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.

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.

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.

Use of infrared thermography to detect reactions to stressful events: does animal personality matter?

The study of the relationship between animal stress and personality for free-ranging animals is limited and provides contrasting results. The perception of stressors by an individual may vary due to its personality, and certain personality traits may help individuals to better cope with them. Using non-invasive infrared thermography (IRT), we investigated the link between physiological and behavioral components expressed during an acute stress event by free-ranging Fremont's squirrels (Tamiasciurus fremonti). We expected that, during the acute stress event of being approached by the researcher, individuals that showed a fast pace-of-life syndrome (bolder, more active, and less social/more aggressive) based on an arena test would exhibit stronger sympathetic-adrenal-medullary system reactivity showing a more intense stress-induced hyperthermia (high core body temperature and low peripheral temperature) than individuals with a slow pace of life (shy, less active, and more social). We successfully employed IRT technology to images of Fremont's squirrels with identification of the individuals' body parts (eye, nose, ear, hind foot). However, we found no support for our hypothesis. Squirrels' body surface temperatures told us more about a squirrel's external environment and less about the thermal state of the body in that environment following a stressful event. Further studies need to assess how to make IRT effective and efficient in the field and improve its performance in studying the relationships between physiology and personality in wildlife.

Living on the edge: morphological and behavioral adaptations to a marginal high-elevation habitat in an arboreal mammal.

Habitats are characterized by different local environmental conditions that influence both behavior and morphology of species, which can result in habitat-dependent phenotypic differences among animals living in heterogeneous environments. We studied 3 alpine populations of Eurasian red squirrels (Sciurus vulgaris), 1 living in a marginal high-elevation habitat at the edge of the species' altitudinal distribution, and 2 occurring in higher-quality habitats. Here, we investigated whether squirrels living in the marginal area differed in 2 morphological parameters (body size and body mass) and/or in the expression of 4 personality traits estimated with an open field test and a mirror image stimulation test (activity, exploration, activity-exploration, and social tendency). Furthermore, we tested whether within-individual variance of the traits (behavioral plasticity) was higher in the edge habitat. Male squirrels in the edge habitat were smaller and weighed less than in the other study areas, while among females, size-habitat relationships were less marked. These sex-specific patterns were explained by a strong association between body mass and reproductive success in female squirrels. Squirrels in the marginal habitat were more active, explorative, and had a more social personality than in the other habitats. However, in contrast to our predictions, behavioral plasticity was smaller in the marginal habitat, but only for the trait exploration. Our results suggest that animals choose the habitat that best fits their personality, and that habitat-related differences in selective pressures may shape animals' morphology.

Diversity and host specificity of coccidia (Apicomplexa: Eimeriidae) in native and introduced squirrel species.

Introduction of alien species into new areas can have detrimental effects on native ecosystems and impact the native species. The present study aims to identify coccidia infecting native and introduced squirrels in Italy, to gain insight into possible transmission patterns and role of monoxenous coccidia in mediating the competition between alien and native hosts. We collected 540 faecal samples of native red squirrels, Sciurus vulgaris, invasive alien grey squirrels, S. carolinensis, and introduced Pallas's squirrels, Callosciurus erythraeus. Total prevalence of Eimeria spp. was 95.6% in S. vulgaris, 95.7% in S. carolinensis and only 4.1% in C. erythraeus. Morphological examination revealed 3 Eimeria morphotypes. Phylogenetic analyses of Eimeria DNA based on 18S, ITS, cox I markers displayed fairly distinct monophyletic clades in the microscopically indistinguishable E2 morphotype, proving indisputable distinction between the isolates from red and grey squirrels. Grey squirrels successfully introduced E. lancasterensis from their native range, but this species does not spill over to native red squirrels. Similarly, there is no evidence for the transmission of E. sciurorum from red to grey squirrels. The possible transmission and the potential role of monoxenous coccidia in mediating the competition between native and invasive squirrels in Italy were not confirmed.