Emerging infectious diseases of wildlife: a critical perspective.

Summary
Invasive organisms and emerging wildlife disease pose two of the greatest threats to global biodiversity and ecosystem functioning.
Typically, when parasites are considered in invasion biology, it is in the context of the enemy release hypothesis, wherein a non-indigenous species has greater probability of invasion success by virtue of leaving its natural enemies, including parasites, behind.
It is also possible that native parasites may prevent invasions, but it is clear that invasive organisms may bring infectious diseases with them that can infect native competitors (via spillover), or act as competent hosts for native diseases, increasing disease prevalence among native species (via spillback).
If the shared disease (either via spillover or spillback) has higher virulence in the native host (which is particularly likely with introduced parasites), there is the potential that the disease can act as a ‘biological weapon’ leading to a disease-mediated invasion (DMI).
Here, we review cases where disease may have been an important factor mediating a wide range of invasions in vertebrates, invertebrates and plants.
We then focus on the invasion of the grey squirrel into the UK as a case study of a DMI, and we discuss how mathematical models have helped us to understand the importance of this shared disease and its implications for the management of invasive species.
We conclude that (i) DMIs are a widespread phenomenon, that (ii) spillover is more common in animal invasions and spillback more common among plant invasions and that (iii) spillover DMIs are particularly important in explaining the replacement of native animals with phylogenetically similar non-indigenous species.

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Invading with biological weapons: the importance of disease-mediated invasions

Infectious disease introduced by non-native species is increasingly cited as a facilitator of native population declines, but direct evidence may be lacking due to inadequate population and disease prevalence data surrounding an outbreak Previous indirect evidence and theoretical models support squirrelpox virus (SQPV) as being potentially involved in the decline of red squirrels (Sciurus vulgaris) following the introduction of the non-native gray squirrel (Sciurus carolinensis) to the United Kingdom The red squirrel is a major UK conservation concern and understanding its continuing decline is important for any attempt to mitigate the decline The red squirrel–gray squirrel system is also exemplary of the interplay between infectious disease (apparent competition) and direct competition in driving the replacement of a native by an invasive species Time series data from Merseyside are presented on squirrel abundance and squirrelpox disease (SQPx) incidence, to determine the effect of the pathogen and the non-native species on the native red squirrel populations Analysis indicates that SQPx in red squirrels has a significant negative impact on squirrel densities and their population growth rate (PGR) There is little evidence for a direct gray squirrel impact; only gray squirrel presence (but not density) proved to influence red squirrel density, but not red squirrel PGR The dynamics of red SQPx cases are largely determined by previous red SQPx cases, although previous infection of local gray squirrels also feature, and thus, SQPV-infected gray squirrels are identified as potentially initiating outbreaks of SQPx in red squirrels Retrospective serology indicates that approximately 8% of red squirrels exposed to SQPV may survive infection during an epidemic This study further highlights the UK red squirrel – gray squirrel system as a classic example of a native species population decline strongly facilitated by infectious disease introduced by a non-native species It is therefore paramount that disease prevention and control measures are integral in attempts to conserve red squirrels in the United Kingdom

https://onlinelibrary.wiley.com/doi/pdf/10.1002/ece3.1216

European red squirrel population dynamics driven by squirrelpox at a gray squirrel invasion interface.

The dramatic decline of the native red squirrel in the UK has been attributed to both direct and disease-mediated competition with the grey squirrel where the competitor acts as a reservoir host of squirrelpox virus (SQPV). SQPV is threatening red squirrel conservation efforts, yet little is known about its epidemiology. We analysed seroprevalence of antibody against SQPV in grey squirrels from northern England and the Scottish Borders in relation to season, weather, sex, and body weight using Generalized Linear Models in conjunction with Structural Equation Modelling. Results indicated a heterogeneous prevalence pattern which is male-biased, increases with weight and varies seasonally. Seroprevalence rose during the autumn and peaked in spring. Weather parameters had an indirect effect on SQPV antibody status. Our findings point towards a direct disease transmission route, which includes environmental contamination. Red squirrel conservation management options should therefore seek to minimize squirrel contact points.

Epidemiology of squirrelpox virus in grey squirrels in the UK

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.

Squirrelpox, caused by a poxvirus, is a major threat to the remaining UK red squirrel population. The spread of antibody-positive grey squirrels has been monitored in the UK for the past decade. In 2005 grey squirrels that had been exposed to the virus appeared in the south of Scotland for the first time, followed approximately two years later by the appearance of squirrelpox disease in the local red squirrels. Four squirrels were examined. They all had gross external lesions and histological lesions typical of squirrelpox disease, but no significant internal lesions. The diagnosis was confirmed by PCR, electron microscopy and serology.

A. M. MacMaster

Papers

First cases of squirrelpox in red squirrels (Sciurus vulgaris) in Scotland.

First cases of squirrelpox in red squirrels (Sciurus vulgaris) in Scotland