Training vervet monkeys to avoid electric wires - Wiley Online Library

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Before being released into a large park enclosed by an electric fence, a wild-caught vervet group (Chlorocebus aethiops)
Zoo Biology 24:145–151 (2005)

Training Vervet Monkeys to Avoid Electric Wires: Is There Evidence for Social Learning? Tony Weingrill,n Coralie Stanisie`re, and Ronald Noe¨ Ethologie et Ecologie Comportementale des Primates, CEPE (CNRS UPR 9010), Universite´ Louis Pasteur, Strasbourg, France Before being released into a large park enclosed by an electric fence, a wild-caught vervet group (Chlorocebus aethiops) had to learn to avoid electrified wires in a smaller cage. During this training, we observed the group continuously for 12 consecutive days to investigate if social learning was involved in the learning process. Results showed that all monkeys received an electric shock (average ¼ 2.5 shocks/individual). Most contacts with the wires occurred during the first few days of training and the vervets were never observed to come into contact with the electric fence in the 18 months after their release into the large park. This suggests that the vervets learned to avoid the electrified wires by trial-and-error learning. It is possible that local and stimulus enhancement may have played a role, but we could not carry out the necessary control experiments to quantify the role of these components. Observational conditioning of fear can be ruled out, however, because the vervets did not show fearful behavior toward the wires. Zoo Biol c 2005 Wiley-Liss, Inc. 24:145–151, 2005. 

Key words: vervet; avoidance learning; social learning; electric fence

INTRODUCTION The Centre de Primatologie in Strasbourg has several large outdoor parks for non-invasive behavioral studies of primates. Electric fences enclose these parks to prevent the monkeys from escaping. Before new monkeys unfamiliar with electric fences are released into a park, they have to learn to avoid electroshocks in a smaller n

Correspondence to: Tony Weingrill, Anthropological Institute and Museum, University of Zurich, CH-8057 Zurich, Switzerland. E-mail: [email protected] Received 24 May 2004; Accepted 16 September 2004 DOI 10.1002/zoo.20041 Published online in Wiley InterScience (www.interscience.wiley.com).

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cage. We received a wild-reared vervet group from the Caribbean (St. Kitts) that also had to go through this training and we used this opportunity to investigate how fast vervets learn to avoid electric wires and whether indications of social learning can be witnessed. Learning to avoid touching an electric wire can be regarded as simple trial and error avoidance learning [Thorpe, 1963]. Because the whole group was present in the cage, however, it is also possible that social learning is involved in the learning process. The simplest mechanisms of social learning are local and stimulus enhancement [Zentall, 1996], where the attention of an observer is drawn to a particular place or an object. In the case of an aversive event, such as the electric shock in our experiment, this has been termed socially mediated aversive conditioning [Zentall, 1996]. An example of this is self-burying behavior to avoid biting flies in mice that can be acquired without previous experience by observing a ‘demonstrator’ mouse [Kavaliers et al., 2001]. Another possible mechanism of social learning is observational conditioning [Heyes, 1994], for example the acquisition of fear of snakes in monkeys [Mineka and Cook, 1988]. A fearful monkey serves as the unconditioned stimulus whereas the snake is the conditioned stimulus. When a naive monkey sees another individual react fearfully toward a snake, it might infer that the object is dangerous and that it too should be afraid. Thus, observational conditioning allows individuals to acquire persistent fear without coming into physical contact with snakes. Because we did not want to subdivide the socially stable vervet group that arrived recently and expose them longer than necessary to electrified wires, we could not carry out controlled experiments to distinguish between individual and social learning components. With these limitations in mind, we can nevertheless predict that if electric wire avoidance is learned mainly by asocial trial and error learning, then all monkeys should be observed to receive an electric shock. Social learning is likely to take place if only a few individuals are observed to touch the wires and the others show fearful behavior toward the wires without having received a shock in the past. MATERIALS AND METHODS A free-ranging social group of vervets was caught at St. Kitts in November 2001 and transported to the primate centre in May 2002. The group comprised of three males (one adult, two subadults), nine females, three juveniles, and two older infants. Initially the group was housed in a 12 m2 indoor compartment with an adjacent 15.8 m2 outdoor cage. These facilities are situated within a 0.5 ha park in which the animals were released after the training period. The vervet park is enclosed with a 2 m high fence. Attached to the fence are electrified wires. The current is provided by standard electric fence chargers used in agriculture (5,000 V, 32 mA). At the Strasbourg primate centre, newly acquired monkey groups are trained to avoid the electric wires before being released into the park. To achieve this, a similar set of wires as in the park is installed inside the outdoor cage (Fig. 1). The animals are usually left inside this setting for 2–3 weeks. Monkeys trained previously have shown no or very little initiative to climb the electrified park fences. With the electric wires we installed a neutral novel object in the cage as a control to determine whether the vervets generally avoided novel objects and after what time they became habituated. The control object was a 4-m

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Electric Wires

Control Rope

Entrances to Indoor Cage

Fig. 1. View of the outdoor cage with the positions of the installed electric wires and the control rope.

long orange-colored rope (diameter of 12 mm) and was attached along the side of the outdoor cage (Fig. 1). The training period lasted 23 days. During the first 12 days we observed the group continuously in the outdoor cage. In the evenings, and if the group was not under observation, the vervets were locked in the indoor facility. Data were collected for approximately 7.5 hr/day during weekdays and 5 hr on the weekend, yielding a total of 85 observation hr. We recorded every contact of the vervets with the electric fence and the control rope. In addition, every individual approaching the electrified wire closer than 20 cm was recorded. We also observed the behavior of the other group members present in the outdoor cage whenever an individual approached the wire. On Days 13–23, the animals were not observed permanently during their presence in the outdoor cage nor locked indoor over night. Due to rain, the group spent a larger proportion of time indoors and we only collected 9.5 hr of data during these days. The electric fence was dissembled on Day 23 and the group was released into the park the following day.

RESULTS Electric Shocks and Reactions Toward the Wires During the 12 fully observed days 16 of 17 monkeys touched the electric wire at least once (average ¼ 2.5 shocks). All shock events (n ¼ 42) for each individual are given in Table 1. The only female not touching the wires during this period was observed receiving a shock on Day 15. When animals received a shock, they jerked back and usually moved away from the wires. In 12% of all shock events they remained within 20 cm of the wires. The only vocalization emitted by shocked animals was a short scream in 19% of all shock events. Shocked animals never gave

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TABLE 1. Number of received electroshocks on the first 12 observation days for each individual of the study group Observation Day Age/Sex Class

ID

1

2

3

4

5

6

7

8

9

10

11

12

Males

Ga Fr Ma Br Do El Ni Oo Pa Ta Ve Zo Al Is Le Ky Co

1 — — — — 1 — — — — — — 1 1 — — 1

— — 1 — — 1 — — — 1 — — 2 — — 1 —

2 1 2 1 1 — — 2 1 — — — — — — 1 1

— 2 — — — 1 — — — — 1 — — — 1 — —

— — — 1 — 1 — — — 1 — — — — — 1 1

1 — — — — — — — — — 1 1 — — — — —

— — — — — — — — — — — 1 — — — — —

— — — — — — — — — — — — — — — — —

— — — — 1 — — — — — — — — — — — —

— — — — — — — — 1 — — — — — — — —

— — — — — 1 — — — — — — 1 — — — —

— — — — — — — — — 1 — — — — — — —

Females

Juveniles Infants

alarm calls. In addition, bystanders observing the incident never gave alarm calls before or after another individual approached the wires. This was also the case when the infants approached and received a shock, despite the presence of their mothers in the cage. In 31% of all cases, individuals close to shock receivers showed a reaction. They followed the shocked animal moving away from the wires or moved away from the receiver if he did not retreat from the wire. Approach and shock rates peaked during the first 3 days of training (Fig. 2). During the first week, animals received shocks significantly more often than during the second 6 days (Wilcoxon signed rank test, Z ¼ 3.2, n ¼ 17, Po0.001), with an average rate per individual of 0.05 shocks/hr during the first half and 0.01 shocks/hr during the second half. Similar to the shock rates, the frequency of approaches within 20 cm of the wires decreased in the second half of the first 12 training days (Wilcoxon signed rank test, Z ¼ 2.9, n ¼ 17, Po0.01). Control Object In contrast to the electric wires, the rope was never voluntarily touched during the first 12 days; only five individuals touched it with their tail while climbing over it. Generally, all animals seemed to take care to avoid the rope. Some juveniles directed an alarm call at the rope, a behavior that was never directed toward the electric wires. In the third week the infants and juveniles started playing with the rope and some adults touched and inspected it. Post Training Period After 3 weeks in the cage the group was released into the park, where we continued to make observations over the following 18 months. We collected

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149 1.8

approaches 1.6

shocks 25

1.4

1.2

1 15 0.8

10

shocks/hour

approaches/hour

20

0.6

0.4 5 0.2

0

0 1

2

3

4

5

6

7

8

9

10

11

12

day

Fig. 2. Hourly rates of approaches within 20 cm of the electric fence (bars) and of received shocks (line). The rates represent group totals for each observation day.

behavioral data for over 1,000 hr and never saw a vervet coming into contact with the electric wires. During this period 12 infants were born and did not undergo the electric fence training. Four of these infants were observed to climb the fence once each but were pulled away by their mother before reaching the electrified wires. Otherwise no vervets were observed to climb the fence. DISCUSSION All individuals touched the electric wires at least once during the training. On average, the vervets received 2.5 shocks before avoiding the wires. This suggests that avoiding the electric wires was mainly learned by trial and error. Nevertheless, social learning cannot be ruled out. It is possible that the study animals performed better within the group (i.e., received fewer shocks) than they would have in isolation, either trough observational conditioning or through other simple learning mechanisms, such as drawing attention to a place or an object associated with reinforcement. To investigate if social learning has played a role in our experiment we should have compared the outcome of this experiment with the performance of

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individuals without the presence of other group members. This was not possible in this study (see Introduction). Although social avoidance learning cannot be ruled out entirely, observational conditioning probably did not play a major role in our experiment for the following reasons. First, the electric wires were present throughout the experiment and did not differ much from the wire screen of the cage. It seems unlikely that observational conditioning takes place if the conditioned stimuli, in this case the electric wires, are always visible to the animals. Second, vervets receiving a shock did not show any fearful behavior toward the wires besides withdrawing rapidly in some cases. Thus, fearful demonstrators, representing the unconditioned stimuli needed for observational conditioning [Mineka and Cook, 1993], were absent in our study. In addition, bystanders probably often did not observe shock receivers touching the wire and only looked at them after they showed a reaction, therefore being unable to make the connection between the wires and the retreating animals. Much research has been directed on selective associations in observational conditioning [Domjan and Galef, 1983; LoLordo and Droungas, 1989]. More specifically, Cook and Mineka [1990] have demonstrated that selective associations also occur in the observational conditioning of fear. In their study, monkeys watched edited videotapes showing other monkeys reacting fearful to snakes and flowers. The observers acquired fear of snakes but not of flowers, indicating that monkeys cannot associate all stimuli with fear trough social learning. Thus, a further explanation for the absence of observational conditioning in this study is that the wires do not resemble stimuli that the monkeys would naturally encounter (e.g., snakes or biting/ stinging insects). In contrast, the colorful rope that was placed in the cage as a control object may have resembled a snake. Although most contacts with the electric wires occurred during the first days of the training, the rope was not touched during the first 12 days and alarm calls were directed against it.

CONCLUSIONS The training of vervet monkeys to avoid electric wires was highly efficient. During a period of 12 days each monkey received on average 2.5 electric shocks. Throughout the following 18 months the monkeys were situated in a large park enclosed with an electric fence and they were never observed to come into contact with it. Although the vervets observed other individuals receiving an electric shock during training, each monkey touched the electric wire. We conclude that they learned the task by trial and error learning. Because we did not compare these results with the performance of isolated individuals, however, an effect of social avoidance learning cannot be ruled out entirely.

ACKNOWLEDGMENTS We wish to thank the staff of the Centre de Primatologie, Strasbourg, for technical support and Y. Gobrecht for the drawing of the outdoor cage. We have complied with the ethical standards in the treatment of animals as laid down by the Guidelines for the Use of Animals in Research, published in Animal Behaviour (Vol. 43, 1992).

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