James K. Kirkwood

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.

Guidance on the transport of laboratory animals

Report of the Transport Working Group established by the Laboratory Animal Science Association (LASA)

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.

Epidemiology of Salmonellosis in Garden Birds in England and Wales, 1993 to 2003

Salmonellosis has been reported as an important cause of mortality of garden birds in several countries, including Norway and Scotland. We investigated the frequency of the disease in garden birds submitted for postmortem examination by members of the public in England and Wales between 1993 and 2003, inclusive. We found salmonellosis to be the most frequent cause of death due to infectious disease in the garden birds submitted. This disease was confirmed in 7 of the 45 bird species that were examined postmortem, with the greenfinch (Carduelis chloris) and the house sparrow (Passer domesticus) most frequently affected. Salmonella Typhimurium definitive phage type (DT) 40, DT56 variant(v), and DT160 accounted for the majority of isolates. Salmonellosis incidents chiefly occurred in the English Midlands, the English/Welsh border region, and southern England. Variation in the temporal and spatial distribution of the phage types occurred over the study period. While birds were examined throughout the year, there was a marked winter seasonality in salmonellosis. A significant sex bias was observed in affected greenfinches, with males more frequently diagnosed with salmonellosis than females. No sex bias was observed for other affected species. Further research is required to determine if salmonellosis is an important constraint to the populations of affected species and if disease outbreaks are driven by human factors, such as provisioning.

Bovine Spongiform Encephalopathy Infectivity in Greater Kudu (Tragelaphus strepsiceros)

Of all the species exposed naturally to the bovine spongiform encephalopathy (BSE) agent, the greater kudu (Tragelaphus strepsiceros), a nondomesticated bovine from Africa, appears to be the most susceptible to the disease. We present the results of mouse bioassay studies to show that, contrary to findings in cattle with BSE in which the tissue distribution of infectivity is the most limited recorded for any of the transmissible spongiform encephalopathies (TSE), infectivity in greater kudu with BSE is distributed in as wide a range of tissues as occurs in any TSE. BSE agent was also detected in skin, conjunctiva, and salivary gland, tissues in which infectivity has not previously been reported in any naturally occurring TSE. The distribution of infectivity in greater kudu with BSE suggests possible routes for transmission of the disease and highlights the need for further research into the distribution of TSE infectious agents in other host species.

Epidemiological Evidence That Garden Birds Are a Source of Human Salmonellosis in England and Wales

The importance of wild bird populations as a reservoir of zoonotic pathogens is well established. Salmonellosis is a frequently diagnosed infectious cause of mortality of garden birds in England and Wales, predominantly caused by Salmonella enterica subspecies enterica serovar Typhimurium definitive phage types 40, 56(v) and 160. In Britain, these phage types are considered highly host-adapted with a high degree of genetic similarity amongst isolates, and in some instances are clonal. Pulsed field gel electrophoresis, however, demonstrated minimal variation amongst matched DT40 and DT56(v) isolates derived from passerine and human incidents of salmonellosis across England in 2000–2007. Also, during the period 1993–2012, similar temporal and spatial trends of infection with these S. Typhimurium phage types occurred in both the British garden bird and human populations; 1.6% of all S. Typhimurium (0.2% of all Salmonella) isolates from humans in England and Wales over the period 2000–2010. These findings support the hypothesis that garden birds act as the primary reservoir of infection for these zoonotic bacteria. Most passerine salmonellosis outbreaks identified occurred at and around feeding stations, which are likely sites of public exposure to sick or dead garden birds and their faeces. We, therefore, advise the public to practise routine personal hygiene measures when feeding wild birds and especially when handling sick wild birds.

Status of wildlife health monitoring in the United Kingdom

There is a clear need to monitor the health of wildlife in the UK, to help to understand the population dynamics of endangered species and to detect any harm to the welfare of wild animals caused by human beings. Despite previous proposals, there has been little progress in the development of a national programme of monitoring. With notable exceptions, the current schemes for investigating the morbidity and mortality of wild animals cover only limited groups of animals and are fragmented and uncoordinated. They consist of statutory schemes of restricted scope, and studies in universities, institutes and wildlife rehabilitation centres with limited funding. As a result, significant disease incidents may remain undetected and others may not be investigated fully, posing risks to the welfare and conservation of wildlife, the welfare of domestic animals, and in some cases to human health. Coordinated national schemes for the surveillance of the health of wildlife are already established in France, the USA and Canada and their best characteristics could be used to develop a scheme for the UK.

Unusual mortality incidents in tit species (family Paridae) associated with the novel bacterium Suttonella ornithocola

BETWEEN March and June 1996, 11 unusual mortality incidents apparently involving only species of tits (family Paridae) in gardens in England and Wales were reported to one of the authors (J. K. K.) by members of the public. In eight of these incidents blue tits (Parus caeruleus) only were seen to be involved, and one case (case 5) involved only long-tailed tits (Aegithalos caudatus). The other two incidents also involved blue tits; in one case (case 3) a coal tit (Parus ater) and a longtailed tit were also found dead, and in another case (case 6), a great tit (Parus major) was also reported to be showing signs of illness (Table 1). Apart from a report in one of these cases (case 8) that two bullfinches (Pyrrhula pyrrhula) appeared unwell, no deaths or signs of disease were reported in other species. In 1993, J. K. K. had started, on a hobby basis, to investigate unusual mortality incidents in garden birds. Members of the public who contacted the Royal Society for the Protection of Birds or the British Trust for Ornithology about deaths in garden birds were referred so that details of the incidents could be collected by telephone. People were encouraged to send carcases, if available, for postmortem examinations, which were undertaken, when time permitted, in the evenings and at weekends. By 1996, this pastime had grown to the extent that during that year, 105 reports were received. The cluster of 11 incidents reported in this short communication thus represented approximately 10 per cent of the total for 1996. It is important to emphasise that this report gives no indication of the frequency of disease outbreaks in garden birds. It is likely that only a very small proportion of incidents were observed and that a still smaller proportion were reported, as this incident investigation scheme had not been advertised and was not well known. Information was collected on the species and numbers affected, signs observed, location, habitat type, when the incident had occurred and Veterinary Record (2006) 158, 203-205

Hematology of Fledgling Manx Shearwaters (Puffinus puffinus) with and without ‘Puffinosis’

Hematological parameters were measured in 14 fledgling Manx shearwaters (Puffinus puffinus), with the disease puffinosis and in 10 birds that did not have the disease, on the Island of Skomer between 2 and 11 September 1991. The mean plasma fibrinogen concentration was significantly higher in the diseased birds and some of these had abnormally elevated monocyte counts. No other significant differences were observed.

Management of a colony of common kestrels (Falco tinnunculus) in captivity

Management and captive breeding techniques of the kestrel are described. 5 pairs of kestrels laid 48 eggs in 1979, 27 of which were artificially incubated producing 19 hatchlings.