Land mammals
Blood sample training for glucose metabolism in woolly monkeys (Lagothrix lagotricha) and chimpanzees (Pan troglodytes)
Daniela Stefany Mayorquin Moreno es médica veterinaria Dipl. ULS, coordinadora de entrenamiento animal de Bioparque Ukumarí, Pereira-Risaralda.
Dayro Alonso Palma Conda es zookeeper Élite del Bioparque Ukumarí en el área de Chimpancés. Pereira-Risaralda.
Elías Silva Revoyedo es promotor senior de Primates en el Zoológico de Cali. Colombia
Jorge Iván Sánchez Quintero es biólogo y entrenador animal, dueño y administrador de Mono Lanudo Pet Shop. Villamaria, Caldas, Colombia.
Introduction
In Latin America in the early 1990s, it was common for people of that generation to witness how animals, especially dogs, were punished in various ways for performing undesired behaviors, with the aim of "correcting" their behavior. Children or young people of that time heard older people assure that dogs lived there solely to guard property; this was due to the belief and perception that dogs or other animals were simply animals, lacking the capacity to feel, reason, and make decisions, meaning they only acted on instinct. In short, they were treated as objects. Fortunately, in other countries like the United States around the same time, discussions about animal welfare were already beginning, demonstrating to the world that animals were not what we had been taught. In various ways, it was shown that they possess cognitive abilities and can perform behaviors similar to ours. But this did not emerge out of nowhere; let us remember some of the behaviorists who dedicated their lives to understanding human behavior and generated science from observations, allowing us to understand the learning process.
In the early 1900s, such as in 1927, Ivan Pavlov introduced his studies on classical conditioning; nine years later, in 1938, psychologist Burrus Frederick Skinner spoke of operant conditioning, followed by Edward Thorndike, who in 1932 explained Skinner's theory through the law of effect. Subsequently, Skinner's students, the Brelands, took all this knowledge and began to apply it to wild animals for the betterment of humanity, becoming the first applied animal psychologists. Another person who contributed to the development of this science is Temple Grandin, a zoologist, ethologist, and advocate for animal welfare, who teaches us to see and interpret animals through images and encourages us to try to think like them. Thanks to all of them and their theories, we had the opportunity to radically change the concept and retrograde practices of animal management, whether in zoos, aquariums, farms, or domestic animals. Science showed us that we were completely wrong when we said that animals were simply animals and acted on simple instinct. Now, our present is very different, as we constantly talk about animal welfare and the proper care we must offer them every day, including factors such as proper nutrition, physical and mental stimulation, and good health practices.
Thanks to the science of conditioning, more appropriate and positive management practices are generated, allowing animals to learn behaviors to actively participate in their care and handling. They learn behaviors previously unimaginable by people and believed to be exclusive to humans. For example, drawing blood from an individual through a slight prick on their finger completely voluntarily, allowing real-time glucose level monitoring, simply through behavior reinforcement. This way, it can be demonstrated that animals are as intelligent as humans, and all animals learn exactly the same way through conditioning.
Old and New World primates learning
The study groups are located in two different places, Ukumari Biopark (Pereira - Risaralda) and the Zoological Foundation of Cali (Cali - Valle del Cauca), in Colombia. These institutions have animal training programs aimed at implementing behavior modification processes for the target species and individuals, 3 chimpanzees (Pan troglodytes), and 3 woolly monkeys (Lagothrix lagotricha).
The training plan was established under the SPIDER model (a scientific methodology developed at Disney's Animal Kingdom for managing environmental enrichment programs and animal training in zoos).
Chimpanzees
a. The execution frequency was 3 days a week with an approximate duration of 15 minutes in each session.
b. Behavior modification was performed through operant conditioning based on positive reinforcement, and classical conditioning was initially applied to establish baseline behaviors.
c. Counter-conditioning, habituation, desensitization techniques, and differential reinforcement of an incompatible behavior were implemented to achieve blood sampling.
d. Palatability tests were conducted, consisting of offering different ingredients simultaneously to evaluate preferences. These ingredients were implemented during desensitization and sample collection. Palatability test comparison in chimpanzees demonstrated that the most preferred ingredient for the male Pancho was pistachios, for the female Karla was peanuts, and for the male Yoko were both peanuts and ripe bananas.
e. The implementation of the individuals' training plan included a step-by-step process, with progress made as the proposed activities were put into practice.
1. Acceptance of the reinforcer and individuals' approach for reinforcement, vocal command implementation with the name of each individual.
2. When the individual exposes the anatomical area to work on, the command "Finger" is established, and the behavior is marked when the area exposure occurs automatically.
Figure 1. Mayorquin, D. (24 de Agosto 2021), Sd “Finger” Pan troglodytes.
3. Desensitization is carried out in the anatomical area to achieve the sample, which includes area disinfection activities and desensitization to puncture with blunt needles size 29. After the individual agrees to this step, the needle puncture with bevel is performed. (Figures 2-3).
4. Habituation process and inclusion of equipment for glucose monitoring were performed, including sharp objects, glucose monitoring strips, and reading equipment.
5. Finally, sessions with all the steps to achieve the behavior are carried out, without taking the sample. This exercise is conducted for 3 sessions for each individual, ensuring that the behavior is fully established.
Figure 2-3 Mayorquin, D. (30th Agust 2021) Desensitization with blunt-tipped needle followed by puncture with beveled needle
Woolly monkey or churuco
a. The execution frequency was 5 days a week with an approximate duration of 15 minutes in each session, 5 minutes per individual. The elements, infrastructure, adaptations, and even the time depend on each organization and the trainer, so we indicate that there are variations depending on the resources available to the trainer. Additionally, each institution has its organizational structure and depends on resources, time, and the amount of personnel.
b. Behavior modification was carried out by simultaneously working on both classical and operant conditioning. For the 2 individuals who gave their hand without difficulty from the beginning, operant conditioning was used. When they gave their hand, the behavior was marked with a whistle, and immediately after, it was reinforced with a 50ml syringe of mixed fruit compote with a catheter tip. For the individual who did not reach out their hand, as a strategy, the trainer would put compote in their hand so that the monkey would stretch out its hand, take the compote, and bring it to its mouth (luring). After several repetitions and once the primate understood the exercise, we moved on to operant conditioning. Techniques such as counter-conditioning, habituation, desensitization, generalization, and differential reinforcement of an incompatible behavior were also applied, including differential reinforcement of other behaviors to achieve blood sampling.
c. Regarding the palatability test conducted among ingredients such as plum compote, vegetables like carrots, green beans, and lettuce, commercial mixed fruit compote, mango, and hibiscus flowers, it was determined that all three individuals prefer the commercial compote and mango, as well as hibiscus tree flowers (Hibiscus elatus). These ingredients were implemented in the process, with the compote used for desensitization and sample collection, while the mango was used as a jackpot (Figure 4).
Figure 4. Sánchez, J. (2021)
d. Unlike chimpanzees, where the desensitization process for injection or puncture is done on the fingers, in woolly monkeys, desensitization is done on the palm of the hand. This is due to their anatomical structure, including the size of their hands relative to the size of their fingers, which are very small for the process (Figures 5 - 7). The training plan for woolly monkeys included a step-by-step process, starting from passing the hand through the window, allowing contact, holding, and various stimuli such as stroking the palm of the hand, pinching it, touching it with a blunt needle (size #21), showing the pen with which we would perform the puncture, the glucometer that would allow glucose reading, and also presenting gauze pads soaked in alcohol (Figures 5 - 11). Additionally, efforts were made to include more people in the process, anticipating the arrival of veterinarians and avoiding any changes in behavior.
Figure 5 - 7 Sánchez, J. (2022) Desensitization process of hands through contact with a blunt or non-sharp needle and through contact with the trainer.
Fiigure 8-11 Sánchez, J. (Mayo 2022) Habituation and desensitization process of primates regarding gauze pads, alcohol, lancets, and equipment.
Figures 12-13 Mayorquin, D. (Mayo 2022) Results of glucose monitoring in Pan troglodytes.
Figures 14-16 Sánchez, J. Photos courtesy of Rivera, V. (May 2022) Glucose monitoring results in Lagothrix lagotricha.
Regarding the training sessions for chimpanzees and woolly monkeys, the following values were obtained in days and an equal number of sessions until the sample could be taken adequately, see graphs 5 and 6.
Graph 5: Number of training sessions per individual until successfully obtaining the blood sample Pan troglodytes
Graph 6: Number of training sessions per individual until successfully obtaining the blood sample in Lagothrix lagotricha.
Based on the above, we see that the individuals responded to the process and allowed us to achieve the goal of obtaining blood samples for glucose monitoring. The execution time varied slightly; however, it should be considered that living beings are like this—each one has its personality and learns at a different pace.
Science in favor of animal health and welfare
The impact of this work lies in the fact that these types of procedures, from behavior modification, give us the possibility to monitor animals in real-time and in a timely manner. Both classical and operant conditioning provide us with different benefits and allow individuals to actively participate in health processes. It also allows the animal welfare team to make decisions about the care of individuals in case the test results are affected. Furthermore, the project demonstrates that through training, we can execute preventive and corrective medicine plans positively for individuals under human care.
The desensitization process in the palms of the hands is recommended for medium-sized primates for blood extraction and glucose sampling. It is more friendly to the individuals and greatly facilitates handling. On the other hand, recognizing the natural history of woolly monkeys, they have more arboreal habits and although they can be on the ground, they spend most of their time in trees using their hands, especially their fingers. This is a reason why we must say that the fingertips of these primates are harder, so they can support and/or resist activities such as hanging or moving between branches. In chimpanzees, there is no such difficulty due to the size of their fingers and similarity to humans. Based on the results obtained from the glucose levels of each individual, it can be seen that the values are within the estimated ranges for the species. For these values to be within the range, individuals must be in adequate welfare conditions, including health, nutrition, routine management, and behavioral management. Regardless of the institution where the animals are located, in this case, Ukumarí Biopark and Cali Zoo, they demonstrate through this study that they are implementing strategies that provide better welfare conditions for the primates housed in their institutions.
Both classical and operant conditioning remain fundamental tools in animal teaching processes, allowing for capillary blood sampling as outlined in this article. This process allows sampling of medium-sized primates and larger primates, thus demonstrating that capillary blood sampling can be obtained from less sensitive areas, favoring processes that are more friendly to the individuals.
We would like to thank the following individuals: Sandra Milena Correa, manager of Ukumarí Biopark; Néstor Várela, scientific director of Ukumarí Biopark; Luisa Del Vasto, Diana Isabel Buitrago, Juliana Peña, Santiago Gonzales, Ana Maria Cardona, and the entire team of the Animal Welfare Unit of Cali Zoo and Ukumarí Biopark. Special thanks to Esteban Marín, Valentina Rivera, Victor García, for their support in the conditioning processes, as well as for sharing some photos and videos. Additionally, we would like to thank the WeZooit team for considering us and giving us the opportunity to share this wonderful article.
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