Ontogeny of Nestmate Recognition Cues in the Red Carpenter Ant (Camponotus Floridanus) Behavioral and Chemical Evidence for the Role of Age and Social Experience
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Behavioral Ecology Behav Ecol Sociobiol (1988) 22:175-183 and Sociobiology Spfinger-Verlag 1988 Ontogeny of nestmate recognition cues in the red carpenter ant (Camponotus floridanus) Behavioral and chemical evidence for the role of age and social experience Laurence Morel 1,, Robert K. Vander Meer 2, and Barry K. Lavine 3 1 CNRS, Equipe Ethologie, Marseille, France 2 USDA-ARS, Insects Affecting Man and Animals Laboratory, Gainesville, Florida, USA a Department of Chemistry, Clarkson University, Postdam, New York, USA Received May 16, 1987 / Accepted September 25, 1987 Summary. A combination of behavioral and chem- quently the recognition response displayed to their ical analyses was used to investigate the nature bearer, change with age. 3) Social experience is of nestmate recognition cues and the effects of necessary to develop or acquire a colony-specific worker age and social experience on these cues in label. The role of age and social experience on nest- the ant Camponotus floridanus. Five categories of mate recognition in social Hymenoptera is dis- workers were tested: foragers, 5-day old and 0-day cussed. old callows, 5-day old and 0-day old naive callows. Bioassays consisted of introductions of dead workers from these categories into their own colo- nies or into an alien colony after the following Introduction treatments: 1) killed by freezing, 2) solvent- An increasing number of papers have been pub- washed, 3) solvent-washed and coated with a nest- lished in the past few years about kin and nestmate mate soak, 4) solvent-washed and coated with a recognition in social Hymenoptera (see review in non-nestmate soak. Soaks were obtained from in- Breed and Bennett 1988). In the special situation dividual ants immersed in hexane and were applied where a haplodiploid species is monogynous and individually to washed workers from the same cat- monoandrous, the relatedness between workers egory. Soaks were analyzed by gas chromatogra- within a colony is predicted to be 0.75. In this phy (GC) and compared by multivariate analyses. case nestmate and kin recognition are indistin- Freeze-killed workers from each category elicited guishable. In situations of polygyny and/or po- more aggressive behavior in the alien colony than lyandry, kin and nestmate recognition can be dis- in its own. By comparing GC profiles, a worker tinguished, since kin recognition would occur with- from any category can be assigned to its colony in the colony between matrilines and/or patrilines, of origin. Thus all studied worker categories are and nestmate recognition would occur between colony-specific. Solvent-washed ants did not in- colonies. If the intra-colonial relatedness between duce more aggressive behaviors in the alien colony workers is not known, as in Camponotusfloridanus, than in their own, but they induced significantly and if discrimination is measured between colo- less aggressivity in an alien colony than non- nies, then the term nestmate recognition must be treated dead ants from the same category. Washed used and no extrapolation to kin recognition is ants induced more aggressive behaviors when possible. coated with a soak from a different colony as op- The recognition mechanism is composed of two posed to a soak from the colony in which they distinct components (Beecher 1982): 1) the cues were introduced. The combination of behavioral provided by a donor animal to be recognized, re- and chemical results lead to the following conclu- ferred to as "labels" and 2) the process of the sions: 1) Information contained in soak derived recipient animal decoding these cues to recognize, from workers was sufficient to allow nestmate rec- often referred as "using a template". The onto- ognition. 2) Nestmate recognition cues, and conse- geny of nestmate recognition, with special atten- * Present address: USDA-Agricultural Research Service, P.O. tion to the template component, has been studied Box 14565, Gainesville, FL 32604, USA in several social wasp species (see review in Gam- 176 boa et al. 1986b). In ants the ontogenetical studies played by workers toward conspecific alien in- have not distinguished between the two recognition truders. The role of chemicals was tested using sol- components. In Camponotus vagus (Morel 1983) vent-washed ant dummies coated with soaks from and C.floridanus (Morel 1988), interactions with either nestmates or non-nestmates. The role of age older nestmates during the first hours of adult life was investigated by comparing the chemistry and are necessary to be completely recognized as a nest- aggressive responses displayed to three age groups: mate and to have the ability to recognize nest- newborn, 5-day old callow workers, and foragers. mates. In Camponotus again, Carlin and H611- Naive callow workers were compared to normal dobler (1986) showed that colony-specific recogni- ones of the same age to investigate the role of social tion labels are learned by workers after their eclo- experience. sion. As is known in many ant species, callow workers of C. floridanus can be successfully cross- fostered between colonies. The resulting young Methods workers are recognized as nestmates by the sisters of their foster nurses. This suggests that colony- Study animals specific recognition cues were transmitted from the Colonies of Camponotusfloridanuswere collected in the Appa- nurses to the adopted callows (Morel and Blum lachicola National Forest and in Gainesville, Florida. In the 1988). laboratory, ants were housed in Petri dish cells (135 mm diame- ter) that had a layer of moistened dental plaster (Castone| Chemical signals are the only nestmate (or kin) For each colony or group of workers, the cells were contained recognition cues known in ants and bees (H611- in a plastic arena (55 x40 x 18 cm), the sides of which were dobler and Michener 1980) and certainly play a coated with Fluon| to prevent escapes. Ants were fed regularly major role in social wasp recognition (Oamboa with honey and immature insects. Water was supplied in test et al. 1986b). These chemical signals are present tubes closed with cotton wool. The following worker categories were tested: on the insect's cUticle as the result of genetically 1) Foraging workers (F) collected at the honey source in controlled production (e.g. in the ant Pseudomyr- the foraging area. mex ferruginea, Mintzer 1982) and/or adsorption 2) Normal callow workers less than 12-h old (referred to from the environment (e.g. in the ant Solenopsis as 0-day old, CO). They were defined by their pigmentation, mobility, and presence of some pupal skin, and were taken invicta, Obin 1986). In small colonies of Campono- directly from the source colony cells. tus, queen derived labels are dominant, but worker 3) Normal 5 day-old callow workers (C5) were initially col- derived labels are clearly noticeable when the lected as described for CO then maintained separately in Petri queen is removed or has a reduced fertility (Carlin dish cells (50 mm diameter) with other C5 callows and always with an equal number of nurses (1 : 1). and H611dobler 1986, 1987a, b). Both environmen- 4) Naive callow workers were artificially removed from tally derived and individually produced (by queens their cocoon with fine forceps and tested between 3 and 12 h and/or workers) chemical cues may be exchanged old (NO). among other colony members through social inter- 5) Naive callow workers artificially emerged from their co- actions. Chemical analyses of artificial groups of coon were maintained separately with other naive eallows of the same age, without nurses, in small Petri dish cells. They Manica rubida and Formica selysi (Errard and Jal- were tested at 5-days old (N5). lon 1987) or of several North American Campono- tus species (Vander Meer and Carlin unpublished) indicated that members of these groups had mixed Behavioral assays chemical profiles characteristic of the species pres- Dead workers from each of these five categories were tested ent. Therefore chemicals are shared and acquired after one of the following treatments: anaong the members of these artificial groups. A 1) Freeze-killed ants: workers were frozen until dead (ca. 3 tl) then warmed to room temperature. study of the integration mechanism of a myrmeco- 2) Washed ants: Each live individual was soaked in 150 gl philous beetle into fire ant (Solenopsis spp.) colo- of hexane for 3 h then rinsed with additional hexane and al- nies also demonstrated a transfer of cuticular com- lowed to air dry for 15 min. The ants were dead after this ponents from host to myrmecophile. This transfer procedure. The soak was transferred to a clean vial, concen- was correlated with the beetle's acceptance into trated under nitrogen to about 20 Id, and used in the two fol- lowing treatments. the ant colony (Vander Meer and Wojcik 1982). 3) Washed ants coated with a nestanate soak: A total nest- We report the results of a behavioral and chem- mate soak was applied with a capillary pipet in three equal ical analysis of the ontogeny of nestmate recogni- aliquots to the head, thorax and abdomen of a washed worker tion cues in the ant Camponotus floridanus. Such of the same category. Treated ants were allowed to air dry for 15 lrfin before testing. a combined ontogenetical study has not been re- 4) Washed ants coated with an alien soak: The above proce- ported in social insects. The criterion used for nest- dure was used to apply a soak from a non-nestmate to a washed mate recognition was the aggressive behavior dis- worker. 177 9 Two queenless groups of ca. 600 workers, each coming from 5 a different colony, were tested between the second and fourth week after they were collected from the field. Just after treat- ment (one of the four described above), individual ants were introduced into the foraging area of their own colony or into the foraging area of the alien colony.