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

Abstract

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.

Figure 1. Seasonal incidence of opportunistic reports in all garden bird mortality 2001–2006.

Hatched bars – winter (Dec-Feb), open bars – spring (March–May), stippled bars – summer (June–Aug) and black bars - autumn (Sept-Nov). Note break in axis indicating an unprecedented level of reporting in autumn 2006.

Figure 2. Necrotic ingluvitis lesions and trichomonad parasite morphology.

(a) Necrotic ingluvitis lesions (arrow) with a characteristic yellow caseous appearance in a greenfinch caused by Trichomonas gallinae infection. (b) Morphology of the greenfinch trichomonad parasite. Scanning electron micrograph. Arrows indicate anterior flagella and axostyle.

Figure 3. Sequence data from British finch trichomonad samples.

(a) Nucleotide sequence (214 nucleotides) from amplification and sequencing of the ITS1/5.8S/ITS2 ribosomal region using TFR1 and TFR2 primers from (A) Consensus sequence from British finch (Genbank GQ150752 and GQ150753) trichomonad samples and (B) Trichomonas gallinae (Rivolta) Stabler (ATCC® Number 30230 TM). (b) Nucleotide sequence (149 nucleotides) from nested PCR with trichomonad SSU rRNA primers followed by TN3 and TN4 nested primers (Genbank GQ214405).

Figure 4. Distribution of finch trichomonosis incidents in 2006.

Gardens reporting at least one incident of finch trichomonosis (large red dots) and all other sites (small yellow dots) contributing to the systematic survey. The shading indicates relative incidence of trichomonosis recorded by the opportunistic survey (incidents per thousand households for each county interpolated from county centroids). The heavy lines delineate areas of High, Intermediate and Low incidence, based on the opportunistic survey data.

Figure 5. Seasonal variation in greenfinch occurrence in gardens.

(a) Reporting rate for greenfinch in all GBW gardens for the years 1996–2005 (grey lines), 2006 (red) and 2007 (blue). (b) Fitted seasonal pattern of mean peak greenfinch count in 828 GBW gardens with complete counts in 2005. (c) Difference in mean peak count throughout the year between 2005 and 2006 for greenfinch, dashed lines represent 95% confidence limits.

Figure 6. Regional change in greenfinch occurrence in gardens in response to trichomonosis.

Mean reporting rate from GBW of greenfinch, chaffinch and dunnock in spring 2005/06 (filled bars) and 2007 (open bars) in areas of Low, Intermediate and High incidence of trichomonosis incidence (see Fig. 3). Bars represent 95% confidence limits.

Figure 7. Annual rate of population change as measured by the BBS in areas of differing disease incidence.

Boxes show mean and quartiles of annual changes and whiskers minimum and maximum annual change observed in the period 1994–2006; points, the population change recorded in 2007. Dotted line indicates no population change.