F. Le Moli

Colony founding in Polyergus rufescens: the role of the Dufour's gland.

Summary: In the European slave-making ant Polyergus rufescens, the occurrence of chemical strategies during the initial phase of dependent colony foundation or usurpation was investigated. To test this idea, we analysed the effect of the secretion of different glands (Dufours, poison, pygidial, rectal, and mandibular) on the behaviour of workers of its common host species, Formica cunicularia (subgenus Serviformica). Workers of another species, Formica rufibarbis (Serviformica), were daubed with these extracts, and introduced into colony fragments of F. cunicularia. The results of a set of laboratory aggression test showed that the secretion of the mandibular, pygidial, rectal, and poison glands do not alter the characteristic aggressive reactions generally performed by resident workers against alien ants. By contrast, the Dufours gland seems to play a crucial role in the appeasement of residents of the target host colony. In fact, its secretion drastically lowers the degree of overt attacks shown by F. cunicularia workers against the intruders. This chemical strategy probably allows an easier invasion and usurpation of host colonies by newly mated females of P. rufescens.

Comparison of reproductive strategies and raiding behaviour in facultative and obligatory slave-making ants: the case of Formica sanguinea and Polyergus rufescens

Summary. A review of field and laboratory research concerning raiding behaviour, mating strategies and colony founding in Formica sanguinea and Polyergus rufescens (respectively facultative and obligatory parasites of the Serviformica species) is presented. The analysis and comparison of these crucial and peculiar moments in the life cycle of dulotic colonies may be a valid tool to clarify the evolutionary origins of slavery in ants.¶Concerning the reproductive behaviour, F. sanguinea females mate only in nuptial flights. P. rufescens females mate on the ground around their natal nest, or return to a dulotic colony after mating flights and wait for a raid, or mate directly during a raid. Moreover, field observations suggest that F. sanguinea adopts a strategy similar to the male aggregation syndrome, whereas P. rufescens mating strategy can be considered similar to the female calling syndrome. In the field, newly-mated queens of both slave-makers participate in raiding swarms: following a slave raid is an advantageous strategy to locate and invade host nests and to establish a new dulotic colony.¶For colony formation, F. sanguinea presents a great variety of possible strategies (independent foundation and dependent foundation including alliance, adoption, usurpation, and brood sack). This provides evidence of a behavioural plasticity that confirms its nature as a facultative parasite. On the contrary, P. rufescens depends only on usurpation, during which the Dufours gland contents seem to play a crucial role in the appeasement of the residents of the target colony.¶Also the raiding behaviour of F. sanguinea is less specialized than that shown by P. rufescens. In fact, in the obligatory slave-maker the important role of scouts in the organization of slave-raids is confirmed, which are rapid and effective. By contrast, raids of F. sanguinea may be regarded as a continuation and expansion of common foraging and predatory activity, as predicted by Darwins hypothesis for the origin and evolution of slavery in ants. Nevertheless, the intraspecific raids conducted by P. rufescens emphasize also the important role of territorial competition as evolutive cause of dulosis.

Mandible associated glands in queens of the slave-making ant Polyergus rufescens (Hymenoptera, Formicidae)

SummaryA first description of the structural organization of two exocrine glands associated with the mandibles of queens of the obligatory slave-making ant Polyergus rufescens is reported. The mandibular gland consists of clustered bicellular secretory units connected by means of cuticular ducts to a big reservoir. The reservoir continues in a duct that opens proximally on the mandible cuticle. Intramandibular glands are isolated bicellular secretory units connected to the external pores through a cuticular duct. No reservoir has been observed. In both cases the secretory cells belong to the 3rd class. Functional aspects of the investigated glands are discussed taking also into account for the parasitic habit of this slave-making species.

Host nest usurpation and colony foundation in the European amazon ant,Polyergus rufescens Latr. (Hymenoptera: Formicidae)

SummaryThe socially parasitic mode of founding new colonies by queens of the European amazon antPolyergus rufescens was analysed in the laboratory. Newly-mated females of this obligatory slave-maker were individually introduced into queenright and queenless artificially established colonies of bothFormica cunicularia (the slave present in the natal dulotic nest) andF. rufibarbis (another potentialServiformica host). Particular attention was devoted to the behavioural patterns displayed by these young queens during the usurpation phases. Our observations, supported also by video-taping, show that the slave-making female, before laying her eggs, must penetrate the host colony, kill the resident queen, become accepted by the adult workers and appropriate the host brood. The parasite was almost always adopted in the colonies ofF. cunicularia, whereas in the presence ofF. rufibarbis it was generally killed in a short time. The failure in the attempt of usurping the colonies ofF. rufibarbis is discussed in relation to the host specificity typical of this slave-maker. Finally, egg-laying byPolyergus successful usurpers, the subsequent eclosion of the brood, and its complete social integration in the newly-established mixed colonies were also recorded.

Nest-area marking with faeces: a chemical signature that allows colony-level recognition in seed harvesting ants (Hymenoptera, Formicidae)

Summary.Nestmate recognition systems in ants are largely based on chemical signals. The hydrocarbon fraction of the lipid layer which covers the insect cuticle plays a determinant role in this context. Here we report a novel extension of nestmate and alien recognition – nest area marking with faeces containing the same hydrocarbons as the cuticle of workers – in a harvesting ant, Messor capitatus. Workers of M. capitatus deposit large quantities of brown-yellow material from the hindgut (termed spots) in the vicinity of the nest. Behavioural investigation showed that such spotting behaviour has a communicative value in the context of nest area identification. Anal fluids deposited in the nest surroundings contain colony-specific cues which the ants use to recognize their own nest areas, and distinguish them from foreign areas even in the absence of nestmate or alien ants. Chemical analyses by gas chromatography-mass spectrometry (GC-MS) of the contents of anal spots, rectal sacs, and cuticular extracts revealed that all contain the same long-chained linear and branched hydrocarbons in varying proportions. Importantly, multivariate analyses showed that the relative proportions of these compounds on the cuticle and in spots are colony-specific. This provides a mechanism by which spot marking could be used by workers to define and recognize their colony area, and would represent a simple extension of the existing nestmate recognition template based on colonial cuticular signatures. The ecological and sociobiological implications of these findings are discussed.

Chemical communication during foraging in the harvesting ant Messor capitatus (Hymenoptera, Formicidae)

Summary: Some aspects of the chemical communication system employed by the harvesting ant Messor capitatus during foraging were investigated in the laboratory. After locating a conspicuous food item the scouts return home dragging their gaster on the ground. Once inside the nest they run among nestmates and perform an excited motor display. Soon after, groups of workers rush out and move towards the food. Bioassays of different gland extracts showed that nestmates are activated and induced to leave the nest by substances from Dufours gland. This gland was also found to be the source of the orientation-recruitment trails by which foragers reach newly discovered food sources. The bioassays showed that poison gland extracts are also active in inducing trail following. However, this response was accompanied by typical aggressive reactions by tested ants, suggesting that the poison gland is involved in alarm communication and recruitment towards a source of danger rather than in foraging activities. Some features of the Dufours gland trail (such as its durability and lack of colony-specificity) are discussed with regard to the ecological requirements of this species.

Why a slave ant species accepts and cares for cocoons of its slave-maker

SummaryIn order to determine the role of early social experience on the ontogeny of cocoon recognition by a slave-ant species, laboratory experiments were carried out inFormica cunicularia, a common slave ofFormica sanguinea. In a choice-test, adultF. cunicularia workers coming from a pure colony tended only the homospecific cocoons, whereas destroyed the heterospecific unfamiliar ones (F. sanguinea andF. lugubris). Subsequently, 3 groups of artificial colonies were set up with callowF. cunicularia workers of the same age experimentally removed from their cocoons. After a 15-day training period with homospecific cocoons (group C),F. sanguinea cocoons (group T), or in absence of any cocoons (group I), these workers were given a choice-test betweenF. cunicularia andF. sanguinea cocoons. The choice of the workers belonging to groups C and T was always directed towards the cocoons with which workers had become familiar during the training period. Moreover, early deprivation of cocoons disrupted the cocoon discrimination and care ability of ants belonging to group I. On the basis of these data and those recently obtained by us on nestmate recognition in the same species, we can assume that social experience immediately following eclosion ofF. cunicularia workers can fully explain their enslavement in nature and, therefore, the interspecific altruism of this host species towards the parasite.ResumeAfin de déterminer le rôle de lexpérience sociale précoce sur lontogenèse de la reconnaissance des cocons par une espèce esclave de fourmi, des expériences de laboratoire ont été réalisées surFormica cunicularia, une espèce communément esclave deFormica sanguinea. Dans un test de choix, des ouvrières adultes deF. cunicularia provenant dune colonie pure soignèrent uniquement des cocons homospécifiques, tandis quelles détruisirent les cocons hétérospécifiques, non familiers (F. sanguinea etF. lugubris). Après quoi, 3 groupes de colonies artificielles ont été constitués avec de jeunes ouvrières deF. cunicularia de même âge, retirées expérimentalement de leurs cocons. Après une période dentraînement de quinze jours avec des cocons homospécifiques (groupe C), des cocons deF. sanguinea (groupe T), on en labsence de tout cocon (groupe I), ces ouvrières furent soumises à un test de choix entre des cocons deF. cunicularia et deF. sanguinea. Le choix des ouvrières des groupes C et T fut toujours en faveur des cocons auxquels elles avaient été familiarisées au cours de la période dentraînement. En outre, la privation des cocons rompit la discrimination des cocons et laptitude aux soins des fourmis du groupe I. Sur la base de ces données et de celles que nous avons obtenues récemment sur la reconnaissance des partenaires du nid chez la même espèce, nous pouvons soutenir que lexpérience sociale suivant immédiatement léclosion chez louvrière deF. cunicularia peut expliquer son esclavage dans la nature et, par conséquent, laltruisme interspécifique de cet hôte à légard de son parasite.

Chemical communication in mating behaviour of the slave-making ant Polyergus rufescens (Hymenoptera, Formicidae): 3-ethyl-4-methylpentanol as a critical component of the queen sex pheromone

Abstract.The aim of the research reported here was to determine whether 3-ethyl-4-methylpentanol, a minor but crucial component of the sex pheromone of the North American slave-making ant species Polyergus breviceps, was also a component of the sex pheromone of the European congener Polyergus rufescens. Thus, the contents of mandibular glands of P. rufescens virgin queen were extracted and analysed. The main component of the extracts was methyl 6-methylsalicylate and 3-ethyl-4-methylpentanol was identified as one of several minor components. Further analyses showed that the insects produce mainly the (R)-enantiomer of the alcohol. Males’ responses to various blends of methyl 6-methylsalicylate with the racemate or the pure enantiomers of 3-ethyl-4- methylpentanol were tested in field behavioural bioassays. The data showed that blends of methyl 6- methylsalicylate and 3-ethyl-4-methylpentanol were strongly synergistic, with the most active ratios being biased toward the first component. The addition of other minor components to the binary blend neither increased nor decreased responses by males. Only the (R)-enantiomer of the alcohol was biologically active; its antipode did not inhibit attraction. The results are discussed in terms of the evolution of signals, and are compared with the results previously obtained for the allopatric species Polyergus breviceps.

Intraspecific slavery inPolyergus rufescens Latr. (Hymenoptera, Formicidae): field and laboratory observations

SummaryFour intraspecific slave raids involving 3 colonies of the European amazon antPolyergus rufescens Latr. occurred during hot and sunny afternoons in July 1992 near Parma, Italy. Generally, no fighting between the resident ants and the invaders was recorded, and pillage of the brood lasted just a few minutes. The brood captured during 3 raids was collected and transported ot the laboratory where slavemaker callow workers eclosed and were accepted by both the raiders and hosts present in artificial mixed colonies. This is the first case of functional intraspecific slavery recorded in the field for the obligatory dulotic formicine antP. rufescens.

Selective acceptance of the brood of two formicine slave-making ants by host and non-host related species

SummaryIn a laboratory choice-test, free-living ant workers ofFormica cunicularia andF. rufibarbis (subgenusServiformica), both potentially slave species of the obligatory slave-makerPolyergus rufescens, cared for cocoons of this parasite and for homocolonial cocoons at comparable rates. Both potential hosts did not differ in their capacity to rear the parasite brood. This fact is discussed in relation to host selection and specificity inP. rufescens. No such attraction and/or tolerance was found towards cocoons of the facultative slave-makerFormica sanguinea, which also enslaves both host species. Workers ofF. lugubris, a species which is never enslaved, destroyed cocoons from both slave-making species. The attractiveness of the brood ofP. rufescens for both potentially slave species could be due to an interspecific brood pheromone in addition to brood mimicry. An alternative hypothesis is a close phylogenetic distance between this slave-maker andServiformica species. The capacity to gain acceptance by adult slave workers might be one of the crucial evolutionary steps separating obligatory from facultative slave-making ants.