Seasonal and environmental determinants of small mammals and their zoonotic potential across a wide latitudinal and altitudinal gradient

The functional role and position of a species within the environment is strongly governed by the interplay between species internal state, abiotic and biotic environmental conditions, as well as by multi-species interactions (predation, competition and parasitism). In this work we have implemented a multifactorial niche-based approach to evaluate the consequences and patterns of environmental, climate and anthropic changes on small mammal populations and assemblages, considering also the cascading effects on parasite loads and thus on emergence of zoonotic and non-zoonotic diseases. To achieve this goal, we carried out a treatment-control experiment with supplemental ad libitum food accessible all-yearround to woodland rodents at two latitudinal extremes i.e. Norway (from 2013 to 2015) and Italy (from 2019 to 2021). Secondly, we assessed the composition of small mammal assemblages across a wide altitudinal gradient (from 500 to 2500 m a.s.l.) in the Italian Alps (2019–2020). In both studies, we livetrapped small mammal species using a capture-mark-recapture approach. In Italy only, we counted the tick burden on rodents and collected biological samples (ear biopsy, blood sample) and molecular and serological screenings were subsequently performed for rodent- and vector-borne pathogens assessment. Within this work, we captured a total of 917 small mammals in Norway and 830 in Italy. In the latitudinal comparison, only bank vole (Myodes glareolus) was sampled in Norway, while two mice species (Apodemus sylvaticus and A. flavicollis) and bank vole in Italy. Within this comparison, we found that individual rodent survivorship seemed to be governed by seasonal cycles and overridden by food availability only when unfavourable conditions occurred. Conversely, local population size generally increased with supplemental food availability, unless when both mice and voles were sympatric (in Italy only). In this case, the dominant species (i.e., Apodemusspp.) performed better both on survival and population size respect to the subordinate one (i.e., M. glareolus). In Italy, rodent abundance and spatial aggregation registered at sites provided with supplemental food favoured also tick burden on rodent hosts, especially on heavier animals. Beyond exploitation of rodent hosts, ticks were also favoured by less-limiting climatic conditions, indeed we sampled them at 2000–2500 m a.s.l., the highest altitude at which ticks were recorded in central Europe. At those altitudes, representing the cold and remote edges of small mammal distribution, we monitored the distributional overlap of snow vole (Chionomys nivalis), field voles (Microtus spp.) and unexpectedly of bank vole, which occupied also woodland habitats in sympatry with mice. Further, we also detected an altitudinal pattern among vector-borne pathogens, with Borrelia spp. infection at low altitudes, while Anaplasma phagocytophilum and Babesia microti mainly occurred at high altitudes. Beyond these common vectorborne pathogens, we also found Hepatozoon spp. along the entire altitudinal gradient and on snow voles for the first time. These findings suggest that modifications in rodent demography and community structure, as well as host-parasite association, were favoured by homogeneous and human-disrupted areas such as at ungulate feeding stations. In these areas, if tick density in the environment is supportive, the presence of both rodents and deer may favour the completion of tick life cycle and enhance pathogens circulation among hosts. Moreover, the generalist species (e.g. M. glareolus), that occurred along a wide altitudinal range in sympatry with more specialist (e.g. Apodemus spp.) and climate-sensitive ones (e.g. C. nivalis), may be prone to upward distributional shifts and further promote the geographic expansion of arthropod vectors. This may also facilitate the spread and transmission of zoonotic pathogens under a climate change context. Overall, this study suggests that the multiple extrinsic and intrinsic environmental facets and biotic interspecific forces governing small mammal demography and communities should be considered ensemble using a multi-factorial approach, especially in perturbed ecosystems. Further, changes in small mammal populations and communities seem to alter host-vectorpathogen interactions, increasing the risk of transmission of infectious diseases both on wildlife and humans.