A Case Study Employing Operant Conditioning to Reduce Stress of Capture for Red-Bellied Tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

The development of an operant conditioning training program for new world primates at the Bronx Zoo

This article describes the development of an operant conditioning training program for 17 species of New World primates at the Bronx Zoo. To apply less invasive techniques to husbandry protocols, the study introduced behaviors-hand feeding, syringe feeding, targeting, scale and crate training, and transponder reading-for formal training to 86 callitrichids and small-bodied cebids housed in 26 social groups. Individual responses to training varied greatly, but general patterns were noted among species. With the exception of lion tamarins, tamarins responded more rapidly than marmosets, Bolivian gray titi monkeys, and pale-headed saki monkeys in approaching trainers and learning behaviors. Marmosets, in comparison to most tamarins, had longer attention spans. This meant that fewer, lengthier sessions were productive whereas shorter, more frequent sessions were most successful for tamarins. Among the cebids, pale-headed saki monkeys needed relatively few sessions to perform basic and advanced behaviors whereas Bolivian gray titi monkeys were less responsive and progressed at a deliberate pace. Marked changes in the animals' behavior during daily husbandry procedures, their voluntary participation in training activities, and the disappearance of aggressive threats toward care staff indicated that training reduced stress and improved the welfare of the animals. During daily training displays, zoo visitors experienced interactive animals while learning the importance of low-stress animal husbandry.     

Positive Reinforcement Training in Squirrel Monkeys Using Clicker Training

Nonhuman primates in research environments experience regular stressors that have the potential to alter physiology and brain function, which in turn can confound some types of research studies. Operant conditioning techniques such as positive reinforcement training (PRT), which teaches animals to voluntarily perform desired behaviors, can be applied to improve behavior and reactivity. PRT has been used to train rhesus macaques, marmosets, and several other nonhuman primate species. To our knowledge, the method has yet to be used to train squirrel monkeys to perform complex tasks. Accordingly, we sought to establish whether PRT, utilizing a hand‐box clicker (which emits a click sound that acts as the conditioned reinforcer), could be used to train adult male squirrel monkeys (Saimiri boliviensis, N = 14). We developed and implemented a training regimen to elicit voluntary participation in routine husbandry, animal transport, and injection procedures. Our secondary goal was to quantify the training time needed to achieve positive results. Squirrel monkeys readily learned the connection between the conditioned reinforcer (the clicker) and the positive reinforcer (food). They rapidly developed proficiency on four tasks of increasing difficulty: target touching, hand sitting, restraint training, and injection training. All subjects mastered target touching behavior within 2 weeks. Ten of 14 subjects (71%) mastered all tasks in 59.2 ± 2.6 days (range: 50–70 days). In trained subjects, it now takes about 1.25 min per monkey to weigh and administer an intramuscular injection, one‐third of the time it took before training. From these data, we conclude that clicker box PRT can be successfully learned by a majority of squirrel monkeys within 2 months and that trained subjects can be managed more efficiently. These findings warrant future studies to determine whether PRT may be useful in reducing stress‐induced experimental confounds in studies involving squirrel monkeys. Am. J. Primatol. 74:712–720, 2012. © 2012 Wiley Periodicals, Inc.     

Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness

Many suggest that operant conditioning techniques can be applied successfully to improve the behavioral management of nonhuman primates in research settings. However, relatively little empirical data exist to support this claim. This article is a review of several studies that discussed applied positive reinforcement training techniques (PRT) on breeding/research colonies of rhesus macaques (Macaca mulatta) and chimpanzees (Pan troglodytes) at The University of Texas M. D. Anderson Cancer Center and measured their effectiveness. Empirical analyses quantified the amount of time required to train rhesus monkeys to come up, station, target, and stay. Additionally, a study found that time spent affiliating by female rhesus was changed as a function of training low affiliators to affiliate more and high affiliators to affiliate less. Another study successfully trained chimpanzees to feed without fighting and to come inside on command. PRT is an important behavioral management tool that can improve the care and welfare of primates in captivity. Published empirical findings are essential for managers to assess objectively the utility of positive reinforcement training techniques in enhancing captive management and research procedures.     

Ground-reaction-force profiles of bipedal walking in bipedally trained Japanese monkeys

Ground-reaction-force (GRF) profiles of bipedal locomotion in bipedally trained Japanese macaques (performing monkeys) were analyzed in order to clarify the dynamic characteristics of their locomotion. Five trained and two ordinary monkeys participated in the experiment. They walked on a wooden walkway at a self-selected speed, and three components of the GRF vector were measured using a force platform. Our measurements reveal that trained monkeys exhibited vertical-GRF profiles that were single-peaked, similar to those of ordinary monkeys; they did not generate the double-peaked force curve that is seen in humans, despite their extensive training. However, in the trained monkeys, the peak appeared relatively earlier in the stance phase, and overall shape was more triangular than that of the more parabolic profile generated by ordinary monkeys. Comparisons of vertical fluctuation of the center of body mass calculated from the measured profiles suggest that this was larger in the trained monkeys, indicating that storage and release of potential energy actually took place in their bipedal walking. This energetic advantage seems limited, however, because efficient exchange of potential and kinetic energy during walking were not completely out of phase as in human walking. We suggest that anatomically restricted range of hip-joint motion impedes the inherently quadrupedal monkeys from generating humanlike bipedal locomotion, and that morphological rearrangement of the hip joint was an essential precondition for protohominids to acquire humanlike bipedalism.     

Effects of positive reinforcement training techniques on the psychological welfare of zoo‐housed chimpanzees (Pan troglodytes)

Captive environments encompass various factors that can elevate stress levels and jeopardize the wellbeing of the captive animals. The use of positive reinforcement training (PRT) techniques enables researchers and caretakers to reduce tension directly associated with potentially stressful procedures and states. The current study tested the general effect of PRT on the wellbeing of zoo‐housed chimpanzees (Pan troglodytes) by measuring behaviors that reflect poor and good welfare and that were not directly connected to the specific aim of the training session. The behavior of a group of twelve chimpanzees was measured throughout the day from the exhibition yard, at baseline (12 weeks) and during the PRT period (10 weeks). The results show a significant decrease in abnormal and stress‐related behaviors and a significant rise in prosocial affiliative behaviors following implementation of the training program. The training was shown to have a greater positive effect on low‐ranking individuals compared with high‐ranking ones. This research shows for the first time that PRT offers an enrichment effect whose general influence lasts throughout the day, irrespective of any direct link to a specific trained behavior. Consequently, it can be claimed that PRT presents an effective enrichment tool that can be implemented with captive animals. Because of the above‐noted differential effect between high‐ and low‐ranking chimpanzees, however, this should be taken into consideration when combining PRT with the non‐human primates' daily routine. Am. J. Primatol. 71:687–695, 2009. © 2009 Wiley‐Liss, Inc.     

Brief threatening events beneficial for captive tamarins?

To evaluate speculation indirectly suggesting that brief arousal may be beneficial to animals, 39 cotton-top tamarins (Saguinus oedipus) living in 4 large families were observed (a) after normal husbandry procedures that excite them (capture and brief removal of infants or older monkeys), (b) after exposure to an over-flying bird model, and (c) compared with control days in which neither of the above occurred. Both arousal conditions caused a decrease in play and locomotion, and an increase in grooming and contact during the remainder of the day. These behavioral changes are similar to the patterns reported as positive effects of enrichment but are dissimilar to negative effects of long-term stressors reported. The pattern of changes in studies of enrichment and of stress enables more objective evaluation of ambiguous events.     

Parasitic Robot System for Waypoint Navigation of Turtle

In research on small mobile robots and biomimetic robots,locomotion ability remains a major issue despite many advances in technology.However,evolution has led to there being many real animals capable of excellent locomotion.This paper presents a "parasitic robot system" whereby locomotion abilities of an animal are applied to a robot task.We chose a turtle as our first host animal and designed a parasitic robot that can perform "operant conditioning".The parasitic robot,which is attached to the turtle,can induce object-tracking behavior of the turtle toward a Light Emitting Diode (LED) and positively reinforce the behavior through repeated stimulus-response interaction.After training sessions over five weeks,the robot could successfully control the direction of movement of the trained turtles in the waypoint navigation task.This hybrid animal-robot interaction system could provide an alternative solution to some of the limitations of conventional mobile robot systems in various fields,and could also act as a useful interaction system for the behavioral sciences.     

Can Auditory Playback Condition Predator Mobbing in Captive-reared <Emphasis Type="Italic">Saguinus oedipus</Emphasis>?

Captive reintroductions often suffer high mortality, with predation as one source. Many species learn about predators; thus training captive-born animals to recognize predators may increase survivorship. We adapted variants of methods developed for birds to attempt to condition monkeys to mob a predator. Captive-reared cotton-top tamarins (Saguinus oedipus) did not differentiate between a snake and a rat, confirming previous research that naïve cotton-top tamarins do not fear snakes. Tamarins then viewed a living snake during playback of mobbing calls. In posttests, tamarins did not mob the snake. We then eliminated the pretest to avoid potential habituation and placed a stillborn tamarin with the snake in an attempt to heighten arousal. In posttests, tamarins again did not mob the snake, although they did increase their rates of calls, indicating mild arousal. Overall, none of 8 groups of cotton-top tamarins learned to mob a predator. Potential reasons for failure include conditioning multiple subjects at once and the lack of an experienced demonstrator. Observing a demonstrator was not necessary for birds to acquire mobbing, but may be necessary for tamarins.     

Effects of training on stress-related behavior of the common marmoset (Callithrix jacchus) in relation to coping with routine husbandry procedures

Using positive reinforcement, J. McKinley trained 12 common marmosets (Callithrix jacchus) to provide urine samples on request. The study then exposed the marmosets to mildly stressful, routine husbandry procedures (i.e., capture and weighing). The nonhuman animals spent less time inactive poststressor as opposed to prestressor. L. Bassett collected matched behavioral data from 12 nontrained marmosets who were less accustomed to human interaction. These animals spent significantly more time self-scratching and locomoting as well as less time inactive, poststressor. Collapsed data from the 2 populations showed increased scent marking, poststressor. These results suggest that locomotion, self-scratching, and scent marking are useful, noninvasive behavioral measures of stress and, thus, reduced welfare in the common marmoset. Overall, nontrained animals showed more self-scratching than did their trained counterparts. It was not possible to collect urine from nontrained marmosets. In response to the stressor, however, trained animals showed no significant change in excreted urinary cortisol. These results suggest that training marmosets may allow them to cope better with routine laboratory procedures.     

The significant features of Japanese macaque coo sounds: a psychophysical study

Japanese macaques, Macaca fuscata, were trained with a positive reinforcement operant procedure to discriminate smooth early high and smooth late high coo sounds recorded during Green's (1975) field study of the speices' vocal repertoire. Subjects labelled the various tokens by maintaining contact with a response device for calls from one category and by breaking contact for those of the second call type. After the completion of discrimination training, the generalization of the operant behaviour to novel natural and synthetic vocalizations was measured. Initial generalization tests established that macaques would respond appropriately both to natural vocalizations and to computer-synthesized prototypes representing the smooth early high-smooth late high contrast. In subsequent tests, individual acoustic features were removed from the synthetic prototypes to determine the minimal elements of functional coo sounds. These tests suggested that those sounds are distinguished by the predominant direction of their frequency change which, in turn, is determined by the temporal position of their highest frequency.     

Color discrimination by the cotton-top tamarin (Saguinus oedipus oedipus) and its relation to fruit coloration

Old World monkeys and apes have been reported to differ from New World monkeys in their abilities to discriminate colors across the visible spectrum. Old World monkeys and apes (Macaca, Pan, Pongo) discriminate colors quite accurately, while some New World monkeys studied (Saimiri, Cebus) have shown lower sensitivity to and poorer discrimination of long wavelength light. This study examined the color discrimination ability of another New World primate, the cotton-top tamarin, Saguinus oedipus oedipus (family Callitrichidae). The tamarins were trained to discriminate a set of Munsell color chips, both within the same hue category and from the 2 hue categories on either side of the training hue. Results indicated that the cotton-top tamarin can make accurate discriminations across the visible spectrum. Human subjects were tested under similar conditions in order to compare their color discrimination abilities to those of the tamarins. The tamarins and human subjects had the most difficulty discriminating the same hues. The discrimination abilities of the monkeys were assessed in relation to the coloration of fruits eaten in a natural environment. A list of the species of fruits commonly eaten by various species of New World monkeys was compiled and the coloration of fruits at maturity was noted. It was found that most New World primate species eat fruits whose mature coloration ranges across most of the spectrum.     

Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes)

Positive reinforcement training (PRT) techniques have received considerable attention for their stress reduction potential in the behavioral management of captive nonhuman primates. However, few published empirical studies have provided physiological data to support this position. To address this issue, PRT techniques were used to train chimpanzees (Pan troglodytes) to voluntarily present a leg for an intramuscular (IM) injection of anesthetic. Hematology and serum chemistry profiles were collected from healthy chimpanzees (n=128) of both sexes and various ages during their routine annual physical examinations over a 7-year period. Specific variables potentially indicative of acute stress (i.e., total white blood cell (WBC) counts, absolute segmented neutrophils (SEG), glucose (GLU) levels, and hematocrit (HCT) levels) were analyzed to determine whether the method used to administer the anesthetic (voluntary present for injection vs. involuntary injection) affected the physiological parameters. Subjects that voluntarily presented for an anesthetic injection had significantly lower mean total WBC counts, SEG, and GLU levels than subjects that were involuntarily anesthetized by more traditional means. Within-subjects analyses revealed the same pattern of results. This is one of the first data sets to objectively demonstrate that PRT for voluntary presentation of IM injections of anesthetic can significantly affect some of the physiological measures correlated with stress responses to chemical restraint in captive chimpanzees.     

Discrimination of Ultrasonic Vocalizations by CBA/CaJ Mice (Mus musculus) Is Related to Spectrotemporal Dissimilarity of Vocalizations

The function of ultrasonic vocalizations (USVs) produced by mice (Mus musculus) is a topic of broad interest to many researchers. These USVs differ widely in spectrotemporal characteristics, suggesting different categories of vocalizations, although this has never been behaviorally demonstrated. Although electrophysiological studies indicate that neurons can discriminate among vocalizations at the level of the auditory midbrain, perceptual acuity for vocalizations has yet to be determined. Here, we trained CBA/CaJ mice using operant conditioning to discriminate between different vocalizations and between a spectrotemporally modified vocalization and its original version. Mice were able to discriminate between vocalization types and between manipulated vocalizations, with performance negatively correlating with spectrotemporal similarity. That is, discrimination performance was higher for dissimilar vocalizations and much lower for similar vocalizations. The behavioral data match previous neurophysiological results in the inferior colliculus (IC), using the same stimuli. These findings suggest that the different vocalizations could carry different meanings for the mice. Furthermore, the finding that behavioral discrimination matched neural discrimination in the IC suggests that the IC plays an important role in the perceptual discrimination of vocalizations.     

Quantitative data on training new world primates to urinate

This study assessed the effectiveness of operant conditioning in training three species of captive callitrichid primates (Leontopithecus rosalia, Callithrix geoffroyi, and Saguinus imperator) to urinate on demand. There were three goals to the study: 1) to develop a system for quantitatively assessing positive reinforcement training; 2) to ascertain whether or not positive reinforcement techniques can be used to train callitrichid monkeys to urinate on demand, and if so, how many training sessions are required; and 3) to determine the effect on urination behavior of the trainer entering the cage to collect a urine sample. Positive reinforcement with a continuous reinforcement schedule was used to capture a natural behavior: urination. Training sessions (30 min each) were conducted at dawn thrice weekly during five consecutive phases: habituation, control, training (animals were rewarded for urinating), maintenance (animals had reached a defined training criteria and continued to be rewarded for urinating), and collection (animals were rewarded for urinating, and the trainer entered the cage to collect the sample). The numbers of 30-min training sessions required to train the three monkey species (L. rosalia, C. geoffroyi, and S. imperator) were five, six, and eight, respectively. For the three species, the mean number of urinations per animal was significantly greater during the training, maintenance, and collection phases compared to the control phase. However, the three species differed significantly in the manner in which the rates of urination changed across the five phases. A higher proportion of subjects urinated during the training, maintenance, and collection phases compared to the control phase. Latency to first urination varied significantly across the five phases, with significantly reduced latencies to urinate during the training, maintenance, and collection phases compared to the control phase. The entry of the trainer into the cage to collect the urine sample did not appear to alter urination behavior. We demonstrate that operant conditioning techniques, which typically incur minimal cost, time investment, and disturbance, can be used to increase the quantity of urine samples collected for physiological analysis, the proportion of animals that urinate, and the speed of sample collection.     

Vocal individual discrimination in Japanese monkeys

The present study determines which features of the coo call are used by Japanese monkeys Macaca fuscata for vocal individual discrimination. First, two female Japanese monkeys were trained to discriminate conspecific individuals vocally, using an operant conditioning. Using as stimuli three unknown individuals with 30 calls per individual, the two monkeys succeeded in discriminating new call exemplars from the three stimulus individuals. A discriminant analysis performed on calls used as stimuli indicated that start frequency of the fundamental and call duration were variables that can differentiate individuals efficiently. Then, playbacks of acoustically modified signals were used to indicate which vocal features are used by monkeys for the individual discrimination. Stimuli signals containing modified pitch or duration, or filtered so as to keep only the fundamental component, were tested. Results indicated that Japanese monkeys use multiple acoustical cues to perform vocal individual discrimination, including at least pitch, call duration, and harmonics. However, harmonics seem to be less important for discrimination than pitch and call duration.     

An Operant Conditioning Method for Studying Auditory Behaviors in Marmoset Monkeys

The common marmoset (Callithrix jacchus) is a small New World primate that has increasingly been used as a non-human model in the fields of sensory, motor, and cognitive neuroscience. However, little knowledge exists regarding behavioral methods in this species. Developing an understanding of the neural basis of perception and cognition in an animal model requires measurement of both brain activity and behavior. Here we describe an operant conditioning behavioral training method developed to allow controlled psychoacoustic measurements in marmosets. We demonstrate that marmosets can be trained to consistently perform a Go/No-Go auditory task in which a subject licks at a feeding tube when it detects a sound. Correct responses result in delivery of a food reward. Crucially, this operant conditioning task generates little body movement and is well suited for pairing behavior with single-unit electrophysiology. Successful implementation of an operant conditioning behavior opens the door to a wide range of new studies in the field of auditory neuroscience using the marmoset as a model system.     

Operant conditioning in the ant Myrmica sabuleti

Operant conditioning could be obtained in the ant Myrmica sabuleti by presenting to the workers, during a six-day period, an apparatus containing either sugared water or meat as a reward. The conditioning obtained using sugared water as a reward was short lasting. A reconditioning was more persistent and lasted four hours. The ants' response was very precise, since they exhibited it only in front of an apparatus identical to that used during the training phase. Operant conditioning obtained using meat as a reward was more pronounced than that obtained by using sugared water, probably because meat is more valuable as a reward than sugar for the species studied, which is essentially a carnivorous one. Such a conditioning was rather persistent. Indeed, a first operant conditioning obtained by using meat as a reward could still be detected after seven hours, and a reconditioning was still significant after eight hours. One day after this eight-hour period without rewarding the ants, the response was higher again and a further day later, it was still significant. Since the operant conditioning is easy to perform and quantify and since the ants' response is very precise, such a conditioning can be used for further studying M. sabuleti workers' visual perception.     

Kinematic analysis of bipedal locomotion of a Japanese macaque that lost its forearms due to congenital malformation

Spontaneously acquired bipedal locomotion of an untrained Japanese monkey (Macaca fuscata) is measured and compared with the elaborated bipedal locomotion of highly trained monkeys to assess the natural ability of a quadrupedal primate to walk bipedally. The subject acquired bipedalism by himself because of the loss of his forearms and hands due to congenital malformation. Two other subjects are performing monkeys that have been extensively trained for bipedal posture and locomotion. We videotaped their bipedal locomotion with two cameras in a lateral view and calculated joint angles (hip, knee, and ankle) and inertial angle of the trunk from the digitized joint positions. The results show that all joints are relatively more flexed in the untrained monkey. Moreover, it is noted that the ankle is less plantar flexed and the knee is more flexed in mid-to-late stance phase in the untrained monkey, suggesting that the trunk is not lifted up to store potential energy. In the trained monkeys, the joints are extended to bring the trunk as high as possible in the stance phase, and then stored potential energy is exchanged for kinetic energy to move forward. The efficient inverted pendulum mechanism seems to be absent in the untrained monkeys locomotion, implying that acquisition of such efficient bipedal locomotion is not a spontaneous ability for a Japanese monkey. Rather, it is probably a special skill that can only be acquired through artificial training for an inherently quadrupedal primate.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Reactions of zoo visitors to free-ranging monkeys

This study assessed the potential of two types of primate exhibit both for enhancing zoo visitors' interest, knowledge, and enjoyment and for promoting conservation education. Visitors' reactions to a free-ranging group of cotton-top tamarins were compared with their responses to caged tamarins in three ways: 1) timing how long visitors spent at each exhibit, 2) recording the comments made by visitors about the exhibits, and 3) asking visitors to respond to questionnaires about the two exhibits. The results showed that the free-ranging group of tamarins provoked wider comment from members of the public than caged groups and that visitors were willing to spend much more time looking for and watching monkeys in trees than monkeys in cages. Visitors felt that improvements in the animals' welfare were obtained from allowing them to live free in the trees, thought that they could learn more from such groups than from caged animals, and enjoyed seeing the free-ranging tamarins more than the monkeys in cages. These results suggest that developing more naturalistic zoo exhibits can have considerable benefits not only for the animals involved, but also for public education in conservation issues. © 1994 Wiley-Liss, Inc.