Sciurus Carolinensis Research Articles

Head arteries of the red squirrel (Sciurus vulgaris)

The red squirrel (Sciurus vulgaris) is a medium-sized rodent protected in most of Europe. The present study aimed to investigate and describe the arterial vascularization of the head of the adult red squirrel. In the study, 48 specimens of adult red squirrels were used. The first preparation method used in the study was corrosion casting using a stained solution of the chemo-setting acrylic material injected into bilateral common carotid arteries resulting in corrosion castings of the vessels on a bone scaffold. The second method was injecting liquid-stained latex into both common carotid arteries. It resulted in a stained arterial vessel on fixed soft tissue preparations. The main vessels providing blood to the head were paired with common carotid arteries that divide into external and internal carotid arteries. The internal carotid artery passes into the stapedial artery. After giving its branches, the stapedial artery exits the cranial cavity through the sphenofrontal foramen and enters the orbit. The suborbital and the mandibular regions were supplied by the maxillary artery, linguofacial trunk, and their branches. Description of the detailed anatomy of the head arteries in red squirrels may contribute to establishing diagnostic and treatment protocols for wildlife rehabilitation centers, which may be crucial since red squirrels are endangered by the spreading of invasive Eastern gray squirrels (Sciurus carolinensis) in Europe. It may also contribute to veterinary care for other members of the Sciuridae family kept as pets.

Gray squirrels consume anthropogenic food waste most often during winter.

The online version contains supplementary material available at 10.1007/s42991-022-00326-3.

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.

An urban cast of characters: Landscape use and cover influencing mammal occupancy in an American midwestern city

With future human population growth concentrating in urban areas, cities are working to counterbalance ecological disturbances resulting from development by incorporating green space that supports greater biodiversity. An initial line of inquiry into designing wildlife-inclusive green space involves evaluating landscapes that are associated with the habitat use of urban species. In this study, we utilized occupancy modeling to estimate select terrestrial mammal presence in a fast-growing mid-sized midwestern city to determine possible taxa-specific associations with multiple land use and cover variables, specifically those associated with higher degrees of human activity. Using motion-triggered infrared trail cameras over eight seasons from winter 2017 to fall 2018, we applied a single-species, single-season stacked design to estimate occupancy for eight urban dwelling mammals. Taxa-specific models contained one of three possible detection variables (null, percent green space, or percent impervious surface) and combinations of three species-specific variables, natural and anthropogenic. We hypothesized that large species, coyote (Canis latrans) and white-tailed deer (Odocoileus virginianus), would exhibit the most positive association to natural land cover and the most negative association to anthropogenic land cover. We also hypothesized that small and medium sized species, eastern cottontail (Sylvilagus floridanus), gray squirrel (Sciurus carolinensis), opossum (Didelphis virginiana), raccoon (Procyon lotor), red fox (Vulpes vulpes), and striped skunk (Mephitis mephitis), would demonstrate a neutral association to land cover type, anthropogenic or natural. Our results indicated that the presence of anthropogenic features rather than any particular natural land cover may be driving wildlife distribution in our study area, as none of our species demonstrated a positive association to natural land cover (percent recreation, residential yards, vacant land, or woodland). Species with a wide range of body sizes, showed a negative association with residential yards, indicating that this type of green space may be an unnecessary or unsuitable subsidizing resource in our study area. With our results in mind, we recommend increasing the amount of natural or less manicured green space to offset the intensity of impervious surface as well as encouraging the establishment of native vegetation in existing and newly constructed residential development to better connect urban green space and residential yards to larger adjoining tracts of natural landscapes. For our study area and other cities in similar phases of development, these suggestions may be essential first steps to reduce biodiversity loss and strengthen community ecology as urban areas continue to grow.

Native species exhibit physiological habituation to invaders: a reason for hope.

Animals cope with environmental perturbations through the stress response, a set of behavioural and physiological responses aimed to maintain and/or return to homeostasis and enhance fitness. Vertebrate neuroendocrine axis activation in response to environmental stressors can result in the secretion of glucocorticoids (GCs), whose acute increases may be adaptive, while chronic elevation may be detrimental. Invasive grey squirrels (Sciurus carolinensis) act as a stressor eliciting elevation of GCs in native red squirrels (Sciurus vulgaris). Here we used 6-year data of variation in faecal glucocorticoid metabolite (FGM) concentrations following invasion by grey squirrels in three red squirrel populations, to identify if red squirrels showed physiological habituation to this stressor. The decrease in FGMs over time was more pronounced shortly after invasion and at high densities of grey squirrels while it decreased less strongly and was no longer influenced by the invader density as time since invasion elapsed. At the individual level, FGMs also decreased more markedly as each red squirrel experienced prolonged contact with the invader. Our study provides compelling new data suggesting that native species in the wild can habituate to prolonged contact with invasive species, showing that they may avoid the potentially harmful effects of chronic elevations in GCs.

College squirrels gone wild? Using Sciurus carolinensis behavior to assess the ecosystem value of urban green spaces

Predicted rapid increases in urbanization in the face of accelerating biodiversity loss underscores the need for urban development that promotes, rather than displaces, native plants and animals. One approach for increasing urban biodiversity is through the development of “green infrastructure”. Although research has explored urban-rural gradients and the overall value of urban green infrastructure, few studies have investigated the habitat value for wildlife of different types of urban greenspace. Here, we use a well-established metric in ecology, giving up-densities (GUDs), to compare foraging costs for a common urban wildlife species, the eastern gray squirrel (Sciurus carolinensis), among three green infrastructure categories: municipal parks, college campuses, and residential yards. We found that GUDs for gray squirrels did not differ significantly among location categories after controlling for proximity to roads, but proximity to roads was associated with significantly higher GUDs in all locations. In an explicit test, we also found that both proximity to roads and traffic volume were associated with higher GUDs. We also found that maximum distance from roads was significantly higher for campuses and parks than for residential yards, indicating a greater proportion of the area of campuses and parks is “away from roads” compared to residential yards. Our results indicate that vehicle traffic may contribute significantly to an “urban landscape of fear” for gray squirrels and suggest that campus and park configurations that reduce road effects could improve habitat quality for squirrels and possibly other animals.

Frontoparietal connectivity as a product of convergent evolution in rodents and primates: functional connectivity topologies in grey squirrels, rats, and marmosets

Robust frontoparietal connectivity is a defining feature of primate cortical organization. Whether mammals outside the primate order, such as rodents, possess similar frontoparietal functional connectivity organization is a controversial topic. Previous work has primarily focused on comparing mice and rats to primates. However, as these rodents are nocturnal and terrestrial, they rely much less on visual input than primates. Here, we investigated the functional cortical organization of grey squirrels which are diurnal and arboreal, thereby better resembling primate ecology. We used ultra-high field resting-state fMRI data to compute and compare the functional connectivity patterns of frontal regions in grey squirrels (Sciurus carolinensis), rats (Rattus norvegicus), and marmosets (Callithrix jacchus). We utilized a fingerprinting analysis to compare interareal patterns of functional connectivity from seeds across frontal cortex in all three species. The results show that grey squirrels, but not rats, possess a frontoparietal connectivity organization that resembles the connectivity pattern of marmoset lateral prefrontal cortical areas. Since grey squirrels and marmosets have acquired an arboreal way of life but show no common arboreal ancestor, the expansion of the visual system and the formation of a frontoparietal connectivity architecture might reflect convergent evolution driven by similar ecological niches in primates and tree squirrels.

Serum biochemistry suggests a physiological response to environmental stress in a native urban Eastern Gray Squirrel (<i>Sciurus carolinensis</i>) population

Urban wildlife populations experience human-driven environmental changes that can be both beneficial and detrimental to individual health. We measured body condition and serum chemistry (electrolyte levels, markers of kidney and liver function, protein, glucose, and cholesterol) in a native urban and rural population of Eastern Gray Squirrel (Sciurus carolinensis) to assess whether we could detect physiological responses to environmental stressors or dietary differences. We found no differences in body condition between habitats and no evidence of malnutrition at either site. However, urban squirrels had higher blood glucose, lower potassium, phosphorus, chloride, and albumin:globulin ratios. These results align with previous findings of increased dietary sugar in cities and suggest that urban populations of gray squirrels are under greater environmental stress than rural populations, providing future directions for studying physiological responses to urbanization.

Characterization of triatomine bloodmeal sources using direct Sanger sequencing and amplicon deep sequencing methods

Knowledge of host associations of blood-feeding vectors may afford insights into managing disease systems and protecting public health. However, the ability of methods to distinguish bloodmeal sources varies widely. We used two methods—Sanger sequencing and amplicon deep sequencing—to target a 228 bp region of the vertebrate Cytochrome b gene and determine hosts fed upon by triatomines (n = 115) collected primarily in Texas, USA. Direct Sanger sequencing of PCR amplicons was successful for 36 samples (31%). Sanger sequencing revealed 15 distinct host species, which included humans, domestic animals (Canis lupus familiaris, Ovis aries, Gallus gallus, Bos taurus, Felis catus, and Capra hircus), wildlife (Rattus rattus, Incilius nebulifer, Sciurus carolinensis, Sciurus niger, and Odocoileus virginianus), and captive animals (Panthera tigris, Colobus spp., and Chelonoidis carbonaria). Samples sequenced by the Sanger method were also subjected to Illumina MiSeq amplicon deep sequencing. The amplicon deep sequencing results (average of 302,080 usable reads per sample) replicated the host community revealed using Sanger sequencing, and detected additional hosts in five triatomines (13.9%), including two additional blood sources (Procyon lotor and Bassariscus astutus). Up to four bloodmeal sources were detected in a single triatomine (I. nebulifer, Homo sapiens, C. lupus familiaris, and S. carolinensis). Enhanced understanding of vector-host-parasite networks may allow for integrated vector management programs focusing on highly-utilized and highly-infected host species.

Discovery of novel DNA viruses in small mammals from Kenya.

Emergence and re-emergence of infectious diseases of wildlife origin have led pre-emptive pathogen surveillances in animals to be a public health priority. Rodents and shrews are among the most numerically abundant vertebrate taxa and are known as natural hosts of important zoonotic viruses. Many surveillance programs focused more on RNA viruses. In comparison, much less is known about DNA viruses harbored by these small mammals. To fill this knowledge gap, tissue specimens of 232 animals including 226 rodents, five shrews and one hedgehog were collected from 5 counties in Kenya and tested for the presence of DNA viruses belonging to 7 viral families by PCR. Diverse DNA sequences of adenoviruses, adeno-associated viruses, herpesviruses and polyomaviruses were detected. Phylogenetic analyses revealed that most of these viruses showed distinction from previously described viruses and formed new clusters. Furthermore, this is the first report of the discovery and full-length genome characterization of a polyomavirus in Lemniscomys species. This novel polyomavirus, named LsPyV KY187, has less than 60% amino acid sequence identity to the most related Glis glis polyomavirus 1 and Sciurus carolinensis polyomavirus 1 in both large and small T-antigen proteins and thus can be putatively allocated to a novel species within Betapolyomavirus. Our findings help us better understand the genetic diversity of DNA viruses in rodent and shrew populations in Kenya and provide new insights into the evolution of those DNA viruses in their small mammal reservoirs. It demonstrates the necessity of ongoing pathogen discovery studies targeting rodent-borne viruses in East Africa.

Seasonal activity patterns of sympatric eastern gray squirrels (Sciurus carolinensis) and fox squirrels (Sciurus niger) in a Midwestern metropolitan region

Seasonal activity patterns of sympatric eastern gray squirrels (Sciurus carolinensis) and fox squirrels (Sciurus niger) in a Midwestern metropolitan region

Wildlife associates of nine-banded armadillo (Dasypus novemcinctus) burrows in Arkansas.

The Nine‐banded Armadillo (Dasypus novemcinctus) is a widespread burrowing species with an expanding geographic range across the southeastern and midwestern United States. Armadillos dig numerous, large burrows within their home ranges and these burrows are likely used by a diverse suite of wildlife species as has been reported for other burrowing ecosystem engineers such as Gopher Tortoises (Gopherus polyphemus), Desert Tortoises (Gopherus agassizi), and Black‐tailed Prairie Dogs (Cynomys ludovicianus). We used motion‐triggered game cameras at 35 armadillo burrows in 4 ecoregions of Arkansas and documented 19 species of mammals, 4 species of reptile, 1 species of amphibian, and 40 species of bird interacting with burrows. Bobcat (Lynx rufus), Coyote (Canis latrans), Eastern Cottontail (Sylvilagus floridanus), Gray Fox (Urocyon cinereoargenteus), Gray Squirrel (Sciurus carolinensis), Northern Raccoon (Procyon lotor), Virginia Opossum (Didelphis virginiana), and unidentified rodents (mice and rats) were documented using burrows in all four ecoregions. We documented wildlife hunting, seeking shelter, rearing young in, and taking over and modifying armadillo burrows. The rate of use was highest in the Mississippi Alluvial Valley, a landscape dominated by agriculture, where natural refugia may be limited and rodents are abundant. Armadillo burrows are clearly visited and used by numerous wildlife species to fulfill various life stage requirements, and this list will likely expand if more attention is devoted to understanding the role of armadillos burrows. Armadillos are important ecosystem engineers, and their ecological role warrants more investigation and attention as opposed to only being viewed and managed as agricultural and garden pests.

A genetic analysis of grey squirrel (Sciurus carolinensis) populations in Ireland

The grey squirrel (Sciurus carolinensis) is an invasive rodent in Ireland that has had detrimental impacts on the native Irish red squirrel (S. vulgaris) as well as on silviculture. This invasive species spread rapidly throughout Ireland, but in recent years appears to be declining in certain areas of the country. This study analysed the genetic profile of grey squirrel populations in Ireland to gain insight into their introduction, evolutionary history in Ireland, and vulnerability to management strategies. The genetic diversity and population structure of eight grey squirrel populations in Ireland was assessed using 11 species-specific microsatellite loci, and was compared to a small population from Tennessee, U.S.A., part of the native range of the grey squirrel. This is the first time these microsatellite markers developed specifically for grey squirrels have been used to study the species in Ireland. We found low to moderate genetic diversity overall across Irish populations as well as the presence of inbreeding. One population in particular, (in Co. Kildare), was differentiated from all other populations, which could indicate genetic isolation between Irish populations or a secondary introduction of S. carolinensis to Ireland.

Parallel evolution of urban\u2013rural clines in melanism in a widespread mammal

Urbanization is the dominant trend of global land use change. The replicated nature of environmental change associated with urbanization should drive parallel evolution, yet insight into the repeatability of evolutionary processes in urban areas has been limited by a lack of multi-city studies. Here we leverage community science data on coat color in > 60,000 eastern gray squirrels (Sciurus carolinensis) across 43 North American cities to test for parallel clines in melanism, a genetically based trait associated with thermoregulation and crypsis. We show the prevalence of melanism was positively associated with urbanization as measured by impervious cover. Urban–rural clines in melanism were strongest in the largest cities with extensive forest cover and weakest or absent in cities with warmer winter temperatures, where thermal selection likely limits the prevalence of melanism. Our results suggest that novel traits can evolve in a highly repeatable manner among urban areas, modified by factors intrinsic to individual cities, including their size, land cover, and climate.

Invasive alien species as an environmental stressor and its effects on coping style in a native competitor, the Eurasian red squirrel

Free-living animals cope with environmental stressors through physiological and behavioural responses. According to the unidimensional model, these responses are integrated within a coping style: proactive individuals (bold, active-explorative and social) have a lower hypothalamic–pituitary–adrenal (HPA) axis reactivity than reactive ones (shy, less active-explorative, less social). These associations may change when individuals are exposed to human-induced rapid environmental change (HIREC), such as the introduction of invasive alien species (IAS). Here, we studied Eurasian red squirrels to investigate the relationship between personality traits and one integrated measure of HPA axis activity, both in areas uncolonized (natural populations) and colonized by an IAS, the Eastern grey squirrel (invaded populations). We expected an association between physiological and behavioural responses, and that activity, exploration and social tendency would covary, forming a behavioural syndrome in natural populations, while competition with the IAS was predicted to disrupt these associations. We used faecal glucocorticoid metabolites (FGMs) as an integrated measure of adrenocortical activity, and measured the levels of four personality traits (exploration, activity, activity-exploration and social tendency) with an open field test and a mirror image stimulation test. We found no correlation between FGMs and personality traits, neither in natural nor invaded populations. However, we found correlations among personality traits in areas without interspecific competition, indicating a behavioural syndrome, which was disrupted in invaded populations. This is one of the few studies showing that an IAS, acting as an environmental stressor, alters a native species' behavioural syndrome, but does not influence its coping style.

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

Simple SummaryIn Europe, squirrelpox virus is carried by non-native grey squirrels and spread into native red squirrel populations. The virus causes a large proportion of infected red squirrels to die and contributes to local declines and the replacement by grey squirrels. There are relatively few published studies quantifying the impact of disease amongst red squirrels. We present findings from a short-term study in north Wales, United Kingdom.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.

Testing the parasite-mediated competition hypothesis between sympatric northern and southern flying squirrels.

Competition is a driving factor in shaping ecological communities and may act directly or indirectly through apparent competition. We examined a classic example of parasite-mediated competition between northern (Glaucomys sabrinus) and southern flying squirrels (G. volans) via the intestinal nematode, Strongyloides robustus, and tested whether it could act as a species barrier in a flying squirrel hybrid zone. We live-trapped flying squirrels (G. sabrinus and G. volans), grey squirrels (Sciurus carolinensis), red squirrels (Tamiasciurus hudsonicus), and chipmunks (Tamias striatus) from June–September 2019 at 30 woodlots in Ontario, Canada. Fecal samples from squirrels were collected and analyzed for the presence of endoparasite eggs. For each individual, we calculated Scaled Mass Index (SMI) as a measure of body condition to assess the effect of S. robustus on squirrels. We found eggs of S. robustus in all species except chipmunks. Infection with S. robustus did not appear to affect body condition of southern flying squirrels and grey squirrels, but we did find a weak negative effect on northern flying squirrels and red squirrels. Despite a weak asymmetric effect of S. robustus on flying squirrels, we did not find any evidence that parasite-mediated competition could lead to competitive exclusion from woodlots. Furthermore, S. robustus eggs were common in feces of the red squirrel, a species largely sympatric with northern flying squirrel.

A nonnative Black Spiny-tailed Iguana, Ctenosaura similis (Squamata: Iguanidae), preying on a native Eastern Gray Squirrel, Sciurus carolinensis (Mammalia: Sciuridae), in southern Florida

A nonnative Black Spiny-tailed Iguana, Ctenosaura similis (Squamata: Iguanidae), preying on a native Eastern Gray Squirrel, Sciurus carolinensis (Mammalia: Sciuridae), in southern Florida

Bone dispersal by vertebrate taxa in an urban park environment in New England, USA

The questions of the frequency, distance, and maximum size of the bones that carnivores, rodents, and other common taxa can disperse have been little addressed, especially in the later phases of skeletonization when individual bones are more subject to transport and loss. The present research utilized a sample of dry white-tailed deer (Odocoileus virginianus) bones in two locations in a forested urban environment dense with eastern gray squirrels (Sciurus carolinensis), chipmunks (Tamias striatus), coyotes (Canis latrans), raccoons (Procyon lotor), and other potential scavenging taxa. Game cameras were used to document their dispersal behavior. A total of 1731 visits were recorded, by a minimum of 12 mammalian and 9 avian taxa. Small amounts of dispersal impacted the bone samples continuously throughout the observation period, with 52.2% of all movement in the range of 1–5 cm. The bones were dispersed a maximum distance of 1252 cm, and the largest bone moved had an initial mass of 194.6 g. Rodent dry-bone gnawing behavior affected 72.7% of the sample. The project also assessed a smaller sample of Tile Mate® tracking chips for their utility in dispersal research, and these were found to have a useful potential though were not pivotal in acquiring the data presented here. Forensic surface search methods and interpretations of skeletal recovery patterns should take into consideration the ability of these common species to disperse even dry bones away from their initial locations, and this behavior may continue years after the time of initial deposition.

Restricted access to private properties limits management of invasive alien species: A literature review and case studies

Biological invasions are one of the major drivers of global environmental change and there is a need to develop integrated strategies to counteract this phenomenon. Eradication is an effective management option to mitigate the deleterious impacts of invasive alien species (IAS). Eradication can be achieved if all reproductive individuals are removed and population recovery is prevented. However, individuals may survive removal operations in private areas if interventions are not allowed. Here, we present 1) three case studies in which restricted private property access prevented the local eradication of invasive alien populations, and 2) a list of reasons for denying access to private properties and a list of actions implemented or suggested by managers to facilitate access and reported in 29 reviewed papers. The restricted access affected the local eradication of three Eastern grey squirrel (Sciurus carolinensis) populations in Italy. In Lombardy region, in one area a planned eradication did not start and in another area the implemented eradication failed due to the refusal from the owner of a large private property to grant access to managers. In Umbria region, the lack of collaboration from an Italian financial institution produced a delay of 15 months in the removal. In our case studies, therefore, a single person or institution denied access for a personal gain or presumed internal security. The reasons behind landowner opposition may be diverse and individual attitudes towards IAS management will depend on interactions with owners. According to our review, in many cases the denial of access takes place in a general perception of mistrust or opposition to the project as the results of a limited engagement of local people. Such opposition often jeopardizes control activities, with profound negative consequences on eradication, expecially at landscape scale. Bottom-up approaches aiming at involving stakeholders can increase the possibility to achieve IAS eradication, however appropriate legislation remains pivotal to enforce eradication in case of non-cooperative behaviour.