Bayesian hierarchical modelling of continuous non-negative longitudinal data with a spike at zero: An application to a study of birds visiting gardens in winter.

The development of methods for dealing with continuous data with a spike at zero has lagged behind those for overdispersed or zero-inflated count data. We consider longitudinal ecological data corresponding to an annual average of 26 weekly maximum counts of birds, and are hence effectively continuous, bounded below by zero but also with a discrete mass at zero. We develop a Bayesian hierarchical Tweedie regression model that can directly accommodate the excess number of zeros common to this type of data, whilst accounting for both spatial and temporal correlation. Implementation of the model is conducted in a Markov chain Monte Carlo (MCMC) framework, using reversible jump MCMC to explore uncertainty across both parameter and model spaces. This regression modelling framework is very flexible and removes the need to make strong assumptions about mean-variance relationships a priori. It can also directly account for the spike at zero, whilst being easily applicable to other types of data and other model formulations. Whilst a correlative study such as this cannot prove causation, our results suggest that an increase in an avian predator may have led to an overall decrease in the number of one of its prey species visiting garden feeding stations in the United Kingdom. This may reflect a change in behaviour of house sparrows to avoid feeding stations frequented by sparrowhawks, or a reduction in house sparrow population size as a result of sparrowhawk increase.

Is supplementary feeding in gardens a driver of evolutionary change in a migratory bird species?

Human activities are causing rapid environmental change at a global scale. Urbanization is responsible for some of the most extreme human-altered habitats and is a known driver of evolutionary change, but evidence and understanding of these processes is limited. Here, we investigate the potential underlying mechanisms contributing to the contemporary evolution of migration behaviour in the Eurasian blackcap (Sylvia atricapilla). Blackcaps from central Europe have been wintering in urban areas of Britain with increasing frequency over the past 60 years, rather than migrating south to the Mediterranean. It has been hypothesized that the popularization of providing supplementary foods for wild birds within Britain may have influenced this marked migratory change, but quantifying the selective forces shaping evolutionary changes remains challenging. Using a long-term national scale data set, we examine both the spatial distribution and interannual variation in blackcap wintering behaviour in Britain in relation to supplementary food availability and local climate. Over a 12-year period, we show that blackcaps are becoming increasingly associated with the provision of supplementary foods in British gardens, and that the reliability of bird food supplies is influencing their winter distribution at a national scale. In addition, local climatic temperatures and broader scale weather variation are also important determinants of blackcap wintering patterns once they arrive in Britain. Based on our findings, we conclude that a synergistic effect of increased availability of feeding resources, in the form of garden bird food, coupled with climatic amelioration, has enabled a successful new wintering population to become established in Britain. As global biodiversity is threatened by human-induced environmental change, this study presents new and timely evidence of the role human activities can play in shaping evolutionary trajectories.

Assessing factors associated with changes in the numbers of birds visiting gardens in winter: Are predators partly to blame?

The factors governing the recent declines observed in many songbirds have received much research interest, in particular whether increases of avian predators have had a negative effect on any of their prey species. In addition, further discussion has centered on whether or not the choice of model formulation has an effect on model inference. The study goal was to evaluate changes in the number of 10 songbird species in relation to a suite of environmental covariates, testing for any evidence in support of a predator effect using multiple model formulations to check for consistency in the results. We compare two different approaches to the analysis of long-term garden bird monitoring data. The first approach models change in the prey species between 1970 and 2005 as a function of environmental covariates, including the abundance of an avian predator, while the second uses a change-change approach. Significant negative relationships were found between Eurasian Sparrowhawk Accipiter nisus and three of the 10 species analyzed, namely house Sparrow Passer domesticus, starling Sturnus vulgaris, and blue tit Cyanistes caeruleus. The results were consistent under both modeling approaches. It is not clear if this is a direct negative impact on the overall populations of these species or a behavioral response of the prey species to avoid feeding stations frequented by Sparrowhawks (which may in turn have population consequences, by reducing available resources). The species showing evidence of negative effects of Sparrowhawks were three of the four species most at risk to Sparrowhawk predation according to their prevalence in the predator's diet. The associations could be causal in nature, although in practical terms the reduction in the rate of change in numbers visiting gardens accredited to Sparrowhawks is relatively small, and so unlikely to be the main driver of observed population declines.

The composition of British bird communities is associated with long-term garden bird feeding.

There is a multi-billion dollar global industry dedicated to feeding wild birds in residential gardens. This extraordinary boost to food resources is almost certainly reshaping entire bird communities, yet the large-scale, long-term impacts on community ecology remain unknown. Here we reveal a 40-year transformation of the bird communities using garden bird feeders in Britain, and provide evidence to suggest how this may have contributed to national-scale population changes. We find that increases in bird diversity at feeders are associated with increasing community evenness, as species previously rarely observed in gardens have increasingly exploited the growing variety of foods on offer over time. Urban areas of Britain are consequently nurturing growing populations of feeder-using bird species, while the populations of species that do not use feeders remain unchanged. Our findings illustrate the on-going, gross impact people can have on bird community structure across large spatial scales.

Health hazards to wild birds and risk factors associated with anthropogenic food provisioning.

Provision of supplementary food for wild birds at garden feeding stations is a common, large-scale and year-round practice in multiple countries including Great Britain (GB). While these additional dietary resources can benefit wildlife, there is a concomitant risk of disease transmission, particularly when birds repeatedly congregate in the same place at high densities and through interactions of species that would not normally associate in close proximity. Citizen science schemes recording garden birds are popular and can integrate disease surveillance with population monitoring, offering a unique opportunity to explore inter-relationships between supplementary feeding, disease epidemiology and population dynamics. Here, we present findings from a national surveillance programme in GB and note the dynamism of endemic and emerging diseases over a 25-year period, focusing on protozoal (finch trichomonosis), viral (Paridae pox) and bacterial (passerine salmonellosis) diseases with contrasting modes of transmission. We also examine the occurrence of mycotoxin contamination of food residues in bird feeders, which present both a direct and indirect (though immunosuppression) risk to wild bird health. Our results inform evidence-based mitigation strategies to minimize anthropogenically mediated health hazards, while maintaining the benefits of providing supplementary food for wild birds.This article is part of the theme issue 'Anthropogenic resource subsidies and host-parasite dynamics in wildlife'.

Spatio-temporal dynamics and aetiology of proliferative leg skin lesions in wild British finches.

Proliferative leg skin lesions have been described in wild finches in Europe although there have been no large-scale studies of their aetiology or epizootiology to date. Firstly, disease surveillance, utilising public reporting of observations of live wild finches was conducted in Great Britain (GB) and showed proliferative leg skin lesions in chaffinches (Fringilla coelebs) to be widespread. Seasonal variation was observed, with a peak during the winter months. Secondly, pathological investigations were performed on a sample of 39 chaffinches, four bullfinches (Pyrrhula pyrrhula), one greenfinch (Chloris chloris) and one goldfinch (Carduelis carduelis) with proliferative leg skin lesions and detected Cnemidocoptes sp. mites in 91% (41/45) of affected finches and from all species examined. Fringilla coelebs papillomavirus (FcPV1) PCR was positive in 74% (23/31) of birds tested: a 394 base pair sequence was derived from 20 of these birds, from all examined species, with 100% identity to reference genomes. Both mites and FcPV1 DNA were detected in 71% (20/28) of birds tested for both pathogens. Histopathological examination of lesions did not discriminate the relative importance of mite or FcPV1 infection as their cause. Development of techniques to localise FcPV1 within lesions is required to elucidate the pathological significance of FcPV1 DNA detection.

Identifying multispecies synchrony in response to environmental covariates.

The importance of multispecies models for understanding complex ecological processes and interactions is beginning to be realized. Recent developments, such as those by Lahoz-Monfort et al. (2011), have enabled synchrony in demographic parameters across multiple species to be explored. Species in a similar environment would be expected to be subject to similar exogenous factors, although their response to each of these factors may be quite different. The ability to group species together according to how they respond to a particular measured covariate may be of particular interest to ecologists. We fit a multispecies model to two sets of similar species of garden bird monitored under the British Trust for Ornithology's Garden Bird Feeding Survey. Posterior model probabilities were estimated using the reversible jump algorithm to compare posterior support for competing models with different species sharing different subsets of regression coefficients. There was frequently good agreement between species with small asynchronous random-effect components and those with posterior support for models with shared regression coefficients; however, this was not always the case. When groups of species were less correlated, greater uncertainty was found in whether regression coefficients should be shared or not. The methods outlined in this study can test additional hypotheses about the similarities or synchrony across multiple species that share the same environment. Through the use of posterior model probabilities, estimated using the reversible jump algorithm, we can detect multispecies responses in relation to measured covariates across any combination of species and covariates under consideration. The method can account for synchrony across species in relation to measured covariates, as well as unexplained variation accounted for using random effects. For more flexible, multiparameter distributions, the support for species-specific parameters can also be measured.

Emergence of a novel avian pox disease in British tit species.

Avian pox is a viral disease with a wide host range. In Great Britain, avian pox in birds of the Paridae family was first diagnosed in a great tit (Parus major) from south-east England in 2006. An increasing number of avian pox incidents in Paridae have been reported each year since, indicative of an emergent infection. Here, we utilise a database of opportunistic reports of garden bird mortality and morbidity to analyse spatial and temporal patterns of suspected avian pox throughout Great Britain, 2006-2010. Reports of affected Paridae (211 incidents) outnumbered reports in non-Paridae (91 incidents). The majority (90%) of Paridae incidents involved great tits. Paridae pox incidents were more likely to involve multiple individuals (77.3%) than were incidents in non-Paridae hosts (31.9%). Unlike the small wart-like lesions usually seen in non-Paridae with avian pox in Great Britain, lesions in Paridae were frequently large, often with an ulcerated surface and caseous core. Spatial analyses revealed strong clustering of suspected avian pox incidents involving Paridae hosts, but only weak, inconsistent clustering of incidents involving non-Paridae hosts. There was no spatial association between Paridae and non-Paridae incidents. We documented significant spatial spread of Paridae pox from an origin in south-east England; no spatial spread was evident for non-Paridae pox. For both host clades, there was an annual peak of reports in August/September. Sequencing of the avian poxvirus 4b core protein produced an identical viral sequence from each of 20 great tits tested from Great Britain. This sequence was identical to that from great tits from central Europe and Scandinavia. In contrast, sequence variation was evident amongst virus tested from 17 non-Paridae hosts of 5 species. Our findings show Paridae pox to be an emerging infectious disease in wild birds in Great Britain, apparently originating from viral incursion from central Europe or Scandinavia.

The emergence and spread of finch trichomonosis in the British Isles.

Finch trichomonosis, caused by the protozoal parasite Trichomonas gallinae, was first recognized as an emerging infectious disease of British passerines in 2005. The first year of seasonal epidemic mortality occurred in 2006 with significant declines of greenfinch Carduelis chloris and chaffinch Fringilla coelebs populations. Here, we demonstrate that large-scale mortality, principally of greenfinch, continued in subsequent years, 2007-2009, with a shifting geographical distribution across the British Isles over time. Consequent to the emergence of finch trichomonosis, the breeding greenfinch population in Great Britain has declined from ca 4.3 million to ca 2.8 million birds and the maximum mean number of greenfinches (a proxy for flock size) visiting gardens has declined by 50 per cent. The annual rate of decline of the breeding greenfinch population within England has exceeded 7 per cent since the initial epidemic. Although initially chaffinch populations were regionally diminished by the disease, this has not continued. Retrospective analyses of disease surveillance data showed a rapid, widespread emergence of finch trichomonosis across Great Britain in 2005 and we hypothesize that the disease emerged by T. gallinae jumping from columbiforms to passeriforms. Further investigation is required to determine the continuing impact of finch trichomonosis and to develop our understanding of how protozoal diseases jump host species.

Evidence of spread of the emerging infectious disease, finch trichomonosis, by migrating birds.

Finch trichomonosis emerged in Great Britain in 2005 and led to epidemic mortality and a significant population decline of greenfinches, Carduelis chloris and chaffinches, Fringilla coelebs, in the central and western counties of England and Wales in the autumn of 2006. In this article, we show continued epidemic spread of the disease with a pronounced shift in geographical distribution towards eastern England in 2007. This was followed by international spread to southern Fennoscandia where cases were confirmed at multiple sites in the summer of 2008. Sequence data of the ITS1/5.8S/ITS2 ribosomal region and part of the small subunit (SSU) rRNA gene showed no variation between the British and Fennoscandian parasite strains of Trichomonas gallinae. Epidemiological and historical ring return data support bird migration as a plausible mechanism for the observed pattern of disease spread, and suggest the chaffinch as the most likely primary vector. This finding is novel since, although intuitive, confirmed disease spread by migratory birds is very rare and, when it has been recognised, this has generally been for diseases caused by viral pathogens. We believe this to be the first documented case of the spread of a protozoal emerging infectious disease by migrating birds.

Emerging infectious disease leads to rapid population declines of common British birds.

Emerging infectious diseases are increasingly cited as threats to wildlife, livestock and humans alike. They can threaten geographically isolated or critically endangered wildlife populations; however, relatively few studies have clearly demonstrated the extent to which emerging diseases can impact populations of common wildlife species. Here, we report the impact of an emerging protozoal disease on British populations of greenfinch Carduelis chloris and chaffinch Fringilla coelebs, two of the most common birds in Britain. Morphological and molecular analyses showed this to be due to Trichomonas gallinae. Trichomonosis emerged as a novel fatal disease of finches in Britain in 2005 and rapidly became epidemic within greenfinch, and to a lesser extent chaffinch, populations in 2006. By 2007, breeding populations of greenfinches and chaffinches in the geographic region of highest disease incidence had decreased by 35% and 21% respectively, representing mortality in excess of half a million birds. In contrast, declines were less pronounced or absent in these species in regions where the disease was found in intermediate or low incidence. Also, populations of dunnock Prunella modularis, which similarly feeds in gardens, but in which T. gallinae was rarely recorded, did not decline. This is the first trichomonosis epidemic reported in the scientific literature to negatively impact populations of free-ranging non-columbiform species, and such levels of mortality and decline due to an emerging infectious disease are unprecedented in British wild bird populations. This disease emergence event demonstrates the potential for a protozoan parasite to jump avian host taxonomic groups with dramatic effect over a short time period.