John Gurnell

Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines

The disease implications of novel pathogens need to be considered when investigating the ecological impact of species translocations on native fauna. Traditional explanations based on competition or predation may often not be the whole story. Evidence suggests that an emerging infectious disease, caused by a parapoxvirus, may be a significant component of the impact that the introduced grey squirrel has had on UK red squirrel populations. Here we validate the potential role of parapoxvirus by proving that the virus is highly pathogenic in the red squirrel while having no detectable effect on grey squirrel health.

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.

The effects of food availability and winter weather on the dynamics of a grey squirrel population in southern England

The population ecology of grey squirrels Sciurus carolinensis living in a 9-ha oak Quercus robur wood in southern England was studied between 1976 and 1987 using live-trapping techniques. Trapping was carried out in winter, spring and summer. The availability of tree seeds during the autumn of each year, and the severity of cold weather over each winter were also measured to examine their effects on squirrel population dynamics. Capture probabilities of squirrels in winter, and to a lesser extent in spring, were inversely related to food availability and data from these two seasons were not considered dependable. The analyses concentrated on the summer populations. The long-term average summer density of squirrels was high at 8.8 ha -1 (SE 3.41 ha -1 ) demonstrating that the oak wood was high quality habitat for grey squirrels. Over 10 of the 12 years, summer densities were remarkably similar, ranging between 7 ha -1 and 10 ha -1 (mean 8.5 ha -1 , SE 0.95 ha -1 ). However, numbers were driven upwards in 1977 to a density approaching 18 ha -1 and downwards in 1982 to a density of about 3 ha -1 : a 6-fold difference. In good seed years, breeding starts in December, in poor seed years the start of breeding is deferred until the spring. There was no or very little spring breeding in 5 years when food supplies were poor. Female reproductive success was positively associated with food availability. Partial correlation analysis showed that the level of association was not improved when the effects of winter weather were taken into account. The number of new adult females in the summer population was positively associated with food availability but there was no association between new males and food. This suggests that food availability is more important to breeding females than breeding males. Persistence from summer to winter was positively associated with food availability, but persistence from summer to spring and to the following summer were not. Partial correlation analyses showed that the severity of winter weather tended to mask the effects of food availability on persistence and the partial correlation coefficients were higher when the effects of weather were held constant. Adult females had the highest persistence between summers (52%, n = 11, SE 6%), followed by juvenile females (38%, n = 7, SE 8%), adult males (36%, n = 11, SE 4%), and juvenile males (21%, n = 7, SE 7%). The persistence of adult males but not females was inversely related to the initial number of males present. In males, there was no significant difference in winter body mass between years and winter body mass was not associated with food availability, although there were very few data for winters when the food supply was good. In 7 years when the food supply was poor to moderate, there was an increase in mean body mass between summer and winter in 4 years, and a decrease in 3 years. The data were explored using ordination techniques; first a standardized principal component analysis and then the canonical form of principal component analysis or redundancy analysis. The analysis was carried out on years derived from MNA of males and females and various combinations of the environmental variables: food availability (FOOD) and the severity of winter weather (TEMP). The ordination biplots clearly showed the high correlation between MNA males and MNA females and that FOOD was the most important environmental variable. TEMP on its own had no effect but FOOD x TEMP was important. Following on the exploratory data analysis and for predictive purposes, a general linear model between the numbers of squirrels in the summer populations and sex, FOOD and FOOD x TEMP as explanatory variables accounted for 77% the variance in squirrel numbers among years. This study shows that tree seed availability is the most important factor limiting grey squirrel densities, but this factor both positively and negatively interacts with the severity of w

Interspecific competition between native Eurasian red squirrels and alien grey squirrels: does resource partitioning occur?

Abstract. In heterogeneous environments, differential niche selection by two competing species will result in niche partitioning so that individuals of each species can maximise their fitness under different sets of environmental variables. Thus, niche partitioning is considered essential to allow co-existence of ecologically related species. To assess whether niche partitioning was occurring between native red squirrels and alien grey squirrels living together in a 13-ha high-quality mixed deciduous woodland in north Italy, we investigated temporal and spatial patterns in their activity and foraging behaviour between 1996 and 1998. We used live trapping and radio-tracking to study numbers, distribution and behaviour of squirrels. Daily and seasonal temporal activity patterns, and activity on the ground and in the trees, were similar in the two species. However, grey squirrels were more tree specialists and had a narrower tree-species niche width than red squirrels, in particular making greater use of oak. Other studies of red and grey squirrels in allopatry show that the two species differ in the extent they utilise oak. Overall, tree-species niche overlap was about 70%. Grey squirrels had larger home ranges than red squirrels. Home ranges and core areas of both species were larger in males than females. Also, intraspecific home range and core-area overlap patterns were similar to those found in allopatric populations of these species. Overall, there was no evidence that the use of space of one species was affected by the other. Our results show that there was no niche partitioning of activity or foraging behaviour in time or space during the study. This suggests that, at moderate grey-squirrel densities, red squirrels are unable to avoid competition with grey squirrels, and that competition for food and/or space will occur when these resources become limiting.

Poxviral disease in red squirrels Sciurus vulgaris in the UK: spatial and temporal trends of an emerging threat.

The squirrel poxvirus (SQPV) is the probable mediator of apparent competition between the introduced invading gray squirrel (Sciurus carolinensis) and the red squirrel (Sciurus vulgaris) in the UK, and modeling studies have shown that this viral disease has had a significant impact on the decline of the red squirrel in the UK. However, given our limited understanding of the epidemiology of the disease, and more generally the effects of invasive species on parasite ecology, there is a need to investigate the transmission dynamics and the relative pathogenicity of the virus between species. We aimed to increase our knowledge of these processes through an empirical study in which we: (i) used pathological signs and transmission electron microscopy (TEM) to diagnose SQPV disease in red squirrels found dead during scanning surveillance between 1993 and 2005; (ii) detected antibody to SQPV using an enzyme-linked immunosorbent assay (ELISA) in the same animals; and (iii) mapped cases of the disease, and the gray squirrel distribution, using a geographical information system. We analyzed the distribution of cases of SQPV disease according to woodland type, a measure of squirrel density. SQPV disease occurred only in areas of England also inhabited by seropositive gray squirrels, and as the geographical range of gray squirrels expanded, SQPV disease occurred in these new gray squirrel habitats, supporting a role for the gray squirrel as a reservoir host of the virus. There was a delay between the establishment of invading gray squirrels and cases of the disease in red squirrels which implies gray squirrels must reach a threshold number or density before the virus is transmitted to red squirrels. The spatial and temporal trend in SQPV disease outbreaks suggested that SQPV disease will have a significant effect on Scottish populations of red squirrels within 25 years. The even spread of cases of disease across months suggested a direct rather than vector-borne transmission route is more likely. Eight juvenile and sub-adult free-living red squirrels apparently survived exposure to SQPV by mounting an immune response, the first evidence of immunity to SQPV in free-living red squirrels, which possibly suggests a changing host-parasite relationship and that the use of a vaccine may be an effective management tool to protect remnant red squirrel populations.

Epidemics of squirrelpox virus disease in red squirrels {Sciurus vulgaris): temporal and serological findings

Squirrelpox virus (SQPV) causes a fatal disease in free-living red squirrels (Sciurus vulgaris) which has contributed to their decline in the United Kingdom. Given the difficulty of carrying out and funding experimental investigations on free-living wild mammals, data collected from closely monitored natural outbreaks of disease is crucial to our understanding of disease epidemiology. A conservation programme was initiated in the 1990s to bolster the population of red squirrels in the coniferous woodland of Thetford Chase, East Anglia. In 1996, 24 red squirrels were reintroduced to Thetford from Northumberland and Cumbria, while in 1999 a captive breeding and release programme commenced, but in both years the success of the projects was hampered by an outbreak of SQPV disease in which seven and four red squirrels died respectively. Valuable information on the host-pathogen dynamics of SQPV disease was gathered by telemetric and mark-recapture monitoring of the red squirrels. SQPV disease characteristics were comparable to other virulent poxviral infections: the incubation period was <15 days; the course of the disease an average of 10 days and younger animals were significantly more susceptible to disease. SQPV disease places the conservation of the red squirrel in jeopardy in the United Kingdom unless practical disease control methods can be identified.

Grey squirrel Sciurus carolinensis management in Italy - squirrel distribution in a highly fragmented landscape

American grey squirrels Sciurus carolinensis introduced to northern Italy in 1948 have caused damage to commercial poplar plantations and have replaced the native red squirrel Sciurus vulgaris from most of the 350 km2 of the Piedmont Po-plain they currently occupy. In order to plan a control programme aiming to stop grey squirrels from further spreading and to decrease their numbers, the current distribution and population size in the highly fragmented landscape of the Po-plain were studied. The probability of finding grey squirrels in woodland fragments increased with habitat quality (diversity of trees producing large, consumable seeds), woodlot size and the proportion of poplar. Adding isolation variables did not improve the fit of the logistic regression model that predicted squirrel presence. The density of squirrel dreys, an index of population density, in the large Stupinigi forest also increased with tree species diversity. An estimate of the minimum population size for all woodlots assessed for squirrel presence was 1,260 animals in the summer of 1996. This extrapolates to a total of ca 2,500 grey squirrels in Piedmont. Grey squirrels continue to increase their range and are getting close to the continuous mixed forests of the pre-Alps and to large hazel plantations. Control measures to stop the spread of grey squirrels, and eventually to eradicate them, should be implemented immediately.

Epidemiology of squirrelpox virus in grey squirrels in the UK

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.

Population ecology of the red squirrel ( Sciurus vulgaris ) in a fragmented woodland ecosystem on the Island of Jersey, Channel Islands

The Channel Island of Jersey is 116 km2 but has only 540 ha of woodland distributed in 237 wooded fragments with mean size of 2.5 ha. Despite this, the island supports 300 to 600 red squirrels Sciurus vulgaris, a species that is under threat in mainland Britain from habitat fragmentation, disease and the spread of the alien grey squirrel S. carolinensis. Grey squirrels are not present on Jersey. Between 1994 and 1997, using trapping and tracking techniques, we studied how red squirrels survive on Jersey by focusing on three local populations in sites B, C and S with contrasting food availability. The primary squirrel foods at site B were autumn tree seeds, at site C autumn tree seeds and summer conifer cones, and at site S autumn tree seeds and ad libitum, year-round supplementary food provided by local people. The densities of squirrels in site C (mean over 3 years 0.97 ha−1) and site S (1.21 ha−1) were more than one and a half times that of site B (0.68 ha−1), which relied on autumn seeds. Body mass and condition, and early breeding (spring litters) were not affected by food availability although conception occurred as early as November, earlier than in mainland Britain. Less than 50% of females produced summer litters, and 88% of non-breeders did not receive supplementary food. Turnover rates were lowest and most stable in site B. Annual residency was not influenced by the size of the natural tree seed crop. Cat and road kills caused two out of three reported deaths. This island population seems to remain viable as a result of an extended breeding season and increased population densities in sites with summer or supplementary food. The results emphasize the beneficial effects of extra food provided by local people. This provides a buffering effect against variations in natural food availability, and seems to be important for their long-term survival.

Modeling impacts and costs of gray squirrel control regimes on the viability of red squirrel populations

The introduced gray squirrel (Sciurus carolinensis) is a principal threat to the populations of the red squirrel (S. vulgaris). We used a spatially explicit population dynamics model to investigate the changes of red and gray squirrel populations in landscapes to assess the effects of gray squirrel population control methods on red squirrel population viability. We analyzed 2 methods of gray squirrel population control: (1) trapping where adults were killed on an annual basis, and (2) immunocontraception where reproduction was suppressed. The model was run under a range of efficiency and intensity of control as well as red and gray squirrel life-history scenarios created by Latin Hypercube Sampling of the realistic parameter range for both demographic and control variables. The viability of squirrel populations in 2 contrasting landscape scenarios was investigated: (1) Thetford Forest, East Anglia, United Kingdom (UK), where a small isolated population of red squirrels is surrounded by a large population of gray squirrels; and (2) Redesdale Forest, Northumberland, UK, where red squirrels are still in abundance and the first gray squirrels were observed to disperse into the area from Scotland. In the absence of population control of gray squirrels, red squirrel populations were predicted to become extinct in both landscapes within 15 years at Thetford and 6 years at Redesdale. Immunocontraception did not lead to persistent populations at Thetford but allowed red squirrels to persist in Redesdale. Removal of gray squirrels by trapping at both sites was predicted to lead to red squirrel population persistence. Our findings suggest that immunocontraception is unlikely to be effective unless it is applied to a large portion of the target and surrounding population. Our results also indicate that an integrated control strategy, incorporating both trapping and immunocontraception, may be the best option for controlling gray squirrels. This integrated strategy needs to include the relative costs of control, and it may be that immunocontraception provides the best overall solution in areas where gray squirrels are low in abundance.