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 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

Postmortem and virological examinations for squirrelpox virus (SQPV) were carried out on 262 red squirrels (Sciurus vulgaris) found dead or moribund in Scotland between September 2005 and July 2009, to determine the likely causes of death and highlight factors that might be threats to the red squirrel population. Most of the squirrels were submitted from Dumfries and Galloway, and 71 per cent of them were adults. Road traffic accidents, squirrelpox, trauma or starvation were responsible for death in a large proportion (73 per cent) of the squirrels. Thin or emaciated body condition was associated with deaths resulting from pneumonia SQPV infection and starvation, and with the presence of external parasites. There were differences between age groups with regard to the cause of death; a large proportion of juveniles died of starvation, whereas a large proportion of subadults and adults died in road traffic accidents. SQPV infection was associated with the presence of external parasites, but was not associated with the sex of the animals.

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Epidemiological and postmortem findings in 262 red squirrels (Sciurus vulgaris) in Scotland, 2005 to 2009

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.

C. Fiegna

Papers

Epidemiological and postmortem findings in 262 red squirrels (Sciurus vulgaris) in Scotland, 2005 to 2009

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

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

Host-pathogen dynamics of squirrelpox virus infection in red squirrels (Sciurus vulgaris).