Non-human Primates: Emotion, Cognition and Welfare

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Human-Animal Interactions, Animal Behaviour and Emotion".

Deadline for manuscript submissions: closed (31 August 2021) | Viewed by 30097

Special Issue Editors


E-Mail Website1 Website2
Guest Editor
1. Basic Psychology Area, Department of Psychology, Faculty of Education and Psychology, University of Girona, 17004 Girona, Spain
2. Institut de Recerca i Estudis en Primatologia—IPRIM, 17005 Girona, Spain
Interests: primatology; non-human primates; animal behavior; animal cognition and sociality; laterality; social; personality and emotions; feeding ecology; psychopathology; animal welfare.

E-Mail
Guest Editor
1. Animal Welfare research Group AWSHEL-IAS and Friends of Thoreau Program, Franklin Institute, University of Alcalá, 28801 Alcalá de Henares, Madrid, Spain
2. Didactic Department of Experimental, Social and Mathematical Science, Faculty of Education, Complutense University of Madrid, Madrid, Spain
Interests: animal welfare; primatology; non-human primates; animal behavior; personality and emotions; animal training; environmental education; biodiversity conservation; animal law, animal ethics, animal cognition and laterality, physiological stress.

Special Issue Information

Dear Colleagues,

Non-human primates are some of the most complex animal species at cognitive, behavioral, emotional and social levels. Thousands of individuals are housed at different types of animal center—principally laboratories, zoological parks and rescue centers. Because of that, welfare-promoting environments need to be designed in order to maintain and improve the quality of life of these complex species. Management policies and keepers, researchers, trainers, educators, visitors and veterinarian procedures become important welfare factors for these animals under human control. The interface between emotion, behavior, cognition and welfare is especially relevant.

Original manuscripts that address any aspects of primate behavior, cognition and emotion and their interaction with welfare in different institutions such as zoos, laboratories or rescue centers are invited for this Special Issue. In particular, aspects such as personality, enclosure designs, environmental enrichment, positive reinforcement training, management practices, education programs, visitor effects, rehabilitation, resocialization, physiological indicators, cognitive challenges and cognitive testing, or emotional processes are welcome.

Dr. Miquel Llorente
Dr. Gloria Fernández-Lázaro
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Animals is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2400 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • welfare
  • cognition
  • behavior
  • emotion
  • personality
  • quality of life
  • environmental enrichment
  • management practices
  • positive-reinforcement training
  • nonhuman primates

Published Papers (8 papers)

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Research

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21 pages, 3963 KiB  
Article
Artificial Termite-Fishing Tasks as Enrichment for Sanctuary-Housed Chimpanzees: Behavioral Effects and Impact on Welfare
by Maria Padrell, Federica Amici, Maria Pau Córdoba, Albert Giberga, Antonio Broekman, Susana Almagro and Miquel Llorente
Animals 2021, 11(10), 2941; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11102941 - 11 Oct 2021
Cited by 6 | Viewed by 2615
Abstract
Artificial termite-fishing tasks are a common enrichment for captive great apes, promoting species-typical behaviors. Nonetheless, whether these activities are linked to changes in other behaviors and whether these changes persist over time has seldom been investigated. We assessed whether the use of an [...] Read more.
Artificial termite-fishing tasks are a common enrichment for captive great apes, promoting species-typical behaviors. Nonetheless, whether these activities are linked to changes in other behaviors and whether these changes persist over time has seldom been investigated. We assessed whether the use of an artificial termite-fishing task was linked to changes in the solitary behavior and social dynamics in two groups of sanctuary-housed chimpanzees (Pan troglodytes). Specifically, we compared chimpanzee behavior during eight enrichment sessions distributed over a two-month period, with similar periods before and after the introduction of the enrichment. Data were collected from combined interval and continuous sampling methods and were analyzed using generalized linear mixed models. We found that participation increased across sessions and that both enrichment and participation predicted an increase in tool use and feeding and a decrease in inactivity, which were all maintained throughout the sessions. Furthermore, participation was positively associated with social proximity, revealing a gathering effect of the task. However, neither enrichment nor participation were linked to changes in abnormal, self-directed, affiliation-related or aggression-related behaviors. Overall, our results support the hypothesis that artificial termite-fishing is a suitable enrichment for captive chimpanzees, maintaining the subjects’ interest and promoting species-typical behaviors, with no negative effects on social activities. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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13 pages, 2353 KiB  
Article
Behavioral Changes of Solitary Housed Female Pygmy Slow Lorises (Nycticebus pygmeaus) after Introduction into Group Enclosures
by Josue Alejandro, Yumi Yamanashi, Kei Nemoto, Fred B. Bercovitch and Michael A. Huffman
Animals 2021, 11(9), 2751; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11092751 - 20 Sep 2021
Cited by 4 | Viewed by 3192
Abstract
Pygmy slow lorises (Nycticebus pygmaeus) are threatened with extinction in the wild. Their nocturnal lifestyle and small size make them difficult to study in their natural habitat, but increasing evidence suggests that they are more social than previously thought. Our study [...] Read more.
Pygmy slow lorises (Nycticebus pygmaeus) are threatened with extinction in the wild. Their nocturnal lifestyle and small size make them difficult to study in their natural habitat, but increasing evidence suggests that they are more social than previously thought. Our study was designed to assess the sociability of pygmy slow lorises by transferring six adult females from solo cages into environmentally enriched group home cages at the Japan Monkey Centre’s Slow Loris Conservation Centre. Two females were paired to create one group, while the other four were placed together in a second group. We compared their social interactions, activity budgets, and postural behaviors before and after social housing was initiated. We found that all-female slow loris groups had a high degree of sociality, preferred to stay close to each other, nested together every night, and spent less time in locomotion and more time grooming than when living alone. These results suggest that female pygmy slow lorises actively seek companions when available. The captive housing of all-female groups of lorises could lead to better husbandry practices and improved animal welfare by allowing them to have conspecific companions. We conclude that isosexual groups of pygmy slow lorises should be preferred over single housing when possible. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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15 pages, 421 KiB  
Article
Strepsirrhine Primate Training Programs in North American Institutions: Status and Implications for Future Welfare Assessment
by Gloria Fernández-Lázaro, Meg H. Dye, Christie Eddie and Gina M. Ferrie
Animals 2021, 11(8), 2462; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11082462 - 21 Aug 2021
Cited by 2 | Viewed by 3102
Abstract
Many articles have shown the benefits of operant conditioning training techniques in the care and welfare of several species of nonhuman primates; however, the information regarding their use in strepsirrhine species is scarce. We assessed the development and current status of training programs [...] Read more.
Many articles have shown the benefits of operant conditioning training techniques in the care and welfare of several species of nonhuman primates; however, the information regarding their use in strepsirrhine species is scarce. We assessed the development and current status of training programs with these species in North American institutions. An online survey was distributed through members of the Association of Zoos and Aquariums using a multiple-choice format. We collected information related to training program details; animals, behaviors, and techniques; the evaluation process; and the impact of training. Seventy-one organizations completed the survey, with the results showing that 97% of respondents trained their strepsirrhines with the main objective of husbandry and veterinary care (around 80%). Sixty-eight percent of organizations did not report any risk in training these species. The benefits reported include increases in positive human–animal interactions (97%), psychological well-being (88%), and staff awareness of animal behaviors (90%). However, a multi-dimensional approach to measure the efficacy of training could provide a deeper understanding of its impact on the welfare of strepsirrhine primates. We hope that the data offered in this survey can help in this future assessment. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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18 pages, 1308 KiB  
Article
An Investigation into the Influence of Different Types of Nesting Materials upon the Welfare of Captive Chimpanzees (Pan troglodytes)
by Naomi Anderson, Bala Amarasekaran and David Riba
Animals 2021, 11(6), 1835; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11061835 - 20 Jun 2021
Cited by 3 | Viewed by 2820
Abstract
Ensuring the welfare of captive chimpanzees (Pan troglodytes) is crucial, in part because they can act as a conservation resource in the case of wild populations becoming extinct. One strategy often adopted to ensure animal welfare is environmental enrichment. In this [...] Read more.
Ensuring the welfare of captive chimpanzees (Pan troglodytes) is crucial, in part because they can act as a conservation resource in the case of wild populations becoming extinct. One strategy often adopted to ensure animal welfare is environmental enrichment. In this study, we investigated the impact of different nesting materials (leaves and branches, long grass, cotton sheets, and shredded newspaper) upon the welfare of chimpanzees housed at Tacugama Chimpanzee Sanctuary (Sierra Leone). Data was collected on 20 subjects (aged 4 to 15 years) between November 2019 and March 2020. Welfare was based on individuals’ relative frequency of affiliative, abnormal and agonistic behaviours, as well as their social and behavioural competence. We found that individuals’ welfare was higher when presented with nesting materials (compared to the control and post-treatment conditions), particularly when given shredded newspaper, regardless of whether the material was presented separately or in conjunction with another. In addition, welfare was highest: during the morning (vs evening); in groups of older individuals (vs younger); with females engaging in less agonistic behaviours compared to males; and males displaying relatively higher behavioural competence. Our results support previous research that captive chimpanzees be supplied with destructible nesting materials, and demonstrate that synthetic enrichments can indeed have a more positive impact upon welfare than their natural alternatives. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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23 pages, 641 KiB  
Article
Recommendations for Abnormal Behaviour Ethograms in Monkey Research
by Andrea Polanco, Brenda McCowan, Lee Niel, David L. Pearl and Georgia Mason
Animals 2021, 11(5), 1461; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11051461 - 19 May 2021
Cited by 6 | Viewed by 4234
Abstract
Laboratory monkey ethograms currently include subcategories of abnormal behaviours that are based on superficial morphological similarity. Yet, such ethograms may be misclassifying behaviour, with potential welfare implications as different abnormal behaviours are likely to have distinct risk factors and treatments. We therefore investigated [...] Read more.
Laboratory monkey ethograms currently include subcategories of abnormal behaviours that are based on superficial morphological similarity. Yet, such ethograms may be misclassifying behaviour, with potential welfare implications as different abnormal behaviours are likely to have distinct risk factors and treatments. We therefore investigated the convergent validity of four hypothesized subcategories of abnormal behaviours (‘motor’, e.g., pacing; ‘self-stimulation’, e.g., self-sucking; ‘postural’, e.g., hanging; and ‘self-abuse’, e.g., self-biting). This hypothesis predicts positive relationships between the behaviours within each subcategory. Rhesus macaque (Macaca mulatta) data on 19 abnormal behaviours were obtained from indoor-housed animals (n = 1183). Logistic regression models, controlling for sex, age, and the number of observations, revealed that only 1/6 ‘motor’ behaviours positively predicted pacing, while 2/3 ‘self-abuse’ behaviours positively predicted self-biting (one-tailed p-value < 0.05). Furthermore, ‘self-stimulation’ behaviours did not predict self-sucking, and none of the ‘postural’ behaviours predicted hanging. Thus, none of the subcategories fully met convergent validity. Subsequently, we created four new valid subcategories formed of comorbid behaviours. The first consisted of self-biting, self-hitting, self-injurious behaviour, floating limb, leg-lifting, and self-clasping. The second comprised twirling, bouncing, rocking, swinging, and hanging. The third comprised pacing and head-twisting, while the final subcategory consisted of flipping and eye-poking. Self-sucking, hair-plucking, threat-biting, and withdrawn remained as individual behaviours. We encourage laboratories to replicate the validation of these subcategories first, and for scientists working with other species to validate their ethograms before using them in welfare assessments. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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23 pages, 3187 KiB  
Article
Learning to Be an Orangutan—Implications of Life History for Orangutan Rehabilitation
by Signe Preuschoft, Ishak Yassir, Asti Iryanti Putri, Nur Aoliya, Erma Yuliani, Siti Nur Badriyah, Paloma Corbi, Yoyok Sugianto, Bina Swastas Sitepu, Mukhlisi and Elfriede Kalcher-Sommersguter
Animals 2021, 11(3), 767; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11030767 - 10 Mar 2021
Cited by 7 | Viewed by 3928
Abstract
Orangutans depend on social learning for the acquisition of survival skills. The development of skills is not usually assessed in rescued orphans’ pre-release. We collected data of seven orphans over an 18-months-period to monitor the progress of ontogenetic changes. The orphans, 1.5–9 years [...] Read more.
Orangutans depend on social learning for the acquisition of survival skills. The development of skills is not usually assessed in rescued orphans’ pre-release. We collected data of seven orphans over an 18-months-period to monitor the progress of ontogenetic changes. The orphans, 1.5–9 years old, were immersed in a natural forest environment with human surrogate mothers and other orphans. Social interactions deviated significantly from those of wild mother-reared immatures. Infants spent more time playing socially with peers, at the expense of resting and solitary play. Infants were also more often and at an earlier age distant from their human surrogate mothers than wild immatures are from their biological mothers. We found important changes towards an orangutan-typical lifestyle in 4- to 7-year-old orphans, corresponding to the weaning age in maternally reared immatures. The older orphans spent less time interacting with human surrogate mothers or peers, started to use the canopy more than lower forest strata and began to sleep in nests in the forest. Their time budgets resembled those of wild adults. In conclusion, juvenile orphans can develop capacities that qualify them as candidates for release back into natural habitat when protected from humanising influences and immersed in a species-typical environment. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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22 pages, 3635 KiB  
Article
A Comparative Perspective on Three Primate Species’ Responses to a Pictorial Emotional Stroop Task
by Lydia M. Hopper, Matthias Allritz, Crystal L. Egelkamp, Sarah M. Huskisson, Sarah L. Jacobson, Jesse G. Leinwand and Stephen R. Ross
Animals 2021, 11(3), 588; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11030588 - 24 Feb 2021
Cited by 11 | Viewed by 4522
Abstract
The Stroop effect describes interference in cognitive processing due to competing cognitive demands. Presenting emotionally laden stimuli creates similar Stroop-like effects that result from participants’ attention being drawn to distractor stimuli. Here, we adapted the methods of a pictorial Stroop study for use [...] Read more.
The Stroop effect describes interference in cognitive processing due to competing cognitive demands. Presenting emotionally laden stimuli creates similar Stroop-like effects that result from participants’ attention being drawn to distractor stimuli. Here, we adapted the methods of a pictorial Stroop study for use with chimpanzees (N = 6), gorillas (N = 7), and Japanese macaques (N = 6). We tested all subjects via touchscreens following the same protocol. Ten of the 19 subjects passed pre-test training. Subjects who reached criterion were then tested on a standard color-interference Stroop test, which revealed differential accuracy in the primates’ responses across conditions. Next, to test for an emotional Stroop effect, we presented subjects with photographs that were either positively valenced (a preferred food) or negatively valenced (snakes). In the emotional Stroop task, as predicted, the primates were less accurate in trials which presented emotionally laden stimuli as compared to control trials, but there were differences in the apes’ and monkeys’ response patterns. Furthermore, for both Stroop tests, while we found that subjects’ accuracy rates were reduced by test stimuli, in contrast to previous research, we found no difference across trial types in the subjects’ response latencies across conditions. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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Review

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17 pages, 58993 KiB  
Review
Bridging Captive and Wild Studies: Behavioral Plasticity and Social Complexity in Theropithecus gelada
by Elisabetta Palagi and Thore J. Bergman
Animals 2021, 11(10), 3003; https://0-doi-org.brum.beds.ac.uk/10.3390/ani11103003 - 19 Oct 2021
Cited by 10 | Viewed by 3459
Abstract
Cognitive ethology explores the ability of animals to flexibly adapt their behavior to rapid physical and social environment fluctuations. Although there is a historical dichotomy between field and captive studies, recently, a growing interest in questions that sit at the intersection of cognitive [...] Read more.
Cognitive ethology explores the ability of animals to flexibly adapt their behavior to rapid physical and social environment fluctuations. Although there is a historical dichotomy between field and captive studies, recently, a growing interest in questions that sit at the intersection of cognitive and adaptive perspectives has helped bridge this divide. By focusing on Theropithecus gelada, we discuss the three main reasons why this hybrid approach is extremely successful. First, captive and wild studies provide data at different social, spatial, and temporal scales that can be synthesized to give a fuller picture of the behavior. Secondly, apparently conflicting results from captive and wild settings are powerful tools to explore behavioral flexibility and latent behavioral tendencies. Third, the different settings provide ways of validating and exploring behaviors that are noticed in the other setting. Although we were able to bring together our captive and wild research to demonstrate these ideas, we could have obtained a more integrated vision on the proximate and ultimate gelada behavioral and cognitive strategies if we had considered this hybrid approach from the beginning. We hope that this manuscript stimulates scholars in designing their studies by taking into account the incredible potential of a complementary captive-wild research approach. Full article
(This article belongs to the Special Issue Non-human Primates: Emotion, Cognition and Welfare)
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