Vole outbreaks may induce a tularemia disease pit that prevents Iberian hare population recovery in NW Spain

Abstract

Iberian hare populations have suffered severe declines during recent decades in Spain. Between 1970 and 1990s, a rapid increase in irrigation crop surface in NW Spain (Castilla-y-León region) was followed by a common vole massive range expansion and complete colonization of lowland irrigated agricultural landscapes from mountainous habitats. The subsequent large cyclic fluctuations in abundance of colonizing common voles have contributed to a periodic amplification of Francisella tularensis, the etiological agent that causes human tularemia outbreaks in the region. Tularemia is a fatal disease to lagomorphs, so we hypothesize that vole outbreaks would lead to disease spill over to Iberian hares, increasing prevalence of tularemia and declines among hare populations. Here we report on the possible effects that vole abundance fluctuations and concomitant tularemia outbreaks had on Iberian hare populations in NW Spain. We analysed hare hunting bag data for the region, which has been recurrently affected by vole outbreaks between 1996 and 2019. We also compiled data on F. tularensis prevalence in Iberian hares reported by the regional government between 2007 and 2016. Our results suggest that common vole outbreaks may limit the recovery of hare populations by amplifying and spreading tularemia in the environment. The recurrent rodent-driven outbreaks of tularemia in the region may result in a "disease pit" to Iberian hares: at low host densities, the rate of population growth in hares is lower than the rate at which disease-induced mortality increases with increased rodent host density, therefore, keeping hare populations on a low-density equilibrium. We highlight future research needs to clarify tularemia transmission pathways between voles and hares and confirm a disease pit process.

Figure 1

Iberian hare population trends. (A) Iberian hare abundance index (AI: number of hares hunted/number of hunting licences ± standard error) per year from 1974 to 2019. (B) Iberian hare abundance index during the study period (1997 to 2019). Brown bars indicate years when vole outbreaks were detected. Note that 1997 is the first year with officially declared human case of tularemia in the region.

Figure 2

(A) Relationships between the Iberian hare population instantaneous growth rate (PGR) and the hare abundance index (AI, number of hunted hares/hunting licences per year) during vole outbreak years (in red) and during all years (in blue). (B) Prevalence (% ± standard error) of Francicela tularensis in Iberian hares collected through passive surveillance from 2007 to 2016. Numbers in bold shows sample size (number of hares screened for tularemia). For some years marked with an asterisk (*), numbers refer to both Iberian hares and wild rabbit (lumped together in the data provided by Rodríguez-Ferri (2017). Note that F. tularensis prevalence during those years was zero, so uncertainty regarding hare sample size was unlikely to affect conclusions. In addition, the mean prevalence of F. tularensis in 2010 was obtained from a total of three samples; one positive hare in the province of Zamora and another positive hare from two hares collected in the province of Valladolid. Although the mean is represented in the graph, this low sample size makes us believe that it is not representative of the real prevalence.