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.

Personality traits, sex and food abundance shape space use in an arboreal mammal.

Animal space use is affected by spatio-temporal variation in food availability and/or population density and varies among individuals. This inter-individual variation in spacing behaviour can be further influenced by sex, body condition, social dominance, and by the animal's personality. We used capture-mark-recapture and radio-tracking to examine the relationship between space use and personality in Eurasian red squirrels (Sciurus vulgaris) in three conifer forests in the Italian Alps. We further explored to what extent this was influenced by changes in food abundance and/or population density. Measures of an individual's trappability and trap diversity had high repeatability and were used in a Principal Component Analysis to obtain a single personality score representing a boldness-exploration tendency. Males increased home-range size with low food abundance and low female density, independent of their personality. However, bolder males used larger core-areas that overlapped less with other males than shy ones, suggesting different resource (food, partners) utilization strategies among personality types. For females, space use-personality relationships varied with food abundance, and bolder females used larger home ranges than shy ones at low female density, but the trend was opposite at high female density. Females' intrasexual core-area overlap was negatively related to body mass, with no effect of personality. We conclude that relationships between personality traits and space use in free-ranging squirrels varied with sex, and were further influenced by spatio-temporal fluctuations in food availability. Moreover, different personality types (bold-explorative vs. shy) seemed to adopt different space-use strategies to increase access to food and/or partners.

Spillover of an alien parasite reduces expression of costly behaviour in native host species.

Understanding the effects of invasive alien species (IAS) on native host-parasite relationships is of importance for enhancing ecological theory and IAS management. When IAS and their parasite(s) invade a guild, the effects of interspecific resource competition and/or parasite-mediated competition can alter existing native host-parasite relationships and the dependent biological traits such as native species' behaviour. We used a natural experiment of populations of native red squirrels Sciurus vulgaris that were colonized by the alien grey squirrel Sciurus carolinensis, comparing repeated measurements of red squirrel parasite infection and personality with those taken in sites where only the native species occurred. We explored two alternative hypotheses: (a) individual differences in personality traits (activity and/or sociability) of native red squirrel positively affect the probability of macroparasite spillover and thus the likelihood to acquire the alien's parasitic helminth Strongyloides robustus; (b) the combined effects of grey squirrel presence and parasite infection result in a reduction of costly personality traits (activity and/or exploration). Using data from 323 arena tests across three experimental (native species and IAS) and three control sites (only native species), we found negative correlations between native species' activity and infection with S. robustus in the sites invaded by the alien species. Activity was also negatively correlated with infection by its native helminth Trypanoxyuris sciuri but only when grey squirrels were present, while in the red-only sites there was no relationship of T. sciuri infection with any of the personality traits. Moreover, individuals that acquired S. robustus during the study reduced their activity after infection, while this was not the case for animals that remained uninfected. Our results show that parasite-mediated competition is costly, reducing activity in individuals of the native species, and altering the native host-native parasite relationships.

Individual improvements and selective mortality shape lifelong migratory performance.

Billions of organisms, from bacteria to humans, migrate each year and research on their migration biology is expanding rapidly through ever more sophisticated remote sensing technologies. However, little is known about how migratory performance develops through life for any organism. To date, age variation has been almost systematically simplified into a dichotomous comparison between recently born juveniles at their first migration versus adults of unknown age. These comparisons have regularly highlighted better migratory performance by adults compared with juveniles, but it is unknown whether such variation is gradual or abrupt and whether it is driven by improvements within the individual, by selective mortality of poor performers, or both. Here we exploit the opportunity offered by long-term monitoring of individuals through Global Positioning System (GPS) satellite tracking to combine within-individual and cross-sectional data on 364 migration episodes from 92 individuals of a raptorial bird, aged 1-27 years old. We show that the development of migratory behaviour follows a consistent trajectory, more gradual and prolonged than previously appreciated, and that this is promoted by both individual improvements and selective mortality, mainly operating in early life and during the pre-breeding migration. Individuals of different age used different travelling tactics and varied in their ability to exploit tailwinds or to cope with wind drift. All individuals seemed aligned along a race with their contemporary peers, whose outcome was largely determined by the ability to depart early, affecting their subsequent recruitment, reproduction and survival. Understanding how climate change and human action can affect the migration of younger animals may be the key to managing and forecasting the declines of many threatened migrants.

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.

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.

Climate is changing, are European bats too? A multispecies analysis of trends in body size.

Animal size, a trait sensitive to spatial and temporal variables, is a key element in ecological and evolutionary dynamics. In the context of climate change, there is evidence that some bat species are increasing their body size via phenotypic responses to higher temperatures at maternity roosts. To test the generality of this response, we conducted a >20-year study examining body size changes in 15 bat species in Italy, analysing data from 4393 individual bats captured since 1995. In addition to examining the temporal effect, we considered the potential influence of sexual dimorphism and, where relevant, included latitude and altitude as potential drivers of body size change. Contrary to initial predictions of a widespread increase in size, our findings challenge this assumption, revealing a nuanced interplay of factors contributing to the complexity of bat body size dynamics. Specifically, only three species (Myotis daubentonii, Nyctalus leisleri, and Pipistrellus pygmaeus) out of the 15 exhibited a discernible increase in body size over the studied period, prompting a reassessment of bats as reliable indicators of climate change based on alterations in body size. Our investigation into influencing factors highlighted the significance of temperature-related variables, with latitude and altitude emerging as crucial drivers. In some cases, this mirrored patterns consistent with Bergmann's rule, revealing larger bats recorded at progressively higher latitudes (Plecotus auritus, Myotis mystacinus, and Miniopterus schreibersii) or altitudes (Pipistrellus kuhlii). We also observed a clear sexual dimorphism effect in most species, with females consistently larger than males. The observed increase in size over time in three species suggests the occurrence of phenotypic plasticity, raising questions about potential long-term selective pressures on larger individuals. The unresolved question of whether temperature-related changes in body size reflect microevolutionary processes or phenotypic plastic responses adds further complexity to our understanding of body size patterns in bats over time and space.

Continental-scale patterns in diel flight timing of high-altitude migratory insects.

Many insects depend on high-altitude, migratory movements during part of their life cycle. The daily timing of these migratory movements is not random, e.g. many insect species show peak migratory flight activity at dawn, noon or dusk. These insects provide essential ecosystem services such as pollination but also contribute to crop damage. Quantifying the diel timing of their migratory flight and its geographical and seasonal variation, are hence key towards effective conservation and pest management. Vertical-looking radars provide continuous and automated measurements of insect migration, but large-scale application has not been possible because of limited availability of suitable devices. Here, we quantify patterns in diel flight periodicity of migratory insects between 50 and 500 m above ground level during March-October 2021 using a network of 17 vertical-looking radars across Europe. Independent of the overall daily migratory movements and location, peak migratory movements occur around noon, during crepuscular evening and occasionally the morning. Relative daily proportions of insect migration intensity and traffic during the diel phases of crepuscular-morning, day, crepuscular-evening and night remain largely equal throughout May-September and across Europe. These findings highlight, extend, and generalize previous regional-scale findings on diel migratory insect movement patterns to the whole of temperate Europe. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

COVID-19 could accelerate the decline in recreational hunting: A natural experiment from Northern Italy.

Although many studies highlighted the potential of COVID-19 to reshape existing models of wildlife management, empirical research on this topic has been scarce, particularly in Europe. We investigated the potential of COVID-19 pandemic to accelerate the ongoing decline in an aging population of recreational hunters in Italy. Namely, we modelled spatiotemporal trends between 2011 and 2021 in the number of recreational hunters in 50 Italian provinces with a varying incidence of COVID-19, and temporally delayed waves of infection. Compared to projections from 2011-2019 data, we detected a lower number of hunters who enrolled for the hunting season, both in 2020 (14 provinces) and in 2021 (15 provinces). The provinces with the highest incidence of COVID-19 in the Lombardy and Emilia-Romagna regions were also those experiencing the most marked decrease in hunting participation. Our findings revealed that a wildlife management system based on recreational hunting can be rapidly destabilized by epidemics and their associated public health measures, particularly when the average age of hunters is high, like in Italy. Considered the high incidence attained by COVID-19 in many European countries, where hunters are pivotal for the management of large ungulates and where they were already declining before the pandemic, our findings call for further large-scale research about the impact of COVID-19 on hunting participation.

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.

Camera Trapping to Assess Status and Composition of Mammal Communities in a Biodiversity Hotspot in Myanmar.

Tropical forests comprise a critically impacted habitat, and it is known that altered forests host a lower diversity of mammal communities. In this study, we investigated the mammal communities of two areas in Myanmar with similar environmental conditions but with great differences in habitat degradation and human disturbance. The main goal was to understand the status and composition of these communities in an understudied area like Myanmar at a broad scale. Using camera trap data from a three-year-long campaign and hierarchical occupancy models with a Bayesian formulation, we evaluated the biodiversity level (species richness) and different ecosystem functions (diet and body mass), as well as the occupancy values of single species as a proxy for population density. We found a lower mammal diversity in the disturbed area, with a significantly lower number of carnivores and herbivores species. Interestingly, the area did not show alteration in its functional composition. Almost all the specific roles in the community were present except for apex predators, thus suggesting that the effects of human disturbance are mainly effecting the communities highest levels. Furthermore, two species showed significantly lower occupancies in the disturbed area during all the monitoring campaigns: one with a strong pressure for bushmeat consumption and a vulnerable carnivore threatened by illegal wildlife trade.

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

Glucocorticoids (GCs) are involved in the regulation of an animal's 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-reactive 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.

Interspecific competition affects the expression of personality-traits in natural populations.

Competition between animal species can cause niche partitioning and shape an individual's phenotype, including its behaviour. However, little is known about effects of interspecific competition on personality, the among-individual variation in behaviour that is consistent across different spatial and temporal contexts. We investigated whether alien grey squirrels (Sciurus carolinensis) influenced the expression of personality traits in native red squirrels (Sciurus vulgaris). In Italy, alien grey squirrels replaced native reds through competition for food resources and space, reducing breeding and recruitment in the native species. We compared personality of red squirrels in red-only (no interspecific competition) and red-grey (with interspecific competition) sites, using arena-tests. The trait activity was measured by Open Field Test while sociability and avoidance were quantified by Mirror Image Stimulation test. Red squirrels co-occurring with the alien species had higher sociability scores and higher between-individual variation in sociability than in red-only sites. Differences in activity and avoidance were not significant. Personality - fitness relationships were not affected by presence or absence of grey squirrels, suggesting that the expression of sociability in red squirrels was not due to short-term selection, but was likely the result of context-related advantages when co-occurring with the competing species.

Analysis of mosses and soils for quantifying heavy metal concentrations in Sicily: a multivariate and spatial analytical approach.

BACKGROUND: The use of vegetal organisms as indicators of contamination of the environment is partially replacing traditional monitoring techniques. Amongst the vegetal organisms available, mosses appear to be good bioindicators and are used for monitoring anthropogenic and natural fall-out on soils. This study has two objectives: the evaluation of the concentrations of heavy metals in soils and mosses of the Sicily Region, in Italy and the identification of the origin of fall-out of heavy metals. METHODS: Mosses and the surface soil were sampled at 28 sites, only the youngest segments of Hylocomium splendens and Hypnum cupressiforme, corresponding to the plant tissues produced during the last 3 years, were taken. The elements Cd, Cu, Ni, Pb and Zn were analysed by ICP-MS and Hg by AAS. Statistical analysis was by PCA and spatial representation by GIS. RESULTS AND DISCUSSION: In the mosses sampled in Sicily, the highest concentrations of Cd were found around the cities of Palermo and Messina. The highest concentrations of Hg were recorded in the northern part of the island between Trapani and Messina, similar to the distribution of Cu. Different areas with the highest concentrations of Ni were found near the south coast, in the vicinity of Palermo and around the Volcano Etna. The highest concentrations of Pb were found in the south-west coast near Agrigento, where important chemical plants and petroleum refineries are located. Except for a few locations, Zn fall-out was found to be evenly distributed throughout Sicily. CONCLUSION: The sites where the concentrations of heavy metals cause greatest concern have been revealed by the PCA analysis and portrayed using GIS. Also of some concern is the diffuse and anthropogenic origin of Hg and Cd. The combined approach of using soil and mosses, together with pedological interpretation and application of multivariate statistical techniques has provided valuable insight into the environmental aspects of heavy metal deposition in a region of southern Europe. RECOMMENDATIONS AND OUTLOOK: Further insight into the deposition of heavy metals will require more detailed sampling of soils and mosses in both new and previous study areas. This needs to be complemented by detailed pedological investigations in the study areas. Future research programmes will address these issues.

Preventing species invasion: A role for integrative taxonomy?

Integrative taxonomy, a multi-disciplinary approach adding modern techniques to traditional morphology-based methods (e.g. molecular and morphological criteria), can play an important role in bioinvasion research to identify introduced taxa, discover pathways of introduction and inform authorities to control and prevent future introductions. The present study is the first on introduced populations of Callosciurus, Asiatic tree squirrels, known as potentially invasive species in Europe (Italy, Belgium and France). We combined molecular (mitochondrial DNA markers: CoxI, D-loop) and morphometric analysis on skulls, comparing them to the widest morphological and molecular datasets ever assembled for Callosciurus. Squirrels collected in Italy and Belgium share the same haplotypes and skull characteristics, but are conspicuously different from the French population in Antibes. Genetic data revealed close similarity between French squirrels and Pallas's squirrels, Callosciurus erythraeus, from Taiwan, China. Italian and Belgian squirrels formed an independent taxonomic lineage in genetic analyses, whose taxonomic rank needs further investigation. The morphological and morphometric characteristics of these 2 populations are, however, similar to known specimens assigned to Callosciurus erythraeus. These results may indicate a common origin for the populations found in Belgium and Italy. In contrast, French specimens suggest an independent introduction event of squirrels originating from Asia.

Macroparasite fauna of alien grey squirrels (Sciurus carolinensis): composition, variability and implications for native species.

Introduced hosts populations may benefit of an "enemy release" through impoverishment of parasite communities made of both few imported species and few acquired local ones. Moreover, closely related competing native hosts can be affected by acquiring introduced taxa (spillover) and by increased transmission risk of native parasites (spillback). We determined the macroparasite fauna of invasive grey squirrels (Sciurus carolinensis) in Italy to detect any diversity loss, introduction of novel parasites or acquisition of local ones, and analysed variation in parasite burdens to identify factors that may increase transmission risk for native red squirrels (S. vulgaris). Based on 277 grey squirrels sampled from 7 populations characterised by different time scales in introduction events, we identified 7 gastro-intestinal helminths and 4 parasite arthropods. Parasite richness is lower than in grey squirrel's native range and independent from introduction time lags. The most common parasites are Nearctic nematodes Strongyloides robustus (prevalence: 56.6%) and Trichostrongylus calcaratus (6.5%), red squirrel flea Ceratophyllus sciurorum (26.0%) and Holarctic sucking louse Neohaematopinus sciuri (17.7%). All other parasites are European or cosmopolitan species with prevalence below 5%. S. robustus abundance is positively affected by host density and body mass, C. sciurorum abundance increases with host density and varies with seasons. Overall, we show that grey squirrels in Italy may benefit of an enemy release, and both spillback and spillover processes towards native red squirrels may occur.