Pathogen avoidance and prey discrimination in ants

Abstract

Insect societies have developed sanitary strategies, one of which is the avoidance of infectious food resources as a primary line of defence. Using binary choices, we investigated whether Myrmica rubra ants can identify prey that has been artificially infected with the entomopathogenic fungus, Metarhizium brunneum . We compared the ants' foraging behaviour towards infected prey at three different stages of fungus development : (i) prey covered with fungal conidia, (ii) prey freshly killed by the fungus and (iii) sporulating prey. Most foragers retrieved a corpse covered with a high number of spores but they consistently avoided a sporulating prey and collected less prey that had recently died from fungal infection. Furthermore, ant responses were highly variable, with some individuals retrieving the first prey they encountered while others inspected both available prey before making a decision. Workers were not repelled by the simple presence of fungal conidia but nevertheless, they avoided retrieving cadavers at later stages of fungal infection. We discuss how these different avoidance responses could be related to: differences in the ants’ perceptive abilities; physico-chemical cues characterizing fungus-infected prey or in the existence of physiological or behavioural defences that limit sanitary risks associated with potentially contaminated resources.

Prophylactic Avoidance of Hazardous Prey by the Ant Host Myrmica rubra

“…This finding confirms that foragers, which are the first ones to discover dead insects, act as a first line of defence against pathogens by hesitating to retrieve potentially hazardous food items. The protective behaviour of foragers thus ranges from a clear-cut avoidance of heavily sporulating prey [ 35 , 38 ] to a mere slowdown of retrieval of slightly infectious prey, as shown in the current study. From a functional perspective, the slower retrieval of conidia-covered flies allows foragers to explore the discovered food item with their antennae and to assess more accurately the presence of conidia over the insect body [ 68 , 69 ].…”

“…For example, some ant or termite species do not cannibalise fungus-killed nestmates (ants: [ 35 ], termites: [ 36 ]). Likewise, several ant species avoid being exposed to entomopathogenic fungi by not collecting items covered with a high amount of Metarhizium anisopliae fungus conidia [ 37 ] or sporulating cadavers [ 38 ]. Such a discrimination may result from the perception of volatile chemical compounds released by the pathogen itself [ 39 ] or by its interaction with the insect host [ 40 ].…”

“…Within the same ant species, colonies may also differ in their response to pathogens, with some avoiding locations contaminated by fungal spores and others preferentially digging their nest inside a spore-containing soil [ 44 ]. In a recent study on the red ant Myrmica rubra [ 38 ], we found that the retrieval of prey differed depending on its state of infection. While M. rubra foragers retrieved most of the prey that were simply covered with M. bruneum fungal conidia, they were less likely to bring back an insect that recently died from fungus infection and did not transport any sporulating prey at all.…”

“…In this context, foragers represent a first line of food quality auditors. For example, by simply avoiding retrieving sporulating prey, Myrmica rubra foragers prevent the uptake of a high load of pathogens inside the nest [ 38 ]. However, we still do not know to what extent this first line of protection is permeable to food items that are weakly infectious or with a delayed pathogenicity—i.e., infected but not yet infectious items.…”

Behaviours indicating cannibalistic necrophagy in ants are modulated by the perception of pathogen infection level

“…Such an elevated number of hygienic behaviours was also observed in other social species, which supports the view that workers can assess the level of risk associated with an infectious agent 6,13,59,62,[72][73][74][75] . For example, although the foragers of Mymica rubra retrieved corpses of prey covered with high number of spores, they consistently avoided sporulating corpses and collected less prey items that had recently died from fungal infection 76 .…”