Prophylactic Avoidance of Hazardous Prey by the Ant Host Myrmica rubra

Abstract

Ants are the hosts of many microorganisms, including pathogens that are incidentally brought inside the nest by foragers. This is particularly true for scavenging species, which collect hazardous food such as dead insects. Foragers limit sanitary risks by not retrieving highly infectious prey releasing entomopathogenic fungal spores. This study investigates whether similar prophylactic strategies are also developed for food associated with weak or delayed risks of fungal contamination. We compared, in Myrmica rubra ant colonies, the retrieval dynamics of dead flies that were (1) conidia-free, (2) covered with a low amount of Metarhizium brunneum entomopathogenic conidia or (3) recently fungus-killed but not yet sporulating. Foragers mostly avoided fungus-killed prey and delayed the retrieval of conidia-covered flies. A second sanitary filter occurred inside the nest through a careful inspection of the retrieved prey. Ultimately, ants mostly consumed conidia-free and conidia-covered flies, but they relocated and discarded all fungus-killed prey outside of the nest. Our study confirms that, as a host of generalist entomopathogenic fungi, Myrmica rubra ants have developed a prophylactic avoidance and a differential management of prey depending on their infectious potential. We discuss the functional value as well as the possible cues underlying pathogen avoidance and prey discrimination in ants.

Spatial distancing by fungus-exposed Myrmica ants is prompted by sickness rather than contagiousness

“…Overall, our data suggest that the mobility and spatial location of M.rubra foragers is not altered by the chemical and mechanical cues associated with the fungal spores. This goes along with previous observations where M.rubra ants were not repelled by the presence of fungal conidia over prey or on foraged areas and were as prone to retrieve these items inside the nest (Pereira & Detrain 2020b, Pereira et al 2021. Further studies should investigate to which extent this lack of early spatial distancing correlates (or not) with social behaviour such as allogrooming by M.rubra nestmates.…”

“…In the case of pathogens that are socially transmitted through physical contacts, a first sanitary strategy is the limitation or even the avoidance of interactions between healthy individuals and infectious items (Pereira & Detrain 2020a, 2020b or diseased nestmates (Stroemeyt et al 2014, Okuno et al, 2012, Romano et al 2020, Stockmaier et al 2021). In the case of entomopathogenic fungi, a contaminated ant remains infectious as long as spores are present over its body.…”

A fungus infected environment does not alter the behaviour of foraging ants

“…Indeed, the number of conidia covering the body of a sporulating fly was estimated to around 10 6 spores following the procedure described in Ref. 49 . In order to prevent any unwanted contamination of the UFA by conidia dispersed through air flows, all the experiments were carried out inside a closed box under still air conditions.…”

Among the shapeshifters: parasite-induced morphologies in ants (Hymenoptera, Formicidae) and their relevance within the EcoEvoDevo framework

“…For ants alone, current scientific publications yield over 1400 records of parasites and parasitoids from 51 families infecting 82 genera of ants [ 22 , 23 ]. This vast number of host–parasite systems has yielded a large amount of publications addressing diverse topics, from the impact of the host’s ecology and life history on its susceptibility to parasitism (reviewed in [ 22 ]) to social immunity [ 24 – 27 ], pest management [ 28 ] and untangling the phylogenies of ant hosts and their behaviour-altering “zombie” parasites [ 29 ]. It therefore becomes apparent that interactions with parasites constitute a significant part of social insects’ ecological interconnections that may have far-reaching effects on both individual and colony.…”