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BEHAVIOURAL and CHEMICAL STUDIES of DISCRIMINATION PROCESSES in the LEAF-CUTTING ANT Acromyrmex Laticeps Nigrosetosus (FOREL, 1908)

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BEHAVIOURAL and CHEMICAL STUDIES of DISCRIMINATION PROCESSES in the LEAF-CUTTING ANT Acromyrmex Laticeps Nigrosetosus (FOREL, 1908) BEHAVIOURAL AND CHEMICAL STUDIES OF DISCRIMINATION PROCESSES IN THE LEAF-CUTTING ANT Acromyrmex laticeps nigrosetosus (FOREL, 1908) SOUZA, D. J.1, DELLA LUCIA, T. M. C.1, ERRARD, C.2, RICHARD, F-J.2 and LIMA, E. R.1 1Departamento de Biologia Animal, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, MG, Brazil 2Institut de Recherche sur la Biologie de l’Insecte, CNRS UMR 6035, Université de Tours, France Correspondence to: Terezinha Maria Castro Della Lucia, Departamento de Biologia Animal, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, MG, Brazil, e-mail: [email protected] Received May 24, 2004 – Accepted August 11, 2004 – Distributed August 31, 2006 (With 5 figures) ABSTRACT Leaf-cutting ants live in symbiosis with a basidiomycete fungus that is exploited as a source of nutrients for ant larvae. Tests of brood transport revealed that Acromyrmex laticeps nigrosetosus workers did not discriminate a concolonial brood from an alien brood. The same result was observed with tests of fungus transport. Adult workers showed no aggressive behaviour to workers from other alien colonies (non-nestmates). There was no qualitative variation in the chemical profiles of larvae, pupae and adult workers from the different colonies. However, quantitative differences were observed between the different colonies. Hypotheses about the lack of intraspecific aggression in this subspecies of ants are discussed. Keywords: leaf-cutting ants, intraspecific aggressiveness, chemical profiles, brood discrimination, fungus discrimination. RESUMO Estudos químico e comportamental dos processos discriminatórios na formiga cortadeira Acromyrmex laticeps nigrosetosus (Forel, 1908) As formigas cortadeiras vivem em simbiose com um fungo basidiomiceto que é utilizado como fonte de nutriente para suas larvas. Testes de transporte de prole revelaram que as operárias de Acromyrmex laticeps nigrosetosus não discriminaram a prole concolonial de prole estranha. O mesmo resultado foi verificado com testes de transporte do fungo. As operárias adultas não exibiram comportamento agressivo frente a operárias de outras colônias (não companheiras de ninho). Não houve variação qualitativa nos perfis químicos de larvas, pupas e operárias adultas de diferentes colônias. No entanto, diferenças quantitativas foram observadas entre as diferentes colônias. Hipóteses sobre a ausência de agressão intra-específica nesta subespécie de formiga são discutidas. Palavras-chave: formigas cortadeiras, agressividade intraespecífica, perfis químicos, discriminação de prole, discriminação de fungo. INTRODUCTION & Michener, 1980). Nestmate recognition in ants is defined by the ability of workers to discriminate The ability to recognize kin is widespread, members from allocolonial among conspecifics and especially important in highly social organisms (Stuart & Herbers, 2000). This capacity to recognize (Vander Meer & Morel, 1998). Different methods nestmates and to distinguish them from non- of recognition, based on the origin of the colony nestmates is based on each colony having its own odour (environment and pheromones produced by “chemical signature”, a specific and characteristic each individual or by the queen), are detected in ant chemical cue mixture for each colony (Hölldobler societies (Whitehouse & Jaffé, 1995). It is generally Braz. J. Biol., 66(3): 863-871, 2006 864 SOUZA, D. J. et al. accepted that cuticular hydrocarbons (CH) play from the fungus garden, but did not reject eggs an important role in nestmate recognition (Lahav directly obtained from previously isolated queens et al., 1999). The harvester ants Pogonomyrmex (Araújo et al., 1996). In Acromyrmex octospinosus, barbatus can perceive different CH variations and workers are able to recognize their concolonial can use these differences in nestmate recognition brood (Febvay et al., 1984). In Ac. subterraneus (Wagner et al., 2000). In Camponotus fellah, social subterraneus workers can discriminate concolonial isolation induced a divergence of the individual fungus from alien fungus (Viana et al., 2001) and hydrocarbon profiles (Boulay et al., 2000). in this subspecies, a chemical analysis of the brood Intolerance towards isolated C. fellah workers revealed a great similarity between its brood profile starts after about 10-20 days, the time necessary for and on the fungus. the CHs to change and assume individual profiles The objective of this study is to evaluate distinct from the colony profile (Boulay et al., behavioural responses of workers from Acromyrmex 2000). These authors determined that individual laticeps nigrosetosus to concolonial or allocolonial hydrocarbon production is dynamic; workers must larvae, pupae and adults. This research also aims exchange hydrocarbons continually (mainly by to establish the cuticular chemical profiles of trophallaxis) to maintain colonial odour. This is brood and adults of this ant subspecies and their referred to as the Gestalt odour, a mixture of odours implications on behaviour. The worker response to from each individual in the colony and odours from either concolonial or allocolonial fungus was also the environment (Crozier & Dix, 1979). Since tested. individual CH production is dynamic, it is essential for nestmates to homogenize their chemical cues MATERIAL AND METHODS often to create a uniform colony-specific profile (Vander Meer et al., 1989). The uniformity of the chemical profiles results from this constant Collection of ants and rearing conditions homogenization of chemical cues produced by In one leaf-cutting ant survey under all colony members. Ant’s species that do not use eucalyptus stands in the region of Paraopeba, trophallaxis, exchange their chemical cues by social Minas Gerais (19° 17’ S and 44° 29’ W; 700 m contacts or allogrooming. Experiments on the non- altitude), Araújo et al. (1997) observed high trophallactic ant Pachycondyla apicalis showed frequencies and densities of Acromyrmex laticeps that physical contacts, as well as allogrooming are nigrosetosus nests throughout the year. These nests able to maintain a uniform colony odour (Soroker were underground, but superficial since they were et al., 1998). On the other hand, Lenoir et al. located at 0.11 m below the soil surface and each (2001) suggested that allogrooming is an important nest generally consisted of a single chamber. behaviour for effective cue transfer in the non- Behavioural and chemical tests were trophallactic ant Aphaenogaster senilis. conducted with workers from Ac. laticeps Colony brood recognition has also been nigrosetosus colonies. These colonies were demonstrated in several ant species. The concolonial collected at Paraopeba, Minas Gerais state (Brazil) brood is accepted and nourished by workers, while 2 years before starting the experiment. They an allocolonial brood may be rejected (Bonavita- were established in the laboratory and consisted Cougourdan et al., 1989; Bonavita-Cougourdan et of approximately 3,000-4,000 individuals and al., 1993). In fact, the brood possesses chemical numerous broods; the fungus volume was about cues that enable workers to recognize it (Araújo et 2 L. Ants were reared in artificial nests, placed in al., 1996; Viana et al., 2001). 3 L recipients (for more details, see Della Lucia Leaf cutting ants live in symbiosis with a et al., 1993). Humidity, temperature and light-dark basidiomycete fungus that is exploited as a source of (LD) cycles in the rearing room were 75 ± 5%, nutrients for ant larvae. In Atta cephalotes, there is 25 ± 2 °C and 12:12 LD, respectively. Each nest some evidence that a nestmate brood is distinguished had access to a foraging arena (30 cm x 20 cm) (Robinson & Cherrett, 1974). Workers of A. sexdens where leaves and petals from flowers, as well as rubropilosa rejected allocolonial larvae and pupae, water were supplied daily. Behavioural tests were as well as eggs when they were directly removed conducted with workers from four colonies (I, II, Braz. J. Biol., 66(3): 863-871, 2006 Behavioural AND CHEMICAL STUDIES 865 III, IV) and chemical tests were performed with following aggression index: 0 = non-aggressive workers of three colonies (I, II, III) due to the death interaction (antennal contacts, trophallaxis and al- of colony IV. logrooming), 1 = threat as indicated by mandibu- lar opening and curling the abdomen, 2 = biting, Behavioural tests 3 = fight and reciprocal mutilation. The frequencies and duration of each behavioural component were Discrimination of pupae and larvae recorded using computer ODlog software and The methodology used in the bioassays with the overall aggressiveness (AI) shown in each the brood was modified from Araújo et al. (1996). encounter was calculated as follows (Errard & Colonies were deprived of food (leaves) for a 24 h Hefetz, 1997): period prior to the test. This procedure enabled n a faster behavioural response of the workers. !AIi* ti AI = i = 1 (1) Larvae and pupae of four colonies were used. T The brood of each colony was removed from the where A.I.i represents the aggression index, ti the fungus garden and isolated in a Petri dish. Fifteen duration of each act, and T the total interaction minutes later, the minimum time necessary for the time. ants to settle, either larvae or pupae were offered Before each encounter, the marked ant was to workers on a glass slide marked with non-toxic allowed to acclimate by remaining isolated inside ink in order to distinguish a nestmate from a non- a glass tube placed in the center of the Petri dish. nestmate. Positions of the slides were modified
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