Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies.

Simon Tragust,Sylvia Cremer,Jürgen Heinze,Michel Chapuisat,Line V Ugelvig

doi:10.1186/1471-2148-13-225

Abstract

BackgroundThe brood of ants and other social insects is highly susceptible to pathogens, particularly those that penetrate the soft larval and pupal cuticle. We here test whether the presence of a pupal cocoon, which occurs in some ant species but not in others, affects the sanitary brood care and fungal infection patterns after exposure to the entomopathogenic fungus Metarhizium brunneum. We use a) a comparative approach analysing four species with either naked or cocooned pupae and b) a within-species analysis of a single ant species, in which both pupal types co-exist in the same colony.ResultsWe found that the presence of a cocoon did not compromise fungal pathogen detection by the ants and that species with cocooned pupae increased brood grooming after pathogen exposure. All tested ant species further removed brood from their nests, which was predominantly expressed towards larvae and naked pupae treated with the live fungal pathogen. In contrast, cocooned pupae exposed to live fungus were not removed at higher rates than cocooned pupae exposed to dead fungus or a sham control. Consistent with this, exposure to the live fungus caused high numbers of infections and fungal outgrowth in larvae and naked pupae, but not in cocooned pupae. Moreover, the ants consistently removed the brood prior to fungal outgrowth, ensuring a clean brood chamber.ConclusionOur study suggests that the pupal cocoon has a protective effect against fungal infection, causing an adaptive change in sanitary behaviours by the ants. It further demonstrates that brood removal–originally described for honeybees as “hygienic behaviour”–is a widespread sanitary behaviour in ants, which likely has important implications on disease dynamics in social insect colonies.

Highlights

The brood of ants and other social insects is highly susceptible to pathogens, those that penetrate the soft larval and pupal cuticle
Whereas grooming is a general response against pathogens in social insects, hygienic behaviour is by definition restricted to the immobile brood of social Hymenoptera
Except for C. smithi, which brought in more larvae (L) than pupae (P) (69% L, 44% P; χ2-test: χ2 = 8.186, d.f. = 1, P = 0.004), both brood types were retrieved at equal rates (Li. humile: 67% L, 51% P, χ2 = 1.699, d.f. = 1, P = 0.192; La. neglectus: 75% L, 75% P, χ2 = 0.037, d.f. = 1, P = 0.847; P. punctata: 100% L, 100% P, χ2-testing inappropriate due to 100% intake for both L and P)

Summary

Introduction

The brood of ants and other social insects is highly susceptible to pathogens, those that penetrate the soft larval and pupal cuticle. Colonies of social insects have evolved collective disease defences to counteract the high risk of disease transmission within social groups (reviewed in [1,2]) This social immunity complements individual immune defences of all group members and comprises sanitary behaviours, use of antimicrobials and modification of interaction frequencies Whereas grooming is a general response against pathogens in social insects (ants: [9,11], termites: [12,13]), hygienic behaviour is by definition restricted to the immobile brood of social Hymenoptera. It was originally reported from honeybees [2,14], and has recently been found in ants [10]. In ants, where brood is placed together in joint brood piles [10], transmission risk among brood items is probably much higher than in wasps and bees, where each brood item is placed in an individual brood cell

Methods

Results

Discussion

Conclusion