Ecology and public healthrodents as reservoirs of zoonoses in the farmland of northwestern Spain

Resumen

Zoonoses are a concerning issue for public health and the last pandemic event caused by covid-19 is a good example of it. Human activity is enhancing the transmission, intensity and emergence of practically all zoonoses. Synantropic qualities of some rodent species provide them with exceptional features as amplifiers of emerging zoonoses. Vectors are also important elements transmitting the pathogen between hosts and make it more likely for a disease to cross the species barrier and become zoonotic. Circulation of pathogens involves several reservoirs and hosts, each one with a different level of competence for vectors and transmission of pathogens. The overlap of infected hosts, competent vectors, and humans in the same habitats and at the same time increase considerably the zoonotic risk. The disease ecology based on the One-Health considers pathogens as elements interconnected with the natural environment, wildlife, domestic animals and humans. An effective monitoring, comprehensive understanding of the system functioning, and determination of the spatial-temporal patterns provide us with crucial information for disease prevention. In this thesis, I studied the zoonotic relevance of wild populations of a sympatric small mammal community (Microtus arvalis, Apodemus sylvaticus, Mus spretus and Crocidura russula) that inhabit intensive farming in NW Spain. Here, M. arvalis is considered a host and amplifier of Francisella tularensis (the etiological agent causing tularemia) but little is known about the circulation of this and other zoonotic pathogens in the system. I focused on improving the scientific knowledge of the dynamic of zoonotic pathogens and vectors of the sympatric small mammal community inhabiting those intensive agricultural landscapes. In the first chapter, I reviewed current knowledge on the role of common vole in tularemia epidemiology and identified relevant knowledge gaps in the “Francisella tularensis–M. arvalis” system. In the second chapter, I characterized the most common arthropod vectors (fleas and ticks) parasitizing the small mammal host community. In the third and four chapters, I screened the host community for some zoonotic micropathogens and macroparasites: bacteria (F. tularensis and Bartonella), viruses (hantaviruses, arenaviruses and orthopoxviruses) and gastrointestinal helminths. Transversely, I examined variations in the parasitological parameters (prevalence, intensity and abundance) according to host species and sex, habitat (crop type), seasonality and the population dynamics of host species, with particular emphasis on the vole population cycles. I have detected F. tularensis, nine Bartonella species, three types of viruses and eight different helminth taxa. Half of those pathogens are considered zoonotic. Results showed that the small mammals surveyed that lives in sympatry with M. arvalis seem to have no relevant role in the circulation and maintenance of F. tularensis. Fluctuating population dynamics of M. arvalis and seasonality can affect the dynamic of vectors and pathogens. High-density periods of M. arvalis (outbreak years and summer) favored the circulation of viruses and bacteria, and increased the abundance of fleas, potentially also increasing the zoonotic risk for human populations. The infestation levels by ticks and gastrointestinal helminths were higher during the crash phase of the vole cycle. These and other pathogens could contribute to the maintenance of a low vole population phase, by limiting and delaying the recovery of the vole population after a crash. This thesis contributed new knowledge of the circulation of zoonotic pathogens and vectors in this farming system, with public health implications. Of particular importance are the roles that vole outbreaks play as an amplifier and spill-over agent of zoonotic diseases; the need to consider new viruses (in particular, hantavirus) in public health surveillance; and the usefulness of community-based monitoring of pathogen circulation, maintenance and transmission to improve prevention.