Squirrelpox Virus in Red Squirrels (Sciurus vulgaris) in the Republic of Ireland

Introduced alien species can act as vectors for disease posing a threat to biodiversity. Two squirrel species are found in Ireland, the European red squirrel (Sciurus vulgaris) and the eastern grey squirrel (Sciurus carolinensis). The grey squirrel was introduced at Castleforbes, County Longford, Ireland, in 1911 and is now found in 26 of 32 counties (Carey et al., 2007). Its rapid expansion was accompanied by a decline in red squirrel numbers and a range contraction of 20%. Red squirrels are listed as near threatened on the Red List for Irish Mammals (Marnell et al., 2009).

In the UK, grey squirrels were introduced at multiple locations between 1876 and 1920 (Gurnell et al., 2008). Red squirrels are now extinct in southern England, except for some offshore islands. A few isolated populations still exist in central England and Wales with the remaining strongholds in northern England and Scotland (Gurnell et al., 2008). Squirrelpox virus (SQPV) has been identified as the probable mediator of competition between the species involved in several UK red squirrel population declines (Rushton et al., 2006). Grey squirrels carry the virus without usually developing the disease (Sainsbury et al., 2000).

In Ireland, while antibodies to SQPV have been detected in grey squirrels from Northern Ireland and the Republic (McInnes et al., 2013), SQPV disease in red squirrels was confirmed only in 2011 in Tollymore Forest, County Down, Northern Ireland. The Tollymore population suffered a 93% decline between 2008 and 2011, but the presence of an adenovirus may have been a contributing factor (Everest et al., 2012). This article describes the first case of SQPV disease in a wild red squirrel in the Republic of Ireland, ca. 180 km from Tollymore.

In November 2011, a dead juvenile female red squirrel found at Hollywood, County Wicklow (53°6′3.04″N, 6°35′43.47″W) was submitted to the School of Veterinary Medicine, University College Dublin for postmortem examination. The carcass was in a good state of preservation and raised alopecic and crusting dermal lesions were observed on the upper and lower lip, periocular (Fig. 1A), vulval folds, and some nail beds, in particular the right forelimb medial digit. The animal had one tick and fleas. The carcass was dry and sticky suggestive of dehydration. There were no body fat stores, and the alimentary tract was empty. Coning of the cerebellum was suggestive of brain edema.

Microscopic examination of skin samples revealed moderate epidermal hyperplasia with multifocal regions of ballooning degeneration of keratinocytes in all levels of the epidermis and in follicular epithelium. These cells frequently contained large oval intracytoplasmic and occasional intranuclear, viral inclusion bodies (Fig. 1B). In other skin samples there were epidermal erosions and full-thickness necrosis (ulceration) with serocellular crusting and extensive mixed neutrophil-rich inflammatory cell infiltrations of the adjacent dermis.

Selected samples of skin lesions were snap-frozen in liquid nitrogen, stored at −80 C, and subsequently submitted for electron microscopic analysis at Animal Health and Veterinary Laboratories Agency, Weybridge, UK, where typical SQPV particles were identified (Fig. 1C). Further evidence of SQPV infection was obtained by PCR amplification of a 143-base pair fragment of the SQPV G8R homologue (sequence kindly provided by Julian Chantrey, University of Liverpool) from a 25 mg snap-frozen segment of a lip lesion. Sequencing of the PCR amplicon [DNA Sequencing Services, University of Dundee, Dundee, Scotland (http://www.dnaseq.co.uk)] confirmed it to be identical to SQPV G8R sequence (Atkin et al., 2010).

This is the first confirmed case of SQPV disease in red squirrels in the Republic of Ireland. Antibody-positive grey squirrels were identified from three of four sites tested in the Republic (McInnes et al., 2013), and thus this first confirmation may be representative of an infection going undetected or may represent the first true occurrence. While this case was largely detected due to the vigilance and enthusiasm of an observer, the location is of interest. The area was first colonized by grey squirrels between 1978 and 1997 (Carey et al., 2007) and represents one of the more recently established populations. However, Wicklow has the highest density of forestry (16.1% of land area) of any Irish county (Nieuwenhuis et al., 2007) and is highly suited to squirrel movement, colonization of the entire county having occurred at a rate of 5 km/yr within 10 yr (Carey et al., 2007). The large number of sightings may also indicate a significant density increase since establishment. Additionally, the dense interconnecting network of habitat patches facilitating movement increases the potential for interspecies contact. The timing of this case is consistent with increased movement during autumn juvenile dispersal (Gurnell et al., 2008). Prevalence of SQPV antibodies in grey squirrels increases from autumn to winter, which correlates with increases in space-use patterns and increases the probability of encountering a carrier (Bruemmer et al., 2010). Following the public announcement including a request for sightings of dead or dying red squirrels (NPWS, 2011), two further cases were reported soon after nearby, in Kilmacanogue, north County Wicklow, and in south County Dublin; however, neither were submitted for confirmation.

The presence of SQPV disease in the Republic of Ireland puts additional pressure on red squirrel conservation efforts. Compared to mainland UK and Northern Ireland, efforts are still at an early stage and have concentrated on conservation introductions at suitable sites beyond the grey squirrel–colonizing front (Waters and Lawton, 2011). This may not prove a long-term effective strategy. Increases in forestry planting (Nieuwenhuis et al., 2007) coupled with the advancing colonizing front make it likely that grey squirrels will eventually reach these sites. The only way to ensure SQPV does not have as devastating effect on red squirrels in Ireland, as it has in the UK, is to focus efforts on minimizing species contact.

Grey squirrels are listed in the third schedule of S.I. 477 of 2011, European Communities (Birds and Natural Habitats) Regulations 2011. As such, if they threaten protected habitats or species, the Minister may develop threat response plans, which include exclusion, control, or eradication. Grey squirrels clearly threaten red squirrels in Ireland and damage forest habitats by bark stripping (Nieuwenhuis et al., 2007). Aside from SQPV, they are also potential reservoirs for adenoviruses (Everest et al., 2009), an additional threat to red squirrels recently confirmed in Northern Ireland (Everest et al., 2012).

We acknowledge the technical assistance of Brian Cloak with photography and Joseph Brady with histopathology preparations.