Jenny C. Dunn

Competition and parasitism in the native White Clawed Crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK

Many crayfish species have been introduced to novel habitats worldwide, often threatening extinction of native species. Here we investigate competitive interactions and parasite infections in the native Austropotamobius pallipes and the invasive Pacifastacus leniusculus from single and mixed species populations in the UK. We found A. pallipes individuals to be significantly smaller in mixed compared to single species populations; conversely P. leniusculus individuals were larger in mixed than in single species populations. Our data provide no support for reproductive interference as a mechanism of competitive displacement and instead suggest competitive exclusion of A. pallipes from refuges by P. leniusculus leading to differential predation. We screened 52 P. leniusculus and 12 A. pallipes for microsporidian infection using PCR. We present the first molecular confirmation of Thelohania contejeani in the native A. pallipes; in addition, we provide the first evidence for T. contejeani in the invasive P. leniusculus. Three novel parasite sequences were also isolated from P. leniusculus with an overall prevalence of microsporidian infection of 38% within this species; we discuss the identity of and the similarity between these three novel sequences. We also screened a subset of fifteen P. leniusculus and three A. pallipes for Aphanomyces astaci, the causative agent of crayfish plague and for the protistan crayfish parasite Psorospermium haeckeli. We found no evidence for infection by either agent in any of the crayfish screened. The high prevalence of microsporidian parasites and occurrence of shared T. contejeani infection lead us to propose that future studies should consider the impact of these parasites on native and invasive host fitness and their potential effects upon the dynamics of native-invader systems.

Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits

The evolution and ecology of consistent behavioural variation, or personality, is currently the focus of much attention in natural populations. Associations between personality traits and parasite infections are increasingly being reported, but the extent to which multiple behavioural traits might be associated with parasitism at the same time is largely unknown. Here, we use a population of great tits, Parus major, to examine whether infection by avian malaria (Plasmodium and Leucocytozoon) is associated with three behavioural traits assayed under standardized conditions. All of these traits are of broad ecological significance and two of them are repeatable or heritable in our population. Here, we show weak correlations between some but not all of these behavioural traits, and sex-dependent associations between all three behavioural traits and parasite infection. Infected males showed increased problem-solving performance whereas infected females showed reduced performance; furthermore, uninfected females were four times more likely to solve problems than uninfected males. Infected females were more exploratory than uninfected females, but infection had no effect on males. Finally, infected males were more risk-averse than uninfected males but females were unaffected. Our results demonstrate the potential for complex interactions between consistent personality variation and parasite infection, though we discuss the difficulty of attributing causality in these associations. Accounting for complex parasite-behaviour associations may prove essential in understanding the evolutionary ecology of behavioural variation and the dynamics of host–parasite interactions.

Trichomonad parasite infection in four species of Columbidae in the UK

Trichomonas gallinae is an emerging pathogen in wild birds, linked to recent declines in finch (Fringillidae) populations across Europe. Globally, the main hosts for this parasite are species of Columbidae (doves and pigeons); here we carry out the first investigation into the presence and incidence of Trichomonas in four species of Columbidae in the UK, through live sampling of wild-caught birds and subsequent PCR. We report the first known UK cases of Trichomonas infection in 86% of European Turtle Doves Streptopelia turtur sampled, along with 86% of Eurasian Collared Doves Streptopelia decaocto, 47% of Woodpigeons Columba palumbus and 40% of Stock Doves Columba oenas. Birds were more likely to be infected if the farm provided supplementary food for gamebirds. We found three strains of T. gallinae and one strain clustering within the Trichomonas tenax clade, not previously associated with avian hosts in the UK. One T. gallinae strain was identical at the ITS/5.8S/ITS2 ribosomal region to that responsible for the finch trichomonosis epizootic. We highlight the importance of increasing our knowledge of the diversity and ecological implications of Trichomonas parasites in order further to understand the sub-clinical impacts of parasite infection.

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.

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

BackgroundPathogens 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.ResultsYellowhammers 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.ConclusionsWe 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 CodeQ5

Nest and foraging‐site selection in Yellowhammers Emberiza citrinella: implications for chick provisioning

Capsule Vegetation structure and invertebrate abundance interact to influence both foraging sites and nestling provisioning rate; when invertebrate availability is low, adults may take greater risks to provide food for their young. Aims To investigate nesting and foraging ecology in a declining farmland bird whose fledging success is influenced by the availability of invertebrate prey suitable for feeding to offspring, and where perceived predation risk during foraging can be mediated by vegetation structure. Methods Provisioning rates of adult Yellowhammers feeding nestlings were measured at nests on arable farmland. Foraging sites were compared with control sites of both the same and different microhabitats; provisioning rate was related to habitat features of foraging‐sites. Results Foraging sites had low vegetation density, probably enhancing detection of predators, or high invertebrate abundance at high vegetation density. Parental provisioning rate decreased with increasing vegetation cover at foraging sites with high invertebrate abundance; conversely, where invertebrate abundance was low, provisioning rate increased with increasing vegetation cover. Conclusions Vegetation structure at foraging sites suggests that a trade‐off between predator detection and prey availability influences foraging site selection in Yellowhammers. Associations between parental provisioning rate and vegetation variables suggest that where invertebrate abundance is high birds increase time spent scanning for predators at higher vegetation densities; however, when prey are scarce, adults may take more risks to provide food for their young.

Post-fledging habitat selection in a rapidly declining farmland bird, the European Turtle Dove Streptopelia turtur

Post-fledging survival plays a vital role in the dynamics of bird populations and yet is the least studied avian life-stage. Habitat requirements post-fledging may have important implications for behaviour and survival, especially for declining populations in landscapes that have undergone wide-scale anthropogenic modification, resulting in an altered distribution and composition of habitats. The European Turtle Dove is a widespread but rapidly declining species both within the UK and across Europe. Reduced seed food availability is thought to influence breeding success of this species, but it is not known whether post-fledging survival may also be influenced by seed availability. Here, we use leg-ring radio-tag attachments to monitor post-fledging survival and movements in 15 Turtle Dove nestlings from eight nests monitored during 2014 as part of a wider autecological study. Fledglings remained in close proximity to their nest for three weeks post-tagging, spending more than half their time in the immediate vicinity (within ∼ 20 m) of the nest. 95% of foraging trips during this period were within 329 m of the nest and fledglings selected seed-rich habitat (semi-natural grassland, low-intensity grazing, fallow and quarries). Fledglings that were heavier and in better body condition at seven days old were more likely to survive for 30 days post-fledging, and the proportion of available seed-rich habitat was a strong predictor of nestling weight and condition at seven days old. Whilst our sample size is modest, this study highlights the crucial role of food availability in juvenile survival, both while adults are feeding nestlings, and to recently fledged young, and the potential for agri-environment schemes providing foraging and nesting habitats in close proximity to provide important benefits.

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

BackgroundUnderstanding 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.ResultsOverall 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.ConclusionsWe 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.

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.

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.