Native Eurasian Red Squirrels Research Articles

Physiological stress response to urbanisation differs between native and invasive squirrel species

Novel pressures derived from urbanisation can alter native habitats and ultimately impact wildlife. Coping with such human-driven changes might induce shifts in species phenotypic traits, such as physiological responses to anthropogenic stressors. Preadaptation to face those challenges has been suggested to favour settlement and spread of invasive alien species in urbanised areas which, consequently, might respond differently than ecologically similar native species to stressors posed by urbanisation. The activation of the hypothalamic-pituitary-adrenal (HPA) axis and the subsequent release of glucocorticoids (GCs) has been suggested to mediate responses to anthropogenic disturbance in vertebrates. Furthermore, intraspecific competition, in conjunction with stressors related to urbanisation, might affect invasive and native species physiological stress responses differently. Using a parallel pseudo-experimental study system we measured faecal glucocorticoid metabolite (FGM) concentrations of the native Eurasian red squirrel and the invasive alien Eastern grey squirrel along a rural-urban gradient and in relation to conspecific density. The two species responded differently to challenges posed by the synergic effect of urbanisation and intraspecific competition. Association of FGMs and conspecific density in native red squirrels varied between rural and suburban sites, potentially depending on differential HPA axis responses. In urban sites, this relationship did not differ significantly from that in rural and suburban ones. Conversely, invasive grey squirrels' FGMs did not vary in relation to conspecific density, nor differed along the rural-urban gradient. Improving knowledge about native and competing invasive species' physiological responses to anthropogenic stressors can support conservation strategies in habitats altered by man. Our findings suggested that the invasive squirrels might be preadapted to cope with these challenges in urbanised areas, potentially increasing their success under the future global change scenario.

The advantage of living in the city: effects of urbanization on body size and mass of native and alien squirrels

AbstractIn an ever more urbanized world, animals have to cope with different challenging conditions that may shape the individual’s phenotype in the urban environment. Since body mass and body size are found to be related to fitness in many species, investigating the variation in these two morphological traits along the rural-urban gradient, is a first step to understand how animals adapt to urbanization. Here we studied two tree squirrels, the native Eurasian red squirrel (Sciurus vulgaris) and the invasive Eastern grey squirrel (Sciurus carolinensis), using a pseudo-experimental design with replicated study sites (2 rural, 2 suburban and 2 urban sites for each species). We investigated whether squirrels differed in body size and body mass along the urbanization gradient and whether the invasive alien squirrels had more marked differences along the gradient, showing a higher adaptation capacity. We did not find variation in body size in red squirrels along the gradient, but invasive grey squirrels were slightly larger in urban than in other area-types. In both species, animals of either sex were heavier in the urban than in the rural sites, while the difference between urban and suburban areas depends on species and sex. Hence, morphologically both native and invasive species showed similar changes, with higher body mass in urban habitat, which could result in higher fitness, since body mass in squirrels species is positively related to reproductive success.

Interactions between native and invasive species: A systematic review of the red squirrel-gray squirrel paradigm

The eastern gray squirrel (Sciurus carolinensis) has been labeled as one of the 100 worst invasive alien species by the IUCN. In Europe, the species has been introduced to Britain, Ireland and Italy, and its subsequent spread has resulted in wide-scale extinction of native Eurasian red squirrels (Sciurus vulgaris) from the areas colonized by the gray squirrel. This replacement of a native by an alien competitor is one of the best documented cases of the devastating effects of biological invasions on native fauna. To understand how this replacement occurs, we present a systematic review of the literature on competition and interactions between red and gray squirrels. We describe the patterns of red and gray squirrel distribution in those parts of Europe where gray squirrels occur and summarize the evidence on the different processes and mechanisms determining the outcome of competition between the native and alien species including the influence of predators and pathogens. Some of the drivers behind the demise of the red squirrel have been intensively studied and documented in the past 30 years, but recent field studies and mathematical models revealed that the mechanisms underlying the red-gray paradigm are more complex than previously thought and affected by landscape-level processes. Therefore, we consider habitat type and multi-species interactions, including host-parasite and predator-prey relationships, to determine the outcome of the interaction between the two species and to better address gray squirrel control efforts.

Health Status of the Eastern Grey Squirrel (Sciurus carolinensis) Population in Umbria: Results of the LIFE Project 'U-SAVEREDS'.

Simple SummaryInvasive alien species are non-native species introduced deliberately or unintentionally beyond their past or present natural distribution, and their introduction and spread threatens local biological diversity. The Eastern grey squirrel is native to North America and was introduced to the British Islands, Italy, and South Africa. Around the year 2000, a new population of grey squirrels was recorded in Perugia, central Italy, where the species populated an area of approximately 50 km2, both in woodland and urban areas. The Eastern grey squirrel represents a huge threat to the conservation of the native Eurasian red squirrel when the two species coexist. Moreover, given their confident behaviour with humans, the non-native squirrels can negatively impact public health. The U-SAVEREDS Project was set up for Eurasian red squirrel conservation in Umbria through the eradication of the alien species and it also provided information on the health status of the Eastern grey squirrel to identify any infectious agents. The recovery of zoonotic pathogens allowed to assess the Eastern grey squirrel’s impact on human and domestic and wild animals’ health, provide helpful feedback for the management and eradication procedures, and raise public awareness through environmental education.The introduction of the Eastern grey squirrel (Sciurus carolinensis) in Europe is one of the best-known cases of invasive alien species (IAS) colonisation, that poses a severe risk to the conservation of biodiversity. In 2003, it was released in a private wildlife park near the city of Perugia (Italy), where it is replacing the native Eurasian red squirrel (Sciurus vulgaris). The LIFE13 BIO/IT/000204 Project (U-SAVEREDS) was set up for the Sciurus vulgaris conservation in Umbria through an eradication campaign of grey squirrels. One hundred and fifty-four animals were analysed for bacteriological, mycological, virological, and serological investigations (C4 action). Sanitary screening showed that Sciurus carolinensis is a dermatophyte carrier, and therefore, it could cause public health issues for humans, considering its confident behaviour. Moreover, it has been marginally responsible for the spreading of Candida albicans, Coxiella burnetii, and Borrelia lusitaniae. Health status evaluation conducted on the Sciurus carolinensis population indicated that it is necessary to raise awareness of its impacts on biodiversity and human health. Moreover, the health status and behaviours of the IAS must be considered when control or eradication campaigns are planned.

Coming in like a wrecking-ball: are native Eurasian red squirrels displacing invasive Siberian chipmunks? A study from an urban park

Alien squirrels may seriously threaten native species by means of interspecific competition. In our work, we analysed whether the distribution of alien Siberian chipmunks within the Sigurta Garden urban park (north-eastern Italy) changed after the natural spread of native Eurasian red squirrels in a 20-year period. Distribution of both squirrels was estimated through a citizen-science approach, in the first 10-year after red squirrel arrival 1 (i.e. Decade 1: 1997–2006) and in the second 10-year interval (i.e. Decade 2: 2007–2017). We compared habitat use of both species and we assessed whether a vertical segregation occurred through a dissimilarity index. Woodlands were selected by both species in both decades. Red squirrels also selected tree lines in Decade 1. A vertical segregation was apparent in Decade 1, whereas in Decade 2 both squirrel species were observed on the lowest branches or on the ground, where they are fed by humans. This was also confirmed by the habitat niche-overlap index, which increased in Decade 2. The extent of occurrence of Sciurus vulgaris increased throughout the park, whereas those of Eutamias sibiricus decreased. Differently from what is usually observed with alien squirrels, the spread of the native species appears to be halting and reversing the expansion of the non-native one.

Stress in biological invasions: Introduced invasive grey squirrels increase physiological stress in native Eurasian red squirrels.

Invasive alien species can cause extinction of native species through processes including predation, interspecific competition for resources or disease-mediated competition. Increases in stress hormones in vertebrates may be associated with these processes and contribute to the decline in survival or reproduction of the native species. Eurasian red squirrels (Sciurus vulgaris) have gone extinct across much of the British Isles and parts of Northern Italy following the introduction of North American invasive grey squirrels (Sciurus carolinensis). We extracted glucocorticoid metabolites from faecal samples to measure whether the presence of the invasive species causes an increase in physiological stress in individuals of the native species. We show that native red squirrels in seven sites where they co-occurred with invasive grey squirrels had glucocorticoid concentrations that were three times higher than those in five sites without the invasive species. Moreover, in a longitudinal study, stress hormones in native red squirrels increased after colonisation by grey squirrels. When we experimentally reduced the abundance of the invasive grey squirrels, the concentration of faecal glucocorticoid metabolites in co-occurring red squirrels decreased significantly between pre- and postremoval periods. Hence, we found that the invasive species acts as a stressor which significantly increases the concentrations of glucocorticoids in the native species. Given that sustained elevations in glucocorticoids could reduce body growth and reproductive rate, our results are consistent with previous studies where the co-occurrence of the invasive grey squirrel was associated with smaller size and lower reproductive output in red squirrels.

A battle of wits? Problem-solving abilities in invasive eastern grey squirrels and native Eurasian red squirrels

Behavioural flexibility has been argued to be an evolutionarily favourable trait that helps invasive species to establish themselves in non-native environments. Few studies, however, have compared the level of flexibility (whether considered as an outcome or as a process) in mammalian invaders and related native species. Here, we tested whether flexibility differs between groups of free-ranging invasive eastern grey squirrels, Sciurus carolinensis, and native Eurasian red squirrels, Sciurus vulgaris, in the U.K., using an easy and a difficult food extraction task. All individuals of both species showed flexibility, at the outcome level, in solving the easy task and solution time was comparable between species across a series of successes. A higher proportion of grey squirrels than red squirrels solved the difficult task. However, for those squirrels that did solve the task, solving efficiency was comparable between species on their first success, and a few red squirrels outperformed the grey squirrels in subsequent successes. Between-species analysis showed that instantaneous flexibility, flexibility at the process level that was measured as the rate of switching between tactics after a failed attempt, was higher in red squirrels than in grey squirrels. Within-species analysis also revealed that red squirrel problem solvers showed higher flexibility at the process level than their nonsolver counterparts. Nonsolvers also failed to make ‘productive’ switches (switching from ineffective to effective tactics). Together, the results suggest that problem-solving ability overlaps in the two species, but is less variable, and on average higher, in grey squirrels than in red squirrels. The superior behavioural flexibility of the grey squirrels, shown here by success at problem solving, may have facilitated their invasion success, but it may also have resulted from selective pressures during the invasion process.

Space invaders: effects of invasive alien Pallas’s squirrel on home range and body mass of native red squirrel

Alien species can affect native species through several ecological processes such as competition. Here we tested the hypothesis of interspecific competition for space and food resources between the native Eurasian red squirrel and the invasive Pallas’s squirrel introduced in Italy. We used an experimental study design comparing space and habitat use and body condition parameters of red squirrels between areas of co-occurrence with the Pallas’s squirrel and areas without it. There were no differences in mean home range size of red squirrels between red-only areas and red-Pallas. However, when Pallas’s squirrels were removed, the red squirrels increased their home ranges. Moreover, in the area of syntopy, red squirrels had a higher degree of intraspecific home range overlap than in the red-only area. We also found indirect evidence for competition for food with red squirrels having a poorer body condition when co-occurring with the alien species. We analyzed the body mass and size of red squirrels in the two areas and our results showed that red squirrels had a reduced body mass and size when in syntopy, confirming that the interspecific competition does not allow red squirrels to reach the optimum body condition that they would have if the competitor was not present. Moreover, tree-species niche overlap was very high and both species fed primarily on the same tree seeds. Differences in vegetation cover between areas are discussed. This is the first study that confirms the invasiveness of the Pallas’s squirrel also in terms of capability to compete with native species.

Interspecific competition between alien Pallas’s squirrels and Eurasian red squirrels reduces density of the native species

When alien species introduced into a new environment have a strong niche overlap with ecologically similar native species, interspecific competition can cause a decrease in abundance and distribution of native species. Pallas’s squirrel (Callosciurus erythraeus) was introduced in Northern Italy where it currently co-occurs with native Eurasian red squirrels (Sciurus vulgaris). The alien species is known for its invasiveness but so far negative effects of Pallas’s squirrels on native tree squirrels have not been demonstrated. Here, we compare demographic parameters of red squirrel populations between sites without (red-only sites) and with (red-Pallas’s sites) C. erythraeus and present results of trapping and removal of Pallas’s squirrel and its effects on red squirrel population dynamics. The native species was patchily distributed and absent in many trapping sites occupied by the Pallas’s squirrel. Red squirrels occurred at much lower densities and showed reduced adult survival in areas of co-occurrence than in red-only sites, but there were no differences in reproductive rate. Removing invasive squirrels throughout the study period resulted in re-colonisation by the native species only in some trapping sites, and several alternatives to explain the lack of a marked increase in population size are discussed. This study is the first to provide evidence that presence of Pallas’s squirrel reduces viability of local red squirrel populations.

Alien shades of grey: new occurrences and relevant spread of Sciurus carolinensis in Italy

Abstract The eastern grey squirrel is listed among the worst invasive species throughout the world. This species of American origin is currently replacing the native Eurasian red squirrel in most of the Great Britain, as well as in parts of Ireland and Italy. It may debark trees and exert damages to woodlands and tree plantations. Therefore, its spread may be deleterious for biodiversity and environment, emphasising the need for a rapid detection in new areas of occurrence. In this work, we reported for the first time, the presence of new populations of this invasive species in Tuscany (Central Italy) and some updates and analyses regarding the status of this species in Veneto (North-Eastern Italy). Occurrences were collected through citizen-science contributory approach supported by photos, road-kills, and/or hair-tube sampling. Field investigations ad hoc were carried out in Veneto and Tuscany to confirm the repeated reports in the surroundings of Arezzo and in the province of Siena. Although records can be possibly related to erratic or single individuals escaped from captivity, reproductive nuclei have also been detected in both regions, with the observations of juveniles and/or lactating females. The occurrence of the species in these regions is still scarce and localised, but considering the surrounding favourable wooded habitats, a rapid removal of the animals would be required to prevent their spread.

Poor Parasite Community of an Invasive Alien Species: Macroparasites of Pallas's Squirrel in Italy

The aim of the present study was to investigate the macroparasite fauna of Pallas's squirrel, Callosciurus erythraeus, native to SE Asia, recently introduced to Italy and co-occurring with the native Eurasian red squirrel Sciurus vulgaris. A total of 161 Pallas's squirrels harboured a poor macroparasite fauna, characterized by two main ectoparasite species, the flea Ceratophyllus (M.) sciurorum sciurorum (prevalence 50%, mean intensity 1.0 ± 0.1) and the tick Ixodes ricinus (prevalence 47%, mean intensity 3.0 ± 0.7), and a few helminths (Rodentoxyuris sciuri, Trichuris muris, Strongyloides callosciureus) all with prevalence below 10%. All parasites, except S. callosciureus, are native to Europe and were acquired in the invaded range. The loss of native parasites might have contributed to their successful invasion. The acquisition of local parasites C. sciurorum and Trichuris sciuri, and the introduction of the Asiatic nematode S. callosciureus may lead to spill-back and spill-over processes towards red sq...

Biodiversity threats from outside to inside: effects of alien grey squirrel (Sciurus carolinensis) on helminth community of native red squirrel (Sciurus vulgaris)

Biological invasions are among the major causes of biodiversity loss worldwide, and parasites carried or acquired by invaders may represent an added threat to native species. We compared gastrointestinal helminth communities of native Eurasian red squirrels (Sciurus vulgaris) in the presence and absence of introduced Eastern grey squirrels (Sciurus carolinensis) to detect alterations induced by the alien species. In particular, we investigated whether spillover of a North American nematode Strongyloides robustus occurs and whether prevalence of a local parasite Trypanoxyuris sciuri in red squirrels is affected by grey squirrel presence. The probability of being infected by both parasites was significantly higher in areas co-inhabited by the alien species, where 61% of examined red squirrels (n = 49) were infected by S. robustus and 90% by T. sciuri. Conversely, in red-only areas, the two parasites infected only 5 and 70% of individuals (n = 60). Overall, our findings support the hypothesis that red squirrels acquire S. robustus via spillover from the alien congener and suggest that invaders' presence may also indirectly affect infection by local parasites through mechanisms diverse than spill-back and linked to the increased competitive pressure to which red squirrels are subjected. These results indicate that the impact of grey squirrel on red squirrels may have been underestimated and highlight the importance of investigating variation in macroparasite communities of native species threatened by alien competitors.

The impact of forest stand structure * on red squirrel habitat use

The native Eurasian red squirrel is considered endangered in the UK and under strict legal protection. Long-term habitat management is a key goal of the UK conservation strategy. Current selection criteria of reserves and subsequent management mainly consider species composition and food availability. However, there exists a critical gap in understanding and quantifying the relationship between squirrel abundance, their habitat use and forest structural factors. This is partly a result of limited availability of structural data along with cost-efficient data collection methods. We investigated the relationship between structural characteristics and squirrel feeding activity in Scots pine. Field data were collected from two study areas: Abernethy and Aberfoyle Forest. Canopy closure, diameter at breast height, tree height and number of trees were measured in 56 plots. Abundance of squirrel feeding signs was used as an index of habitat use. We used a generalized linear model to model the response of cones stripped by squirrel in relation to field-collected structural variables. Results show that forest structural characteristics are significant predictors of feeding sign presence; canopy closure and number of trees contribute to explain 43 per cent of the variation in stripped cones. Our findings critically highlight the need to consider stand structure in management for red squirrels.

APPLICATION OF MODELLING TECNIQUES TO MANAGE A POPULATION OF GREY SQUIRRELS (SCIURUS CAROLINENSIS) IN LOMBARDY, NORTHERN ITALY, AND ANALYSIS OF PARAMETERS ESTIMATES USED IN SIMULATIONS

Grey squirrel (Sciurus carolinensis), an invasive alien species, is currently replacing the native Eurasian red squirrel (Sciurus vulgaris) in British Isles and north-west Italy. Grey squirrel has recently been reported in the Ticino Park (Lombardy region, NW Italy) and the species is likely to spread in the woodlands connecting Italy to other European countries. We used GRASS Geographical Information System (GIS) and Spatially Explicit Population Dynamics Models (SEPM) as a conservation tool to predict the spread of grey squirrels and to test different management options in the Ticino Regional Park and sur- rounding areas in a 40 years time frame. The integrated approach of SEPM and GIS allowed us to suggest public administration a cost effective action plan to stop the invasion process. We also analyse the parameters used in the model highlighting some missing data in litera- ture: we can address future field study with the aim to improve model performance.

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

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.

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

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.