Lab

RATS - Rodent Adaptive Tracking and Surveillance

About the lab

Ecological and evolutionary aspects of unstable population dynamics in rodents

Featured projects (1)

Project
Emerging Infectious Diseases (EID) are a growing burden for public health and global economies, and most are of zoonotic nature. Effective approaches to prevention and control of zoonoses necessarily require a broad view. To enhance our understanding of zoonotic outbreaks we need long-term, empirical and integrative ecological and epidemiological studies. Because animal populations are dynamic, it is also paramount to account for fluctuations in abundance to understand zoonoses maintenance, disease spill-over and transmission routes that ultimately affect people. Many rodents (rats, mice, voles) act as hyper-reservoirs of zoonoses, and some species are characterized by very large fluctuations in abundance (boom-bust dynamics). When overabundant, they become major agricultural pests and disease spreaders, and a burden to societies worldwide. The study of zoonoses linked to boom-bust rodents requires a dynamic approach that evaluates 'who' participates in the transmission cycles, 'how' the pathogen is transmitted to humans and 'why' these aspects vary in space and time. On this research proposal we will focus on Francisella tularensis, the etiological agent of the notifiable human infectious disease known as tularemia which recurrently affects northwest Spain (Castilla y León; >1,500 human cases to date since 1997). We have identified the boom-bust populations of common vole (Microtus arvalis) as a main amplification factor of F. tularensis in NW Spain (project ECOTULA 2016-2019). With this new project, we aim to link the density-dependent disease amplification within vole populations and the environmental spill-over of the bacteria leading to human tularemia outbreaks. We will: (i) elucidate the nature of the epidemiological relationship between F. tularensis and voles; (ii) test the hypothesis that recurrent tularemia epidemics result from the periodic concatenation of two disease "jumps" that are driven by vole dynamics (jump 1: from a reservoir to voles during increase phase and jump 2: from voles to the environment during peak phase, after amplification within voles during increase phase); and (iii) elucidate the role that hares and rabbits, mosquitoes and ticks, and vole predators have in circulating and maintaining F. tularensis, as well as which species may act as environmental spreaders of F. tularensis. We will provide new knowledge on the genomics, dynamics and short-to-long range circulation of F. tularensis in NW Spain and beyond. Other highly infective zoonotic pathogens of bacterial origin also deserve further research, as have been also putatively linked to fluctuating vole populations. We will therefore study the occurrence, genomics and dynamic prevalence in wildlife and vectors of a suite of relevant rodent-borne zoonotic bacteria suspected to circulate among voles in NW Spain (Coxiella, Ricketsiia and Borrelia) In order to successfully mitigate the impacts of episodic tularemia outbreaks, it is paramount to ensure that comprehensive scientific-based information reaches society. We will enhance education and knowledge-transfer about rodent-borne zoonoses in NW Spain, informing both to the general public and public health professionals and managers. We ultimately aim to produce tangible returns to society arising from the public investment in our scientific research line on zoonotic disease ecology and dynamics.

Featured research (5)

We screened 526 wild small mammals for zoonotic viruses in northwest Spain and found hantavirus in common voles (Microtus arvalis) (1.5%) and high prevalence (48%) of orthopoxvirus among western Mediterranean mice (Mus spretus). We also detected arenavirus among small mammals. These findings suggest novel risks for viral transmission in the region.
The dynamics of cyclic populations distributed in space result from the relative strength of synchronising influences and the limited dispersal of destabilising factors (activators and inhibitors), known to cause multi-annual population cycles. However, while each of these have been well studied in isolation, there is limited empirical evidence about how the processes of synchronisation and activation-inhibition act together, largely owing to the scarcity of datasets with sufficient spatial and temporal scale. We assessed a variety of models that could be underlying the spatio-temporal pattern, designed to capture both theoretical and empirical understandings of travelling waves using large-scale (> 35,000 km2), multi-year (2011-2017) field monitoring data on abundances of common vole (Microtus arvalis), a cyclic agricultural rodent pest. We found most support for a pattern formed from the summation of two radial travelling waves with contrasting speeds that together describe population growth rates across the region.
The expansion and intensification of agriculture are driving profound changes in ecosystems worldwide, favoring the (re)emergence of many human infectious diseases. Muroid rodents are a key host group for zoonotic infectious pathogens and frequently invade farming environments, promoting disease transmission and spillover. Understanding the role that fluctuating populations of farm dwelling rodents play in the epidemiology of zoonotic diseases is paramount to improve prevention schemes. Here, we review a decade of research on the colonization of farming environments in NW Spain by common voles (Microtus arvalis) and its public health impacts, specifically periodic tularemia outbreaks in humans. The spread of this colonizing rodent was analogous to an invasion process and was putatively triggered by the transformation and irrigation of agricultural habitats that created a novel terrestrial-aquatic interface. This irruptive rodent host is an effective amplifier for the Francisella tularensis bacterium during population outbreaks, and human tularemia episodes are tightly linked in time and space to periodic (cyclic) variations in vole abundance. Beyond the information accumulated to date, several key knowledge gaps about this pathogen-rodent epidemiological link remain unaddressed, namely (i) did colonizing vole introduce or amplified pre-existing F. tularensis? (ii) which features of the "Francisella-Microtus" relationship are crucial for the epidemiology of tularemia? (iii) how virulent and persistent F. tularensis infection is for voles under natural conditions? and (iv) where does the bacterium persist during inter-epizootics? Future research should focus on more integrated, community-based approaches in order to understand the details and dynamics of disease circulation in ecosystems colonized by highly fluctuating hosts.
Background Fleas frequently infest small mammals and play important vectoring roles in the epidemiology of (re)emerging zoonotic disease. Rodent outbreaks in intensified agro-ecosystems of NW Spain have been recently linked to periodic zoonotic disease spillover to local human populations. Obtaining qualitative and quantitative information about the composition and structure of the whole flea and small mammal host coexisting communities is paramount to understand disease transmission cycles and to dilucidate the disease-vectoring role of flea species. The aims of this research were to: i) characterise and quantify the flea community parasiting a small mammal guild in intensive farmlands in NW Spain, and ii) determine and evaluate patterns of co-infection and the variables that may influence parasitological parameters. Methods We conducted a large scale survey stratified by season and habitat of fleas parasitizing the small mammal host guild. We report on the prevalence, mean intensity, and mean abundance of flea species parasitizing Microtus arvalis, Apodemus sylvaticus, Mus spretus and Crocidura russula. We also report on aggregation patterns (variance-to-mean ratio and Discrepancy index), co-infection by different flea species in hosts (Fager Index), and used Generalized Linear Mixed Models (GLMM) to study flea parameter variation according to season, habitat and host sex. Results Three flea species dominated the system (99.4%), namely: Ctenophthalmus apertus gilcolladoi, Leptopsylla taschenbergi and Nosopsyllus fasciatus. Results showed a high aggregation pattern of fleas in all hosts. All host species in the guild shared C. a. gilcolladoi and N. fasciatus, but L. taschenbergi mainly parasitized mice (M. spretus and A. sylvaticus). We found significant male-biased infestation patterns in mice, seasonal variations in flea abundances for all rodent hosts (M. arvalis, M. spretus and A. sylvaticus), and relatively lower infestation values for voles inhabiting alfalfas. Simultaneous infections by two or three flea species occurred in 36.8% of all hosts, and N. fasciatus was the commonest flea co-infecting small mammal hosts. Conclusions The generalist N. fasciatus and C. a. gilcolladoi dominated the flea community, and a high percentage of co-infections with both species occurred within the small mammal guild. Nosopsyllus fasciatus may show higher competence of inter-specific transmission, and future research should unravel its role in the circulation of rodent-borne zoonoses.
Diseases and host dynamics are linked, but their associations may vary in strength, be time lagged, and depend on environmental influences. Where a vector is involved in disease transmission, its dynamics are an additional influence, and we often lack a general understanding on how diseases, hosts and vectors interact. We report on the occurrence of six zoonotic arthropod-borne pathogens (Anaplasma, Bartonella, Borrelia, Coxiella, Francisella and Rickettsia) in common voles (Microtus arvalis) throughout a population fluctuation and how their prevalence varies according to host density, seasonality, and vector prevalence. We detected Francisella tularensis and four species of Bartonella, but not Anaplasma, Borrelia, Coxiella or Rickettsia. B. taylorii and B. grahamii prevalence increased and decreased with current host (vole and mice) density, respectively, and increased with flea prevalence. B. doshiae prevalence decreased with mice density. These three Bartonella species were also more prevalent during winter. B. rochalimae prevalence varied with current and previous vole density (delayed-density dependence), but not with season. Coinfection with F. tularensis and Bartonella occurred as expected from the respective prevalence of each disease in voles. Our results highlight that simultaneously considering pathogen, vector and host dynamics provides a better understanding of the epidemiological dynamics of zoonoses in farmland rodents.

Lab head

Juan José Luque-Larena
Department
  • Instituto Universitario de Investigación en Gestión Forestal Sostenible
About Juan José Luque-Larena
  • I am mainly interested in the ecology and evolution of wild rodent populations, and in BIOLOGY in general. We study the ecology and public health impacts of colonizing populations of common voles in agricultural landscapes of NW Spain. We have recently demonstrated empirically the role of wild rodents as amplification and spillover agents of tularemia, and that fluctuations in the abundance of wild mammals play a key role in the epidemiology and risk of this zoonotic disease across Europe.

Members (5)

Francois Mougeot
  • Spanish National Research Council
Dolors Vidal
  • University of Castilla-La Mancha
Constantino Caminero
  • Instituto Tecnológico Agrario de Castilla y León, Spain
Silvia Herrero-Cófreces
  • Universidad de Valladolid
Eva Trapote
  • Universidad de León