The red squirrel population in Great Britain has declined dramatically in recent decades, principally due to squirrelpox. Concern exists that red squirrels may become extinct nationally and, as there has been limited research in to diseases other than squirrelpox, this study aimed to identify additional causes of mortality. Post-mortem examinations on 163 red squirrels found dead on Isle of Wight (IoW) England, in Scotland and at other locations in Great Britain showed that 41.7% (n = 68) were killed by road traffic and 9.2% (n = 15) by predators, principally domestic cats and dogs. The overall male/female ratio was 1.08/1. Fleas were recorded on 34.9% of IoW squirrels and on 43.8% of Scottish squirrels but sucking lice and ixodid ticks were only seen on Scottish squirrels. Bacterial infections were significant, particularly in association with respiratory disease (n = 16); two squirrels died of Bordetella bronchiseptica bronchopneumonia. Cases of fatal exudative dermatitis (n = 5) associated with a lukM-positive clone of Staphylococcus aureus occurred only on the IoW. Toxoplasmosis (n = 12) was also confined to IoW where it was responsible for almost one tenth (9.5%) of all deaths. Hepatozoonosis was common, especially in IoW squirrels, but was not considered a primary cause of mortality. Hepatic capillariasis affected four IoW squirrels and one from Scotland. Fungal infections included oral candidiasis, adiaspiromycosis and pulmonary phaeohyphomycosis. Neoplastic conditions diagnosed were: pulmonary carcinoma, gastric spindle cell tumour, renal papillary adenoma and trichoepithelioma. Epidermal hyperplasia of unknown aetiology was seen in squirrels showing crusty lesions of the ear pinnae on IoW (n = 3) and Brownsea Island (n = 1), associated in two cases with cutaneous wart-like growths. Miscellaneous diagnoses included chylothorax, electrocution, intussusception, suspected cholecalciferol rodenticide poisoning and foetal death and mummification. No cases of squirrelpox were diagnosed. Red squirrels in Britain suffer premature or unnatural mortality due to a number of conditions in addition to squirrelpox, many of which result, directly or indirectly, from human activities: road traffic trauma, pet predation, toxoplasmosis, trap injuries, rodenticide poisoning and electrocution accounted for 61% of all recorded mortality in this study. Red squirrels are also affected by several diseases of unknown aetiology which merit further research.

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Causes of mortality and pathological lesions observed post-mortem in red squirrels (Sciurus vulgaris) in Great Britain

Red squirrels (Sciurus vulgaris) declined in Great Britain and Ireland during the last century, due to habitat loss and the introduction of grey squirrels (Sciurus carolinensis), which competitively exclude the red squirrel and act as a reservoir for squirrelpox virus (SQPV). The disease is generally fatal to red squirrels and their ecological replacement by grey squirrels is up to 25 times faster where the virus is present. We aimed to determine: (1) the seropositivity and prevalence of SQPV DNA in the invasive and native species at a regional scale; (2) possible SQPV transmission routes; and, (3) virus degradation rates under differing environmental conditions. Grey (n = 208) and red (n = 40) squirrel blood and tissues were sampled. Enzyme-linked immunosorbent assay (ELISA) and quantitative real-time polymerase chain reaction (qPCR) techniques established seropositivity and viral DNA presence, respectively. Overall 8% of squirrels sampled (both species combined) had evidence of SQPV DNA in their tissues and 22% were in possession of antibodies. SQPV prevalence in sampled red squirrels was 2.5%. Viral loads were typically low in grey squirrels by comparison to red squirrels. There was a trend for a greater number of positive samples in spring and summer than in winter. Possible transmission routes were identified through the presence of viral DNA in faeces (red squirrels only), urine and ectoparasites (both species). Virus degradation analyses suggested that, after 30 days of exposure to six combinations of environments, there were more intact virus particles in scabs kept in warm (25°C) and dry conditions than in cooler (5 and 15°C) or wet conditions. We conclude that SQPV is present at low prevalence in invasive grey squirrel populations with a lower prevalence in native red squirrels. Virus transmission could occur through urine especially during warm dry summer conditions but, more notably, via ectoparasites, which are shared by both species.

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Squirrelpox Virus: Assessing Prevalence, Transmission and Environmental Degradation

The native red squirrel Sciurus vulgaris population in Britain has been on the decline for many years. A poxvirus associated with the introduced American grey squirrel S. carolinensis has been recognized as having a major role in the reduction of red squirrel numbers by causing a deleterious disease, known as squirrelpox, from which they seldom recover. In Ireland, red squirrel numbers have also been reducing while the grey squirrel population, first introduced in 1911, has been expanding. Until now, no poxvirus-associated disease had been found in Irish red squirrels and therefore, the role of squirrelpox in the displacement of red squirrels by grey squirrels in Ireland has been questioned. Here we report, for the first time, confirmed squirrelpox disease in two populations of red squirrels in Northern Ireland. In addition, we present serological evidence of the extent of poxvirus infection in the grey squirrels from both the Republic of Ireland and Northern Ireland, including an apparent increase in the seroprevalence of antibodies against the virus in grey squirrels over the period of the study, and discuss the implications of our findings for the conservation tactics employed to protect red squirrels.

The emergence of squirrelpox in Ireland.

1. Adenovirus is an emerging threat to red squirrel Sciurus vulgaris conservation, but confirming clinically significant adenovirus infections in red squirrels is challenging. Rapid intestinal autolysis after death in wild animals frequently obscures pathology characteristic of the disease in animals found dead.
2. We review the available literature to determine current understanding of both subclinical and clinically significant adenovirus infections in free-living wild and captive red squirrel populations.
3. Benefits of scientific testing for adenovirus incorporating both transmission electron microscopy (TEM) and polymerase chain reaction (PCR) technologies are compared and contrasted. We favour viral particle detection using TEM in animals exhibiting enteropathy at post-mortem and the use of PCR to detect subclinical cases where no enteric abnormalities are observed.
4. Adenoviral infections associated with re-introduction studies are evaluated by examination of sporadic cases in wild populations and of data from captive collections used to service such studies.
5. The paucity of data available on adenovirus infection in grey squirrel Sciurus carolinensis populations is documented, and we highlight that although subclinical virus presence is recorded in several locations in Great Britain and in Italy, no clinically significant disease cases have been detected in the species thus far.
6. Current speculation about potential interspecific infection between sciurids and other woodland rodents such as wood mice Apodemus sylvaticus is examined. Where subclinical adenovirus presence has been detected in sympatric populations using the same point food sources, husbandry methods may be used to diminish the potential for cross-infection.
7. Our findings highlight the importance of controlling disease in red squirrel populations by using clearly defined scientific methods. In addition, we propose hypothetical conservation benefits of restricting contact rates between red squirrels and sympatric grey squirrels and of limiting competition from other woodland rodent species.

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Adenovirus: an emerging factor in red squirrel Sciurus vulgaris conservation

ENTERIC adenovirus (AdV) infection of red squirrels ( Sciurus vulgaris ) suffering from diarrhoea was first seen in Great Britain, in the county of Norfolk (Sainsbury and others 2001). The squirrels had been translocated from Cumbria in north-west England. Subsequently, further cases have been documented in Cumbria (Duff and others 2007), on the Isle of Anglesey in Wales (Everest and others 2008), in Scotland (Everest and others 2010a) and in further areas of Great Britain (Everest and others 2010b). AdV particles were detected by electron microscopy in intestinal contents, from which an AdV was isolated on first passage in mouse L cells. A short fragment from the gene of the major capsid protein, the hexon, was amplified by PCR and sequenced. Phylogenetic calculations indicated that the isolated virus is different from the known AdVs and represents a novel virus species (Sainsbury and others 2001). The International Committee on Taxonomy of Viruses listed the squirrel adenovirus type 1 (SqAdV-1) as a preliminary, yet not approved species of mastadenoviruses (Benko and others 2005).

This short communication reports the first description of an enteric AdV infection in red squirrels outside the UK, namely in Germany. The preliminary results indicate a very close relationship between the AdVs demonstrated in squirrels in Germany and in the UK.

Three seven-month-old red squirrel siblings (two females and one male kept privately; ie, not as part of a zoo or wildlife collection) were found dead unexpectedly in their enclosure. They had been bred on site and had never left their enclosure. Other animals had not been introduced into the group. The carcases were submitted for postmortem examination. The squirrels were in a good nutritional condition, weighing 180, 220 and 240 g. The main pathological findings included …

Squirrel adenovirus type 1 in red squirrels (Sciurus vulgaris) in Germany.

Transmission electron microscopy identified adenovirus particles in 10 of 70 (14.3 per cent) samples of large intestinal content collected at postmortem examination from free-living wild red squirrels (Sciurus vulgaris) across Great Britain between 2000 and 2009. Examination was limited to cases in which an enteropathy was suspected on the basis of predetermined macroscopic criteria such as semi-solid or diarrhoeic faeces, suspected enteritis or the presence of intussusception. In most cases, meaningful histological examination of enteric tissue was not possible due to pronounced autolysis. Two (2.9 per cent) of the samples were negative for adenovirus but were found to contain rotavirus particles, a novel finding in this species.

Retrospective detection by negative contrast electron microscopy of faecal viral particles in free-living wild red squirrels (Sciurus vulgaris) with suspected enteropathy in Great Britain

M. Wilkinson

Papers

Retrospective detection by negative contrast electron microscopy of faecal viral particles in free-living wild red squirrels (Sciurus vulgaris) with suspected enteropathy in Great Britain