Correction: Miller et al. Behavioral Diversity as a Potential Indicator of Positive Animal Welfare. Animals 2020, 10, 1211.

In the original publication [...].

Enrichment Is Simple, That's the Problem: Using Outcome-Based Husbandry to Shift from Enrichment to Experience.

Over the decades, the use of environmental enrichment has evolved from a necessary treatment to a "best practice" in virtually all wildlife care settings. The breadth of this evolution has widened to include more complex inputs, comprehensive evaluation of efficacy, and countless commercially available products designed to provide for a myriad of species-typical needs. Environmental enrichment, however, remains almost inexorably based on the provision of inputs (objects, manipulanda, or other sensory stimuli) intended to enhance an environment or prolong a specific behavior. Considerable effort has been put into developing enrichment strategies based on behavioral outcomes to shift the paradigm from the traditional input-heavy process. We believe that this trajectory can be enhanced through Outcome-Based Husbandry using an ethologically based workflow tool with a universal application (regardless of species) that flushes out inputs based on desired outcomes, which can then be incorporated into daily care or layered to create sensory cue-based multi-day events. Furthermore, we believe that this strategy can drive practitioners from the confines of traditional enrichment and the object-based approach into a dynamic and holistic husbandry program that synthesizes complex experiences into regular animal care, rather than supplementing husbandry with input-based enrichment. Focusing on an animal's complete experience and outcomes that promote competence building and the highest level of agency allows the animals, not care staff, to make meaningful decisions that impact their present and future selves.

Behavioral Diversity as a Potential Indicator of Positive Animal Welfare.

Modern day zoos and aquariums continuously assess the welfare of their animals and use evidence to make informed management decisions. Historically, many of the indicators of animal welfare used to assess the collection are negative indicators of welfare, such as stereotypic behavior. However, a lack of negative indicators of animal welfare does not demonstrate that an individual animal is thriving. There is a need for validated measures of positive animal welfare and there is a growing body of evidence that supports the use of behavioral diversity as a positive indicator of welfare. This includes an inverse relationship with stereotypic behavior as well as fecal glucocorticoid metabolites and is typically higher in situations thought to promote positive welfare. This review article highlights previous research on behavioral diversity as a potential positive indicator of welfare. Details are provided on how to calculate behavioral diversity and how to use it when evaluating animal welfare. Finally, the review will indicate how behavioral diversity can be used to inform an evidence-based management approach to animal care and welfare.

Impacts of natural history and exhibit factors on carnivore welfare.

To improve the welfare of nonhuman animals under professional care, zoological institutions are continuously utilizing new methods to identify factors that lead to optimal welfare. Comparative methods have historically been used in the field of evolutionary biology but are increasingly being applied in the field of animal welfare. In the current study, data were obtained from direct behavioral observation and institutional records representing 80 individual animals from 34 different species of the order Carnivora. Data were examined to determine if a variety of natural history and animal management factors impacted the welfare of animals in zoological institutions. Output variables indicating welfare status included behavioral diversity, pacing, offspring production, and infant mortality. Results suggested that generalist species have higher behavioral diversity and offspring production in zoos compared with their specialist counterparts. In addition, increased minimum distance from the public decreased pacing and increased offspring production, while increased maximum distance from the public and large enclosure size decreased infant mortality. These results have implications for future exhibit design or renovation, as well as management practices and priorities for future research.

Animal Welfare in Conservation Breeding: Applications and Challenges.

Animal welfare and conservation breeding have overlapping and compatible goals that are occasionally divergent. Efforts to improve enclosures, provide enriching experiences, and address behavioral and physical needs further the causes of animal welfare in all zoo settings. However, by mitigating stress, increasing behavioral competence, and enhancing reproduction, health, and survival, conservation breeding programs must also focus on preparing animals for release into the wild. Therefore, conservation breeding facilities must strike a balance of promoting high welfare, while minimizing the effects of captivity to increase population sustainability. As part of the Hawaii Endangered Bird Conservation Program, San Diego Zoo Global operates two captive breeding facilities that house a number of endangered Hawaiian bird species. At our facilities we aim to increase captive animal welfare through husbandry, nutrition, behavior-based enrichment, and integrated veterinary practices. These efforts help foster a captive environment that promotes the development of species-typical behaviors. By using the "Opportunities to Thrive" guiding principles, we outline an outcome-based welfare strategy, and detail some of the related management inputs, such as transitioning to parental rearing, and conducting veterinary exams remotely. Throughout we highlight our evidence-based approach for evaluating our practices, by monitoring welfare and the effectiveness of our inputs. Additionally we focus on some of the unique challenges associated with improving welfare in conservation breeding facilitates and outline concrete future steps for improving and evaluating welfare outcomes that also meet conservation goals.

Intensity of play behavior as a potential measure of welfare: A novel method for quantifying the integrated intensity of behavior in African elephants.

To the authors' knowledge there is currently no discrete index to measure the integrated intensity of a play bout in mammals, despite the potential for using intensity and duration of play bouts as a measure of physical activity and welfare. This study was developed to test an equation that quantified the intensity and duration of play bouts in a particularly gregarious mammal, African elephants (Loxodonta africana) housed at the San Diego Zoo Safari Park in Escondido, CA. To quantify these behaviors, we created a scale of intensity and a subsequent equation that produces an index value, giving each unique bout a score. A compilation of these scores provides a range of intensity of play behavior that is a representative value for that particular herd at that point in time, and thus a database to which later bouts can be compared. It can be argued that play behavior is an indicator of positive welfare, and if quantifiable, it is our belief that it can be used as an additional measure of positive welfare in zoo housed animals. Here we present the methods and technique used to calculate a standardized Integrated Play Index (IPI) that has potential for use in other socially living species that are known to exhibit play behavior.

Winning the genetic lottery: biasing birth sex ratio results in more grandchildren.

Population dynamics predicts that on average parents should invest equally in male and female offspring; similarly, the physiology of mammalian sex determination is supposedly stochastic, producing equal numbers of sons and daughters. However, a high quality parent can maximize fitness by biasing their birth sex ratio (SR) to the sex with the greatest potential to disproportionately outperform peers. All SR manipulation theories share a fundamental prediction: grandparents who bias birth SR should produce more grandoffspring via the favored sex. The celebrated examples of biased birth SRs in nature consistent with SR manipulation theories provide compelling circumstantial evidence. However, this prediction has never been directly tested in mammals, primarily because the complete three-generation pedigrees needed to test whether individual favored offspring produce more grandoffspring for the biasing grandparent are essentially impossible to obtain in nature. Three-generation pedigrees were constructed using 90 years of captive breeding records from 198 mammalian species. Male and female grandparents consistently biased their birth SR toward the sex that maximized second-generation success. The most strongly male-biased granddams and grandsires produced respectively 29% and 25% more grandoffspring than non-skewing conspecifics. The sons of the most male-biasing granddams were 2.7 times as fecund as those of granddams with a 50∶50 bias (similar results are seen in grandsires). Daughters of the strongest female-biasing granddams were 1.2 times as fecund as those of non-biasing females (this effect is not seen in grandsires). To our knowledge, these results are the first formal test of the hypothesis that birth SR manipulation is adaptive in mammals in terms of grandchildren produced, showing that SR manipulation can explain biased birth SR in general across mammalian species. These findings also have practical implications: parental control of birth SR has the potential to accelerate genetic loss and risk of extinction within captive populations of endangered species.