by dietary risk categories, so dietary exposure to neonicotinoids via ingestion of treated seeds and seedlings could not be confirmed as a causal factor in farmland bird declines. Although it is not possible to infer any generic effect of dietary exposure to neonicotinoids on farmland bird populations, our analysis identifies three species with significant negative estimates that may warrant further research (house sparrow Passer domesticus, skylark Alauda arvensis and red-legged partridge Alectoris rufa). We conclude that there was either no consistent effect of dietary exposure to neonicotinoids on farmland bird populations in England, or that any over-arching effect was not detectable using our study design. The potential for indirect effects of insecticide use on bird populations via reduced food availability was not considered here and should be a focus for future research.

New universal ITS2 primers for high-resolution herbivory analyses using DNA metabarcoding in both tropical and temperate zones.

DNA metabarcoding is a rapidly growing technique for obtaining detailed dietary information. Current metabarcoding methods for herbivory, using a single locus, can lack taxonomic resolution for some applications. We present novel primers for the second internal transcribed spacer of nuclear ribosomal DNA (ITS2) designed for dietary studies in Mauritius and the UK, which have the potential to give unrivalled taxonomic coverage and resolution from a short-amplicon barcode. In silico testing used three databases of plant ITS2 sequences from UK and Mauritian floras (native and introduced) totalling 6561 sequences from 1790 species across 174 families. Our primers were well-matched in silico to 88% of species, providing taxonomic resolution of 86.1%, 99.4% and 99.9% at the species, genus and family levels, respectively. In vitro, the primers amplified 99% of Mauritian (n = 169) and 100% of UK (n = 33) species, and co-amplified multiple plant species from degraded faecal DNA from reptiles and birds in two case studies. For the ITS2 region, we advocate taxonomic assignment based on best sequence match instead of a clustering approach. With short amplicons of 187-387 bp, these primers are suitable for metabarcoding plant DNA from faecal samples, across a broad geographic range, whilst delivering unparalleled taxonomic resolution.

The decline of the Turtle Dove: Dietary associations with body condition and competition with other columbids analysed using high-throughput sequencing.

Dietary changes linked to the availability of anthropogenic food resources can have complex implications for species and ecosystems, especially when species are in decline. Here, we use recently developed primers targeting the ITS2 region of plants to characterize diet from faecal samples of four UK columbids, with particular focus on the European turtle dove (Streptopelia turtur), a rapidly declining obligate granivore. We examine dietary overlap between species (potential competition), associations with body condition in turtle doves and spatiotemporal variation in diet. We identified 143 taxonomic units, of which we classified 55% to species, another 34% to genus and the remaining 11% to family. We found significant dietary overlap between all columbid species, with the highest between turtle doves and stock doves (Columba oenas), then between turtle doves and woodpigeons (Columba palumbus). The lowest overlap was between woodpigeons and collared doves (Streptopelia decaocto). We show considerable change in columbid diets compared to previous studies, probably reflecting opportunistic foraging behaviour by columbids within a highly anthropogenically modified landscape, although our data for nonturtle doves should be considered preliminary. Nestling turtle doves in better condition had a higher dietary proportion of taxonomic units from natural arable plant species and a lower proportion of taxonomic units from anthropogenic food resources such as garden bird seed mixes and brassicas. This suggests that breeding ground conservation strategies for turtle doves should include provision of anthropogenic seeds for adults early in the breeding season, coupled with habitat rich in accessible seeds from arable plants once chicks have hatched.

High prevalence of Trichomonas gallinae in wild columbids across western and southern Europe.

BACKGROUND: Avian trichomonosis is known as a widespread disease in columbids and passerines, and recent findings have highlighted the pathogenic character of some lineages found in wild birds. Trichomonosis can affect wild bird populations including endangered species, as has been shown for Mauritian pink pigeons Nesoenas mayeri in Mauritius and suggested for European turtle doves Streptopelia turtur in the UK. However, the disease trichomonosis is caused only by pathogenic lineages of the parasite Trichomonas gallinae. Therefore, understanding the prevalence and distribution of both potentially pathogenic and non-pathogenic T. gallinae lineages in turtle doves and other columbids across Europe is relevant to estimate the potential impact of the disease on a continental scale. RESULTS: We examined 281 samples from four wild columbid species for Trichomonas infection and determined the genetic lineages. The overall prevalence was 74%. There were significant differences between the species (P = 0.007). The highest prevalence was found in stock doves Columba oenas (86%, n = 79) followed by wood pigeons Columba palumbus (70%, n = 61) and turtle doves (67%, n = 65), while three of five collared doves Streptopelia decaocto (60%) were infected. We found seven different lineages, including four lineages present in columbids in the UK, one lineage already described from Spain and three new lineages, one of those found in a single turtle dove migrating through Italy and another one found in a breeding stock dove. Stock doves from Germany and collared doves from Malta were infected with a potentially pathogenic lineage (lineage A/B), which is known to cause lesions and mortality in columbids, raptors and finches. CONCLUSIONS: Generally, turtle doves showed high prevalence of Trichomonas infection. Furthermore, the potentially pathogenic lineage A/B (or genotype B according to previous literature) was found in a recovering stock dove population. Both findings are worrying for these columbid species due to the occasional epidemic character of trichomonosis, which can have severe negative effects on populations.

High rates of infection by blood parasites during the nestling phase in UK Columbids with notes on ecological associations.

Studies of blood parasite infection in nestling birds rarely find a high prevalence of infection. This is likely due to a combination of short nestling periods (limiting the age at which nestlings can be sampled) and long parasite prepatent periods before gametocytes can be detected in peripheral blood. Here we examine rates of blood parasite infection in nestlings from three Columbid species in the UK. We use this system to address two key hypotheses in the epidemiology of avian haemoparasites: first, that nestlings in open nests have a higher prevalence of infection; and second, that nestlings sampled at 14 days old have a higher apparent infection rate than those sampled at 7 days old. Open-nesting individuals had a 54% infection rate compared with 25% for box-nesters, probably due to an increased exposure of open-nesting species to dipteran vectors. Nestlings sampled at 14 days had a 68% infection rate compared with 32% in nestlings sampled at 7 days, suggesting that rates of infection in the nest are high. Further work should examine nestlings post-fledging to identify rates of successful parasite infection (as opposed to abortive development within a dead-end host) as well as impacts on host post-fledging survival and behaviour.

Can hedgerow management mitigate the impacts of predation on songbird nest survival?

Nest predators can have significant impacts on songbird reproductive success. These impacts may be amplified by habitat simplification and here we test whether sympathetic management of farmland hedgerows can reduce nest depredation, especially by corvids. We test whether songbirds select nest sites according to structural features of hedgerows (including nest visibility and accessibility), and whether these features influence nest predation risk. Songbirds selected nesting sites affording higher vegetation cover above the nest, increased visibility on the nest-side of the hedgerow and reduced visibility on the far side of the hedge. Nest survival was unrelated to corvid abundance and only weakly related (at the egg stage) to corvid nest proximity. Nest survival at the chick stage was higher where vegetation structure restricted access to corvid-sized predators (averaging 0.78 vs. 0.53), and at nests close to potential vantage points. Overall nest survival was sensitive to hedgerow structure (accessibility) particularly at low exposure to corvid predation, while the overall impact of corvid exposure was dependent on the relationship involving proximity to vantage points. Nest survival over the chick stage was much higher (0.67) in stock-proof, trimmed and mechanically cut hedgerows, (which tended to provide lower side visibility and accessibility) than in recently laid, remnant or leggy hedgerows (0.18). Long-term reductions in the management of British hedgerows may therefore be exposing nesting songbirds to increased predation risk. We recommend regular rotational cutting of hedgerows to maintain a dense woody structure and thereby reduce songbird nest predation.

Genomic evidence of demographic fluctuations and lack of genetic structure across flyways in a long distance migrant, the European turtle dove.

BACKGROUND: Understanding how past climatic oscillations have affected organismic evolution will help predict the impact that current climate change has on living organisms. The European turtle dove, Streptopelia turtur, is a warm-temperature adapted species and a long distance migrant that uses multiple flyways to move between Europe and Africa. Despite being abundant, it is categorized as vulnerable because of a long-term demographic decline. We studied the demographic history and population genetic structure of the European turtle dove using genomic data and mitochondrial DNA sequences from individuals sampled across Europe, and performing paleoclimatic niche modelling simulations. RESULTS: Overall our data suggest that this species is panmictic across Europe, and is not genetically structured across flyways. We found the genetic signatures of demographic fluctuations, inferring an effective population size (Ne) expansion that occurred between the late Pleistocene and early Holocene, followed by a decrease in the Ne that started between the mid Holocene and the present. Our niche modelling analyses suggest that the variations in the Ne are coincident with recent changes in the availability of suitable habitat. CONCLUSIONS: We argue that the European turtle dove is prone to undergo demographic fluctuations, a trait that makes it sensitive to anthropogenic impacts, especially when its numbers are decreasing. Also, considering the lack of genetic structure, we suggest all populations across Europe are equally relevant for conservation.

Anthropogenically-Mediated Density Dependence in a Declining Farmland Bird.

Land management intrinsically influences the distribution of animals and can consequently alter the potential for density-dependent processes to act within populations. For declining species, high densities of breeding territories are typically considered to represent productive populations. However, as density-dependent effects of food limitation or predator pressure may occur (especially when species are dependent upon separate nesting and foraging habitats), high territory density may limit per-capita productivity. Here, we use a declining but widespread European farmland bird, the yellowhammer Emberiza citrinella L., as a model system to test whether higher territory densities result in lower fledging success, parental provisioning rates or nestling growth rates compared to lower densities. Organic landscapes held higher territory densities, but nests on organic farms fledged fewer nestlings, translating to a 5 times higher rate of population shrinkage on organic farms compared to conventional. In addition, when parental provisioning behaviour was not restricted by predation risk (i.e., at times of low corvid activity), nestling provisioning rates were higher at lower territory densities, resulting in a much greater increase in nestling mass in low density areas, suggesting that food limitation occurred at high densities. These findings in turn suggest an ecological trap, whereby preferred nesting habitat does not provide sufficient food for rearing nestlings at high population density, creating a population sink. Habitat management for farmland birds should focus not simply on creating a high nesting density, but also on ensuring heterogeneous habitats to provide food resources in close proximity to nesting birds, even if this occurs through potentially restricting overall nest density but increasing population-level breeding success.

The protozoan parasite Trichomonas gallinae causes adult and nestling mortality in a declining population of European Turtle Doves, Streptopelia turtur.

Studies incorporating the ecology of clinical and sub-clinical disease in wild populations of conservation concern are rare. Here we examine sub-clinical infection by Trichomonas gallinae in a declining population of free-living European Turtle Doves and suggest caseous lesions cause mortality in adults and nestlings through subsequent starvation and/or suffocation. We found a 100% infection rate by T. gallinae in adult and nestling Turtle Doves (n = 25) and observed clinical signs in three adults and four nestlings (28%). Adults with clinical signs displayed no differences in any skeletal measures of size but had a mean 3.7% reduction in wing length, with no overlap compared to those without clinical signs. We also identified T. gallinae as the suggested cause of mortality in one Red-legged Partridge although disease presentation was different. A minimum of four strains of T. gallinae, characterized at the ITS/5.8S/ITS2 ribosomal region, were isolated from Turtle Doves. However, all birds with clinical signs (Turtle Doves and the Red-legged Partridge) carried a single strain of T. gallinae, suggesting that parasite spill over between Columbidae and Galliformes is a possibility that should be further investigated. Overall, we highlight the importance of monitoring populations for sub-clinical infection rather than just clinical disease.

Active blood parasite infection is not limited to the breeding season in a declining farmland bird.

Avian blood parasites can have significant impacts on adult breeding birds but studies of parasitism outside the breeding season are rare, despite their potentially important implications for host-parasite dynamics. Here we investigate temporal dynamics of blood parasite infection in adult yellowhammers Emberiza citrinella . We screened blood samples collected between December and April of 2 consecutive winters using PCR. We found a high prevalence of both Haemoproteus and Leucocytozoon parasites, with a mean prevalence of 50% across 2 winters. Prevalence of both parasites was higher during the second, colder winter of the study. Temporal trends differed between the 2 genera, suggesting that chronic Haemoproteus infections gradually disappear throughout the winter but that Leucocytozoon infections exhibit a relapse during late winter, possibly coincident with reduced food availability. Our results highlight the difference in temporal dynamics between 2 blood parasite genera infecting the same host population and emphasize the need for accurate assessment of infection status at appropriate time periods when examining impacts of, and associations with, blood parasite infection. We suggest that further research should investigate the implications of over-winter infection for birds' physiology, behavior, and survival.

Avian blood parasite infection during the non-breeding season: an overlooked issue in declining populations?

BACKGROUND: Pathogens and parasites can have major impacts on host population dynamics, both through direct mortality and via indirect effects. Both types of effect may be stronger in species whose populations are already under pressure. We investigated the potential for blood parasites to impact upon their hosts at the immunological, physiological and population level during the non-breeding season using a declining population of yellowhammers Emberiza citrinella as a model. RESULTS: Yellowhammers infected by Haemoproteus spp. showed both a reduced heterophil to lymphocyte (H:L) ratio, and an elevated standardised white blood cell (WBC) count compared to uninfected birds, indicating an immunological response to infection. Infected birds had shorter wings during the first winter of sampling but not during the second, colder, winter; survival analysis of 321 birds sampled across four winters indicated that increased wing length conferred a survival advantage. CONCLUSIONS: We suggest that the potential impacts of blood parasite infections on over-wintering birds may have been underestimated. Further research should consider the potential impacts of sub-clinical parasite infections on the dynamics of vulnerable populations, and we suggest using declining populations as model systems within which to investigate these relationships as well as examining interactions between sub-clinical disease and other environmental stressors. JEL CODE: Q5.