Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain

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.

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Natural strongholds for red squirrel conservation in Scotland

Nature Conservation ◽

10.3897/natureconservation.43.62864 ◽

2021 ◽

Vol 43 ◽

pp. 93-108

Author(s):

Andrew Slade ◽

Andy White ◽

Kenny Kortland ◽

Peter W. W. Lurz

Keyword(s):

Management Practice ◽

Management Policy ◽

Sciurus Carolinensis ◽

Red Squirrel ◽

Grey Squirrel ◽

Case Scenario ◽

Red Squirrels ◽

Worst Case ◽

Standard Management ◽

Grey Squirrels

The Eurasian Red Squirrel (Sciurus vulgaris) is under threat from the invasive North American eastern Grey Squirrel (Sciurus carolinensis) with 80% of the remaining red squirrel populations in the British Isles found in Scotland. In this study we develop a spatially explicit mathematical model of the red and grey squirrel system and use it to assess the population viability of red squirrels across Scotland. In particular, we aim to identify existing forests – natural strongholds for red squirrels – that can successfully support red squirrels under UK Forestry Standard management and protect them from potential disease-mediated competition from grey squirrels. Our model results indicate that if current levels of grey squirrel control, which restrict or reduce the distribution of grey squirrels, are continued then there will be large expanses of forests in northern Scotland that support viable red squirrel populations. Model results that represent (hypothetical) scenarios where grey squirrel control no longer occurred indicated that grey squirrel range expansion and the process of red squirrel replacement would be slow. Model results for an assumed worst-case scenario where grey squirrels have expanded to all regions in Scotland identified forest regions – denoted natural strongholds – that could currently support red squirrels under UK Forestry Standard management practice. The results will be used to inform forest management policy and support a strategic review of red squirrel management by land management agencies and other stakeholders.

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Native and invasive squirrels show different behavioural responses to scent of a shared native predator

Royal Society Open Science ◽

10.1098/rsos.191841 ◽

2020 ◽

Vol 7 (2) ◽

pp. 191841 ◽

Cited By ~ 3

Author(s):

Joshua P. Twining ◽

W. Ian Montgomery ◽

Lily Price ◽

Hansjoerg P. Kunc ◽

David G. Tosh

Keyword(s):

Species Interactions ◽

Native Species ◽

Prey Species ◽

Red Squirrel ◽

Pine Marten ◽

Grey Squirrel ◽

Red Squirrels ◽

Behavioural Responses ◽

Grey Squirrels ◽

Native Predator

Invasive species pose a serious threat to native species. In Europe, invasive grey squirrels ( Sciurus carolinensis ) have replaced native red squirrels ( Sciurus vulgaris ) in locations across Britain, Ireland and Italy. The European pine marten ( Martes martes ) can reverse the replacement of red squirrels by grey squirrels, but the underlying mechanism of how pine martens suppress grey squirrels is little understood. Research suggests the reversal process is driven by direct predation, but why the native red squirrel may be less susceptible than the invasive grey squirrel to predation by a commonly shared native predator, is unknown. A behavioural difference may exist with the native sciurid being more effective at avoiding predation by the pine marten with which they have a shared evolutionary history. In mammals, olfactory cues are used by prey species to avoid predators. To test whether anti-predator responses differ between the native red squirrel and the invasive grey squirrel, we exposed both species to scent cues of a shared native predator and quantified the responses of the two squirrel species. Red squirrels responded to pine marten scent by avoiding the feeder, increasing their vigilance and decreasing their feeding activity. By contrast, grey squirrels did not show any anti-predator behaviours in response to the scent of pine marten. Thus, differences in behavioural responses to a shared native predator may assist in explaining differing outcomes of species interactions between native and invasive prey species depending on the presence, abundance and exposure to native predators.

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New World origins for haemoparasites infecting United Kingdom grey squirrels (Sciurus carolinensis), as revealed by phylogenetic analysis of bartonella infecting squirrel populations in England and the United States

Epidemiology and Infection ◽

10.1017/s0950268802007768 ◽

2002 ◽

Vol 129 (3) ◽

pp. 647-653 ◽

Cited By ~ 12

Author(s):

K. J. BOWN ◽

B. A. ELLIS ◽

R. J. BIRTLES ◽

L. A. DURDEN ◽

J. LELLO ◽

...

Keyword(s):

United States ◽

United Kingdom ◽

New World ◽

Phylogenetic Analyses ◽

The United States ◽

Sciurus Carolinensis ◽

Red Squirrel ◽

Red Squirrels ◽

The United Kingdom ◽

Grey Squirrels

Phylogenetic analyses of bartonella have suggested divergence between bartonellae that infect mammals native to the Old and New Worlds. We characterized bartonella isolated from Eastern grey squirrels (Sciurus carolinensis) in the United States and from grey and red squirrels (Sciurus vulgaris) in the United Kingdom by nucleotide sequence comparison (gltA and groEL). Isolates from grey squirrels in the United States and the United Kingdom were identical, and most similar to Bartonella vinsonii, a species associated with New World rodents. A single and novel bartonella genotype was obtained from all 12 red squirrel isolates. Although grey squirrels were first introduced into the United Kingdom over 125 years ago, they continue to be infected solely by the bartonella associated with grey squirrels native to the United States. These results illustrate that exotic species may be accompanied by the introduction and maintenance, over many generations, of their microparasites.

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An Opportunistic Assessment of the Impact of Squirrelpox Disease Outbreaks upon a Red Squirrel Population Sympatric with Grey Squirrels in Wales

Animals ◽

10.3390/ani12010099 ◽

2022 ◽

Vol 12 (1) ◽

pp. 99

Author(s):

Craig M. Shuttleworth ◽

David Everest ◽

Paul Holmes ◽

Suzi Bell ◽

Rachel Cripps

Keyword(s):

Survival Rates ◽

Disease Outbreaks ◽

Sciurus Carolinensis ◽

Red Squirrel ◽

Grey Squirrel ◽

Red Squirrels ◽

Local Survival ◽

Temporal And Spatial ◽

The Impact ◽

Grey Squirrels

Native red squirrels (Sciurus vulgaris) persisted in the coastal mainland woodlands of northern Gwynedd whilst sympatric with an invasive grey squirrel (Sciurus carolinensis) population suppressed by culling. Squirrelpox disease in the red squirrel population was recorded in 2017 and 2020/21. An autumn 2020 outbreak was associated with only 17.4% of animals caught and marked in the preceding June known to be present in March 2021. Despite an opportunistic data collection lacking the rigour of empirical experimental design, we observed low local survival rates similar to previously published accounts reported during major squirrelpox outbreaks. The use of a conservation dog to detect red squirrel carcasses resulted in positive detection and confirmation of a temporal and spatial expansion of one disease outbreak. The study is the first in Wales to use conservation dogs and the findings reinforce the vital strategic importance of geographical isolation reducing sympatry of red with grey squirrels in European regions where the introduced congener is a source of the squirrelpox infection.

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The preference for yew (Taxus baccata) by a red (Sciurus vulgaris) only squirrel population

Wildlife Research ◽

10.1071/wr15009 ◽

2015 ◽

Vol 42 (5) ◽

pp. 426 ◽

Cited By ~ 3

Author(s):

Amy Haigh ◽

Ruth O'Riordan ◽

Fidelma Butler

Keyword(s):

Tree Species ◽

Tree Planting ◽

Taxus Baccata ◽

Grey Squirrel ◽

Red Squirrels ◽

Coniferous Species ◽

Coniferous Tree Species ◽

Term Maintenance ◽

Grey Squirrels

Context As invasive grey squirrels continue to spread, red only areas are becoming rarer. It has been reported that red squirrels can outcompete greys only in pure coniferous woodland. In areas of sympatry with grey squirrels, there are concerns about red squirrels’ dependence on certain coniferous tree species in light of recent tree diseases. Aims This study aimed to investigate tree selection by red squirrels in an area vulnerable to the spread of the grey squirrel, but currently free of this species. Methods During 2013–14, squirrels were trapped and monitored on a 315-ha managed island, with a woodland characterised by a mixture of deciduous and coniferous species. Radio-tracking revealed that squirrels clustered their activity along a network of yew trees, a preference they showed throughout the year. Trap success was also higher in traps placed on yew trees. Yew and beech were selected most commonly, but squirrels were also observed foraging on other items, such as sycamore flowers and lichen. Squirrels spent 35% of their time foraging, utilising the greatest number of tree species in June (n = 13). In spring, squirrels foraged to a greater extent on the ground than in the trees, and exploited a lower number of tree species. Conclusions There has been little previous data on the use of yew trees by red squirrels, but they have previously been listed as a species that is preferred by red squirrels rather than greys. This study has further emphasised the importance of this tree species to red squirrels. Implications The continued spread of the grey squirrel may lead to red squirrels becoming restricted to areas of intense management such as parks and, accordingly, optimum tree planting is required from the onset for the long-term maintenance of red squirrels. With recent concern about the disease vulnerability of other coniferous species, this study emphasises the relative importance of yew and other tree species in the distribution of red squirrels.

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Imagining Rabbits and Squirrels in the English Countryside

Society and Animals ◽

10.1163/156853001753639260 ◽

2001 ◽

Vol 9 (2) ◽

pp. 163-175 ◽

Cited By ~ 1

Author(s):

Hilda Kean

Keyword(s):

Red Squirrel ◽

Way Of Life ◽

Grey Squirrel ◽

Red Squirrels ◽

The Past ◽

Country Life ◽

Post War

AbstractDrawing on contemporary coverage, particularly in The Field and Country Life, this article considers the construction of rabbits and squirrels as images of the past in England. By the 1930s, the red squirrel had become increasingly rare in the English countryside. Particularly in towns and suburbs, the population of the grey squirrel was growing rapidly. Those who saw themselves as the custodians of the countryside depicted the grey squirrel as a foreign force inimical to a mythical English way of life as epitomized by the red squirrel. In the post war period, the debate resurfaced about the nature of the countryside and who had a right to defend it. The focus then was upon the spread of myxomatosis from France, which was depicted as a foreign disease. Wild rabbits, who died in the thousands from this infection, became appropriated, as red squirrels before them, as symbols of a lyrical and ordered past in the countryside.

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Epidemiology of squirrelpox virus in grey squirrels in the UK

Epidemiology and Infection ◽

10.1017/s0950268810000816 ◽

2010 ◽

Vol 138 (7) ◽

pp. 941-950 ◽

Cited By ~ 26

Author(s):

C. M. BRUEMMER ◽

S. P. RUSHTON ◽

J. GURNELL ◽

P. W. W. LURZ ◽

P. NETTLETON ◽

...

Keyword(s):

Disease Transmission ◽

Structural Equation ◽

Reservoir Host ◽

Red Squirrel ◽

Grey Squirrel ◽

Management Options ◽

Contact Points ◽

Squirrelpox Virus ◽

The Uk ◽

Grey Squirrels

SUMMARYThe 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.

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Bacterial Pathogens and Symbionts Harboured by Ixodes ricinus Ticks Parasitising Red Squirrels in the United Kingdom

Pathogens ◽

10.3390/pathogens10040458 ◽

2021 ◽

Vol 10 (4) ◽

pp. 458

Author(s):

Lisa Luu ◽

Ana M. Palomar ◽

Gemma Farrington ◽

Anna-Katarina Schilling ◽

Shonnette Premchand-Branker ◽

...

Keyword(s):

United Kingdom ◽

Ixodes Ricinus ◽

Bacterial Pathogens ◽

Parasitic Wasp ◽

Borrelia Burgdorferi Sensu Lato ◽

Borrelia Miyamotoi ◽

Grey Squirrel ◽

Red Squirrels ◽

The United Kingdom ◽

Ixodes Ricinus Ticks

Red squirrels (Sciurus vulgaris) are native to most of Eurasia; in much of the United Kingdom, they have been supplanted by the non-native grey squirrel, and are considered an endangered species. Very little is known about the range of tick-borne pathogens to which UK red squirrels are exposed. As part of trap-and-release surveys examining prevalence of Mycobacterium spp. in red squirrel populations on two UK islands, Ixodes ricinus ticks were removed from squirrels and PCR screened for Borrelia spp., intracellular arthropod-borne bacteria and the parasitic wasp Ixodiphagus hookeri. At both sites, the most commonly encountered tick-transmitted bacterium was Borrelia burgdorferi sensu lato (overall minimum prevalence 12.7%), followed by Anaplasma phagocytophilum (overall minimum prevalence 1.6%). Single ticks infected with Spiroplasma were found at both sites, and single ticks infected with Borrelia miyamotoi or an Ehrlichia sp. at one site. Ticks harbouring Wolbachia (overall minimum prevalence 15.2%) were all positive for I. hookeri. Our study shows that UK red squirrels are potentially exposed to a variety of bacterial pathogens via feeding ticks. The effects on the health and survival of this already vulnerable wildlife species are unknown, and further studies are needed to evaluate the threat posed to red squirrels by Borrelia and other tick-borne pathogens.

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A novel poxvirus lethal to red squirrels (Sciurus vulgaris)

Journal of General Virology ◽

10.1099/vir.0.19464-0 ◽

2003 ◽

Vol 84 (12) ◽

pp. 3337-3341 ◽

Cited By ~ 35

Author(s):

Kathryn Thomas ◽

Daniel M. Tompkins ◽

Anthony W. Sainsbury ◽

Ann R. Wood ◽

Robert Dalziel ◽

...

Keyword(s):

Sequence Data ◽

Electron Microscopic Examination ◽

Skin Lesions ◽

Comparative Sequence Analysis ◽

Red Squirrel ◽

Electron Microscopic ◽

Red Squirrels ◽

North East ◽

The North ◽

The United Kingdom

A parapoxvirus has been implicated in the decline of the red squirrel in the United Kingdom. Virus was isolated from an outbreak of lethal disease in red squirrels in the north-east of England. Experimental infection of captive-bred red squirrels confirmed that this virus was the cause of the severe skin lesions observed. Electron microscopic examination of the virus showed that it had a morphology typical of parapoxviruses whilst preliminary sequence data suggested a genomic G+C composition of approximately 66 %, again similar to that found in other parapoxviruses. However Southern hybridization analysis failed to detect three known parapoxvirus genes, two of which have been found so far only in the genus Parapoxvirus. Comparative sequence analysis of two other genes, conserved across the eight recognized chordopoxvirus genera, suggests that the squirrel virus represents a previously unrecognized genus of the Chordopoxviridae.

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Spacing behaviour, kinship, and population dynamics of grey squirrels in a newly colonized broadleaf woodland in Italy

Canadian Journal of Zoology ◽

10.1139/z01-109 ◽

2001 ◽

Vol 79 (9) ◽

pp. 1533-1543 ◽

Cited By ~ 17

Author(s):

John Gurnell ◽

Luc A Wauters ◽

Damiano Preatoni ◽

Guido Tosi

Keyword(s):

Home Range ◽

Home Range Size ◽

Core Area ◽

Adult Survival ◽

Sciurus Carolinensis ◽

Red Squirrel ◽

Grey Squirrel ◽

Colonization Process ◽

Juvenile Males ◽

Grey Squirrels

Eastern grey squirrels, Sciurus carolinensis, introduced to Britain and northern Italy are replacing the native Eurasian red squirrel, Sciurus vulgaris. We studied the pattern of colonization of a high-quality broadleaf woodland by grey squirrels by means of livetrapping and radio-tracking. The studies started in July 1996, when six grey squirrels (four males, two females) first colonized the woodland, and lasted until November 1998, when densities exceeded those of the local red squirrel population. Grey squirrel colonization was rapid, with a high proportion of adult and yearling females breeding. Juvenile recruitment was also higher than in stable populations in Britain. Adult survival was better in 1997 (83%) than in 1998 (47%), with predation accounting for 67% of losses in 1998. This indicates the effects of local predator communities on the colonization process. Densities of grey squirrels were moderate in 1998, with a maximum of 1.9 squirrels/ha and we expect density to increase further. Adult home range sizes were three to four times larger than those of subadults, and male ranges were larger than those of females. Body mass was positively correlated with both total home range size and core-area size. Core-area size for adults was inversely correlated with food availability. Juvenile female grey squirrels were philopatric, forming female kin groups, while most juvenile males settled outside the mother's home range.

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