The authors have declared that no competing interests exist.
Limited resources result in competition among social animals. Nevertheless, social animals also have innate preferences for cooperative behavior. In the present study, 12 dyads of food-deprived rats were tested in four successive trials, and then re-tested as eight triads of food-deprived rats that were unfamiliar to each other. We found that the food-deprived dyads or triads of rats did not compete for the food available to them at regular spatially-marked locations that they had previously learnt. Rather, these rats traveled together to collect the baits. One rat, or two rats in some triads, lead (ran ahead) to collect most of the baits, but "leaders" differed across trials so that, on average, each rat ultimately collected similar amounts of baits. Regardless of which rat collected the baits, the rats traveled together with no substantial difference among them in terms of their total activity. We suggest that rats, which are a social species that has been found to display reciprocity, have evolved to travel and forage together and to share limited resources. Consequently, they displayed a sort of 'peace economy' that on average resulted in equal access to the baits across trials. For social animals, this type of dynamics is more relaxed, tolerant, and effective in the management of conflicts. Rather than competing for the limited available food, the food-deprived rats socialized and coexisted peacefully.
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Competing for limited resources is a major driving force in the animal kingdom. In the context of social species, there is an apparent conflict between competing over resources on the one hand, and preserving group cohesion on the other hand. Indeed, living in groups has both benefits and costs, and a prerequisite for social species is to establish a balance between cooperation and competition among individuals. Group living usually involves the establishment of various social ranks and, accordingly, the distribution of resources is biased toward the highly-ranked individuals. Even then, however, conflicts among group members arise, with the two main conflicts being over mating partners [
As noted above, recent studies have revealed that rats with limited access to food may display a type of prosocial behavior rather than provoking competition [
A past study with rat dyads revealed that the spatial choices of individual rats may affect the future spatial choices of their partners in a foraging task [
In the present study we expanded the previous studies [
Twenty-four male Sprague–Dawley rats (age 6–7 months; weight 450–600 g) were housed in a temperature-controlled room (22 ± 1°C) under an inverse 12/12-h light/dark cycle (dark phase 8:00–20:00). Rats were held in standard rodent cages (40 x 25 x 20 cm; two rats per cage) with sawdust bedding and were provided with
We confirm that this study was carried out in strict accordance with the recommendations of the Guide for the Care and Use of the Institutional Animal Care and Use Committee (IACUC) of Tel-Aviv University, Permit Number L-14-051. In this permit, Tel-Aviv IACUC approved the specific procedures in this study. No animals were sacrificed for the purpose of this study.
Rats were tested in a 6 x 5.6 m arena, comprising the white floor of a light-proofed air-conditioned room (22 ± 1°C). The room door had the same cover of that of the walls, and was located 50 cm above the floor so that there was no distinct visual or tactile landmark on the room perimeter. The room was illuminated with four cool-white LED projectors (65W each), sufficient to distinguish between subjects but subtle enough to prevent discomfort to the rats. Sixteen objects (each a 12 x 12 x 6 cm cement cube) were placed in a grid layout, equispaced at 90 cm from each other in the center of the arena (see
The large circumference represents the 6 x 5.6 m arena, and the 16 dark squares (■) represent the 16 equispaced objects. The dashed square around each object represents the 36 X 36 cm object zone.
Training and testing were carried out during the dark phase of the rats’ dark/light cycle, in order to test the rats during the period when they are most active. Each rat underwent a series of training sessions preceded by 12 hrs of food deprivation with access only to water. Fifteen minutes before each session, rats were brought to a room adjacent to the apparatus and their backs were gently painted in blue, green, or red with a waterproof marker, enabling the tracking system to differentiate among them. Each of the 16 objects was then baited with a small piece of chocolate-flavored cereal, placed in the center of the top surface of each object. An individual rat was then placed gently in the near right corner of the arena, and the experimenter left the room. Dyads and triads of rats were each hand-held by one or two experimenters and gently released simultaneously near the right corner of the arena, with all of them facing the arena center. Training sessions continued until each rat had collected food from at least 14 objects in less than 20 min. Each rat underwent a different number of training sessions depending on its learning rate (mean ± SEM = 3.60 ± 0.15 training sessions). When three rats from different cages had completed the training sessions, they underwent two additional sets of 15-min trials: (i)
Data acquisition was performed automatically for all rats, and the experimenter was blind to the role of the rat in previous trials. For the lone and dyad/triad trials the following parameters were extracted from ‘Ethovision’, and further analyzed with Microsoft Excel 2010 and STATISTICA 8 (Statsoft, UK):
One way ANOVA was used to compare the behavior of the same rats across trials. Two-way ANOVA was used to compare the behavior of leader and follower rats (between-group effect) in the lone and triad trials (within-group effect). For this, rats in the lone trials which preceded the first dyad trial were classified as "leaders" and "followers" according to their behavior with partners in the first dyad trial.
Rats in the dyad/triad trials could have divided the task among them, with each consuming a different set of baits, enabling them together to accomplish the task of consuming the 16 baits faster than the lone-trial rats. For example, each of the three rats in a triad could have collected baits from 5–6 objects and the triad could thereby complete together the task of collecting all the baits faster than lone individuals. However, this was not the case and the duration of consuming the 16 baits by two or three rats together (regardless of which rat collected them) did not differ from the performance of the same individuals in the lone preceding trials (
As shown, two rats (top two rows) were continuously leading in terms of the number of baits they collected. Another three rats (bottom three rows) were followers, always collecting a few baits. The other 19 rats greatly varied in the number of baits they collected across trials.
Dyad trials | Triad trial | ||||
---|---|---|---|---|---|
1st | 2nd | 3rd | 4th | ||
14 | 16 | 16 | 16 | 9 | Always leaders |
11 | 11 | 11 | 12 | 14 | |
14 | 9 | 8 | 10 | 1 | Transient states of leading or following |
13 | 14 | 9 | 2 | 0 | |
12 | 16 | 12 | 14 | 3 | |
12 | 13 | 9 | 2 | 11 | |
12 | 9 | 1 | 3 | 9 | |
11 | 6 | 9 | 9 | 0 | |
10 | 9 | 1 | 7 | 8 | |
10 | 5 | 0 | 3 | 7 | |
9 | 14 | 12 | 7 | 4 | |
9 | 7 | 6 | 14 | 0 | |
7 | 9 | 10 | 2 | 7 | |
7 | 2 | 4 | 9 | 7 | |
6 | 11 | 16 | 13 | 12 | |
6 | 7 | 15 | 9 | 1 | |
5 | 10 | 7 | 6 | 1 | |
4 | 7 | 15 | 13 | 9 | |
4 | 3 | 7 | 14 | 6 | |
2 | 7 | 8 | 6 | 3 | |
2 | 2 | 7 | 12 | 7 | |
5 | 5 | 5 | 4 | 5 | Always Following |
4 | 0 | 4 | 2 | 1 | |
2 | 0 | 0 | 0 | 3 |
Further, each rat was categorized as a "leader" or a "follower" according to the number of baits it had collected during the first dyad trial, with leaders collecting more than 8 baits and followers less than 8 baits. Retaining this assignment into "leaders" and "followers", we then calculated how many baits were collected by each of the 'first-trial leaders' and 'first-trial followers' in the subsequent trials. The means (± SEM) for these data, depicted in
Rats were categorized as leaders or followers in the first dyad trial (left hand columns). These first-trial categories as leaders and followers were retained for the subsequent trials, regardless of the actual number of baits collected by the rats in these subsequent trials. The mean of the actual performance in subsequent trials is thus depicted according to the original categories, illustrating a diminishing difference between leaders and followers, reaching equity from the third trial on. * indicates a significant difference between the leaders and followers in that trial, as well as between the leaders in this trial and both leaders and followers in the triad trial. Note that this does not mean that there were no leaders and followers from Trial #3 on. Conversely, there were always leaders and followers but their identity changed.
The question arose as to whether it was possible to identify "leaders" and "followers" already in the preceding lone trial, when they were tested individually before being exposed to the baits together with partners. For this, data of the rats during the triad trial were divided into leaders and followers in accordance with their performance in the triad trial, and compared for the lone and triad trials (
In each trial, rats were classified as leaders or followers according to their performance in the triad trial. For each parameter, the results of a two-way ANOVA are depicted at the right for within-trial comparison (between leaders and followers), for between trial comparison (between lone and triad trials), and for the interaction of trial x leading. Significance is depicted in boldface. The results of a post-hoc Tukey HSD comparison are depicted in superscript, as specified at the bottom of the Table.
Parameter | Lone trial | Triad trial | Within trial F1,22 P | Between trials F1,22 P | Interaction F1,22; P | ||
---|---|---|---|---|---|---|---|
Leader | Follower | Leader | Follower | ||||
118.4 ± 6.1 | 111.8 ± 4.6 | 145.1 ± 4.6 |
129.7 ± 5.72 | 1.3; 0.26 | 1.26; 0.27 | ||
65.5 ± 4.5 | 59.5 ± 3.4 | 97.9 ± 4.4 |
70.6 ± 6.1 | 2.45; 0.13 | |||
49.6 ± 8.5 | 92.3 ± 14.8 | 93.9 ± 13.1 | 144.3 ± 14.2 | 0.05; 0.810 | |||
363.8 ± 40.9 | 374.7 ± 23.8 | 521.1 ± 31.6 | 412.6 ± 36.4 | 1.5; 0.235 | 3.4; 0.076 | 1.2; 0.268 | |
14.4 ± 0.8 | 12.2 ± 0.9 | 15.3 ± 0.2 |
10.4 ± 0.9 | 3.6; 0.068 | 3.6; 0.068 | ||
29 ± 1.5 | 22 ± 1.43 | 31.93 ± 1.6 |
20.1 ± 2.1 | 0.07; 0.8 | 1.56; 0.22 | ||
14.8 ± 1.4 | 10.1 ± 1.5 | 8.6 ± 0.6 |
6.4 ± 0.6 | 3.53; 0.07 | 0.68; 0.41 | ||
45.9 ± 3 | 54.5 ± 3.2 | 62.9 ± 3.3 |
68.2 ± 4 | 1.49; 0.23 | 0.22; 0.65 |
1Significantly different from leader in the same trial; Tukey HSD test
2Significantly different from its behavior in the lone trial; Tukey HSD test
Followers trailed the leaders; in 53% of the arrivals of a leader to a baited object, a follower rat arrived at the same object within 15 seconds, and in another 21% of arrivals the follower rat arrived at the same object in less than one minute. In 43% of arrivals of the leader to a baited object, the third rat also arrived at the same object (see for example Vidoeclip I and
The 16 objects are ranked on the abscissa according to the order in which each was visited, and the time of visiting each of the objects by each of the rats is given along the ordinate. Accordingly, for each object the order of symbols from bottom to top (time) reflects the order in which the rats arrived at that object. In the triad with one leader, the red rat (
In most trips to the objects, leader and follower rats tended to travel with one or two partners (75% and 76% of all trips, respectively). Moreover, in each of the shared trips, leaders and followers visited together most of the objects visited in that trip (74% and 73%, respectively). Altogether, the rats took most of the trips to objects together, mostly visiting the same objects in each of these shared trips. Similarly, the baits were usually collected during shared trips (see videoclip 1). Only 26% and 37% of the baits were collected, respectively, by leading and following rats during trips without partners, when only one of the rats was in the object zone and the other rat (or the other two other rats in the triad trial) were in the perimeter zone. These data demonstrate the tendency of the rats to travel together and visit the same objects in the same trips, regardless of being a leader or a follower. In other words, the rats that collected more baits during the trial ("leaders") did not acquire their status by traveling alone, but mainly by traveling ahead of their partners in shared trips.
In triads in which two of the rats were first to arrive at about the same number of objects, these leading rats shared, on average, about 79% ± 5% of the objects in each trip. That is, they mostly traveled together, temporally exchanging leadership between them, with being first at some point and eventually collecting the same number of baits (
Videoclip 1.
In the present study, 24 food-deprived rats were first trained individually to collect baits placed on each of 16 equispaced objects. Having learned to collect the baits, they were then tested with the 16 baited objects first as cage-mate dyads over four trials, and afterwards as triads of three rats that were unfamiliar to one another. We found that when tested in dyads or triads, the rats did not split up to collect the baits independently, but mostly traveled together to the various objects, with either one, or two of them in some triads, leading and arriving first at the majority of objects and collecting the baits. Nevertheless, regardless of which arrived first, the rats mostly traveled together (Videoclip 1) with no substantial difference among them in terms of their total activity. It would seem that rats in dyads and triads focus more on socializing, tending to travel to the objects with partner(s). In consequence, the time taken to collect all 16 baits was approximately the same for lone rats, dyads, or triads of rats. In terms of collecting baits, leading and following states in individual rats were exchanged over repeated trials. In other words, leading and following in collecting the baits were transient states that were usually preserved within a trial [specific session of testing a dyad] but changed across trials (subsequent testing of the same dyad). In the following discussion we interpret the puzzling preference of the food-deprived rats to travel together rather than splitting up and collecting the baits independently. We suggest that the change in "leadership" over trials, as observed in the present study, may reflect a sort of 'peace economy' in which all individuals equally benefit from the available resources over trials.
The present results offer a follow-up to our previous studies, which showed that rats prefer to travel together [
The present results do not provide substantial support for leadership and followership in rats. A social hierarchy with dominant and subordinate individuals characterizes rats, including laboratory rats [
When a rat dyad or triad was traveling, one or two of the rats followed and collected only a few baits, and sometimes not even one, yet the rats kept traveling together. A possible explanation for this could be that of the model of spontaneous emergence of leadership in foraging pairs [
Rats tend toward social affiliation, as revealed in early reports [
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We are grateful to Naomi Paz for language editing, and to Hezi Buba for his support in the experimentation.