Lesser of Two Evils? Foraging Choices in Response to Threats of Predation and Parasitism

Abstract

Predators have documented post-encounter (density-mediated) effects on prey but their pre-encounter impacts, including behavioural alterations, can be substantial as well. While it is increasingly evident that this “ecology of fear” is important to understand for natural enemy-victim relationships, fear responses of hosts to the threat of infection by a parasite are relatively unknown. We examined larval amphibian (Lithobates pipiens) foraging choices by experimentally manipulating the presence of cues relating to predator (larval odonate) or parasite (the trematode Ribeiroia ondatrae) threats. Tadpoles avoided foraging where predator or parasite cues were present; however, they did not treat these as equal hazards. When both threats were simultaneously present, tadpoles strongly preferred to forage under the threat of parasitism compared to predation, likely driven by their relative lethality in our study. Our results indicate that altered spatial use is an important anti-parasite behaviour, and demonstrate that parasite avoidance can affect foraging in a manner similar to predators, warranting greater study of the pre-encounter effects of this enemy type.

Learned parasite avoidance is driven by host personality and resistance to infection in a fish–trematode interaction

“…For example, exploration behaviour needed in locating suitable food items and assessing other sources of risk may result in time spent also in areas that contain parasites, particularly, if the level of exposure is not lethal. A recent study on tadpoles demonstrated that parasite avoidance can be governed by trade-offs between the avoidance of different threats depending on their lethality: while foraging in areas with parasite cues was avoided if the alternative was a threat-free area, it was preferred over foraging in areas with predator cues [41].…”

Parasite avoidance behaviours in aquatic environments

“…In aquatic systems, several studies have illustrated such conflicts in amphibian tadpoles. For example, Koprivnikar & Penelva [101] reported stronger behavioural responses of Lithobates pipiens tadpoles to predation than parasitism. Similar results have been reported, for example, in P. regilla and Anaxyrus boreas [83].…”

A review of the role of parasites in the ecology of reptiles and amphibians

“…Conversely, ephemeral breeding frog species that encountered less trematodes also lacked the behavioural response, suggesting selection may occur on such behavioural traits (Szuroczki & Richardson ). Parasite avoidance behaviour is complex and interacts with predators, whereby tadpoles ( L. pipiens ) preferred areas without trematodes ( Ribeiroia ondatrae) unless their alternative was predator exposure by larval odonates (Koprivnikar & Penalva ). American toad tadpoles ( Bufo americanus ) fleed from the touch of a trematode ( Echinostoma sp.…”