Emerging Infectious Disease leads to Rapid Population Decline 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

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

Phylogenetic analysis of avipoxvirus from British birds based on the 4b core protein.

<p>Neighbor-joining phylogram with bootstrap values (1000 replicates) of >90% shown. Sequences derived in this study are indicated with an asterisk. Details of avian pox isolates from UK non-Paridae species are in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0040176#pone.0040176.s006" target="_blank">Table S2</a>. Details of Genbank listed avian pox isolates are in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0040176#pone.0040176.s007" target="_blank">Table S3</a>. The evolutionary distances were computed using the Maximum Composite Likelihood method and are in the units of the number of base substitutions per site.</p

Spatial distribution and clustering patterns of avian pox in Paridae and non-Paridae hosts, 2006–2010.

<p>Maps showing the spatial distribution of avian pox in Paridae and non-Paridae hosts in each year of the study, as well as the results of K-function analysis to detect clustering of pox cases. Standardised K values (L<i>(d)</i> values, solid line) are presented as a function of increasing distance (0 to 350 km), and in relation to the 95% null simulation envelope (dotted lines). The location and spatial extent of statistically significant pox clusters accounting for heterogeneity in reporting rate (determined from SatScan spatial cluster analysis using county human household numbers as the background population) are shown by orange circles. Counties encompassed within clusters are shaded in red. Also shown are the log-likelihood ratio (LLR), the relative risk of infection (RR) and the significance (P value) of each of the identified SatScan clusters. Note that while pox cases were assigned to their county of origin for this analysis, they are plotted on these maps at their actual locations.</p

Seasonality of avian pox incidents in Paridae and non-Paridae species, 2007–2010.

<p>In 2006, a single suspect Paridae incident was reported in January and a second in August; all five non-Paridae incidents were reported from July to September inclusive.</p

Spatio-temporal clustering of avian pox infections in Paridae and non-Paridae hosts from 2006 to 2010.

<p>Maps showing locations of avian pox incidents in Paridae and non-Paridae hosts in each year of the study, along with the locations and spatial extent of significant (P<0.05) spatiotemporal clusters detected by the space-time permutation scan statistic model. The temporal extent of clusters is given in the tables below the maps.</p

Transmission electron micrograph of avian pox virions from a skin lesion in a great tit (Case 4, Sussex, October 2007).

<p>Transmission electron micrograph of avian pox virions from a skin lesion in a great tit (Case 4, Sussex, October 2007).</p

Typical avian pox lesions in a great tit at a garden feeding station (Sussex, September 2007).

<p>Typical avian pox lesions in a great tit at a garden feeding station (Sussex, September 2007).</p