The Role of Various Glands in Raiding Activities of Polyergus rufescens Ants, Study notes of Communication

Download The Role of Various Glands in Raiding Activities of Polyergus rufescens Ants and more Study notes Communication in PDF only on Docsity! Glandular sources of recruitment, trail, and propaganda semiochemicals in the slave-making ant Polyergus rufescens R. VISICCHIO, A. MORI, D.A. GRASSO, C. CASTRACANI and F. LE MOLI 1 Dipartimento di Biologia Evolutiva e Funzionale, Università degli Studi, Parco Area delle Scienze 11/A, I-43100 Parma, Italy Received 14 August 2001, accepted 9 October 2001 The chemical sources involved in raiding activities of the slave-making ant Polyergus rufescens were investigated in the laboratory. In particular, we identi- fied the sources of substances the raiding workers employ to convey information to nestmates and to disrupt reactions by defending workers during host nest invasion. Different secretions were offered to the dulotic ants on the tip of a blotting paper strip inserted a few centimetres into the nest entrance. The Dufour’s gland secretion induced the characteristic mass exit from the nest and is likely the source of a recruitment signal. Moreover, laboratory tests with secre- tions from different anatomical structures revealed that the trail signals for hom- ing raiding workers are conveyed by their hindgut contents released during the outbound trip. Finally, to ascertain if P. rufescens raiding workers use “propagan- da” pheromones, the behavioural response of the Formica (Serviformica) cunicu- laria host workers to different secretions of the slave-makers was investigated. Only mandibular secretions caused the typical panic reactions shown by resi- dents at the moment of nest invasion. This probably facilitates both nest inva- sion and brood sacking by raiding workers. KEY WORDS: Polyergus rufescens, recruitment, trail-following, propaganda, Dufour’s gland, hindgut, mandibular glands, pygidial gland. Introduction . . . . . . . . . . . . . . . . . 362 Materials and methods . . . . . . . . . . . . . . 364 Results 365 Recruitment . . . . . . . . . . . . . . . . 365 Trail-following . . . . . . . . . . . . . . . 365 Propaganda . . . . . . . . . . . . . . . . 367 Discussion . . . . . . . . . . . . . . . . . 368 Acknowledgements . . . . . . . . . . . . . . . 370 References . . . . . . . . . . . . . . . . . 370 Ethology Ecology & Evolution 13: 361-372, 2001 1 Author for correspondence at the above-mentioned address (E-mail: lemoli@biol.unipr.it). 362 R. Visicchio et alii INTRODUCTION The complex organization of ant societies depends on the efficiency of differ- ent forms of communication, involving a great diversity of cues, such as chemical, acoustical, tactile and visual (HÖLLDOBLER & WILSON 1990). Olfaction is the princi- pal sensory modality involved in integration and social coordination in ants. Hence, the complex interactions among nestmates in a colony are either partially or com- pletely dependent upon semiochemicals (ATTYGALLE & MORGAN 1985, TRANIELLO & ROBSON 1995). Chemicals discharged from various exocrine glands that induce a specific behavioural response in members of the same colony are referred to as “pheromones” (KARLSON & LÜSCHER 1959). Like most communication patterns, recruitment and trail-following are medi- ated by pheromones. The definition of recruitment has varied greatly: here, we refer to recruitment as the induction of nestmates to leave their nest, assemble and perform a task at a target area. In this context, a chemical signal may stimulate ants that are inactive or engaged in some other work to leave their nest and form part of a newly-mobilized group. Ants have evolved an astonishing array of strategies to recruit nestmates. The behavioural mechanisms involved in recruitment communication have been investi- gated and different organizational levels of recruitment behaviour have been described and arranged in a series of increasing complexity (HÖLLDOBLER 1978, HÖLLDOBLER & WILSON 1990). Various ant species rely on idiosyncratic combina- tions of different cues to achieve this aim; however the chemical cue most likely prevails (HÖLLDOBLER & WILSON 1990). In trail communication, already excited individuals are led (along a trail) to the target area where their cooperation is required (HÖLLDOBLER & WILSON 1990, TRANIELLO & ROBSON 1995). This pheromonal communication system is based on the release of chemicals from a variety of glands which then form a trail (MORGAN 1990). Recruitment and trail-following behaviour are often used improperly as syn- onyms. This is because the chemical trace can serve (but not always) as a recruit- ment signal and an orientation cue. In the present investigation, we refer to trail- following behaviour as an activity in which the ants are able to follow chemical traces previously laid down by nestmates. The aim of our investigations was to determine the sources of recruitment and trail semiochemicals in the formicine social parasite Polyergus rufescens, an obligate slave-making ant distributed throughout the European Palaearctic regions. This species exploits the labour of workers obtained as pupae during raids conducted against neighbouring colonies of related species (subgenus Servi- formica) (EMERY 1909). Hundreds of workers (specialized for this function) file out of their nest and conduct highly organized incursions against host colonies to pillage resident brood, from which they will obtain the slaves (MORI et al. 1991a, 1991b; LE MOLI et al. 1994). To attack and exploit newly discovered target colonies, P. rufescens requires both communication and orientation signals. Raiding activity begins early in the afternoon with a small number of workers (the scouts) that leave the nest searching for suitable host colonies. When they return home after a successful trip, they mobilize their nestmates for the raid organization. This phase is followed by pre- raid activity during which recruitment occurs: the excitation of a few workers (the first to get in touch with the scouts) provokes the mass exit of other raiding work- ers. A few minutes later, hundreds of workers mill frantically around the nest 365Semiochemical sources in raiding activities of P. rufescens as controls. Water was used because preliminary observations showed that hexane (and other similar solvents, i.e. pentane) disturbed the ants. Propaganda Three artificial colony fragments of Formica (Serviformica) cunicularia, each containing 350 workers and abundant brood, were housed in the laboratory in cylindrical plastic boxes (Ø 20 cm, height 4 cm), covered by a red-glass plate. Colonies were maintained as described in the previous section. The artificial nests were divided into four identical sectors, each provided with a fis- sure. In order to test the panic effect of some secretions of P. rufescens raiding workers, the response of F. cunicularia workers to the hindgut material and to the mandibular, Dufour’s, poison and pygidial gland contents was recorded. Three specimens of each type of organ were crushed at the end of a blotting paper strip (5 × 0.5 cm), which was then introduced into one of the fissures, chosen randomly. In this case, no solvent was used because a dilution of the glandular secretions was not needed. For 3 min thereafter, the reaction of the residents was video-recorded. The orientation of the reaction (expressed by the number of individuals counted every 30 sec in the experimental sector) and excitement level (expressed by the linear speed of three ants randomly chosen from those in the experimental sector at the beginning of the trial) were recorded. Controls were performed by introducing an untreated blotting paper strip into the fis- sure. For each type of test, six trials were conducted. RESULTS Recruitment The recruitment effect of the extracts is presented in Fig. 1. The number of recruited ants differed significantly among treatments (0.01 < P < 0.02; Kruskal- Wallis test). In particular, the Dufour’s gland secretion caused a significant increase of the number of exits (72.75 ± 13.22) compared to controls (14.37 ± 3.99; P < 0.05; Two-tailed Multiple Comparisons test). By contrast, the responses to extracts from the hindgut (59.25 ± 21.23) and the poison (15.12 ± 1.87), pygidial (35.87 ± 11.13) and mandibular (17.25 ± 2.69) glands did not differ from controls (Two-tailed Mul- tiple Comparisons test). Moreover, only the Dufour’s gland contents elicited the typ- ical patterns of behaviour performed by the ants in the field before a raid (see MORI et al. 1991a, 1991b; LE MOLI et al. 1994). The ants appeared very excited and left the nest en masse to mill around. Most of the recruited raiding workers per- formed a peculiar movement (also recorded in the field during the frantic pre-raid phase) consisting in rubbing their legs against the tip of their gaster. Trail-following Trail-following responses of the ants to different secretions are illustrated in Fig. 2. The percentage of ants following artificial trails made from extracts of the pygidial gland (4.7%, 7/148), poison gland (2.3%, 5/213), Dufour’s gland (2.3%, 6/262) and tarsi (1.8%, 4/217) were not significantly different from controls (0.4%, 1/264) (χ2 test). By contrast, the percentage of ants following the artificial trail was 366 R. Visicchio et alii Dufourpygidialhindgutmandibularpoisoncontrol 100 80 60 40 20 0 M ea n nu m be r (± S E ) of r ec ru ite d an ts 0 5 10 15 20 25 30 35 40 45 50 pure water poison tarsi hindgut pygidial Dufour % o f t ra il fo llo w in g an ts Fig. 1. — Mean number of P. rufescens workers recruited by hexane (controls), hindgut contents, or poison, mandibular, pygidial or Dufour’s gland secretions. Fig. 2. — Percentage of P. rufescens workers induced to abandon natural trails and to rely on artifi- cial ones made of pure water (controls), hindgut contents, tarsi, or poison, pygidial or Dufour’s gland secretions. 367Semiochemical sources in raiding activities of P. rufescens significantly higher in response to the hindgut contents (47.3%, 61/129) than to controls and the other secretions (P < 0.001; χ2 test). Almost half of the raiding workers encountering the hindgut artificial trail left the natural path to move along the artificially marked trail, performing the typical trail-following behaviour, while the other half continued to move on the natural trail. Propaganda The results are presented in Figs 3 and 4. All the secretions (except the hindgut contents) induced an increase of locomotor activity of the resident ants (Formica cunicularia). The linear speed of the ants differed significantly among treatments (P < 0.001; Kruskal-Wallis test). In particular, extracts of the mandibular glands caused a strong panic reaction in resident workers. In this case, not only the linear speed (0.75 ± 0.05 cm/sec) (see Fig. 3), but also the number of workers that abandoned the experimental sector (see Fig. 4) was statistically higher [P < 0.05 (Two-tailed Multiple Comparisons test) in the former case, P < 0.005 (t-test) in the latter] than in the controls and the other treatments. Moreover, before fleeing, sev- eral F. cunicularia workers seized cocoons with their mandibles, as usually observed in the field when the raiding workers enter the target host nest (see MORI et al. 1991a, 1991b). Quantitatively and qualitatively different reactions were induced with the other secretions. Although the linear speed of Formica workers recorded in trials Dufourpygidialhindgutmandibularpoisoncontrol 1.0 0.8 0.6 0.4 0.2 0.0 M ea n (± S E ) sp ee d Fig. 3. — Mean speed of Serviformica workers in response to untreated blotting paper strips (con- trols), hindgut contents, or poison, mandibular, pygidial or Dufour’s gland secretions. 370 R. Visicchio et alii least part of the panic reaction of the raided Serviformica colonies is caused by an alarm pheromone discharged by resident workers themselves, as suggested by TOPOFF et al. (1989) for slave-raids of the American species P. breviceps. HÖLLDOBLER (1984b) first discovered a pygidial gland in Polyergus spp., the only case known to date in formicine ants; its function could have evolved in con- nection with the highly specialized slave-raiding behaviour of these parasitic species. The author suggested that this glandular secretion might function as a kind of propaganda pheromone or as an arousal signal discharged by the leader ant at the front of the raiding column. In our experiments we found no propaganda effect of this glandular secretion. However, we cannot exclude an involvement of the pygidial gland in raid organization. Given its peculiar anatomical position (between the last two gastral tergites), the pygidial gland of P. rufescens probably evolved to produce semiochemicals secreted by raiding workers during the out- bound trip in order to maintain close-packing of the swarming column and ulti- mately acting as short-range attractants for neighbouring nestmates. The use of this kind of propaganda pheromone may be regarded as an addi- tional specialization in the slave-making habitus evolved by P. rufescens to reduce casualties and, above all, to make invasion of a colony and brood sacking an extremely rapid process (on average only a few minutes) (MORI et al. 1991a, 1991b; LE MOLI et al. 1994). BRADSHAW & HOWSE (1984) suggested that the metabolic cost to the raiding workers of releasing such large amounts of chemicals must be high and that this could be counterbalanced by a reduction of casualties. Thus, a main advantage of this chemical warfare could be conservation of resources in proximity to the dulotic nest: workers from the raided colony are not killed and can return to their nest to rear the younger brood left behind by the slave-makers. 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