Social Isolation of Mature Workers Affects Nestmate Recognition in the Ant Camponotus Fellah
Total Page：16
File Type：pdf, Size：1020Kb
Behavioural Processes 55 (2001) 67–73 www.elsevier.com/locate/behavproc Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah R. Boulay *, A. Lenoir Institut de Recherche sur la Biologie de l’Insecte, UPRES A CNRS 6035, Faculte´ des Sciences et Techniques, Parc de Grandmont, Uni6ersite´ Franc¸ois Rabelais, F-37200 Tours, France Received 28 July 2000; received in revised form 12 November 2000; accepted 10 January 2001 Abstract This study investigates the role of social stimulation on nestmate recognition in mature workers of Camponotus fellah. We isolated 4-week-old workers before examining their behaviour in dyadic reunion tests. At the age of 4 weeks, workers are normally intolerant towards both allospecific and homospecific but allocolonial individuals. However, when they were isolated for up to 20 days, allocolonial aggressions decreased while allospecific aggression remained constant. Workers isolated for 20 days also engaged in allocolonial trophallaxis. These results suggest that workers need to be reinforced by social stimulation during their adult life to keep precise nestmate recognition capacities. We discuss our data under the perspective of recent neuroethological data in social insects to propose a mechanism for the formation of the neural template used in the nestmate recognition process. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Nestmate recognition; Social isolation; Camponotus fellah; Learning; Template formation 1. Introduction 1995), one trait that characterises most eusocial insect species was quietly neglected: individuals It is generally accepted that eusociality means have a particular tendency to search for and to that individuals living in a colony unequally share keep social contacts with their nestmates and this reproductive tasks and that there is an overlap of has many consequences on colony life. For in- at least two generations allowing offspring to help stance, worker–worker interactions are responsi- parents rear immature siblings. While the central ble for the plasticity in division of labour in regard question of eusociality excited sociobiologists over to specific needs of the colony in the honeybee the last three decades (see recent arguments from (Huang et al., 1998; Huang and Robinson, 1992, Sherman et al., 1994 and Crespi and Yanega, 1996) and in harvester ants (Gordon, 1989, 1996). Interactions between nestmates also mediate the colony activity cycle in Leptothorax allardycei * Corresponding author. Tel.: +33-972-36408766; fax: + 33-972-36406991. (Cole, 1991a,b) and the ethogenesis in Ectatomma E-mail address: [email protected] (R. Boulay). tuberculatum (Champalbert and Lachaud, 1990). 0376-6357/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S0376-6357(01)00163-2 68 R. Boulay, A. Lenoir / Beha6ioural Processes 55 (2001) 67–73 In ants, worker–worker interactions also influ- 2. Materials and methods ence colony defence. Most ant species are aggres- sive animals that attack any allospecificor 2.1. Collection of ants and rearing conditions allocolonial intruder. This general aggressiveness is partly controlled by behavioural and chemical Experiments were conducted with workers from cues originating from nestmates. For instance, in five queenright colonies of C. fellah Dalla Torre Pheidole pallidula behavioural stimulations from and from two queenless colonies of Camponotus minor workers are responsible for the ontogeny of 6agus Scop. Only minor workers that were in- aggressive behaviours in soldiers (Aarab and Jais- volved in intra-nest tasks (mostly nurses) and that son, 1992). The occurrence of releaser and maybe showed some degree of gaster distension were primer pheromones that elicit aggressive be- used. Preliminary observations during which haviours, are also reported in many species (see workers were marked just 2 days after emergence review from Van der Meer and Alonso, 1998). indicated that they showed such gaster distension Worker–worker interactions also affect the ca- when at least 4 weeks old. pacity to discriminate between nestmates and Colonies of C. fellah were established in the aliens. This mechanism consists of the comparison laboratory from newly mated queens that were of the phenotype (olfactory signature) of any en- collected at Ramat Aviv (Israel) 1 year before the 6 countered individuals with a reference (template). experiment. Colonies of C. agus were composed Of course, nestmates’ signatures must have simi- of approximately 300–400 individuals and some brood. They were collected at Rilly-sur-Vienne larities and the template must reflect these similar- (France) and maintained in the lab for 2 months ities. At least in some formicines and myrmicines, before the experiment. Colonies of both species callows acquire both the signature and the tem- were reared in artificial nests made of plaster to plate from their nestmates (see Lenoir et al., maintain a constant humidity (see Boulay et al., 1999). However, in the carpenter ant Camponotus 1999 for more details). Temperature, humidity fellah and several other species, the colony signa- and light–dark cycle in the rearing room were ture is not static, but changes over time, suggest- 2592°C, 6095% and 12:12 LD, respectively. ing that the template does so as well (Van der Each nest was connected to a foraging area (30× Meer et al., 1989; Provost et al., 1993; Nielsen et 40×20 cm) where food (Bee Happy, Koppert, al., 1999; Boulay et al., 2000a). Biological system and Tenebrio larvae) was sup- The aim of the present study was to determine plied ad libitum. whether social stimulation is necessary to main- tain the capacity to reject aliens and to accept 2.2. Experiment 1: social isolation effect on nestmates. Changing the social environment just allocolonial aggression after emergence from pupal stage increase toler- ance of aliens when the individuals become ma- Two hundred and sixty-six C. fellah minor ture. The originality of the present report is that it workers were sampled in almost the same propor- concerns mature individuals. Because old carpen- tions from each of the five colonies, depending on ter ants are aggressive, it is not possible to trans- availability. They were isolated in test tubes (18× fer them to another colony as was done in 180 mm) where they had ad libitum access to previous experiments with callows. However, old water and food (Bee Happy and Tenebrio larvae). workers can survive for few weeks even if de- They were kept in the tubes for 20 min (the prived of any contact with nestmates. Thus, minimum time for the ants to calm down), 5, 10 rather than changing the social environment, we or 20 days. Bioassays consisted of dyadic reunions suppressed it for up to 20 days and then we between individuals that were previously submit- conducted bioassays to measure the relative toler- ted to the same isolation duration, but that origi- ance between nestmates and between allocolonial nated either from two different colonies and allospecific aliens after isolation. (allocolonial encounters) or from the same colony R. Boulay, A. Lenoir / Beha6ioural Processes 55 (2001) 67–73 69 (homocolonial encounters, control). The tubes ‘type of encounter’ and ‘isolation duration’. Spe- were connected one to each other to let the work- cific effects were determined by LSD post hoc ers enter into contact by themselves without any tests. Total durations of trophallaxis were com- manipulation that could generate stress. Be- pared by the same statistics. havioural items were recorded for 5 min from the In experiment 2 we compared aggression in- first interaction. dexes and the total duration of trophallaxis in allospecific encounters after 20 min (control) and 2.3. Experiment 2: social isolation effect on 20 days of isolation by t-tests. allospecific aggression Eighteen C. fellah workers and 18 C. 6agus 3. Results workers were sampled in almost the same propor- tions from the five colonies and two colonies, 3.1. Social isolation effect on allocolonial respectively. They were isolated in test tubes as aggression previously described for 20 min or 20 days. Then, their behaviour was recorded while they were In the field, C. fellah is a monogynous species reunited in allospecific dyads for 5 min, as de- that builds very widespread nests. Although the scribed in experiment 1. border between neighbouring nests seems to over- lap, the social closure is very high. In our labora- 2.4. Recorded beha6ioural items and statistics tory tests, the aggression index A.I. was significantly higher in allocolonial than in homo- We recorded the frequency and duration of all colonial encounters (Fig. 1, two-tailed B interactions using a Psion organiser. In order to MANOVA: F1,133=64.0, P 0.001). The factor assess the effect of the duration of isolation on the ‘isolation duration’ also had a highly significant aggression expressed in homocolonial, allocolo- effect on A.I. (Fig. 1, two-tailed MANOVA: nial and allospecific encounters we used the ag- F3,133=4.0, P=0.008). Moreover, there was a sig- gression index (A.I.) elaborated by Hefetz et al. nificant interaction between the factor ‘type of 1996: encounter’ (homo- vs. allocolonial) and the factor n ‘isolation duration’ (Fig. 1, two-tailed MANOVA: % A.I.i t × i F3,133=4.9, P=0.003). A.I.= i=1 In homocolonial encounters, A.I. was low T whatever the duration of isolation. On the con- where T is the total time of interaction, A.I.i is a trary, A.I. in allocolonial encounters significantly factor applied to each act regarding its degree of decreased from 0.5690.10 to 0.1090.03 (LSD aggressiveness: non-aggressive interactions (anten- post hoc test, PB0.001). Most interactions be- nal contacts, trophallaxis and allogrooming) were tween workers originating from different colonies scored A.I.i=0; openings of the mandibles were and maintained for 20 min in the test tubes were scored A.I.i=1; flexions of the abdomen with or threatening.