The disease implications of novel pathogens need to be considered when investigating the ecological impact of species translocations on native fauna. Traditional explanations based on competition or predation may often not be the whole story. Evidence suggests that an emerging infectious disease, caused by a parapoxvirus, may be a significant component of the impact that the introduced grey squirrel has had on UK red squirrel populations. Here we validate the potential role of parapoxvirus by proving that the virus is highly pathogenic in the red squirrel while having no detectable effect on grey squirrel health.

Red squirrels are declining in the United Kingdom. Competition from, and squirrel poxvirus (SQPV) disease carried by, grey squirrels are assumed to be determining the decline. We analyse the incidence of disease and changes in distribution of the two species in Cumbria, from 1993 to 2003 and compare these to the predictions of an individual-based (IB) spatially explicit disease model simulating the dynamics of both squirrel species and SQPV in the landscape. Grey squirrels increased whilst red squirrels declined over 10 years. The incidence of disease in red squirrels was related to the time since grey squirrels arrived in the landscape. Analysis of rates of decline in red squirrel populations in other areas showed that declines are 17-25 times higher in regions where SQPV is present in grey squirrel populations than in those where it is not. The IB model predicted spatial overlap of 3-4 years between the species that was also observed in the field. The model predictions matched the observed data best when contact rates and rates of infection between the two species were low. The model predicted that a grey squirrel population control of>60% effective kill was needed to stop the decline in red squirrel populations in Cumbria.

Translocations of species are expected to be used increasingly to counter the undesirable effects of anthropogenic changes to ecosystems, including loss of species. Methods to assess the risk of disease associated with translocations have been compiled in a comprehensive manual of disease-risk analysis for movement of domestic animals. We used this manual to devise a qualitative method for assessing the probability of the occurrence of disease in wild animals associated with translocations. We adapted the method such that we considered a parasite (any agent of infectious or noninfectious disease) a hazard if it or the host had crossed an ecological or geographical barrier and was novel to the host. We included in our analyses hazards present throughout the translocation pathway derived from the interactions between host immunity and the parasite, the effect of parasites on populations, the effect of noninfectious disease agents, and the effect of stressors on host-parasite interactions. We used the reintroduction of Eurasian Cranes (Grus grus) to England to demonstrate our method. Of the 24 hazards identified, 1 was classified as high risk (coccidia) and 5 were medium risk (highly pathogenic avian influenza virus, Mycobacterium avium, Aspergillus fumigatus, tracheal worms [Syngamus sp. and Cyathostoma sp.], and Tetrameres spp.). Seventeen other hazards were considered low or very low risk. In the absence of better information on the number, identity, distribution, and pathogenicity of parasites of wild animals, there is uncertainty in the risk of disease to translocated animals and recipient populations. Surveys of parasites in source and destination populations and detailed health monitoring after release will improve the information available for future analyses of disease risk. We believe our method can be adapted to assess the risks of disease in other translocated populations.

The squirrel poxvirus (SQPV) is the probable mediator of apparent competition between the introduced invading gray squirrel (Sciurus carolinensis) and the red squirrel (Sciurus vulgaris) in the UK, and modeling studies have shown that this viral disease has had a significant impact on the decline of the red squirrel in the UK. However, given our limited understanding of the epidemiology of the disease, and more generally the effects of invasive species on parasite ecology, there is a need to investigate the transmission dynamics and the relative pathogenicity of the virus between species. We aimed to increase our knowledge of these processes through an empirical study in which we: (i) used pathological signs and transmission electron microscopy (TEM) to diagnose SQPV disease in red squirrels found dead during scanning surveillance between 1993 and 2005; (ii) detected antibody to SQPV using an enzyme-linked immunosorbent assay (ELISA) in the same animals; and (iii) mapped cases of the disease, and the gray squirrel distribution, using a geographical information system. We analyzed the distribution of cases of SQPV disease according to woodland type, a measure of squirrel density. SQPV disease occurred only in areas of England also inhabited by seropositive gray squirrels, and as the geographical range of gray squirrels expanded, SQPV disease occurred in these new gray squirrel habitats, supporting a role for the gray squirrel as a reservoir host of the virus. There was a delay between the establishment of invading gray squirrels and cases of the disease in red squirrels which implies gray squirrels must reach a threshold number or density before the virus is transmitted to red squirrels. The spatial and temporal trend in SQPV disease outbreaks suggested that SQPV disease will have a significant effect on Scottish populations of red squirrels within 25 years. The even spread of cases of disease across months suggested a direct rather than vector-borne transmission route is more likely. Eight juvenile and sub-adult free-living red squirrels apparently survived exposure to SQPV by mounting an immune response, the first evidence of immunity to SQPV in free-living red squirrels, which possibly suggests a changing host-parasite relationship and that the use of a vaccine may be an effective management tool to protect remnant red squirrel populations.

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