What explains tick proliferation following large-herbivore exclusion?

Abstract

Our study [1] explored the effects of large-herbivore exclusion on tick abundance and tick-borne pathogens across a rainfall gradient, using a replicated long-term (5-6 years at the time of our study) size-selective exclosure experiment in Kenya. During our 13-month study, we found that tick abundance varied across time and among tick species, but that the total number of questing adult ticks was significantly greater within exclosures than in unfenced control plots (and increased with each successive level of large-herbivore removal). This effect was the strongest in the driest locations (cf. [2]), indicating that climatic context and wildlife removal can interact to affect tick abundance; we interpreted our results as being driven by increases in smaller mammalian hosts in the absence of megafauna and concluded by suggesting that the prevention of wildlife loss might help to prevent an escalation in the number of questing ticks infected with zoonotic pathogens. Esser et al. [3] and Buck & Perkins [4] suggest a different interpretation for our results, namely that they might be an artefact of our experimental plot sizes (each 1 ha), and that in the absence of final hosts, ticks might have dispersed into the exclosure plots via rodent hosts. Specifically, these authors propose that immature ticks were imported into the plots, leading to a proliferation of questing adult ticks that were not subsequently 'removed' by final hosts and were therefore present to be picked up in our drag samples. If this is the case, then the observed pattern is scale-dependent, and ticks might not proliferate following large-scale large-mammal extirpation scenarios because final hosts are entirely lost. Such scale dependence has been observed in North American deer exclosures [5]. Available data are not sufficient to establish the relative support for these two interpretations, which are not mutually exclusive. These commentaries make an important contribution by outlining a hypothesis that must be explicitly tested in future research. Until a more conclusive verdict can be rendered, however, we welcome the opportunity to clarify several points and explain why we still consider our original interpretation to be a more probable explanation for our results. Both comments point out that in the absence of final hosts, entire tick life cycles cannot be sustained [6]. Importantly, however, the total elimination of all final hosts is unlikely in our study system, and did not actually occur for any of the tick species within our 1 ha study plots. Adults of the three tick species in our study, R. praetextatus, R. pravus and R. pulchellus, have been documented on 25, 19 and 29 host species, respectively, that occur in our experimental plots [7], which range in size from ground squirrels (less than 1 kg) to elephants (greater than 2000 kg) [8]. It is therefore possible that tick populations in the exclosure plots are sustained by small-to-medium-sized mammalian final hosts that occur within most if not all of the large-herbivore-exclusion treatme...