To cool or not to cool? Intestinal coccidians disrupt the behavioral hypothermia of lizards in response to tick infestation

Abstract

It is generally accepted that parasites exert negative effects on their hosts and that natural selection favors specific host responses that mitigate this impact. It is also known that some components of the host immune system often co-evolve with parasite antigens resulting in a host-parasite arms race. In addition to immunological components of the anti-parasitic response, host behavioral responses are also important in this arms race and natural selection may favor avoidance strategies that preclude contact with parasites, or shifts in the host’s thermoregulatory strategy to combat active infections (e.g., behavioral fever). Ticks are widespread parasites with direct and indirect costs on their vertebrate hosts. Their saliva provokes hemolysis in the blood of their hosts and can transmit a plethora of tick-borne pathogens. We enquired whether tick infestation by Ixodes pacificus can provoke a thermoregulatory response in Sceloporus occidentalis. For this, we compared the thermoregulatory behavior of tick-infested lizards against tick-infested lizards co-infected with two different species of coccidians (Lankesterella occidentalis and Acroeimeria sceloporis). After this, lizards were kept in individual terraria with a basking spot and fed ad libitum. We found that tick-infested lizards sought cooler temperatures in proportion to their tick load, and this response was independent of the co-infection status by L. occidentalis. This was consistent in April and June (when tick loads were significantly lower) and suggests a conservative strategy to save energy which might have been selected to overcome tick infestations during phenological peaks of this parasite. However, this behavior was not observed in lizards co-infected with A. sceloporis, suggesting that co-infection with this intestinal parasite prompt lizards to be active. Cost of tick infestation was confirmed because housed lizards lost weight at a constant ratio to initial tick load, independently of other infections. The broader implications of these findings are discussed in the context of climate change.