The Itchy and Scratchy Show: Association Between Co-Occurring Parasites and Exploratory Behaviour in Mice

Abstract

Host-parasite interactions are complex, involving host behaviour, host condition, and possible antagonism or mutualism between co-occurring parasites. The white-footed mouse (Peromyscus leucopus) is a small, abundant, generalist rodent, and the primary host for the black-legged tick (Ixodes scapularis) in its larval stage. Since larval ticks do not actively pursue their hosts (they wait for possible hosts to come to them), individual differences in mouse exploratory behaviour might be expected to correlate with tick burden. However, mice may also prevent tick attachment with defensive behaviour such as grooming. Yet, the relationships between tick parasitism and host exploratory and grooming behaviours have never been assessed. I analysed data from a capture-mark-recapture study conducted over 5 summers (2016-2020) in eastern Ontario, Canada, in which 1,035 mice were captured a total of 4,333 times. The probability of tick parasitism occurring and being more intense was significantly higher when the mouse was also parasitized by fleas, suggesting co-occurrence of these two parasites on host mice. A total of 510 mice were subjected to an open-field test to quantify exploratory and grooming behaviours. Exploration had a negative relationship with tick presence and a positive relation with flea presence. Most interestingly, there was a significant “tick × flea” interaction on exploratory behaviour such that fleas were positively associated with exploration only when ticks were absent. Surprisingly, there was no relationship between grooming behaviour in the open-field test and parasite presence, although grooming increased with mouse activity. This study shows that co-occurring parasite species (ticks and fleas) may interact to affect their host’s exploratory behaviour. Alternatively, individual differences in exploratory behaviour of hosts may differentially affect their susceptibility to being infested with ticks, fleas, or both. Future manipulative studies should use experimental design to determine the causality of the parasitism-behaviour relationships observed.