Response thresholds to recruitment signals and the regulation of foraging intensity in the ant Myrmica sabuleti (Hymenoptera, Formicidae)

Behavioural Processes 48 (2000) 137 – 148 www.elsevier.com/locate/behavproc

Response thresholds to recruitment signals and the regulation of foraging intensity in the ant Myrmica sabuleti (Hymenoptera, Formicidae) Jean-Christophe de Biseau *, Jacques M. Pasteels Laboratoire de Biologie Animale et Cellulaire-CP 160 /12, Uni6ersite´ Libre de Bruxelles, 50 A6enue F.D. Roose6elt, 1050 Brussels, Belgium Received 12 April 1999; received in revised form 29 September 1999; accepted 1 October 1999

Abstract The optimal foraging theory predicts that colonies of social insects must be able to adjust the intensity of their foraging behaviour as a function of the quality of the food discovered. Here, the mechanisms allowing the regulation of recruitment as a function of food concentration in the ant Myrmica sabuleti were analyzed. Although the total number of foragers engaged in food collection during recruitments increased with increasing concentration of sucrose solutions (0.1 vs. 1 M), neither the proportion of recruiting scouts nor the invitation behaviour performed by the scouts in the nest can explain this relationship. Foragers trail more when coming back from a 1 M than from a 0.1 M sucrose solution. However, this alone cannot explain the collective patterns observed since the mean numbers of workers leaving the nest after the entry of a scout coming back from either 0.1 or 1 M sources were not significantly different. We suggest that a spatial distribution of the foragers in the nest as a function of their motivational state could be part of the regulation process. The ants located near the nest entrance would respond to both low and high trail pheromone signals, but those located deeper in the nest would respond only to high level signals, resulting in higher recruitment rate towards richer sources. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Ant; Foraging; Formicidae; Recruitment; Trail; Myrmica sabuleti

1. Introduction The optimal foraging theory assumes that natural selection has favoured individual and social behaviours that maximize energy gain in different ways, for example, the choice of food exploited * Corresponding author. E-mail address: [email protected] (J.-C. de Biseau)

(optimum diet) and the choice of time devoted to different tasks (optimum time budget). In social insects, this approach has led to the idea that colonies must be able to adjust their foraging intensity (i.e. the number of foragers engaged in food collection) as a function of food quality (see for example Hangartner, 1970; Taylor, 1978). In ants, this has been demonstrated at the colony level by comparison of the flow of workers going

0376-6357/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 6 - 6 3 5 7 ( 9 9 ) 0 0 0 7 7 - 7

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toward the food (Taylor, 1977) or of the number of workers feeding together at the food (Wilson, 1962; Pasteels et al., 1987; Beckers et al., 1990; de Biseau et al., 1991) as a function of sucrose concentration. The mechanisms involved in the regulation process have been investigated by several authors (Ho¨lldobler and Wilson, 1990). A first regulatory mechanism (the ‘electorate’ process) seems to be the proportion of foragers returning to the nest and laying a trail (Wilson, 1962; Hangartner, 1970; Breed et al., 1987), since at least in some species, the number of workers leaving the nest increases with increasing quantity of trail pheromone (Wilson, 1962). Other studies have suggested that single foragers are also able to modulate the quantity of trail pheromone laid in one foraging trip as a function of sucrose concentration (Hangartner, 1969, 1970; Cammaerts, 1977; Verhaeghe, 1982; Crawford and Rissing, 1983; Beckers et al., 1993). However, all these works were devoted to either the collective or the individual level of food recruitment and studies investigating the problem at both levels in an effort to understand the link between them are scarce (Pasteels et al., 1987; Beckers et al., 1990, 1993). Here, we investigated the regulation of food recruitment as a function of sucrose concentration in the ant Myrmica sabuleti Meinert, both at the collective and individual levels. M. sabuleti is a European species living mainly in dry grasslands and on south slopes (Gaspar, 1971). The mean size of their colonies is about 1000 workers and a few queens (Brian, 1972). Foragers individually collect small arthropods, but use recruitment to collectively exploit sugar solutions or large prey (Cammaerts and Cammaerts, 1980; de Biseau and Pasteels, 1994; de Biseau et al., 1997). Experimental analyses have shown that the dynamics of this recruitment is explosive: a few minutes after the discovery of a sucrose solution, several tens of workers are present at the food source (de Biseau et al., 1992; de Biseau and Pasteels, 1994; de Biseau et al., 1997). The number of foragers feeding at a sucrose solution increases with increasing concentrations of food and colonies are able to select 1 M over 0.1 M sucrose solutions (de Biseau et al., 1991). However, the behavioural mecha-

nisms of this regulation remain unknown and cannot be extrapolated from analyses on other ants with more progressive recruitment dynamics (Beckers et al., 1990, 1993). In this paper, we first examine whether foragers that did not participate in the exploitation of a 0.1 M sucrose solution respond to recruitment signals if the sucrose concentration increases to 1 M. Secondly, we describe the invitation behaviour performed by the scouts inside the nest and the trail laying behaviour of the foragers between the food and the nest during recruitment to the sucrose solutions, as well as their modulation as a function of food concentration. We finally determined whether these mechanisms alone can explain the collective patterns observed.

2. Materials and methods Five colonies of Myrmica sabuleti, each composed of 500 workers, two queens and brood, were kept in plastic trays (26× 33 cm2) with artificial plaster nests. The bottom of the trays were covered with paper. The colonies were kept in the laboratory at 209 1°C in a 12:12 h light:dark cycle. Outside the experimental periods, the colonies were supplied with a 0.5 M sucrose solution and a water distributor. Every week, they received dead cockroaches. Four days before each experiment, they were deprived of food. The food sources offered during the experiments were drops (3 cm of diameter) of a 0.1 or 1 M sucrose.

2.1. Response thresholds to recruitments toward food sources of different concentrations Recruitments to food sources of different qualities were performed in order to determine if new workers are recruited to a rich food source replacing a poor one, or if the whole population of foragers is recruited toward the first source discovered. A 0.1 M sucrose solution was placed 15 cm from the nest entrance. Each forager feeding at the source was marked with a dot of paint on the abdomen until all ants joining the source were marked. At this moment, the 0.1 M sucrose solution was replaced by a 1 M solution and the

J.-C. de Biseau, J.M. Pasteels / Beha6ioural Processes 48 (2000) 137–148

marking was started again. This experiment was repeated six times (three colonies). A control experiment was designed in which the 1 M sucrose solution was given before the 0.1 M one (three replicates, three colonies).

2.2. Beha6iour of scouts in the nest and reaction of nestmates A food source (0.1 or 1 M sucrose solution) was placed 15 cm from the nest entrance. The first scout feeding at the source was marked with a dot of paint (Humbrol, Enamel) on the gaster. Any ants that subsequently discovered the food were removed. The time spent by the marked scout while feeding was observed. In order to record the behaviour of the scout in the nest and the reactions of nestmates, the chamber of the nest was filmed with a VHS video system from 5 min before the placement of the source until 10 min after the entry of the marked scout into the nest. This experiment was performed 30 times for each concentration of sucrose. To minimize the effect of the variation of the state of the colonies, 1 day of experimentation with a given colony was organized in the following way: in the morning (09:00 h), three scouts were tested at 30-min intervals with one concentration of sucrose solution; in the afternoon (15:00 h), three scouts were tested with the other concentration of sucrose solution (the order of presentation of the two sucrose concentrations was alternated daily). As previous experiments showed that the great majority of workers recruited by one scout left the nest during the minute following its entry (de Biseau and Pasteels, 1994), response of the nestmates to the entry of the scout was quantified by calculating the difference (DN) between the number of workers leaving the nest 1 min before and 1 min after the entry of the marked scout into the nest. As a control, the DN was calculated for 30 workers entering the nest without having discovered any food. We took as a criterion of recruitment a DN greater than the highest value of DN observed in the control, i.e. DN ]10 (de Biseau and Pasteels, 1994), and considered that a good approximation of the number of workers recruited by the scout was given by the DN value.

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2.3. Recruiting power of the content of the poison gland The trail pheromone is produced by the poison gland (Cammaerts and Cammaerts, 1980). In order to study the recruiting effect of the content of this gland, artificial trails were laid on Y-shaped cardboard bridges. Each branch of the bridge was 12 cm long and 0.5 cm wide, and the two branches departing from the choice point formed an angle of 60°. One bridge was deposited in the foraging area of a colony for 24 h to allow its exploration by the ants. It was then presented in front of the nest entrance for 10 min. After this control test, a trail corresponding to 0.032 poison gland/cm in hexane solution (optimal concentration: Cammaerts, 1989) was deposited along the common branch and along one of the two other branches of the bridge, while a same quantity of hexane was deposited along the second one. Two minutes later, the bridge was again presented to the colony and the number of workers travelling on the bridge and choosing one or the other branch was noted for 10 min. The experiments were repeated six times.

2.4. Trail laying beha6iour A Y-shaped cardboard bridge (identical to that described previously) was placed in front of the nest entrance of a colony. A 0.1 M sucrose solution was placed at the end of one of the two distal branches. Foragers feeding at the source were marked with a dot of paint on the abdomen. When the recruitment toward the source was well initiated (i.e. when 20–30 workers were feeding together at the source), a 1 M sucrose solution was placed at the end of the second branch. Foragers feeding at the second source were marked with another colour. Foragers which shifted from sources were removed immediately. Marked foragers travelling toward the nest on the common branch of the Y bridge were filmed laterally with a S-VHS video system with macro function (25 frames/s). The video tape was then analyzed frame by frame. The trajectories of 30 workers coming back from each source were recorded. Four types of frames were distinguished during the analysis of the video recording:

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1. the sting of the forager was not visible and the abdomen did not touch the substrate; 2. the sting of the forager was not visible but the abdomen touched the substrate; 3. the sting of the forager was visible but did not touch the substrate; 4. the sting of the forager was visible and touched the substrate. We assumed that 2 and 4 corresponded to trail laying behaviour.

2.5. Statistical analysis All analyses were performed using non-parametric statistics (Siegel and Castellan, 1988). Unless otherwise specified (Tables 1 and 5), two-tailed tests were used.

3. Results

3.1. Response thresholds to recruitments toward food sources of different concentrations From a total of 500 workers in a colony, the total number of recruits toward a 0.1 M sucrose solution ranged from 42 (8.4%) to 229 (45.8%) workers (Table 1). The rate of workers newly recruited toward a 0.1 M sucrose solution stabiliTable 1 Cumulated percentages of workers recruited to two sucrose sources given in succession (0.1 M solution followed by 1 M) Replicates

a

0.1 M

1M

1

39.4

51.4

2

28.2

43.4

3

8.4

15.6

4

12.2

21.6

5

45.8

55.2

6

40.8

51.6

X( 9 S.E. a

29.1 9 6.4

Colonies of 500 workers.

39.896.9

Chi-square test x 21 = 14.0, P= 0.0002 x 21 = 24.5, P=0.0001 x 21 = 11.6, P=0.0007 x 21 = 15.1, P= 0.0001 x 21 = 8.5, P= 0.004 x 21 = 11.3, P= 0.0005

Fig. 1. Cumulative number of recruited workers and population at the food source during a recruitment toward a 0.1 M sucrose solution replaced by a 1 M one after 18 min of exploitation by the colony (replication no. 2, see Table 1).

sized 9–39 min after the discovery of the source but systematically increased again when the richer source replaced the first offered (reaching from 15.6 to 59.2% of the worker population) (Table 1 and Fig. 1). In the same way, the population of foragers feeding together at the 0.1 M sucrose solution decreased 5–15 min after the discovery of the source but increased again soon after the source was replaced by a 1 M sucrose solution,

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surpassing the maximum reached at the first source (Fig. 1). A second recruitment was never observed in the control experiments, i.e. when the 1 M solution was given before the 0.1 M one.

3.2. Beha6iour of scouts in the nest and reaction of nestmates The mean feeding time was significantly greater (Wilcoxon–Mann–Whitney test, z= − 3.4, N1 =N2= 30, P= 0.0006) for the scouts which fed at a 1 M sucrose solution (X( 9S.E. = 206 9 12 s, N =30) than for the scouts which fed at a 0.1 M source (X( 9 S.E. = 87 96 s, N =30). After feeding at the sucrose solution, all scouts went back to the nest. After entering the nest, the scouts: “ either moved quickly, running toward and bumping nestmates, or moved slowly, without bumping nestmates; “ either made a trophallaxis or did not; “ either left the nest within the 10 min of its entry or did not. The frequencies associated with these behaviours are similar for both concentrations in sucrose (Table 2). The reaction of the nestmates to the entry of a scout varied from no visible response to a massive exit of recruited workers. The distributions of the DN values are significantly different from the control for both 0.1 M and 1 M sucrose solutions (Fig. 2) (Wilcoxon– Mann – Whitney test; 0.1 M sucrose solution: z= −2.64, N1 =N2 = 30, P = 0.008; 1 M sucrose solution: z= −3.60, N1 = N2 =30, P= 0.0003). Two criteria can be used to define a recruiter: a scout that moves quickly, rushing its nestmates or

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a scout that elicits a DN greater than the DN values in the control distribution (i.e. DN ] 10). The correlation between these two criteria is highly significant (Table 3) (Phi coefficient test, x 21 = 25.9, rf = 0.69; N=60, P =0.0001) showing that scouts which rushed their nestmates generally elicited their departure. When a recruitment was elicited (DN ] 10), there was a positive correlation (Spearman rankorder correlation coefficient, rS = 0.78, N= 17, PB 0.001) between the DN value and the number of nestmates rushed by a recruiter (Fig. 3A). However, the number of recruits was generally greater than the number of nestmates directly contacted by the recruiter. The mean time spent in the nest was  1 min (X( 9S.E.= 629 21 s, N=25) for scouts that rushed their nestmates, while this mean time was 5 min (X( 9 S.E.= 2779 31 s, N=31) for scouts that did not exhibit this behaviour (Fig. 3B) (Wilcoxon–Mann–Whitney test; z= − 4.6, N1=25, N2= 31, PB 0.0001). There is a positive correlation (Spearman rank-order correlation coefficient, rS = 0.59, N= 48, PB 0.001) between the running speed of the scout in the nest and the DN (Fig. 3C). The mean running speed was 3.869 0.28 mm/s (X( 9 S.E.), N=25) for scouts which rushed their nestmates, and 1.969 0.15 mm/s (X( 9 S.E., N= 35) for the other scouts. Finally, non recruiters usually engaged in a trophallaxis, contrary to the recruiters (Table 4). The distribution of the DN values obtained with a 0.1 M sucrose solution is not significantly different from the one obtained with a 1 M sucrose solution (Fig. 2) (Wilcoxon–Mann–Whitney test, z = −1.00, N1= N2= 30, P= 0.3). Scouts having fed at either a 0.1 M or a 1 M sucrose solution

Table 2 Frequencies of behaviours of scouts entering the nest after having fed at a 0.1 or a 1 M sucrose solution 0.1 M source (N= 30)

1 M source (N = 30)

Chi-square test

Run fast and rushed nestmates

0.37

0.47

Trophallaxis

0.60

0.50

Exit within 10 min

0.97

0.90

x 21 =0.62, P =0.43 x 21 =0.61, P =0.44 x 21 =1.07, P =0.31

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N1= 11, N2=14, P= 0.5). The mean number of workers recruited by one recruiter (using the DN] 10 as criteria) was 21.8 93.8 workers (X( 9 S.E., N= 9) for a recruiter returning from a 0.1 M sucrose solution and 24.494.0 workers (9 S.E., N= 11) for a recruiter returning from a 1 M sucrose source. The difference between these two values is not significant (Wilcoxon–Mann–Whitney test, z = −0.53, N1= 9, N2= 11, P= 0.6). On summary, between 37 and 47% of scouts entering the nest after finding a sucrose solution recruit nestmates. This proportion of recruiters is not significantly different between scouts returning from a 0.1 or from a 1 M sucrose solution. No behavioural differences were detected between scouts returning from a 1 or from a 0.1 M sucrose solution and no quantitative difference was detected in the response of nestmates.

3.3. Recruiting power of the content of the poison gland

Fig. 2. Number of recruited workers (DN) leaving the nest (solid bars) compared to control exit rate (open bars) during recruitments toward a 1 or a 0.1 M sucrose solution. DN= NA −NB, NA = number of workers leaving the nest during the minute following the entry of a scout (solid bars) or a non forager (control, open bars), NB= number of workers leaving the nest during the minute preceeding its entry (see text). Wilcoxon – Mann – Whitney test, N1 = N2= 30, z = − 3.60, P =0.0003 for the 1 M source; z= − 2.64, P= 0.008 for the 0.1 M source.

elicited massive exits of nestmates with comparable frequencies and intensities. No significant difference was found between the number of nestmates rushed by recruiters coming back from a 0.1 or a 1 M sucrose solution (Wilcoxon–Mann–Whitney test, z= − 0.68,

When a bridge with no trail was presented to a colony, 0.59 0.3 workers (X( 9 S.E., N=6) climbed on it within 10 min, while 41.09 11.9 workers (X( 9 S.E., N= 6) crossed the bridge during the same period when a trail corresponding to 0.032 poison gland/cm was deposited. The mean number of recruited workers climbing the bridge decreased exponentially with time (Fig. 4). Of a total of 246 workers that climbed the bridge during the 10 min and reached the choice point between the trail and the control branch with pure hexane, all but three chose the trail. Table 3 Correlation between the behaviour of the scout and the number of recruited workers a Run fast and rushed nestmates

DN]10 DNB10 Total

Yes No Total

18 2 20

7 33 40

25 35 60

a DN=NA−NB, NA and NB being, respectively, the number of ants leaving the nest 1 min after and 1 min before the entry of a successful scout. Phi coefficient test, x 21 =25.9, rf =0.69; N = 60, P= 0.0001.

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3.4. Trail laying beha6iour When the foragers discovered the 1 M sucrose solution while a recruitment toward the 0.1 M source had already been initiated, a shift of the main activity from the poor source to the rich one occurred. The mean proportion of the four types of frames observed per source-nest trajectory for the two concentrations of sucrose solutions is given in Table 5. The frames showing a possible trail laying behaviour are those where a contact abdomen/substrate or a contact sting/substrate were seen. Only the mean proportion of frames showing a contact sting/substrate is significantly greater for foragers coming back from the 1 M sucrose solution than for those coming back from the 0.1 M source (Wilcoxon–Mann–Whitney test, one-tailed, z= − 1.94, N1= N2=30, P= 0.0262). The distributions of the proportion of frames corresponding to a contact sting/substrate shows a great variability, both for 1 and 0.1 M sucrose solutions (Fig. 5). In order to understand more precisely the modulation of trail laying behaviour, we have considered its two components: collective and individual modulations. Collective modulation corresponds to the proportion of foragers that lay a trail during a source–nest trajectory. This proportion of trailing foragers (foragers showing at least one contact sting-substrate) was 33% for the ants returning from a 0.1 M and 57% from a 1 M sucrose solution. The difference between these proportions is not significant (x 21 = 3.3, N1= N2= 30, p =0.069). Individual modulation corresponds to the proportion of frames ‘contact sting-substrate’ per source-nest trajectory, but cal-

Fig. 3. Relationships between the number of ants recruited (estimated by DN, see Fig. 2) toward either a 0.1 or a 1 M sucrose solution and: (A) the number of nestmates rushed by the recruiter (Spearman rank-order correlation coefficient, rS =0.78, N =17, P B0.001); (B) the time spent by a scout in the nest; (C) the speed of run of a scout in the nest (Spearman rank-order correlation coefficient, rS =0.59, N =48, P B 0.001). Solid symbols indicate scouts which rushed their nestmates; open symbols indicate those which did not rush them. Fig. 3.

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Table 4 Correlation between recruitment behaviour and trophallaxis a Recruitment behaviour

Yes No Total

Trophallaxis Yes

No

Total

4 29 33

20 3 23

24 32 56

a Recruitment behaviour: inside the nest, the scout run fast and rushed nestmates. Phi coefficient test, x 21 = 28, rf = 0.74; N= 56, P = 0.0001.

Fig. 4. Mean number of workers (and standard error) recruited by an artificial trail as a function of the age of the trail. 0.032 poison gland eq./cm was deposited on the trails.

culated only for trailing foragers. The values obtained were 319 7% (X( 9S.E., N= 10) and 399 7% (X( 9S.E., N =17) frames per trajectory for the workers coming back from a 0.1 and a 1 M sucrose solutions, respectively. The difference between these values is not significant (Wilcoxon – Mann–Whitney test, one-tailed, z = −0.74, N1 =10, N2= 17, P =0.23). However, as stated above, significant modulation is obtained when the collective and individual modulations are combined. 4. Discussion

4.1. Recruitment beha6iour of scouts Our results show that in M. sabuleti, the popu-

lation of scouts can be divided into two categories: recruiters and non recruiters. Inside the nest, recruiters, as opposed to non recruiters, characteristically moved quickly, ran toward and bumped their nestmates, seldom made a trophallaxis, and left the nest after a mean time of 1 min. Currently, we do not know whether these two categories of scouts correspond to a stable division of labour or not. Nestmates are recruited both by a rushing behaviour performed by the recruiter and by the trail pheromone. The rushing behaviour of the recruiter is a collective excitation rather than an individual invitation as described for example in Camponotus socius (Ho¨lldobler, 1971). One scout is able to recruit from ten to 65 nestmates in 1 min. The mechanical excitation seems to be complemented by a chemical one, as supported by the recruiting effect of the content of the poison gland. Indirect arguments also suggest this chemical component. We have observed a recruiter entering the nest for 8 s and rushing only three nestmates, while 20 recruits left the nest during the minute following the entry of the recruiter. Moreover, several examples showed that while leaving the nest, the recruits followed the same trajectory as that of the recruiter in the nest, suggesting that the recruiter also laid a recruiting trail in the nest.

4.2. Regulation of trail laying As in many other ant species (Hangartner, 1969, 1970; Cammaerts, 1977; Verhaeghe, 1982; Beckers et al., 1993), M. sabuleti foragers seem to trail more when coming back from a 1 M sucrose solution than from a 0.1 M one. The trail laying behaviour is about two times more frequent when a forager comes back from a 1 M sucrose solution than from a 0.1 M one. This probably plays a central role in the collective choice of the richer food source, as previously reported (de Biseau et al., 1991). However, as already pointed out by Wilson (1962), evaluation of the frequency and intensity of trail laying behaviours to estimate the quantity of pheromone deposited, although commonly used (Wilson, 1962; Hangartner, 1969, 1970; Cammaerts, 1977; Verhaeghe, 1982; Beckers

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Table 5 Behaviours of foragers coming back from a 1 M or from a 0.1 M sucrose solution a Behaviour

0.1 M source

1 M source

Wilcoxon–Mann–Whitney test, one-tailed

ANS AS SNS SS N

23 94 63 95 49 1 1094 30

209 4 529 5 591 229 5 30

z=−0.71, z=−1.29, z=−0.88, z=−1.94,

P =0.239 P =0.098 P =0.189 P =0.026

a The ants were video recorded (25 frames/s); the records were analyzed frame by frame. ANS, percentage of frames per trajectory in which the abdomen did not touch the substrate and the sting was not visible; AS, the abdomen touched the substrate but the sting was not visible; SNS, the sting was visible but did not touch the substrate; SS, the sting touched the substrate. X( 9 S.E., N =30.

et al., 1993), is an indirect method, based on an hypothetical correlation between these twoparameters. A direct method allowing precise measurement of the actual pheromone quantity would be very helpful in verifying this correlation.

4.3. Regulation of recruitment intensity The total number of workers recruited to a sucrose solution was highly variable but an enhancement of food quality always induced the recruitment of new foragers who did not participate in the on-going recruitment. These observations, together with previous results (de Biseau et al., 1991), showing that the mean number of workers feeding at the food was on average two times greater for 1 M than for 0.1 M sucrose solutions, suggest that the forager population standing in the nest is made of workers having different response thresholds to recruitment signals. However, this regulation could not be detected in the response of workers to the recruitment signals of single scouts having fed at a 0.1 or a 1 M sucrose solution. Moreover, both the proportion of recruiters and the mean number of nestmates recruited by the first recruiters, although slightly greater for scouts coming back from a 1 M than from a 0.1 M sucrose solution, were not significantly related to the concentration of the food source. Two hypotheses could explain these paradoxical results. The first one is that there is a difference between the number of workers recruited by scouts coming back from a 0.1 M and a 1 M sucrose

solution but that this difference is too weak to be statistically detected in samples of 30 scouts. However, owing to the auto-catalytic property of the recruitment process, this difference would be quickly amplified and would be detected at the collective level. This is unlikely in the present case because of the characteristic explosive dynamic of recruitment in M. sabuleti (de Biseau et al., 1992, 1997). A second explanation could be a spatial organisation of the foragers in the nest as a function of their motivation. We can hypothesize a simple scenario in which foragers stand nearer the nest exit as a function of their increasing internal motivation to forage. At a very high level of motivation, they leave the nest without being

Fig. 5. Trail laying behaviour of foragers coming back from a 0.1 M (open bars) or a 1 M (solid bars) sucrose solutions. The abcissa gives the proportion of frames showing a contact between the sting and the substrate in video records (25 frames/s).

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recruited and become scouts. Following this scenario, foragers having a low threshold of response (high motivation) would be near the nest entrance, while the foragers having a high threshold of response (low motivation) would be farther in the nest. If this is the case, the first recruiters entering the nest encounter only foragers responding both to low and high signals (e.g. trail pheromone quantity). Later in the recruitment, the recruiters encounter foragers responding only to high signals of recruitment and, therefore, only the recruiters coming back from a 1 M sucrose solution recruit new nestmates effectively. If this hypothesis is correct, differences in nestmate reactions could not be detected at the beginning of the recruitment. By contrast, without spatial organisation in the nest as a function of internal motivation, we should expect to detect a difference in the number of nestmates recruited by scouts coming back from 0.1 and 1 M sucrose solutions, even at the beginning of the recruitment. In social insects, division of labor based on response threshold distribution has been proposed by several authors (Wilson, 1985; Robinson, 1987; Calabi, 1988; Page and Robinson, 1991; Detrain and Pasteels, 1991; Bonabeau et al., 1996). In Pheidole pallidula, for example, majors have higher thresholds of response to mechanical and chemical invitation than minors. This difference explains why majors, contrary to minors, participate only to massive recruitments (Detrain and Pasteels, 1991). It is interesting to note that, at least in artificial laboratory nests, few majors are found near the nest exit, where minors are in majority (Detrain, personal communication). The relation between spatial localisation in the nest and division of labor is very poorly documented in ants. In Leptothorax unifasciatus, however, Sendova-Franks and Franks (1994, 1995) have demonstrated that workers are spatially organized inside the nest and that individuals located at the periphery are most likely to leave the nest. Spatial organisation in the nest could be an important regulatory mechanism of the foraging activity in social insects.

4.4. The link between indi6idual and colony le6els In social insects, optimal foraging theory pre-

dicts that foraging behaviour must be regulated as a function of food quality. Although adjustment of recruitment intensity as a function of food concentration is well known in ants, the link between individual and colony levels is poorly illustrated. Most studies suggest that the number of recruited foragers is regulated by the quantity of pheromone laid by individual scouts, but none quantitatively demonstrates this relationship. Few papers have investigated precisely the relation between the concentration of food and the number of workers recruited by one scout. Szlep and Jacobi (1967) reported that the strength of the invitation behaviour of scouts was related to the concentration of sugar and that the size of the recruited group was determined by the strength of the invitation, but no quantitative information about this relationship is given. Breed et al. (1987) did not detect any significant difference between the number of workers recruited by individual scouts of Paraponera cla6ata having fed on 0.1 and 1 M sucrose solutions. Our results on M. sabuleti show the same absence of relationship. The other mechanism of regulation is the ‘electorate’ process first described in Solenopsis in6icta (= S. sae6issima) by Wilson (1962), in which the adjustment of the recruitment is achieved only by the percentage of recruiting scouts as a function of the food concentration. In P. cla6ata, this process seems to be the main mechanism both for sucrose solutions of different sizes and different concentrations (Breed et al., 1987). In M. sabuleti, the same is true for sucrose solutions of different sizes (de Biseau and Pasteels, 1994); however, we were unable to detect a significant difference in the proportion of recruiting scouts coming back from 0.1 and 1 M food sources. In conclusion, although single scouts seem able to modulate their trail-laying behaviour as a function of sucrose concentration, there is no evidence than this is correlated with the number of recruited nestmates per recruiter. However, a spatial organisation of the foragers in the nest could lead to the regulation observed at the colony level: if the foragers standing in the nest have different thresholds of response to recruitment pheromone(s), and if the less motivated foragers stand in the back of the nest, the individual

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modulation of pheromone quantity laid could make a difference later in the recruitment process. On the other hand, the modulation of trail laying could be a key mechanism in the choice of foragers between different trails outside the nest in M. sabuleti (de Biseau et al., 1991), as well as in other ant species (Crawford and Rissing, 1983; Pasteels et al., 1987; Beckers et al., 1990, 1993). Food recruitment has been considered to be regulated by the scouts’ behaviours. Response threshold distribution among foragers and the spatial relationship of the foragers within the nest could be additional mechanisms. Acknowledgements This research was supported by a grant (no. 890674) from the Belgian ‘Institut pour l’encouragement de la Recherche Scientifique dans l’Industrie et l’Agriculture (I.R.S.I.A)’ to J.C. de Biseau, by the Venture Research Unit of British Petroleum and by a grant (no. 2.4513.93) from the Fund for Joint Basic Research. We thank S. Aron, Y. Roisin and particularly J.L. Deneubourg for critical discussions and D. Vanhauwermeiren for her help in the realisation of the experiments. References Beckers, R., Deneubourg, J.L., Goss, S., Pasteels, J.M., 1990. Collective decision making through food recruitment. Insectes Soc. 37, 258 – 267. Beckers, R., Deneubourg, J.L., Goss, S., 1993. Modulation of trail laying in the ant Lasius niger (Hymenoptera: Formicidae), and its role in the collective selection of a food source. J. Insect Behav. 6, 751–759. Bonabeau, E., Theraulaz, G., Deneubourg, J.L., 1996. Quantitative study of the fixed threshold model for the regulation of division of labor in insect societies. Proc. R. Soc. Lond. B 263, 1565 – 1569. Breed, M.D., Fewell, J.H., Moore, A.J., Williams, K.R., 1987. Graded recruitment in a Ponerine ant. Behav. Ecol. Sociobiol. 20, 407 – 411. Brian, M.V., 1972. Population turnover in wild colonies of the ant Myrmica. Ekol. Pol. 20, 43–53. Calabi, P., 1988. Behavioral flexibility in Hymenoptera: a re-examination of the concept of caste. In: Trager, J.C. (Ed.), Advances in Myrmecology. Brill Press, Leiden, pp. 237 – 258.

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