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.     

The effects of the distribution of training on learning feedback-assisted cardiac acceleration

In order to test a hypothesis derived from a motor skills learning model of cardiac acceleration control, groups of subjects were given biofeedback training for four sessions to learn cardiac acceleration under four different training schedules: (1) all sessions in one day, (2) daily sessions, (3) sessions every other day, and (4) weekly sessions. Ability to accelerate heart rate both with and without feedback was determined at each session. Also ability to accelerate heart rate without feedback was determined 1 week after the last training session as a measure of retention. Although there was highly significant (p less than.0001) evidence of heart rate control both with and without feedback, there were no differences in degree of control attributable to distribution of training sessions. There was, however, a trend (p less than .10) for subjects trained under the most distributed training schedule (weekly) to show more retention than subjects trained under a less distributed schedule (daily).     

Case study: Training a chimpanzee (Pan troglodytes) to use a nebulizer to aid the treatment of airsacculitis

Bacterial airsacculitis has been reported in a variety of nonhuman primates, and is widely treated using a combination of surgery and oral antibiotics. This case study details an alternative method of administering antibiotics (via the use of a nebulizer) when the chimpanzee subject developed resistance to all available oral preparations. Training the chimpanzee to use the nebulizer was performed using positive reinforcement techniques (PRT). It took a total of 89 sessions (<7 hr 25 min) to train the chimpanzee to use the nebulizer. The airsacculitis infection was treated using colistin in the nebulizer twice a day for 9 days. Out of 18 potential treatment sessions, full doses were administered on 13 occasions. The final dose of colistin was given via slow brachial intravenous injection under general anesthesia. The infection was successfully treated with colistin. Although there was a training time investment involved, it was felt to be outweighed by the success of the treatment. Also in the likelihood of the infection re-occurring at a later date, the now learnt behavior of using a nebulizer means that future treatment should now be considerably quicker. This is another example of how PRT is a useful tool in the successful welfare and management of captive animals.     

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.     

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.     

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.     

Effect of exercise training on swimming performance,survival under predation and hypoxia tolerance in an endangered fish species in China

Poor swimming performance and low hypoxia tolerance have been suggested as the main reasons for the dramatic decrease in the wild population of Chinese sucker. The present study aimed to investigate the potential for exercise training to enhance swimming performance and hypoxia tolerance in this fish species targeted for stocking enhancement. Fish were exercise trained (force to swim against a flow) once daily, twice daily or not exercise trained for 20 d and then detrained for 10 d (a period of nontraining). Training showed no significant effect on anaerobic swimming performance.. The fish from both training groups showed lower hypoxia tolerance and a lower survival rate under predation. Thus, the present study suggested thatexercise training showed little effect or even a negative effect on physiological function in Chinese sucker, and the forced training might not be the proper protocol to apply for improving the stocking enhancement of Chinese sucker..     

Successful implementation of cooperative handling eliminates the need for restraint in a complex non-human primate disease model

Background Streptozotocin‐induced diabetic non‐human primates are used to study efficacy and safety of innovative immunosuppression after islet transplantation. We implemented a training program for medical management of a chronic disease state. Methods Cooperation with hand feeding and drinking, shifting, and limb presentation were trained utilizing predominately positive but also negative reinforcement in 52 animals compared with 28 macaques subjected to conventional physical and/or chemical restraint. The success and timing of behavior acquisition was evaluated in a representative subset of 14 animals. Results Over 90% of animals were successful in behavior acquisition. Programmatically this resulted in complete elimination of chair restraint and negligible requirement for sedation. About half of the trained animals had no‐to‐moderate thymic involution, indicative of a substantial reduction in stress. Conclusion Cooperative handling enhances animal well‐being. This contributes to validity of scientific results and eliminates model‐induced confounding that can obstruct interpretation of safety and efficacy data.     

Positive Reinforcement Training for a Trunk Wash in Nepal's Working Elephants: Demonstrating Alternatives to Traditional Elephant Training Techniques

Many trainers of animals in the zoo now rely on positive reinforcement training to teach animals to voluntarily participate in husbandry and veterinary procedures in an effort to improve behavioral reliability, captive management, and welfare. However, captive elephant handlers in Nepal still rely heavily on punishment- and aversion-based methods. The aim of this project was to determine the effectiveness of secondary positive reinforcement (SPR) in training free-contact elephants in Nepal to voluntarily participate in a trunk wash for the purpose of tuberculosis testing. Five female elephants, 4 juveniles and 1 adult, were enrolled in the project. Data were collected in the form of minutes of training, number of offers made for each training task, and success rate for each task in performance tests. Four out of 5 elephants, all juveniles, successfully learned the trunk wash in 35 sessions or fewer, with each session lasting a mean duration of 12 min. The elephants' performance improved from a mean success rate of 39.0% to 89.3% during the course of the training. This study proves that it is feasible to efficiently train juvenile, free-contact, traditionally trained elephants in Nepal to voluntarily and reliably participate in a trunk wash using only SPR techniques.     

Generalization and discrimination of positive and negative acoustic stimuli in the common carp (Cyprinus carpio)

Groups of common carp (Cyprinus carpio) were trained for 33 days to discriminate between two acoustic signals differing in frequency and temporal pattern. One signal (positive stimulus) was reinforced by food, while the other (negative stimulus) was not rewarded. When exposed to 3 positive and 3 negative stimuli per day (training Paradigm 1) the fish responded similarly to the two signals. When daily negative stimuli outnumbered positive stimuli (3 positive and 33 negative, training Paradigm 2) the fish responded similarly to the two signals for the first 2 weeks and then began to discriminate between them. Discriminatory response was statistically significant from Day 21 of training. After 33 days, training was switched from Paradigm 2 to Paradigm 1 and the fish maintained their discriminatory capability. The results are interpreted in terms of anticipatory frustration and risk management.     

Temperament correlates with training success in adult rhesus macaques

In recent years there has been a marked increase in awareness of issues involving the psychological well-being of nonhuman primates (NHPs) used in biomedical research. As a result, many facilities are starting to train primates to voluntarily cooperate with veterinary, husbandry, and research procedures, such as remaining still for blood draws or injections. Such training generally reduces the stress associated with these procedures, resulting in calmer animals and, ultimately, better research models. However, such training requires great investments in time, and there can be vast individual differences in training success. Some animals learn tasks quickly, while others make slower progress in training. In this study, we examined whether temperament, as measured by response to a novel food object, correlated with the amount of time it took to train 20 adult female rhesus macaques to perform a simple task. The monkeys were categorized as "exploratory" (i.e., inspected a novel object placed in the home cage within 10 sec), "moderate" (i.e., inspected the object within 10-180 sec), or "inhibited" (i.e., did not inspect the object within 3 min). We utilized positive reinforcement techniques to train the monkeys to touch a target (PVC pipe shaped like an elbow) hung on their cage. Temperament correlated with training success in this study (Pearson chi2=7.22, df=2, P=0.03). We easily trained over 75% of the animals that inspected the novel food (i.e., exploratory or moderate individuals) to touch the target. However, only 22% of the inhibited monkeys performed the task. By knowing which animals may not respond to conventional training methods, we may be able to develop alternate training techniques to address their specific needs. In addition, these results will allow us to screen monkeys to be assigned to research projects in which they will be trained, with the goal of obtaining the best candidates for those studies.     

Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques.

Social housing, whether continuous, intermittent, or partial contact, typically provides many captive primates with opportunities to express affiliative behaviors, important components of the species-typical behavioral repertoire. Positive reinforcement training techniques have been successfully employed to shape many behaviors important for achieving primate husbandry goals. The present study was conducted to determine whether positive reinforcement training techniques could also be employed to alter levels of affiliative interactions among group-housed rhesus macaques. Twenty-eight female rhesus were divided into high (n = 14) and low (n = 14) affiliators based on a median split of the amount of time they spent affiliating during the baseline phase of the study. During the subsequent training phase, half of the low affiliators (n = 7) were trained to increase their time spent affiliating, and half of the high affiliators (n = 7) were trained to decrease their time spent affiliating. Trained subjects were observed both during and outside of training sessions. Low affiliators significantly increased the amount of time they spent affiliating, but only during nontraining sessions. High affiliators on the other hand, significantly decreased the amount of time they spent affiliating, but only during training sessions. These data suggest that positive reinforcement techniques can be used to alter the affiliative behavior patterns of group-housed, female rhesus monkeys, although the two subgroups of subjects responded differently to the training process. Low affiliators changed their overall behavioral repertoire, while high affiliators responded to the reinforcement contingencies of training, altering their proximity patterns but not their overall behavior patterns. Thus, positive reinforcement training can be used not only as a means to promote species-typical or beneficial behavior patterns, but also as an important experimental manipulation to facilitate systematic analyses of the effects of psychosocial factors on behavior and potentially even immunology.     

Differences between simultaneous and blocked training detected by a transfer test

Secondary data analysis was used to compare responding early on a transfer test from rats previously trained simultaneously or successively on multiple temporal discriminations for the same number of trials [Guilhardi, P., Church, R.M., 2005 a. Dynamics of temporal discrimination. Learn. Behav., 33, 399-416]. Three fixed intervals (30, 60, and 120 s) were signaled by three stimuli (light, noise, and clicker). Twelve rats were trained with the three stimulus-interval pairs intermixed on each experimental session (simultaneous condition); 12 other rats were trained in successive blocks of 10 sessions on each pair (blocked condition). Then, all rats had a transfer test in which all three stimulus-interval pairs were presented intermixed on each session. Rats in the simultaneous and blocked condition responded similarly during training, but differently during early stages of the transfer test. One possibility is that rats in the blocked condition were controlled by the previous interval, not by the current stimulus. These results challenge the usual assumptions from models of timing and conditioning that both simultaneous and blocked training produce learning of the associations between stimulus and interval in a multiple interval training task.     

Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: ease of training and time investment

The first author trained 12 laboratory-housed common marmosets (Callithrix jacchus) in pairs to assess the practicality of positive reinforcement training as a technique in the management of these nonhuman animals. Behaviors taught were (a) target training to allow in homecage weighing and (b) providing urine samples. Between 2 to 13, 10-minute training sessions established desired behaviors. Training aggressive animals only after they had been fed eliminated aggression during training. Trained animals proved extremely reliable, and data collection using trained animals was considerably faster than collection using current laboratory techniques. The results suggest that positive reinforcement training is a practical option in the management of laboratory-housed marmosets.     

Metformin blunts muscle hypertrophy in response to progressive resistance exercise training in older adults: A randomized,double‐blind,placebo‐controlled,multicenter trial: The MASTERS trial

Progressive resistance exercise training (PRT) is the most effective known intervention for combating aging skeletal muscle atrophy. However, the hypertrophic response to PRT is variable, and this may be due to muscle inflammation susceptibility. Metformin reduces inflammation, so we hypothesized that metformin would augment the muscle response to PRT in healthy women and men aged 65 and older. In a randomized, double‐blind trial, participants received 1,700 mg/day metformin (N = 46) or placebo (N = 48) throughout the study, and all subjects performed 14 weeks of supervised PRT. Although responses to PRT varied, placebo gained more lean body mass (p = .003) and thigh muscle mass (p < .001) than metformin. CT scan showed that increases in thigh muscle area (p = .005) and density (p = .020) were greater in placebo versus metformin. There was a trend for blunted strength gains in metformin that did not reach statistical significance. Analyses of vastus lateralis muscle biopsies showed that metformin did not affect fiber hypertrophy, or increases in satellite cell or macrophage abundance with PRT. However, placebo had decreased type I fiber percentage while metformin did not (p = .007). Metformin led to an increase in AMPK signaling, and a trend for blunted increases in mTORC1 signaling in response to PRT. These results underscore the benefits of PRT in older adults, but metformin negatively impacts the hypertrophic response to resistance training in healthy older individuals. ClinicalTrials.gov Identifier: NCT02308228.     

Effect of running training on uncoupling protein mRNA expression in rat brown adipose tissue

The effect was investigated of endurance training on the expression of uncoupling protein (UCP) mRNA in brown adipose tissue (BAT) of rats. The exercised rats were trained on a rodent treadmill for 5 days per week and a total of 9 weeks. After the training programme, a marked decrease in BAT mass was found in terms of weight or weight per unit body weight; there was a corresponding decrease in DNA content and a downward trend in RNA and glycogen levels. The UCP mRNA was present at a markedly decreased level in BAT of trained animals. In consideration of the reduced levels of mRNAs for hormone-sensitive lipase and acylCoA synthetase, the brown adipose tissue investigated appeared to be in a relatively atrophied and thermogenically quiescent state.     

PGF2alpha facilitates the training of sexually active boars for semen collection

The objective was to determine the effects of PGF2alpha on the training of sexually active boars (i.e., boars experienced with natural mating) to mount an artificial sow for semen collection. Boars were moved to a semen collection pen twice weekly for 4 wk. After entering the pen, boars received im treatment with 10 mg PGF2alpha (n = 7) or 2 mL deionized water (n = 7). Boars were classified as trained when after a successful collection, the animals mounted the artificial sow and allowed semen collection on the next scheduled day without first receiving an injection of PGF2alpha or deionized water. The semen from 6 of 7 PGF2alpha-treated boars and 2 of 7 control boars was collected during the first exposure to the artificial sow (P < .03). After 4 training sessions, 7 of 7 PGF2alpha-treated boars and 4 of 7 controls were successfully trained (P < .05). The number of false mounts (mounting artificial sow but not allowing semen collection) per session was lower (P < .07) for PGF2alpha-treated boars (.6 +/- 1.0), compared to boars receiving deionized water (3.9 +/- 1.0) or trained boars receiving no treatment (3.4 +/- .7). Reaction time (elapsed time after entering collection pen until the start of ejaculation) was lower (P < .04) for PGF2alpha-treated boars (267.4 +/- 63.4 sec), compared to boars treated with deionized water (628.4 +/- 98.3 sec) or boars receiving no treatment (440.4 +/- 46.4 sec). In summary, use of PGF2alpha facilitated the training of sexually active boars to mount an artificial sow for semen collection.     

Changes in the size of the long tubular bones and body weight of rats exercised at different times of the day

The observations were performed in autumn in 100 rats at the age of 1 month. The animals were trained in a horizontal treadmill with the speed 40 m/min, beginning with 3 min/day and gradually increasing the time up to 30 min. The control animals were not trained, the test animals were trained either once a day (at 7 a. m., 3 p. m., 11 p. m.), or three times a day and the total loading was equal to a single loading. The animals were weighed daily. Elongation of the bones, increase in their mass and in the body mass were different at training during different time of the day and the effect was not similar in different bones. Certain sexual differences of the training effect were revealed.     

Growth factors and glucose homeostasis in diabetic rats: effects of exercise training

To investigate the alterations of glucose homeostasis and variables of the insulin‐like growth factor‐1 (IGF‐1) growth system in sedentary and trained diabetic (TD) rats, Wistar rats were divided into sedentary control (SC), trained control (TC), sedentary diabetic (SD), and TD groups. Diabetes was induced by Alloxan (35 mg kg^?1 b.w.). Training program consisted of swimming 5 days week^?1, 1 h day^?1, during 8 weeks. Rats were sacrificed and blood was collected for determinations of serum glucose, insulin, growth hormone (GH), IGF‐1, and IGF binding protein‐3 (IGFBP‐3). Muscle and liver were removed to evaluate glycogen content. Cerebellum was extracted to determinate IGF‐1 content. Diabetes decreased serum GH, IGF‐1, IGFBP‐3, liver glycogen, and cerebellum IGF‐1 peptide content in baseline condition. Physical training recovered liver glycogen and increased serum and cerebellum IGF‐1 peptide in diabetic rats. Physical training induces important metabolic and hormonal alterations that are associated with an improvement in glucose homeostasis and serum and cerebellum IGF‐1 concentrations. Copyright © 2009 John Wiley & Sons, Ltd.     

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.