Few vertebrate species dominate the Borrelia burgdorferi s.l. life cycle

Abstract

Background. In the northern hemisphere, ticks of the Ixodidae family are vectors of diseases such as Lyme borreliosis, Rocky Mountain spotted fever and tick-borne encephalitis. Most of these ticks are generalists and have a three-host life cycle for which they are dependent on three different hosts for their blood meal. Finding out which host species contribute most in maintaining ticks and the pathogens they transmit, is imperative in understanding the drivers behind the dynamics of a disease.Methods. We performed a systematic review to identify the most important vertebrate host species for Ixodes ricinus and Borrelia burgdorferi s.l. as a well-studied model system for tick-borne diseases. We analyzed data from 66 publications and quantified the relative contribution for 15 host species.Review results. We found a positive correlation between host body mass and tick burdens for the different stages of I. ricinus. We show that nymphal burdens of host species are positively correlated with infection prevalence with B. burgdorferi s.l., which is again positively correlated with the realized reservoir competence of a host species for B. burgdorferi s.l. Our quantification method suggests that only a few host species, which are amongst the most widespread species in the environment (rodents, thrushes and deer), feed the majority of I. ricinus individuals and that rodents infect the majority of I. ricinus larvae with B. burgdorferi s.l.Discussion. We argue that small mammal-transmitted Borrelia spp. are maintained due to the high density of their reservoir hosts, while bird-transmitted Borrelia spp. are maintained due to the high infection prevalence of their reservoir hosts. Our findings suggest that Ixodes ricinus and Borrelia burgdorferi s.l. populations are maintained by a few widespread host species. The increase in distribution and abundance of these species, could be the cause for the increase in Lyme borreliosis incidence in Europe in recent decades.

The wild life of tick-borne pathogens

“…In our two sites where deer were naturally absent, alternative hosts for adult ticks were available in the form of European hare (Lepus europaeus), European hedgehog (Erinaceus europaeus), European pine marten (Martes martes), or Red fox (Vulpes vulpes), as indicated by our camera trap data. Although all of these host species can support feeding adult I. ricinus 190 (Chapter 2), their presence appeared insufficient for sustaining an I. ricinus population, as questing larvae were nearly absent where there were no deer. The difference was smaller, but still substantial, for the nymphal and adult stages.…”

“…This difference could be due to differences in host assemblage composition between different studies. Small mammals are considered the most important hosts for larval I. ricinus 190 (Chapter 2), however, when small mammals are absent, deer are able to feed a substantial number of larvae. This might be the explanation for a linear correlation of I. ricinus density and estimates of deer density in several studies in Scotland 38,[206][207][208] where small mammals occur in low abundance and carry few ticks in some habitats 209 .…”

“…Most larvae feed from small mammals, while most adult ticks feed on deer 190 (Chapter 2). It is widely assumed that deer are essential hosts for ticks in the I. ricinus complex.…”

“…Both I. ricinus and I. scapularis are three-host ticks. They feed mainly on rodents as larvae, on rodents, birds and deer as nymphs, and on deer as adults 36,190 (Chapter 2). The number of larvae in the environment is related to the density and activity of deer, which determine the reproductive success of adult ticks 32 (Chapter 4).…”

“…In Europe and North America, the most common vector-borne pathogens are transmitted by two tick species from the Ixodes ricinus complex 60 : I. ricinus in Europe and I. scapularis in North America. Both species are three-host ticks, mainly feeding on small rodents as larvae, on multiple host species as nymphs, and on deer as adults 36,190 (Chapter 2). While feeding on these hosts, ticks can become infected with pathogens that are transmitted by the host 8 .…”