T. W. Pennycott

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.

The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species

OBJECTIVES A previously unidentified mecA homologue, mecA(LGA251), has recently been described in methicillin-resistant Staphylococcus aureus (MRSA) from humans and dairy cattle. The origin and epidemiology of this novel homologue are unclear. The objective of this study was to provide basic descriptive information of MRSA isolates harbouring mecA(LGA251) from a range of host animal species. METHODS A number of S. aureus isolates from historical animal isolate collections were chosen for investigation based on their similarity to known mecA(LGA251) MRSA isolates. The presence of mecA(LGA251) was determined using a multiplex PCR and antimicrobial susceptibility testing performed by disc diffusion. RESULTS MRSA harbouring mecA(LGA251) were found in isolates from a domestic dog, brown rats, a rabbit, a common seal, sheep and a chaffinch. All of the isolates were phenotypically MRSA, although this depended on which test was used; some isolates would be considered susceptible with certain assays. All isolates were susceptible to linezolid, rifampicin, kanamycin, norfloxacin, erythromycin, clindamycin, fusidic acid, tetracycline, trimethoprim/sulfamethoxazole and mupirocin. Five multilocus sequence types were represented (2273, 130, 425, 1764 and 1245) and six spa types (t208, t6293, t742, t6594, t7914 and t843). CONCLUSIONS The discovery of MRSA isolates possessing mecA(LGA251) from a diverse range of host species, including different taxonomic classes, has important implications for the diagnosis of MRSA in these species and our understanding of the epidemiology of this novel mecA homologue.

Isolation of different serovars of Salmonella enterica from wild birds in Great Britain between 1995 and 2003

Postmortem examinations were carried out on the carcases of 779 wild birds. Salmonellosis was a common cause of death in greenfinches (Carduelis chloris), house sparrows (Passer domesticus) and chaffinches (Fringilla coelebs), and was also responsible for the deaths of other birds such as goldfinches (Carduelis carduelis), feral pigeons and different species of gulls. Most cases of salmonellosis in finches occurred between January and March, whereas salmonellosis in house sparrows tended to occur between October and March. Salmonella Typhimurium DT40 and DT56 (variant) predominated in finches and sparrows, DT41 and DT195 were the most common strains isolated from gulls, and DT2 and DT99 were recovered from feral pigeons. These ‘wild bird’ strains of Salmonella made up less than 0·5 per cent of the isolates of Salmonella recovered from cattle, sheep, pigs, chickens or turkeys in Great Britain over the same period, but they made up nearly 3 per cent of the isolates from more extensively reared avian livestock such as gamebirds, ducks and geese.

Causes of death of wild birds of the family Fringillidae in Britain.

The provision of supplementary food for wild birds in gardens during the winter months is common in the UK, but it is possible that it may precipitate infectious diseases in the birds. This paper describes the results of postmortem examinations of 116 wild finches carried out over a period of four years. The two commonest causes of death in areas where high mortality had been reported were infections with the bacteria Salmonella typhimurium DT4o and Escherichia coli O86. Coccidia of the genera Atoxoplasma or Isospora were found in several of the birds but were considered to be incidental. Megabacteria were also identified in some of the birds, for the first time in flocks of wild birds in the UK, but they were not considered to be significant.

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.

Salmonella enterica subspecies enterica serotype Typhimurium and Escherichia coli 086 in wild birds at two garden sites in south-west Scotland

Salmonella enterica subspecies enterica serotype Typhimurium and Escherichia coli 086:K61 :NM are two bacteria that can cause outbreaks of mortality in garden birds visiting bird tables and other feeding stations. Two sites in south-west Scotland were monitored for the two organisms for 12 months. At site A, large numbers of birds fed throughout the year, and at site B smaller numbers of birds fed only in the winter months. Samples of composite faeces were collected from the feeding stations and screened for the organisms, and any dead birds were also screened. S Typhimurium definitive type (DT) 56 (variant) was found to be endemic at site A, and was recovered from 48 per cent of samples of composite faeces collected from the bird table, from 42 per cent of composite faeces from underneath a hanging feeder, and from 33 per cent of composite faeces from below a roost used by house sparrows; the organism was also isolated from the carcases of six wild birds found dead at the site. In contrast, S Typhimurium (DT41) was recovered only once at site B, from 2 per cent of the composite faeces from below a hanging feeder, and no dead birds were recovered from the site. E coli 086 was not recovered from the faeces collected from either site, but was isolated from a bird that died from trauma at site A.

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.

Mycoplasma sturni and Mycoplasma gallisepticum in wild birds in Scotland

ORGANISMS of the genus Mycoplasma belong to the class Mollicutes, which contains the smallest known prokaryotes able to replicate in cell-free media. Bradbury (2002) lists 23 recognised avian species of this genus, of which Mycoplasma gallisepticum, Mycoplasma synoviae, Mycoplasma meleagridis and Mycoplasma iowae have been associated with significant economic losses in domestic poultry or game birds. M gallisepticum and M synoviae have occasionally been isolated from healthy wild birds (Poveda and others 1990, Ley and Yoder 1997). A different strain of M gallisepticum caused outbreaks of severe conjunctivitis in wild songbirds at bird feeding stations in North America (Fischer 1994, Ley and others 1996, Luttrell and others 1996, Hartup and others 2001, Mikaelian and others 2001). There is little information on the occurrence of mycoplasmas in different species of wild birds in the UK, or the significance of wild birds as reservoirs of infection for poultry and gamebirds. This short communication describes the screening for mycoplasmas in a small number of wild bird carcases examined as part of an ongoing study looking at the causes of mortality of wild birds. The study was primarily looking for M gallisepticum and M synoviae, but the opportunity was also taken to look for other species of mycoplasma. Samples were collected from the carcases of 41 wild birds that had either been found dead by members of the public, had died in a wildlife rehabilitation centre, or had been found alive but euthanased on welfare grounds. A gross postmortem examination, supported by bacteriology, parasitology and histopathology where appropriate, was carried out on each carcase. To screen for mycoplasmas, an oropharyngeal swab was collected from each bird and a conjunctival swab was obtained from 32 of the 41 birds. Conjunctival swabs were not collected from the remaining nine birds because gross contamination of the eyes had occurred following death. Additional samples were collected from some birds on the basis of clinical history or postmortem findings: five swabs were collected from the infraorbital sinus, airsac or trachea, and 10 samples of lung or brain tissue were collected. Swabs collected at postmortem examination were dipped in mycoplasma broth immediately before use to maintain viability during storage of up to three days at 4°C, and overnight transit. On receipt at the laboratory, each swab was first inoculated onto mycoplasma agar and then placed in 2 ml of mycoplasma broth and held for one hour at room temperature. The mycoplasma broths were then divided into two aliquots, one of which was incubated in air at 37°C while the other was frozen at –70°C for subsequent examination by PCR. The mycoplasma agar plates and broths were processed as described by Welchman and others (2002). The frozen aliquots of mycoplasma broth were later thawed and examined for M gallisepticum and M synoviae by PCR (IDEXX Laboratories). Tissues collected at postmortem examination were placed directly into mycoplasma broth for transit, and on arrival at the laboratory swabs were collected from freshly cut surfaces of the tissues and processed as described above. Information about the species of birds tested, the cause of death and the results of mycoplasma culture are given in Table 1. Rapidly growing mycoplasmas subsequently identified as Mycoplasma sturni were isolated from 18 of the 41 birds tested. Table 2 provides details of the samples from which M sturni was isolated. Mycoplasma columbinum was isolated from one bird, a woodpigeon (Columba palumbus). Neither M gallisepticum nor M synoviae was cultured from any of the birds, but the PCR for M gallisepticum was positive in four mature rooks (Corvus frugilegus). The PCR for M synoviae was negative in all 41 birds. The recovery of M sturni was unexpected and, to the authors’ knowledge, this is the first report of the isolation of this organism from wild birds in Europe. Conjunctivitis associated with M sturni has been described in wild birds in North America such as the European starling (Sturnus vulgaris) (Forsyth and others 1996, Frasca and others 1997), blue jay (Cyanocitta cristata) and northern mockingbird (Mimus polyglottos) (Ley and others 1998) and American crow (Corvus brachyrhynchos) (Wellehan and others 2001). M sturni has also been recovered from asymptomatic wild birds in the USA, including American crows, American robins (Turdus migratorius) and European starlings (Luttrell and others 2001, Wellehan and others 2001). Northern mockingbirds and European starlings belong to the family Sturnidae, American robins to the family Turdidae, and blue jays and American crows to the family Corvidae, and the birds found to be positive for M sturni in Scotland belonged to the same three families. In addition, all the birds from which M sturni was isolated were immature birds. Birds that were positive for M sturni were suffering from a range of infectious and non-infectious conditions including aspergillosis, malnutrition, parasitism, trauma and the encephalitis of starlings described by Pennycott and others (2002). The significance of the isolation of M sturni from birds with such diverse diseases is unclear. M gallisepticum was not cultured from any bird but was detected by PCR in four birds, all mature rooks with pericarditis and pneumonia, submitted from two gamebird-rearing sites. In a study carried out on 53 corvids from a gamebird site with a persistent problem of sinusitis in pheasants, M gallisepticum was detected by PCR in 50 per cent of rooks, 38 per cent of carrion crows (Corvus corone) and 13 per cent of jackdaws (Corvus monedula), all of which were Number Species and age tested Cause of death or culling Mycoplasma culture

Surveillance for West Nile virus in British birds (2001 to 2006)

WEST Nile virus (wnv) is an arbovirus of the genus Flavivirus (family Flaviviridae), which is transmitted and amplified in enzootic cycles between avian hosts and many species of mosquito vectors ([Higgs and others 2004][1]). At least 59 mosquito species have been identified as vectors for wnv,

Marek's disease, candidiasis and megabacteriosis in a flock of chickens (Gallus gallus domesticus) and Japanese quail (Coturnix japonica).

An outbreak of mortality in chickens and Japanese quail sharing the same airspace was investigated. Mareks disease was diagnosed in five of 11 chickens examined, and in 20 of 24 quail; crop candidiasis was found in four of the chickens and in five of the quail, and moderate to large numbers of organisms referred to as megabacteria were observed in eight of the chickens and 16 of the quail. The disease was so severe that almost all of the quail in the flock died or were culled during the following six months. In contrast, only approximately 5 per cent of the chickens died from Mareks disease.