Anim. Behav., 1992, 43, 787-794 Effects of early experience on interactions between the parasite ant Formicoxenus provancheri and its host Myrmica incompleta (Hymenoptera: Formicidae) CHRISTINE ERRARD*, ALAIN LENOIR* & ANDRI~ FRANCOEUR t *Laboratoire d'Ethologie et Sociobiologie, U.R.A. CNRS667, Universitk Paris XIII, Av. J. B. Clbment, 93430 Villetaneuse, France t Laboratoire de Biosystbmatique, Universitb du Qubbec ~ Chicoutimi, 555 Boulevard de l'Universitb, G7H ZB1 Chicoutimi, Quebec, Canada (Received 2 November 1990; initial acceptance 11 December 1990; final acceptance 27 September 1991; MS. number: 3667) Abstract. The influence of early experience on interspecific recognition in the parasite ant Formicoxenus provancheri and its host Myrmica incompleta was studied by investigating the interactions of each species with adults and with larvae. The adults tested were reared heterospecifically (host and parasite together) or homospecifically (with or without mature conspecific ergates). Adults of each species were tested with both conspecific and allospecific larval brood, Homospecifically reared M. incompleta were more aggressive towards their parasite than when reared with the latter. Formicoxenus provancheri were always attracted to M. incompleta brood and adults. This parasite thus prefers to rear the host- brood, especially when the parasite's early experience has been either of its own species or where it has been reared alone. Ants of the genus Formicoxenus are social parasites F, provaneheri on M. incompleta, particularly on in colonies of other ant species. Their nests may be their antennae. established at the edge of or in the wall of the nest of The intraspecific interactions of F. provancheri their host, but the parasite always rears its brood in and M. incompleta adults have been described chambers separate from the brood chambers of the elsewhere (Lenoir et al., in press). host. Formicoxenus nevertheless are completely In the present study we carried out experiments dependent on their host for feeding (Francoeur et on the development of interspecific recognition in al. 1985). This form of social parasitism has been order to elucidate the possible influence of early named xenobiosis (see Buschinger 1986). social experience on this phenomenon. We wanted Until recently behavioural studies had been to know whether young M. incompleta reared in made only on F. nitidulus and F. diversipilosus. Both the absence of the parasite would later accept of these are found in nests of species in the Formica F. provancheri, and whether homospecifically reared rufa group. We studied the North American associ- young F, provancheri would later accept M. incom- ation of Formicoxenus provancheri with its host pleta, and consequently be able to parasitize it. Myrmica incompleta using material collected in Our first concern was to analyse the inter- Quebec, Canada. specific behaviour of adult M. incompleta and Adult F. provancheri are strongly attracted by F. provancheri and to discover the effect of rearing M. incompleta and lick them very frequently. In the schemes on the development of aggressive behav- laboratory, under our experimental conditions, iour. We then studied how adults of both species aggression between the species is rare and brief interact with conspecific or allospecific brood. unless the species have been previously separated. In F. provancheri, the laying 'queen' can be an Under these circumstances F. provancheri adopts inseminated worker, so the usual terminology for an appeasement posture resembling sexual calling the castes is not suitable. We therefore use the terms (Lenoir et al. 1989). However, in mother stock ergates and gynes rather than workers and queens colonies, we observed frequent attacks by (cf. Loiselle & Francoeur 1988). 0003-3472/92/050787 + 08 $03.00/0 1992 The Association for the Study of Animal Behaviour 787 788 Animal Behaviour, 43, 5 Table I. Composition of-the experimental groups Myrmica Formicoxenus incompleta provancheri 1 gyne 1 gyne Newborn Newborn 40 mature ergates 10 mature ergates M. incompleta F. provancheri Group* and brood and brood 40 ergates 10 ergates 1 + + - + MY+FO+ 2 - + - + MY-FO+ 3 + - - + MY+FO- 4 - - - + MY - FO - 5 + + + - MY+FO+ 6 - + + - MY-FO+ 7 + - + - MY+FO- 8 - - + - MY - FO - *For example, group 1 is composed of 1 gyne, 40 mature ergates and brood ofM. incompleta plus 1 gyne, 10 mature ergates, brood and 10 newborn F. provaneheri. Groups 1-4: F. provancheri experimental groups. Groups 5-8: M. incompleta experimental groups. METHODS We amputated a hind tarsus of mature ants so that they could be distinguished from the young Ants were maintained in the laboratory at 20~ in ergates. petri dishes using the technique described by All the tests (each of 15 min) were carried out Alloway (1979). In control colonies (heterospecific in small petri dishes (50mm diameter) with stock cultures) the petri dishes contained a drinking experimental groups from numerous colonies: we trough and two circular nests, one for each species. performed 10 tests per experimental group. Young We gave the F. provancheri nest an entrance of very ergates were tested 15 days after their emergence as small diameter so that M. incompleta were unable it is known that when a sensitive period for post- to enter. In homospecific colonies (homospecific emergence experience was observed, it is no longer stock cultures) each species was maintained in a than 10 days (Jaisson & Fresneau 1978; Jaisson separate single circular nest. Using ants from the 1985). stock cultures we created eight groups of exper- imental colonies (Table I). Four of these, two with Interactions of Adults each species, came from homospecific colonies. The Tests with F. provancheri homospecific colonies (M. incompleta and F. provancheri) were formed either by adding young For each test, a single young F. provancheri ergates to nests containing conspecific gynes, ergate from a colony in one of the experimental mature workers and brood (groups 2 and 7) or by groups 1-4 was placed in a small petri dish with five rearing newborn ergates alone (groups 4 and 8). mature M. incompleta ergates. These M. incompleta Two groups of heterospecific colonies (groups 1 were mature ergates taken at random from a and 5) were formed by adding either young homospecific stock culture. The behaviour of F. provancheri or young M. incompleta ergates to the F. provancheri ant and its interactions with nests containing gynes, mature workers and brood M. incompleta ergates were recorded every 5 s of both species, in the same proportions as in during the first 5min. After a further 15min homospecific colonies (groups 2 and 7). Two behavioural observations were continued for two further groups of heterospecific colonies were additional 5-min periods, separated by a 15-min formed by including young F. provancheri ergates interval. Ten of these tests were conducted. in a M. incompleta colony (group 3) or by including The behaviour of F. provancheri (previously young M. incompleta in a F. provancheri colony described by Lenoir et al. 1989) was assigned to (group 6). four categories. Errard et al.: Parasite-host interactions in ants 789 (1) Aggression against M. incompleta: even if the larvae are of a different species. We F. provancheri sometimes seize the limbs or anten- noted all forms of brood care behaviour: antennal nae of their host. This behaviour appears relatively examination, carrying (or simple mandibulation), rarely in our experimental context. licking and passive immobility near to a larva. (2) Aggression by M. incompleta: more frequent Adults sometimes anally stimulate larvae with their than category 1, and occasionally prolonged. antennae. The larvae then produce a droplet of (3) Appeasement behaviour by F. provancheri: clear liquid (Le Masne 1953; Wilson 1971). similar to that described for F. nitidulus (Staeger 1925). The ant raises its abdomen and extrudes Tests with M. incompleta the sting from which it then produces a droplet of volatile liquid. This liquid does not repel The tests with F. provancheri were repeated using M. incompleta but has a pacifying action, calming M. incompleta young ergates from each of the ex- the host. perimental groups (5-8). The origin of the larvae (4) Non-aggressive behaviour: including all and the observation technique were the same as for forms of behaviour with no aggressive component. F. provancheri. The most frequent in this category are intense and prolonged licking of M. incompleta by F. provancheri. This behaviour may occupy up to RESULTS 40% of the active time of a mature F. provancheri ergate. Solicitation, trophallaxis and very occasional Interactions of Adults licking ofF. provancheri by M. incompleta were also Behaviour of the parasite noted (Lenoir et al. 1989). Aggressive behaviour by F. provancheri towards Tests with M. incompleta M. incompleta was infrequent and there were no Ten young M. ineompleta 15-day-old ergates significant differences between the groups (Fig. la). from groups 5-8 were tested against F. provancheri In contrast, young F. provancheri reared together mature ergates in a small petri dish. In each of the with mature ones in the absence of M. incompleta 10 tests one M. incompleta ergate was confronted (group 2) were attacked by M. incompleta signifi- with five F. provancheri (from a homospecific stock cantly more often than were young F. provancheri culture). Behaviour was classified in the same way ergates reared in the absence of mature conspecifics as in the tests with F. provancheri. (F1,36=2.47, P<0.05; Fig. lb). This difference occurred whether or not the F. provancheri had been reared with M. incompleta. Interactions with Brood Appeasement behaviour towards M. incompleta Tests with F. provancheri was significantly more frequently shown by Formicoxenus provancheri ergates (groups 1-4) F. provancheri reared in the absence of mature con- were tested against brood of both species. For specifics (FI,36 =7-56, P<0.01), or in the absence each of 10 tests, five ergates were put into a petri of M.