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      Exploratory Investigation of Infrared Thermography for Measuring Gorilla Emotional Responses to Interactions with Familiar Humans

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          Abstract

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          Interactions between zoo professionals and animals, such as positive reinforcement training, occur regularly and are thought to be enriching for animals. However, there is little empirical information on how animals perceive these interactions or on the interactions’ effects on animals’ emotional states. Our objective was to assess the effectiveness of infrared thermography for measuring the emotional responses of three western lowland gorillas at the Detroit Zoo to routine interactions (positive reinforcement training and cognitive tasks) with familiar humans. In addition to thermal images, we collected saliva samples for hormone analysis before and after human–animal interactions and a control condition, and we recorded behavioral data during all conditions. Nasal temperatures consistently decreased for two gorillas during interactions, while the third gorilla showed repeated increases. The behavior of all three gorillas suggested that they were engaged in the interactions, without exhibiting behaviors that could indicate negative welfare impacts. Oxytocin and cortisol both decreased following all conditions, including the control, and were thus equivocal for interpreting the meaning of the changes in nasal temperature. As mixed results in previous research show, infrared thermography may detect emotional arousal; however, additional indicators are necessary to determine the valence of the observed changes. The variability in responses we observed do not lend themselves to making firm conclusions about the validity of infrared thermography (IRT) for measuring emotion in this context or about how these gorillas responded to interactions. Challenges and suggestions for future studies using infrared thermography to examine interactions between humans and zoo animals are discussed.

          Abstract

          Interactions between zoo professionals and animals occur regularly and are believed to be enriching for animals. Little empirical information exists on how animals perceive these interactions, and particularly how the interactions affect the emotional states of animals. Infrared thermography (IRT) has shown some promise in the assessment of emotions in a variety of species, but further research is needed to determine if this method is useful in a zoo setting. We conducted a pilot study to determine if IRT is a valid measure of the emotional responses to routine interactions (positive reinforcement training and cognitive tasks, compared to a control condition) with familiar humans on three western lowland gorillas at the Detroit Zoo. We measured nasal temperatures associated with emotional change using IRT. To examine the validity of the IRT data, we collected saliva samples for hormone analysis before and after each condition, in addition to behavioral data during the interactions and control condition. Decreases in nasal temperatures for two gorillas and an increase in the third indicate that arousal changed consistently within individuals following the interactions but not the control condition. Pre-post cortisol levels and oxytocin concentrations decreased for all conditions, but the decreases seen did not differ among the conditions. The gorillas were highly engaged in the interactions, and two produced more grumble vocalizations during the human-animal interactions (HAIs) compared to the control condition. Additionally, the gorillas performed self-directed behaviors more often during the control condition, also suggesting HAIs were not a negative experience. In summary, we were able to measure changes in arousal using IRT, but we were unable to determine the emotional valence of these changes based on the additional indicators employed. Additionally, the inconsistency across these measures precluded firm conclusions about either the validity of IRT for measuring emotion in this context or how the interactions impacted these gorillas. These findings highlight the challenges of using IRT to measure emotional states in non-human animals, and we discuss further steps necessary to apply this method in future studies.

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          Most cited references66

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          Social evolution. Oxytocin-gaze positive loop and the coevolution of human-dog bonds.

          Human-like modes of communication, including mutual gaze, in dogs may have been acquired during domestication with humans. We show that gazing behavior from dogs, but not wolves, increased urinary oxytocin concentrations in owners, which consequently facilitated owners' affiliation and increased oxytocin concentration in dogs. Further, nasally administered oxytocin increased gazing behavior in dogs, which in turn increased urinary oxytocin concentrations in owners. These findings support the existence of an interspecies oxytocin-mediated positive loop facilitated and modulated by gazing, which may have supported the coevolution of human-dog bonding by engaging common modes of communicating social attachment.
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            A framework for studying emotions across species.

            Since the 19th century, there has been disagreement over the fundamental question of whether "emotions" are cause or consequence of their associated behaviors. This question of causation is most directly addressable in genetically tractable model organisms, including invertebrates such as Drosophila. Yet there is ongoing debate about whether such species even have "emotions," as emotions are typically defined with reference to human behavior and neuroanatomy. Here, we argue that emotional behaviors are a class of behaviors that express internal emotion states. These emotion states exhibit certain general functional and adaptive properties that apply across any specific human emotions like fear or anger, as well as across phylogeny. These general properties, which can be thought of as "emotion primitives," can be modeled and studied in evolutionarily distant model organisms, allowing functional dissection of their mechanistic bases and tests of their causal relationships to behavior. More generally, our approach not only aims at better integration of such studies in model organisms with studies of emotion in humans, but also suggests a revision of how emotion should be operationalized within psychology and psychiatry. Copyright © 2014 Elsevier Inc. All rights reserved.
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              A modest proposal: displacement activities as an indicator of emotions in primates

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                Author and article information

                Journal
                Animals (Basel)
                Animals (Basel)
                animals
                Animals : an Open Access Journal from MDPI
                MDPI
                2076-2615
                25 August 2019
                September 2019
                : 9
                : 9
                : 604
                Affiliations
                Center for Zoo and Aquarium Animal Welfare and Ethics, Detroit Zoological Society, Royal Oak, MI 48067, USA
                Author notes
                [* ]Correspondence: sallard@ 123456dzs.org ; Tel.: +1-248-336-5720
                [†]

                These authors contributed equally to this work.

                Article
                animals-09-00604
                10.3390/ani9090604
                6770422
                31450716
                4a9f5068-b7c0-4ddc-b553-1f3892ecbea6
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 29 July 2019
                : 21 August 2019
                Categories
                Article

                animal welfare,human–animal interactions,infrared thermography,cortisol,oxytocin,positive reinforcement training,cognitive task,gorilla,emotion

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