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Hygienic Behavior, Liquid-Foraging, and Trophallaxis in the Leaf Journal of Insect Science: Vol. 9 | Article 63 Richard et al. Hygienic behavior, liquid-foraging, and trophallaxis in the leaf- cutting ants, Acromyrmex subterraneus and Acromyrmex Downloaded from https://academic.oup.com/jinsectscience/article/9/1/63/900050 by guest on 24 September 2021 octospinosus Freddie-Jeanne Richard1,2 and Christine Errard2 1 University of Poitiers, Laboratoire Ecologie, Evolution, Symbiose, UMR CNRS 6556, 40 avenue du Recteur Pineau, Poitiers, France 2 Institut de Recherche sur la Biologie de l’Insecte, IRBI - UMR CNRS 6035, Faculté des Sciences et Techniques, Université François Rabelais, F-37200 Tours, France Abstract Neotropical leaf-cutting ants (tribe Attini) live in obligate symbiosis with fungus they culture for food. To protect themselves and their fungus garden from pathogens, they minimize the entry of microorganisms through mechanical and chemical means. In this study, focusing on the species Acromyrmex subterraneus and A. octospinosus, (Hymeoptera: Formicidae). Self- and allo-grooming behavior were quantified and it was found that A. octospinosus workers spend less time in self-grooming than A. subterraneus. In the experimental absence of fungus in A. subterraneus, the times spent in these two behaviors are not affected; however workers spend significantly more time immobile. Hygienic and trophallaxis behaviors were examined as well as the possibility that workers exchange food, and the grooming behavior of foraging and non-foraging workers were compared. Behavioral observations revealed that large workers spent more time grooming than small workers, and more than 62% of replete foragers passed collected liquid food via trophallaxis to a nestmate. However, trophallaxis was rarely observed between non-forager workers. These results suggest that trophallaxis permits the exchange of alimentary liquid between colony members, but it is not important for spreading the colony odor signature. Keywords: fungus-growing ants, grooming, fungus privation, foragers Abbreviations: LW: large workers, SW: small workers Correspondence: [email protected], Received: 31 October 2007 | Accepted: 15 October 2008 | Published: 3 December 2009 Associate Editor: Michael Breed was editor of this paper. Copyright: This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 9, Number 63 Cite this paper as: Richard F, Errard C. 2009. Hygienic behavior, liquid-foraging, and trophallaxis in the leaf-cutting ants, Acromyrmex subterraneus and Acromyrmex octospinosus. 9pp. Journal of Insect Science 9:63, available online: insectscience.org/9.63 Journal of Insect Science | www.insectscience.org 1 Journal of Insect Science: Vol. 9 | Article 63 Richard et al. Introduction material with anti-fungal or other noxious compounds that might harm the cultivated fungus (Wiemer 1985; Social insects, such as ants, honeybees, wasps and ter- Howard and Wiemer 1986; Howard 1987, 1988; North mites provide a highly favorable environment for the de- et al. 1997). velopment of pathogenic bacteria, fungi, and other mi- crobes. In order to prevent pathogen or disease transmis- Another challenge fungus-growing ants face for successful sion within the colony many social insects have de- fungal cultivation is the contamination of garden by dif- veloped various strategies including behavioral adapta- ferent strains of the symbiotic fungus, which is called tions ( Cremer et al. 2007). Honey bees, for example, can “symbiont mixing” (Poulsen and Boomsma 2005). Differ- detect and reduce the impact of bacteria, fungi or mites ent strains of the symbiotic fungus can result in incom- through hygienic behavior, which consists of removing patibility reactions, leading to a reduction in the yield of infested brood from the wax cells (Spivak and Reuter the fungus to the ants. This could occur through the acci- 2001 and references therein). Fungus growing ants also dental fusing of neighboring colonies or invasion by Downloaded from https://academic.oup.com/jinsectscience/article/9/1/63/900050 by guest on 24 September 2021 perform hygienic behavior consisting of fungus raising spores that are produced after the rare sporulation of the and weeding, in which they remove parasitic fungi spores fungal symbiont in some colonies in the population. The (Escovopsis) and other pathogens from the fungus garden domesticated fungi actively reject mycelial fragments of (Currie and Stuart 2001). Social interactions, such as other strains of cultivar, and the strength of these reac- allo-grooming, also appear to decrease the susceptibility tions is in proportion to the overall genetic difference of both ant and termite colonies to disease (Hughes et al. between these symbionts (Poulsen and Boomsma 2005). 2002; Traniello et al. 2002). Fungus yield (and thus colony fitness) would thus be max- imized if workers are able to distinguish between their Leaf-cutting ants (Formicidae: Myrmicinae, Attini) are own strain and alien strains of the fungal symbionts, restricted to the New World. They belong to a unique which is a known behavior in leaf-cutting ants (Viana et group of ants that are referred to as fungus-growers, be- al. 2001; Richard et al. 2007b), and this discrimination is cause they cultivate symbiotic fungi for food. The genera correlated with between-colony differences in the chem- Atta and Acromyrmex, which are the most phylogenetically ical profile of the fungus (Richard et al. 2007a). This in- derived fungus-growers, cut the leaves and flowers of a dicates that both genetic and environmental factors influ- diverse collection of plant species. The size of Acromyrmex ence the fungus chemical profile. Discrimination between colonies can reach several hundreds of thousands of indi- nestmates and non-nestmates appears to be based on a viduals, while colonies of their sister genus Atta can form composite colony-specific “gestalt” profile common to all colonies of to 5–10 million workers (Weber 1972; Hölldo- colony members (Crozier and Dix 1979; Fletcher and bler and Wilson 1990). Fungal cultivars serve as the Michener 1987). This colony “gestalt” is maintained by primary food source for the ants, and they are carefully the continuous exchange of recognition cues via trophal- manured by the ants with foraged plant material, fruits, laxis and allo-grooming (Soroker et al. 1994), and it is af- insect frass, or seeds. An additional energy source for fected, for example, by seasonal variation in diet (Nielsen leaf-cutting ant colonies comes from foragers drinking et al. 1999; Silverman and Liang 2001; Richard et al. plant sap from the leaves that they cut (Littledyke and 2004) and nesting substrate (Heinze et al. 1996; Richard Cherrett 1976; Bass and Cherrett 1995). In a fungus- et al. 2007b). Grooming behaviour seems fundamental growing ants’ colony, both the ants and fungus cultivar for passing of the colony odor within the colony (Meskali are exploited by pathogens (Currie et al. 1999a; Currie et al. 1995) via transfer of substances between workers, 2001a). The ants are known to minimize the entry of as, for example, in A. subterraneus brunneus (Camargo et al. such micro-organisms by both mechanical means 2006). (licking, weeding) and chemical means via the production of antibiotics by the metapleural gland and symbiotic In spite of the workers’ ability to recognize their own Pseudonocardia bacteria (Boyd and Martin 1975; Quinlan fungus, foragers are continuously exposed to many po- and Cherrett 1977; Currie et al. 1999b; Currie 2001b; tential invasive alien fungal spores. Hygienic and allo- Currie and Stuart 2001). The ant’s infrabuccal pocket grooming behaviors appear to be very important as also produces antibiotics, which inhibit and kill spores of collective ant-parasite defenses in leaf-cutting ants. In this the parasite Escovopsis (Little et al. 2006). In addition, context, cleaning returning foragers seems more import- workers remove waste from fungus garden that minim- ant than in non-fungus-growing ants. One aim of the izes potential pathogen development (Hart and Ratnieks present work, therefore, was to study the grooming beha- 2001). Moreover, workers show aggressive behaviour dir- vior (self grooming and allo-grooming) in leaf-cutting ected toward nestmates contaminated with garbage (Hart ants. and Ratnieks 2001). Indeed, absconding of the ants from their nest causes the fungus garden to be rapidly over- We hypothesized that foragers returning from the extern- whelmed by alien microorganisms (Boyd and Martin al environment into the colony should spend more time 1975; Quinlan and Cherrett 1977; Currie et al. 1999a). engaging in grooming behavior than do non-foraging The ants’ foraging behaviors avoid harvesting of plant workers. To test this, hygienic behaviors were quantified Journal of Insect Science | www.insectscience.org 2 Journal of Insect Science: Vol. 9 | Article 63 Richard et al. and compared for two leaf-cutting ant species, Acromyrmex in A. subterraneus and 50 workers (30 LW, 20 SW) in A. oc- subterraneus and A. octospinosus. Due to the high poly- tospinosus, with an individual color mark (UniPaint morphism between workers and previous studies on the PX-20, Mitsubishi Pencil Co. Ltd., www.uniball.com) on division of labor (Wilson 1980a, 1980b), workers were the thorax and/or on the abdomen. The colonies were subdivided into two size categories (small and large). subsequently left undisturbed for one week,
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