Relationships among parasites, physiological stress and personality in the interactions between invasive alien and native species

The thesis explored the interactions between Invasive Alien Species (IAS) and native species in the light of potential effects of parasitic infections, physiological stress and personality on individual fitness (reproductive success/investment). In particular, this study investigated the interspecific competition between the North American invasive Eastern grey squirrel (Sciurus carolinensis) and the native Eurasian red squirrel (Sciurus vulgaris), describing techniques and methods that successively have been applied to evaluate the relationships between personality, stress and parasite load. Chapter 1 reported the validation of a method to measure physiological stress in Eurasian red squirrel; Chapter 2 showed the application of this method to evaluate physiological stress in the native species in co-occurrence with Eastern grey squirrels. Chapter 3 presented estimates of personality of individual squirrels using indirect indices and their validation through correlation with direct personality measurements from arena tests. Chapter 4 examined the methods previously identified to explore the relationship between personality and parasite infections in Eastern grey squirrels. Reproductive success/investment could be influenced by the cumulative effect of factors analysed above. Chapter 5 presented the application of a staining technique of uterine scars count to estimate fecundity in invasive squirrel populations. Finally, Chapter 6 examined the relationships between parasite load, physiological stress, reproductive success and/or investment and the potential mediatory role of personality

Relationships among parasites, physiological stress and personality in the interactions between invasive alien and native species

The thesis explored the interactions between Invasive Alien Species (IAS) and native species in the light of potential effects of parasitic infections, physiological stress and personality on individual fitness (reproductive success/investment). In particular, this study investigated the interspecific competition between the North American invasive Eastern grey squirrel (Sciurus carolinensis) and the native Eurasian red squirrel (Sciurus vulgaris), describing techniques and methods that successively have been applied to evaluate the relationships between personality, stress and parasite load. Chapter 1 reported the validation of a method to measure physiological stress in Eurasian red squirrel; Chapter 2 showed the application of this method to evaluate physiological stress in the native species in co-occurrence with Eastern grey squirrels. Chapter 3 presented estimates of personality of individual squirrels using indirect indices and their validation through correlation with direct personality measurements from arena tests. Chapter 4 examined the methods previously identified to explore the relationship between personality and parasite infections in Eastern grey squirrels. Reproductive success/investment could be influenced by the cumulative effect of factors analysed above. Chapter 5 presented the application of a staining technique of uterine scars count to estimate fecundity in invasive squirrel populations. Finally, Chapter 6 examined the relationships between parasite load, physiological stress, reproductive success and/or investment and the potential mediatory role of personality

The impact of urbanisation on chipmunks, arboreal and flying squirrels: a global systematic review

The current, rapid urbanisation process impacts global biodiversity and can be a driver for phenotypic changes in mammals that persist in cities. Animals display different response strategies in urban environments compared to natural areas, but patterns may differ among species. To better comprehend this process, we focused on a limited number of species that are present in many urban green spaces around the globe.The aim of this systematic review is to investigate which response strategies chipmunks, arboreal and flying squirrels use to cope with urban environments, exploring whether there are general response patterns, and to reveal potential adaptations to life in urban areas. We included studies that compared trait differences among conspecifics living in different areas along an urbanisation gradient (rural-urban) and studies comparing individuals or populations between urban areas with different environmental characteristics.The effects of urbanisation on chipmunks, arboreal and flying squirrels, at the individual and at the population levels, were identified in nine topics. Included articles explored at least one of these topics and their key findings were described.Effects of urbanisation are evident in all considered topics. However, we found contrasting patterns between species or even among individuals of the same species studied in different geographical areas. Overall, we reported two knowledge gaps: some phenotypic traits were considered in few studies, and many species, especially those living in the Global South, where urban growth rate is higher, have not been studied.This systematic review suggests that urbanisation can be an important driver for adaptation in small mammals, underlining the complexity and differentiation of response patterns. Since target species have important ecological and social roles, additional comparative studies, increasing our understanding of processes that determine their presence in cities, are essential for urban green planning which aims to conserve biodiversity

Habitat effects on hoarding plasticity in the Eurasian red squirrel (Sciurus vulgaris).

Hoarding patterns can be classified into two general types: scatter-hoarding and larder-hoarding, but there are intermediate types. Various factors affect hoarding patterns. Animals hoarding identical seeds in different habitats may use different hoarding patterns to adapt to habitat variation. We used a sample-plot investigation method to study cache features and recovery rate of seeds of Arolla pine (Pinus cembra) by Eurasian red squirrels (Sciurus vulgaris) in 2009 and 2010 in two subalpine forests with different tree-species composition in the Italian Alps. Hoarding patterns of red squirrels varied among habitats: the typical scatter-hoarding pattern with most caches including 2-6 seeds is found in spruce (Picea abies) dominated forest, while a combination of few large caches (10 seeds) and many small caches (less than 10 seeds) is found in Arolla pine dominated forest. Consequently, average number of seeds/cache was higher in the latter habitat. Among five microhabitats, shrubs, grass, moss, fallen leaves, and stone, Eurasian red squirrels preferred fallen leaves and moss as hoarding substrate. Cache recovery investigation indicated that recovery rate was 62% in spruce forest and only 21% in Arolla pine forest. A lower availability of suitable hoarding microhabitat resulted in changes in hoarding patterns of red squirrels in Pinus cembra dominated forest. We suggest that the main factor influencing differences in recovery rate was a higher cone production per tree in Pinus cembra forest

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

In 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

Invading parasites: spillover of an alien nematode reduces survival in a native species

It is widely assumed that spillover of alien parasites to native host species severely impacts na\uefve populations, ultimately conferring a competitive advantage to invading hosts that introduced them. Despite such host-switching events occurring in biological invasions, studies demonstrating the impact of alien macroparasites on native animal hosts are surprisingly few. In Europe, native red squirrels (Sciurus vulgaris) are replaced by introduced North American grey squirrels (S. carolinensis) mainly through resource competition, and, only in the United Kingdom and Ireland, by competition mediated by a viral disease. In Italy such disease is absent, but spillover of an introduced North American nematode (Strongyloides robustus) from grey to red squirrels is known to occur. Here, we used long-term (9 years) capture-mark-recapture and parasitological data of red squirrels in areas co-inhabited by grey squirrels in Northern Italy to investigate the impact of this alien helminth on na\uefve native squirrels\u2019 body mass, local survival, and reproduction of females. We found no negative effect of the alien parasite on body mass or reproductive success, but intensity of infection by S. robustus reduced survival of both male and female squirrels. Significantly, survival of squirrels co-infected by their native nematode, Trypanoxyuris sciuri, was less affected by S. robustus, suggesting a protective effect of the native helminth against the new infection. Hence, we demonstrate that alien S. robustus spillover adds to the detrimental effects of resource competition and stress induced by grey squirrels, further reducing the fitness of the native species in the presence of the invasive competitor

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 hypothalamicpituitary-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

Physiological stress and spatio-temporal fluctuations of food abundance and population density in Eurasian red squirrels

In continuously changing environments, variation of different ecological factors could affect the functioning of the hypothalamic-pituitary-adrenal (HPA) axis in wild mammals, increasing the secretion of glucocorticoids (GCs). In different animal species, GC concentrations are often used as a measure of the physiological stress response to environmental pressures, such as fluctuations in food abundance, population density, intra-and interspecific competition, and predation risk. However, previous studies reported contrasting results or did not find clear associations between physiological stress and environmental variables. Here, we used concentrations of faecal glucocorticoid metabolites (FGMs) as an integrated measure of physiological stress in wild Eurasian red squirrels (Sciurus vulgaris) from three study areas in the Italian Alps, to investigate whether variations in conifer-seed crop size and/or population density affected HPA axis activity. Squirrel density was estimated in each trapping session using the minimum number of animals alive, and annual counts of fresh cones from different conifer species were used to estimate annual food abundance (MJ/ha). We expected higher FGMs in response to increasing population density and/or decreasing food abundance, since these two variables could act as environmental stressors. Our results showed a lack of association between population density and FGMs and a significant effect of food abundance on FGMs. When conifer seed-crops were poor to moderate, FGMs increased with food abundance, while in the range of high seed-crops, FGMs remained first constant and then slightly decreased with a further increase in seed abundance. We also found differences in FGMs among seasons, as previously observed in this species. Our study adds further evidence that physiological stress can be influenced in different ways by environmental pressures and that long-term studies using individually marked animals are needed to disentangle the potential adaptive outcome of the physiological stress response in pulsed resource systems

Relationships between personality traits and the physiological stress response in a wild mammal

Glucocorticoids (GCs) are involved in the regulation of an animal\u2019s energetic state. Under stressful situations, they are part of the neuroendocrine response to cope with environmental challenges. Animals react to aversive stimuli also through behavioral responses, defined as coping styles. Both in captive and wild populations, individuals differ in their behavior along a proactive\u2013reactive continuum. Proactive animals exhibit a bold, active-explorative and social personality, whereas reactive ones are shy, less active-explorative and less social. Here, we test the hypothesis that personality traits and physiological responses to stressors covary, with more proactive individuals having a less pronounced GC stress response. In wild populations of invasive gray squirrels Sciurus carolinensis, we measured fecal glucocorticoid metabolites (FGMs), an integrated measure of circulating GCs, and 3 personality traits (activity, sociability, and exploration) derived from open field test (OFT) and mirror image stimulation (MIS) test. Gray squirrels had higher FGMs in Autumn than in Winter and males with scrotal testes had higher FGMs than nonbreeding males. Personality varied with body mass and population density. Squirrels expressed more activity-exploration at higher than at lower density and heavier squirrels had higher scores for activity-exploration than animals that weighed less. Variation in FGM concentrations was not correlated with the expression of the 3 personality traits. Hence, our results do not support a strong association between the behavioral and physiological stress responses but show that in wild populations, where animals experience varying environmental conditions, the GC endocrine response and the expression of personality are uncorrelated traits among individuals