Corrigendum: Utilizing vocalizations to gain insight into the affective states of non-human mammals.

[This corrects the article DOI: 10.3389/fvets.2024.1366933.].

Utilizing vocalizations to gain insight into the affective states of non-human mammals.

This review discusses how welfare scientists can examine vocalizations to gain insight into the affective states of individual animals. In recent years, researchers working in professionally managed settings have recognized the value of monitoring the types, rates, and acoustic structures of calls, which may reflect various aspects of welfare. Fortunately, recent technological advances in the field of bioacoustics allow for vocal activity to be recorded with microphones, hydrophones, and animal-attached devices (e.g., collars), as well as automated call recognition. We consider how vocal behavior can be used as an indicator of affective state, with particular interest in the valence of emotions. While most studies have investigated vocal activity produced in negative contexts (e.g., experiencing pain, social isolation, environmental disturbances), we highlight vocalizations that express positive affective states. For instance, some species produce vocalizations while foraging, playing, engaging in grooming, or interacting affiliatively with conspecifics. This review provides an overview of the evidence that exists for the construct validity of vocal indicators of affective state in non-human mammals. Furthermore, we discuss non-invasive methods that can be utilized to investigate vocal behavior, as well as potential limitations to this line of research. In the future, welfare scientists should attempt to identify reliable, valid species-specific calls that reflect emotional valence, which may be possible by adopting a dimensional approach. The dimensional approach considers both arousal and valence by comparing vocalizations emitted in negative and positive contexts. Ultimately, acoustic activity can be tracked continuously to detect shifts in welfare status or to evaluate the impact of animal transfers, introductions, and changes to the husbandry routine or environment. We encourage welfare scientists to expand their welfare monitoring toolkits by combining vocal activity with other behavioral measures and physiological biomarkers.

Integrating Reference Intervals into Chimpanzee Welfare Research.

Animal welfare researchers are committed to developing novel approaches to enhance the quality of life of chimpanzees living in professional care. To systematically monitor physical, mental, and emotional states, welfare scientists highlight the importance of integrating non-invasive, animal-based welfare indicators. This study aimed to create species-specific reference intervals for behavioral measures and physiological biomarkers. Specifically, we analyzed data from 40 adult chimpanzees (22 females, 18 males) residing at 16 zoological facilities to generate reference intervals for behavioral states and events, behavioral diversity, fecal glucocorticoid metabolites (GCMs), and fecal immunoglobulin-A (IgA). Comparisons of sex and age using linear regression models revealed significant differences for several behaviors. The proportion of time spent engaged in mutual/multiple social grooming significantly decreased as individuals aged. Furthermore, males spent a higher proportion of time performing aggressive contact behaviors and displaying to other chimpanzees when compared to females. Males also performed sexual examination behaviors at a higher rate than females. Behavioral diversity, fecal GCM, and fecal IgA did not vary by sex or age. In the future, values for individual chimpanzees can be compared to the ranges reported here for particular age/sex classes. Ultimately, animal care professionals can utilize reference intervals to make evidence-based decisions regarding management practices and environmental conditions.

Beyond Glucocorticoids: Integrating Dehydroepiandrosterone (DHEA) into Animal Welfare Research.

Animal welfare researchers are committed to identifying novel measures for enhancing the quality of life of individual animals. Recently, welfare scientists have emphasized the need for tracking multiple indicators of an animal's behavioral, emotional and mental health. Researchers are currently focused on integrating non-invasive physiological biomarkers to gain insight into an individual's welfare status. Most commonly, the animal welfare community has analyzed glucocorticoid hormones and their metabolites as a measure of stress. While glucocorticoids provide valuable information about hypothalamic-pituitary-adrenal (HPA) axis activity, there are limitations to utilizing these hormones as the sole measure of long-term stress and welfare. Other biomarkers, such as dehydroepiandrosterone and its sulfate ester-collectively referred to as DHEA(S)-help provide a more complete picture of HPA activity. DHEA(S) counteracts the effects glucocorticoids by having anti-aging, immune-enhancing and neuroprotective properties. Recent studies have examined the ratio of glucocorticoids to DHEA(S) as a way to better understand how the HPA axis is functioning. There is evidence that this ratio serves as an indicator of immune function, mental health, cognitive performance and overall welfare. We review studies that employed the glucocorticoid:DHEA(S) ratio, outline methodological considerations and discuss how researchers can integrate glucocorticoids, DHEA(S) and the glucocorticoid:DHEA(S) ratio into welfare assessments.

Animal-based welfare monitoring: using keeper ratings as an assessment tool.

Zoological institutions are in urgent need of identifying and implementing welfare assessment tools that allow for ongoing, quantitative monitoring of individual animal well-being. Although the American Zoological Association's (AZA) Animal Welfare Committee (AWC) promotes the use of such tools in internal review processes, current approaches to institutional welfare assessment are resource-based and outline the resources, environmental parameters and "best practices" recommended for promoting good welfare in a species in general. We highlight the value of incorporating animal-based monitoring tools that capture the individual animal's perspective and subjective experiences, including positive events and feelings, by validating zookeepers' qualitative assessments. We present evidence that, across a variety of species, caretakers' assessments of traits related to the well-being of individual animals can be both reliable and valid. Furthermore, we demonstrate that among researchers investigating the welfare of farm, laboratory, companion and even zoo animals, support already exists for developing and validating instruments that objectively evaluate the qualitative assessments of caretakers. Finally, we outline a process currently being evaluated at Brookfield Zoo for developing, validating and testing a cost-effective, user-friendly monitoring tool that will help to quantify keepers' qualitative assessments of individual well-being and can be integrated into daily operations. This tool (i.e. species-specific Welfare Score Sheets designed through consultation with animal experts) will result in weekly scores of individual well-being that are expected to provide a first indicator of welfare issues in the collection. Specifically, scores can be reviewed during regular workgroup meetings to identify welfare issues proactively, to assess whether particular conditions, practices or events impact individual well-being, and finally, to evaluate the effectiveness of efforts to address welfare issues. Upon completion of the tool validation and testing phases, we plan to make the Welfare Score Sheets for our 12 study species available to other institutions, and the methods we applied may serve as a "blueprint" for creating similar tools for additional species and institutions.

Who needs a forelimb anyway? Locomotor, postural and manipulative behavior in a one-armed gibbon.

Given the predominance of brachiation and other forms of suspension in gibbon locomotion, we compared the locomotor, postural, and manipulative behaviors of a captive, juvenile, one-armed gibbon to the behavioral profiles of his family members. We expected Kien Nahn, whose arm was amputated in response to an untreatable injury approximately 1 year before observations began, to avoid suspensory locomotion, to spend more time immobile, and to be less likely to exhibit postures involving forelimb suspension. Data were collected using scan sampling to record the behaviors and postures of Kien Nahn, his younger brother, and his parents. Additional postural and manipulative behaviors were recorded ad lib. Kien Nahn and his younger sibling had similar activity levels, and although differences in postural profiles existed, they were surprisingly few. Specifically, Kien Nahn spent significantly less time in motion and in non-suspensory forms of locomotion than his brother. When compared to his parents, Kien Nahn was found to be both active and in motion more often, but was less likely to exhibit the forelimb suspension posture. Despite the increased energetic demands associated with one-armed brachiation, Kien Nahn preferred suspensory locomotion to other forms of locomotion. Furthermore, he found unique solutions for foraging and locomoting, often making use of his feet and teeth, and he was generally the first to approach and manipulate enrichment objects. We found no evidence to suggest that Kien Nahn's injury has altered his activity levels. Although the one-armed gibbon displayed slightly different locomotor, postural, and manipulative behaviors than his family members, he seems to have adapted well to his injury. Zoo Biol 0:1-8, 2007. (c) 2007 Wiley-Liss, Inc.

Relative digit lengths and testosterone levels in Guinea baboons.

A growing body of literature suggests that the ratio of the lengths of the second to fourth digits (2D:4D) on human hands is sexually dimorphic and associated with prenatal exposure to gonadal hormones, circulating serum testosterone, and a number of psychological and behavioral measures. Little research has investigated digit ratios in nonhuman species. In the present study, we investigated sex differences in digit ratios and their possible association with serum testosterone in a captive group of Guinea baboons (Papio papio). Contrary to the sex difference typically reported in humans, male baboons exhibited a substantially larger 2D:4D than did female baboons. Consistent with the human data, however, lower 2D:4D was associated with higher serum testosterone among the males. The present findings suggest that the relationship between digit ratios and male gonadal hormones may be phylogenetically well-conserved, although they also suggest possible species differences in the causal relationships between developmental mechanisms and sex-differentiated digit length patterns.