Variation in leukocyte indices and immunoglobulin levels according to host density, sex, flea burden and tularemia prevalence in the common vole Microtus arvalis

Abstract

Rodent populations often undergo large, regular fluctuations. We studied immunological condition and physiological stress in the common vole and how it varied with environmental factors linked with population fluctuations, namely flea and Francisella tularensis (the bacterium causing tularemia) prevalence. We used two leukocyte indices, neutrophil-to-lymphocyte ratio (N:L) and proportion of eosinophils, as physiological long-term stress indicators, and measured levels of immunoglobulins (Ig) as a generic index of immunological condition. Leukocyte indices showed a hump-shaped relationship with Ig levels, consistent with an interdependence between physiological stress and immunological condition. N:L was negatively associated with vole density only in males. Eosinophil proportion was explained by the interaction between flea burden and tularemia prevalence, with highest levels in flea-infested voles also infected with tularemia. Ig levels did not vary with sex or flea prevalence but increased in tularemia-infected voles. When Ig levels were included as covariates in our models, the associations between leukocyte indices and environmental factors remained significant. Results suggest sex-specific associations between physiological stress and population density, and an influence of tularemia infection depending on ectoparasite load. We recommend using immunological parameters complementarily to leukocyte indices when studying physiological stress and infection dynamics in wild populations.