Ecology of rodent outbreaks and zoonotic diseasescommon voles in the farmland of north-west spain

Laburpena

Some rodent populations fluctuate in abundance by several orders of magnitude and are characterized by multi-annual “boom-bust” dynamics. The temporal overabundance of rodents favours the spreading of individuals in humanized landscapes, which causes damage to agriculture and/or forestry producing significant economic losses. Noteworthy, such irruptive spatial-temporal spreading of rodents also contributes to the amplification and spill-over of zoonotic pathogens of risk to humans, pets, livestock or other wildlife. Identifying the causative mechanisms and factors behind unstable rodent populations remains an enduring challenge to population ecology, largely motivated by rodent-borne socio-economical and public health impacts. Studying the dynamics of rodent-borne zoonotic diseases, identifying the key hosts, reservoirs and vectors involved in their transmission routes, is thus crucial for a better understanding of epidemiological cycles of zoonoses in nature. Moreover, examining the dynamics of habitat use by fluctuating rodent hosts in humanized landscapes contributes to a better understanding of the spatial-temporal patterns of spill-over processes of zoonotic diseases in the environment, which in turn contributes to more precise surveillance and disease prevention efforts. In this thesis, I studied wild populations of common vole (Microtus arvalis) from northwest Spain (Castilla-y-León region) that have recently invaded (<20 years) irrigated agricultural areas where large boom-bust periodic outbreaks are now endemic. To better understand the impacts of such temporal alternating density scenarios, that is, lots of voles present everywhere during outbreaks to virtually none between outbreaks, I studied: (i) the “contraction-expansion” dynamics of habitat use by voles in recently-colonised farmlands analysing space use patterns, (ii) the role of these unstable vole populations in the processes of amplification and spill-over of zoonotic diseases of risk to humans in the environment, and (iii) the dynamics and nature of ecological interactions between key irruptive hosts like voles and their parasitic arthropod-vectors, and their relative role in the transmission cycles of zoonotic micro-parasites (pathogens). The combination of these study approaches, incorporating the ecological context, intends to contribute new knowledge for the vole control and outbreak management, and disease prevention by providing key aspects about how zoonotic pathogens circulate through wildlife in farmlands. I specifically explored: (i) how common voles are distributed in intensively-farmed ecosystems and which crops (cereals and alfalfas) or semi-natural habitats (fallows and field margins) act as reservoirs during low density phases, and which are more prone to be colonized by common voles at high density phases, (ii) the main zoonotic pathogens of bacterial origin carried by voles, and the density-dependent relationship between pathogen prevalence (specifically of Francisella tularensis and Bartonella spp.) and host abundance, (iii) the role of voles as reservoirs and spill-over agents in the epidemiological cycle of F. tularensis and the associations between vole outbreaks and tularemia cases in humans, (iv) whether a rodent host (common vole) and its main arthropod-vector (fleas) share the same zoonotic pathogens, and (v) the density-dependent relationship between flea burdens and common voles, and how fleas can affect key aspects of the dynamics and numbers of this irruptive rodent host (i.e., body condition, reproduction, population growth rate). I showed that common vole habitat use was dynamic, with a greater overall abundance of voles in field margins and alfalfas and an invasion process of cereal crops from the field margins during population increases. Spill-over of voles through the farming landscape is thus density dependent and originates in a matrix of linear semi-natural habitats interconnecting crops. I also found that tularemia cases in humans coincided in space and time with common vole outbreaks, and that F. tularensis prevalence in voles increased with vole density, highlighting that voles act as amplifiers and spill-over agent of the bacterium in the environment. I also contribute to propose a conceptual model based on my data in which fluctuating mammalian host populations have a key role in the epidemiology of tularemia across Europe. Other zoonotic pathogens found at a high prevalence in the studied common vole populations were Bartonella spp. Different species of Bartonella can be found among voles, showing different seasonal dynamics and associations with vole density. The main ectoparasites of common voles in intensive farmland were fleas, which also carried F. tularensis and Bartonella ssp., suggesting a potential role as vectors of both pathogens. Flea burden on voles varied with vole density in a delayed density-dependent manner. Temporal variations in flea burden can be explained by a dilution effect, as fleas concentrate on fewer hosts during population declines. Greater flea burdens were associated with reduced reproduction outputs and vole population growth rate, suggesting that fleas could contribute to maintain low density phases of common vole populations. I discuss the benefits of considering ecological interactions to better understand the dynamics of rodent fluctuations and prevent their impacts, such as crop damages and zoonotic outbreaks, as well as the need to consider the dynamic interactions between host, vectors and pathogens to improve predictions of disease emergence, disease control programs and bio-control initiatives.