Scale-dependent release of Borrelia burgdorferi sensu lato infected Ixodes ricinus larvae from vertebrates

Abstract

AbstractBackground:The multi-host tickIxodes ricinusis the principal vector of zoonotic diseases in Europe. Quantifying the contribution of each host species in the tick’s pathogen transmission cycles is imperative in spatio-temporal pathogen exposure assessments, but remains challenging in the absence of techniques identifying the previous host on which (infectious) host-searching ticks have fed. Based on European literature data, we here investigate the capacity of vertebrate species to infect naïve larvae with particularBorreliagenospecies belonging to the multi-host pathogen complexBorrelia burgdorferisensu lato (the causative agent of Lyme Borreliosis in humans).Methods:We calculated the number of infected larvae generated by an infectious host. This measure (‘realized release’) was subsequently used to investigate intrinsic host infectiousness (through adjustment for tick exposure), lifetime release, and spatial dilution. Host abundances from naturally occurring vertebrate communities were subsequently used to estimate their local contributions to the population of infectious host-searching nymphs.Results:Thirty-one vertebrates were identified as amplifying hosts; vertebrate species that successfully generate larvae infected with aBorreliagenospecies. In 1-ha forest plots, per genospecies one vertebrate species released a disproportional amount of infected larvae. Several bird species show (high) infectiousness for non-avian genospecies:B. lusitaniae,B. burgdorferisensu stricto andB. afzelii. At population level, due to their smaller home ranges in combination with higher densities and tick exposures, several mammal species locally intensely contributed to mammalian genospecies (B. afzelii,B. burgdorferis.s. andB. bavariensis). In contrasts, due to their larger home ranges and lower tick exposure, the birds’ local contributions were more restricted – this despite their higher intrinsic infectiousness (reservoir competence). Given their seemingly lower specificity in amplification, birds are the main driver in the maintenance of pathogen diversity across macro-geographic scales.Conclusions:Ecological factors that affect the infection pressures and reservoir competence are still poorly understood in one of the best-studied tick-borne zoonoses (B. burgdorferis.l.). To anticipate current rapidly changing abiotic environmental conditions – inevitably affecting tick exposures and zoonotic risks - we advocate the generation of field-experimental data on host reservoir competence based on larval infections.