Remnant red squirrel populations in the UK mainland are threatened by squirrelpox viral disease and the reservoir of the squirrelpox virus, the invasive grey squirrel, is expanding its range. Until this threat can be effectively mitigated, there is a high risk from disease outbreaks, following proposed conservation translocation of red squirrels

Chantrey, J

Ewen, JG

Gurnell, J

Hudson, P

Karesh, WB

Kock, RA

Lurz, PWW

Meredith, A

Sainsbury, AW

Tompkins, DM

English

UCL Discovery

L E T T E R S AND COMMENT SImplications of squirrelpox virus for successful red squirreltranslocations within mainland UKAnthony W. Sainsbury1 | Julian Chantrey2 | John G. Ewen1,3 |John Gurnell4 | Peter Hudson5 | William B. Karesh6 | Richard A. Kock7 |Peter W. W. Lurz8 | Anna Meredith8,9 | Daniel M. Tompkins101Institute of Zoology, Zoological Society ofLondon, Regent's Park, London, UK2School of Veterinary Science, Universityof Liverpool, Liverpool, UK3IUCN SSC Conservation TranslocationSpecialist Group, UK4Queen Mary, University of London,London, UK5Nelson Mandela African Institute—Arusha, A co-hire of The HuckInstitutes & The Institutes of Energy &The Environment, Penn State University,Pennsylvania6IUCN SSC Wildlife Health SpecialistGroup Chair, EcoHealth Alliance,New York, New York7Royal Veterinary College, London, UK8Royal (Dick) School of Veterinary Studiesand Roslin Institute, University ofEdinburgh, Roslin, Midlothian, UK9Melbourne Veterinary School, Faculty ofVeterinary and Agricultural Sciences,University of Melbourne, Parkville, VIC,Australia10University of Otago, Auckland,New ZealandCorrespondenceAnthony W. Sainsbury, Institute ofZoology, Zoological Society of London,Regent's Park, London NW1 4RY, UK.Email: tony.sainsbury@ioz.ac.ukAbstractRemnant red squirrel populations in the UK mainland are threatened bysquirrelpox viral disease and the reservoir of the squirrelpox virus, the invasivegrey squirrel, is expanding its range. Until this threat can be effectively miti-gated, there is a high risk from disease outbreaks, following proposed conser-vation translocation of red squirrels.KEYWORD Sanimal welfare, epidemiology, impact of disease on populations, infectious disease, pathology,reintroduction biology, Sciuridae, squirrelpoxIn the later decades of the 20th century, researchersestablished that infectious diseases could regulate and neg-atively impact population numbers of free-living wild ani-mals (Hudson, Dobson, & Newborn, 1998; McCallum &Dobson, 1995; Tompkins et al., 2001) and potentially leadto species extinction (de Castro & Bolker, 2005). Extinc-tions have subsequently been shown to be strongly associ-ated with infectious diseases, for example chytridiomycosisReceived: 5 January 2020 Revised: 10 March 2020 Accepted: 12 March 2020DOI: 10.1111/csp2.200This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, providedthe original work is properly cited.© 2020 The Authors. Conservation Science and Practice published by Wiley Periodicals, Inc. on behalf of Society for Conservation BiologyConservation Science and Practice. 2020;e200. wileyonlinelibrary.com/journal/csp2 1 of 4https://doi.org/10.1111/csp2.200in amphibians (Cheng, Rovito, Wake, & Vredenburg, 2011;Lips et al., 2006; Scheele et al., 2019). In the early part ofthe current century evidence from seroprevalence, experi-mental infection, spatial epidemiology and modeling stud-ies (Rushton et al., 2006; Sainsbury et al., 2008; Sainsbury,Nettleton, Gilray, & Gurnell, 2000; Tompkins, Sainsbury,Nettleton, Buxton, & Gurnell, 2002) showed thatsquirrelpox viral disease (SQPx) has a negative impact onUK red squirrel (Sciurus vulgaris) populations through epi-demics, and that grey squirrels (Sciurus carolinensis) arethe reservoir host of squirrelpox virus (SQPV). Where theSQPV and grey squirrels are present, red squirrel decline isestimated to be 25 times faster than in locations where redsquirrels and grey squirrels co-exist without SQPV(Rushton et al., 2006). Seroprevalence and PCR studieshave shown that a high proportion of grey squirrels areexposed to SQPV (Sainsbury et al., 2000) and frequentlyshed it sub-clinically for extended periods (Chantrey, Dale,Jones, Begon, & Fenton, 2019). Experimental translocationof red squirrels to an area where grey squirrels were pre-sent, and controlled through trapping and culling, was ini-tially successful but later failed due to an epidemic of SQPx(Carroll, Russell, Gurnell, Nettleton, & Sainsbury, 2009).Epidemics of SQPx continue to occur in the UK whereremnant red squirrel populations are in contact with greysquirrels (Chantrey et al., 2014; Everest et al., 2017) leadingto the gradual extirpation of an important part of woodlandbiodiversity possibly with unique haplotypes (Ogden,Shuttleworth, McEwing, & Cesarini, 2005). However, thegradual spread of SQPx epidemics across the UK mainlandlandscape for over 100 years (Chantrey et al., 2014;Edwards, 1962; Middleton, 1930; Sainsbury et al., 2008;Sainsbury & Ward, 1996; Shorten, 1954), suggests contactbetween some red squirrel populations and SQPV may bedelayed for years/decades.Over the last 10 years, there have been discussions onthe pros and cons of translocating red squirrels to, andwithin, mainland UK for conservation purposes. We arewriting to remind readers that, given the current scien-tific understanding of the epidemiology of SQPV in UKsquirrel populations, and the absence of an effectivemethod to permanently remove grey squirrels from pro-posed release areas with a suitable buffer, justifying suchtranslocations is currently difficult. The IUCN Guidelinesfor Reintroductions and Other Translocations(IUCN, 2013) recommend that conservation plannersshould establish “strong evidence that the threat(s) whichcaused any previous extinction have been correctly iden-tified and removed or sufficiently reduced.” The causes ofprior red squirrel extinction have been identified but thethreat in mainland UK, in the long term, remains largelyunchanged because the reservoir of SQPV has a wide-spread and expanding distribution. The undertaking ofmainland conservation translocations therefore would becontrary to recommended best practice because the origi-nal causes of decline (grey squirrel competition and theSQPV reservoir) cannot currently be managed to a pointwhere reintroductions are justified. Any translocatedpopulation of red squirrels should be safeguarded againstcontact with SQPV over the long term. Failure to guaran-tee long-term commitments to grey squirrel eradicationat appropriate spatial scales equates to a very high riskthat translocations will be unsuccessful at establishinghealthy viable populations due to the key reasons whythe species declined in the first place.Reduction in grey squirrel density in Wales andnorthern England by culling reduced SQPV seropreva-lence in grey squirrel populations (4% seroprevalence,n = 28, Schuchert, Shuttleworth, McInnes, Everest, &Rushton, 2014; 27% seroprevalence, n = 160, Chantreyet al., 2014). Such management would thus likely reducethe risk to red squirrels from SQPx and provides hope forred squirrel recovery. However, even if temporary redsquirrel (re-)establishment is possible in sites where greysquirrels are controlled (Schuchert et al., 2014), the fun-damental problem is that the reservoir of SQPV, the greysquirrel, remains and is capable of prolific breeding anddispersal (Gurnell, 1996). Illustrating this threat,Schuchert et al. (2014) and Chantrey et al. (2019)reported high seroprevalences of SQPV in grey squirrelpopulations surrounding control zones (67%, samplenumbers not reported, Schubert et al 2014; 80–100%,n = 103, Chantrey et al., 2019). SQPx outbreaks in geo-graphic regions where grey squirrels have been con-trolled (Carroll et al., 2009; Everest et al., 2017) areanother reminder of the difficulty of managing thisthreat. While epidemics of SQPx are initiated throughtransmission of the virus from grey squirrels to red squir-rels, once the virus has spilled over, they are sustained bythe red squirrel population (Chantrey et al., 2014). Thus,single inter-species transmission events can cause epi-demics. Unfortunately, available evidence suggests cur-rent grey squirrel culling programs do not prevent allincursions and epidemics are still to be expected(Chantrey et al., 2014) even if red squirrel and grey squir-rel populations may co-exist for several years before spill-over of SQPV occurs and epidemics are seen (McInneset al., 2009; Rushton et al., 2006; Sainsbury et al., 2008).If re-established red squirrel populations on the mainlandare to be protected in the face of SQPx, ceaseless andintensive grey squirrel control operations will be needed,requiring continuous and substantial resources, unlessresearch efforts can develop enhanced methods.Where local grey squirrel control operations are notsufficient in scale or intensity, we thus believe that trans-locations of red squirrels to sites on the mainland2 of 4 SAINSBURY ET AL.increase the risk of SQPx epidemics in the long term.SQPV can cause multifocal, erythematous, exudative der-matitis and cutaneous ulceration in red squirrels leadingto pain and stress lasting days (Carroll et al., 2009;Sainsbury & Ward, 1996; Tompkins et al., 2002), indicat-ing established signs of an anthropogenic welfare prob-lem in free-living wild animals (Kirkwood, Sainsbury, &Bennett, 1994; Sainsbury, Bennett, & Kirkwood, 1995).Hence, in addition to the potential conservation failure,the consequential disease, emanating from purposefultranslocation, represents a serious animal welfare con-cern, for which the translocation planners have aresponsibility.Efforts to better understand and mitigate the causesfor red squirrel decline, including studies to remove thedisease threat (for example, Ballingall et al., 2016), andcontinued work to design and implement consistentlandscape level removal of grey squirrels could make apositive contribution to red squirrel conservation. Weremain optimistic that red squirrel recovery is possible inthe UK, but only once the original causes of extinctionhave been sufficiently managed.CONFLICT OF INTERESTNo conflict of interest is disclosed by the authors.AUTHOR CONTRIBUTIONSTony Sainsbury wrote the original manuscript. ProfessorsChantry, Kock and Meredith contributed to the paperwith refinements regarding epidemiology and pathology.Professors Tompkins and Hudson revised the paper inthe context of ecology and epidemiology. ProfessorGurnell and Dr Lurz provided input on epidemiology inthe context of squirrel ecology. Dr Ewen modified themanuscript with respect to reintroduction biology andwith Dr Karesh, provided an IUCN perspective. TonySainsbury revised the paper to incorporate reviewers sug-gestions and received comments prior to submission fromthe other authors.ETHICS STATEMENTThis paper is a review and scientific opinion piece andthe work involved has not been considered by an ethicalreview committee.ORCIDAnthony W. 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Implications ofsquirrelpox virus for successful red squirreltranslocations within mainland UK. ConservationScience and Practice. 2020;e200. https://doi.org/10.1111/csp2.2004 of 4 SAINSBURY ET AL.

Implications of squirrelpox virus for successful red squirrel translocations within mainland UK

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Implications of squirrelpox virus for successful red squirrel translocations within mainland UK

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