Social Prophylaxis Through Distant Corpse Removal in Ants

Naturwissenschaften (2012) 99:833–842 DOI 10.1007/s00114-012-0965-6 ORIGINAL PAPER Social prophylaxis through distant corpse removal in ants Lise Diez & Jean-Louis Deneubourg & Claire Detrain Received: 7 May 2012 /Revised: 21 August 2012 /Accepted: 23 August 2012 /Published online: 7 September 2012 # Springer-Verlag 2012 Abstract Living in groups raises important issues concerning Introduction waste management and related sanitary risks. Social insects such as ants live at high densities with genetically related One of the major drawbacks of social life is the increased individuals within confined and humid nests, all these factors risk of exposure to pathogens due to high population densi- being highly favorable for the spread of pathogens. Therefore, ties and frequent contact rates with conspecifics (Anderson in addition to individual immunity, a social prophylaxis takes and May 1979; Schmid-Hempel 1998). In social insects, the place, namely, by the removal of risky items such as corpses breaking of a pathogen into the colony can become life- and their rejection at a distance from the ant nest. In this study, threatening since most pathogens will proliferate under the we investigate how Myrmica rubra workers manage to reduce warm and humid conditions found within the nest and will encounters between potentially hazardous corpses and nest- easily spread out within those groups of genetically related mates. Using both field and laboratory experiments, we de- individuals. scribe how the spatial distribution and the removal distance of At the individual level, there are two lines of defense waste items vary as a function of their associated sanitary risks against pathogens that are common to both solitary and (inert item vs. corpse). In the field, corpse-carrying ants social insects: the cuticular barrier and the innate immunity. walked in a rather linear way away from the nest entrance First, the tough cuticle covering the entire body of insects as and had an equal probability of choosing any direction. There- well as the thin cuticular layer on mouthparts, pharynx, and fore, they did not aggregate corpses in dedicated areas but intestinal tract act as efficient physical barriers against scattered them in the environment. In both field and laboratory invaders such as bacteria, viruses, and fungi. But, if patho- experiments, ants carrying corpses dropped their load in more gens break this first line of defense, innate immunity kicks remote—and less frequented—areas than workers carrying in by triggering a physiological defensive reaction in the inert items. However, for equidistant areas, ants did not avoid hemolymph of infected individuals. Innate immunity dropping corpses at a location where they perceived area involves a cellular response (i.e., phagocytosis and encap- marking as a cue of high occupancy level by nestmates. Our sulation of pathogens) and a humoral response (production results suggest that ants use distance to the nest rather than of antimicrobial compounds or melanization) (Schmid- other occupancy cues to limit sanitary risks associated with Hempel 2005; Siva-Jothy et al. 2005; Feldhaar and Gross dead nestmates. 2008). In insects, adaptive immune responses have also been reported: a prior exposure to a pathogen will launch a Keywords Necrophoresis . Myrmica rubra . Ants . Social more efficient defense the next time the same pathogen insects . Area marking . Threshold distance attacks and will improve protection of the individual against further challenges (e.g., in social insects such as termites, Rosengaus et al. 1998;bumblebees,SaddandSchmid- Communicated by: Sven Thatje Hempel 2006; and ants, Konrad et al. 2012). Despite the L. Diez (*) : J.-L. Deneubourg : C. Detrain potentially higher exposure to pathogens due to group liv- Unit of Social Ecology, Université Libre de Bruxelles, ing, social insects such as honeybees surprisingly lack sev- CP 231, Bd du Triomphe, 1050 Brussels, Belgium eral genes involved in immune responses that are present in e-mail: [email protected] nonsocial insects such as fruit flies and mosquitoes (Evans 834 Naturwissenschaften (2012) 99:833–842 et al. 2006). This suggests that immunity in social insects harvester ants (Hölldobler and Wilson 1990), or occasion- does not rely only on physiological and physical defenses at ally of inflorescences near Myrmica schencki and Myrmica the individual level but rather on lines of defenses against rubra nests entrances (Czechowski et al. 2008). Likewise, pathogens specifically achieved at the colony level (Wilson- corpses can be occasionally gathered at a location—so- Rich et al. 2009). called a cemetery. In the field, such cemeteries are mainly Social insects proved to be very successful in colonizing observed in some species living in populous colonies with almost all terrestrial ecosystems, and a reason of this success corpses being put with other wastes on the refuse pile like in is that they developed efficient ways to prevent or to limit army ants (Hölldobler and Wilson 1990)orleaf-cutting mortality due to pathogens through collective defenses species (Moser 1963). In other species, corpses can be (Cremer et al. 2007). First, social insects can upregulate scattered in the nest surroundings and individually aban- their immune response while the adult population is rapidly doned at remote locations (Howard and Tschinkel 1976). increasing (Ruiz-González et al. 2009). Social insects also From a prophylaxis perspective, the rejection of wastes and display a wide range of prophylactic behaviors (Cotter and corpses in areas that are remote from the nest or weakly Kilner 2010). Autogrooming and allogrooming (Rosengaus foraged could be a simple and efficient way to reduce encoun- et al. 1998) combined with the secretion of antibiotic com- ters between workers and those potentially hazardous items. pounds produced by the metapleural glands (Hart et al. To achieve this spatial segregation of corpses, transporting 2002) are common ways to remove most pathogens from ants should decide to drop their load at locations where the the cuticle. Another line of prophylaxis consists in reducing local density or activity level of nestmates is expected to be the density of pathogens within the confined space of the low. Therefore, corpses carrying ants should be able to assess nest. This is achieved by avoiding to dig the nest chambers nestmate density either through the number of interactions into infected soils (Drees et al. 1992), by using antimicrobial with congeners (Gordon et al. 1993; Detrain and Deneubourg material into the nest such as propolis in honeybees (Bankova 2009) or through the density of footprint marks (Devigne and et al. 2000) or tree resin in wood ants (Chapuisat et al. 2007), Detrain 2006; Lenoir et al. 2009) that are passively laid by and by removing food wastes (Zeh et al. 1999; Hart et al. walking ants. Such an area marking is used by workers as a 2002). A last way to prevent the spread of pathogens is density cue to tune their foraging behavior (e.g., in Lasius through the spatial isolation of dead or diseased individuals niger workers, Devigne et al. 2004) and could influence the from the healthy nestmates. In honeybees, dead or diseased behavior of corpse-carrying ants. adults and larvae are dropped outside the hive (Visscher In this paper, we investigate how ants manage sanitary 1983). In termites, corpses are buried into the nest (Crosland risks associated through the removal of corpses. We deter- et al. 1997; Ulyshen and Shelton 2012), while in most ant mine whether hazardous items—i.e., corpses—or inert items species, they are rejected and transported away from the nest are spatially segregated from areas usually explored by ants (Wilson et al. 1958; Choe et al. 2009; Diez et al. 2011). outside the nest. Therefore, we perform both field and In ants, necrophoresis—i.e., corpse removal—can be an laboratory experiments. First, we observe at which locations important issue for the survival of the colony. Indeed, ants the common red ant, M. rubra (L.), chooses to remove and that died from infectious diseases are potentially contagious: drop dead nestmates in the field. We investigate which they may contaminate nestmates staying in their vicinity parameters, such as the distance to the nest, the level of inside the nest or foragers fortuitously encountering corpses occupancy by nestmates, or the local abiotic conditions, are on commonly explored areas. Some studies have reported the most influential on the decision of ants to deposit corp- cases in which diseased or moribund ants leave the nest on ses. Then, we study during laboratory experiments whether their own and die away from their congeners (Heinze and area marking is used by carrying ants as a cue for ant Walter 2010; Bos et al. 2012). When workers die inside the occupancy and accordingly shape the spatial distribution nest, there are several ways for the colony to set them apart of corpses or inert items outside the nest. from healthy congeners and larvae. Dead individuals may be buried into the nest (Renucci et al. 2010) or may be put with other wastes in refuse chambers as in the case of leaf cutting Material and methods ants (Bot et al. 2001). Besides, several ant species exhibit necrophoresis by actively rejecting dead workers outside the Field experiments nest as they usually do for any other waste items. The rejection of waste items is known to lead to the formation Ant species and field site of piles around the ant nest, providing those items are available in high quantities such as heaps of scavenged The red ant M. rubra is a common species inhabiting forests insects (Czechowski et al. 2009), fungal wastes in leaf- or open areas and is widespread in Northern Europe. This cutting ants (Hart and Ratnieks 2001), seed husks in polygynous and polydomous species became invasive in Naturwissenschaften (2012) 99:833–842 835 Northern USA and Eastern Canada (Groden et al.

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