Symposium Review: Wild Animal Welfare is in Our Backyards

Ecology is everywhere—including our backyards, which are rich with wildlife. In our urban landscapes, we cohabitate with a multitude of species, including bats, birds, deer, and frogs. Despite their proximity, we have a limited understanding of these animals' subjective experiences and quality of life, as opposed to fitness. These understudied elements of wild animal welfare likely impact animal ecology and potentially broader ecological processes. We must integrate wild animal welfare science with ecological knowledge to ensure that wildlife management strategies and interventions have a positive impact, and that urban wildlife is well cared for. The study of animal ecology has progressively probed deeper into the lives of wild animals, not just animals' environments and behaviors, but also delving into many aspects of their physiology, such as stress responses, epigenetics, and immunology. No longer are animals perceived as black boxes, with their internal workings remaining a mystery to us. However, there is one aspect of the internal functioning of animals that has remained nearly untouched by ecologists: their mental states. Although consciousness researchers have amassed strong evidence that at least all mammals and birds, and likely at least all vertebrates have conscious mental experiences, ecologists mostly ignore this aspect of animals' lives. Although many ecologists openly acknowledge that animals possess mental states, they have nonetheless seemed beyond the reach of scientific measurement to most ecologists. However, comparative psychology and animal welfare science have been assessing the mental states of animals for decades. Drawing on knowledge from captive animal welfare science and other relevant fields, the emerging field of wild animal welfare science seeks to integrate welfare research into animal ecology, conservation, and wildlife management. Currently, ecologists largely engage with welfare science solely to inform the development of ethical research methods. Deeper synergies between the two fields are being neglected. To understand how ecology and animal welfare science intersect, it first helps to define “welfare.” Welfare is the valenced subjective mental experience of an individual over a given time period. Breaking down this definition shows that welfare research operates at the organism scale and considers how animals experience the world over time. It focuses on the subjective quality of the animal's mental experiences—in other words, whether a mental experience feels positive or negative to the individual. Examples of subjective mental states include pain, hunger, thirst, comfort, and pleasure. A researcher might define the time period over which an animal experiences the world as anything from a few minutes to the full lifetime of an individual. For example, one can visualize a timeline of experiences that occur over an individual's lifespan, each carrying a negative or positive valence, which collectively form that individual's lifetime welfare (Fig. 1). This framework for welfare research can be leveraged to ask ecologically relevant questions. What kind of ecological questions relate to welfare? One is how human disturbances impact the ecologically relevant behaviors of wild animals—a question that May Jiang, a recent graduate of UCLA, addressed during her undergraduate research. Specifically, Jiang investigated how a common method of blood sampling in reptiles, orbital blood draws, impacted the short-term foraging behavior of western fence lizards (Sceloporus occidentalis). Foraging is considered a positively valenced experience in welfare science and a functional trait in ecology, so measuring foraging behavior provided information on human impacts on both the ecology and the welfare of these animals. Field experiments showed that lizards took longer to capture and fully ingest crickets after undergoing the blood sampling, compared to when they were either left alone or captured but not sampled. Jiang's research addressed a classic question in animal welfare—how research methods influence animal well-being—and produced findings that have implications for both wild animal welfare science and ecology. Another example of how wild animal welfare research intersects with ecology comes from Dave Daversa's epigenomics research. Returning to the temporal framework for wild animal welfare (a timeline of positive and negative subjective experiences), Daversa is applying quantitative and computational genomics tools to develop measures of cumulative welfare, which incorporates the breadth of positive and negative subjective experiences that occur over an individual's lifespan. Using western toads (Anaxyrus boreas) as a focal animal system, Daversa is constructing “epigenetic clocks,” which describe the relationship between individual age and levels of DNA methylation—an epigenetic process whereby methyl groups bind to cytosine sites along the genome. Because methylated DNA accumulates as individuals age and is triggered by environmental stress, epigenetic clocks can offer clues about the cumulative impact of negative experiences (e.g., stress) on rates of aging. In fact, DNA methylation levels are associated with numerous welfare indicators, including disease risk and physiological regulation. In addition to telling us something about their lifetime welfare, measuring DNA methylation across a wild animal's lifespan has exciting ecological applications. Characterizing DNA methylation can reveal new insights into how wild animals are impacted by and respond to environmental stressors (e.g., human disturbance, infectious disease, extreme weather). Such insights will lead to a richer, more mechanistic understanding of species resilience to the stresses of rapid global change. By focusing on the valenced subjective experiences of individuals, wild animal welfare science has the potential to offer a deeper understanding of organismal biology from which ecologists stand to benefit. In turn, ecological frameworks provide a scaffolding for linking the subjective experiences of animals to the broader functioning of animal populations, communities, and ecosystems. At the intersection of these two fields lies a wealth of opportunity for new research that advances basic and applied understanding of wild animals. The World Organization for Animal Health (WOAH) defines animal welfare as “the physical and mental state of an animal in relation to the conditions in which it lives and dies.” By prioritizing the welfare of urban wildlife, we can prevent or reduce the risk of disease outbreaks and health challenges in these populations. Free-ranging wildlife health is not just the absence of disease. It is the ability of wildlife populations to bounce back from stressors (i.e., resilience), which includes consideration of factors that can be impacted by welfare (fitness, habitat quality, and level of exposure to disease). Wildlife population resilience is one of the three conservation biology Rs (the others being redundancy and representation) included in US Fish and Wildlife Service's Species Status Assessments, which characterize a species' ability to sustain populations in the wild over time. Nonresilient species are considered for enhanced conservation efforts and potential listing under the Endangered Species Act. The UK Farm Animal Welfare Council in 1965 developed a framework to achieve high welfare called The Five Freedoms. These underpin the animal welfare guidance described in WOAH's Terrestrial Animal Health Code. Yet scientific literature is sparse on how to incorporate these five freedoms when assessing the resilience of wildlife populations, especially those in our backyards. The five freedoms include (1) freedom from hunger, malnutrition, and thirst; (2) freedom from fear and distress; (3) freedom from heat stress and physical discomfort; (4) freedom from pain, injury, and disease; and (5) freedom to express normal patterns of behavior. By leveraging this framework, we can better understand the welfare challenges facing urban wildlife and work with natural resource agencies to reduce these threats to free-ranging wildlife health and resilience. Three examples were reviewed in this presentation to show the link between urbanization and wildlife welfare related to freedom from hunger, freedom to express normal patterns of behavior, and freedom from physical discomfort. An example of the linkage between freedom from hunger and urban wildlife welfare and resilience comes from Estes and Mannan (2003), who found that urban Cooper's Hawks (Accipiter cooperii) have a higher rate of prey delivery to nestlings in urban areas compared to those in rural locations. However, there was a welfare trade-off in that urban prey diversity was low (mostly Columbiformes-like doves) that were more likely to be infected with Trichomonas gallinae, a protozoan parasite. As a result, hawk nestling mortality was higher in urban areas. So, in this case, while hunger might be reduced in urban locations, the quality of prey in terms of infection status was lower. Interestingly, this is reminiscent of human health in urban food deserts where lower food quality may increase the risk of foodborne illness in residents (Kim et al. 2023). Regarding freedom to express normal patterns of behavior, there is evidence that the urban environment may change wildlife behavior (phenotype), reducing welfare and resilience. Prange and Gehrt (2004) found that abundant food in urban areas causes raccoons (Procyon lotor) to form larger social groups compared to relatively solitary behavior in rural raccoons. Urban raccoons have the potential to spread diseases (e.g. raccoon roundworms (Baylisascaris procyonis) and rabies) to humans and other animals, in part due to their behavioral changes. So, urban environmental impacts on raccoon behavior not only impact their welfare and health, but also that of humans, domesticated animals, and other wildlife. This exemplifies One Health, which is “an integrated, unifying approach that aims to sustainably balance and optimize the health of people, animals, and ecosystems. It recognizes the health of humans, domestic and wild animals, plants, and the wider environment (including ecosystems) are closely linked and interdependent (One Health High Level Expert Panel 2022).” In fact, animal welfare is highlighted in one of the five key One Health principles: “Stewardship and the responsibility of humans to change behavior and adopt sustainable solutions that recognize the importance of animal welfare and the integrity of the whole ecosystem, thus securing the well-being of current and future generations.” Finally, an urban wildlife welfare freedom whose impact on resilience is evident, but requires further exploration, is freedom from heat stress and physical discomfort. We know that the urban heat island effect impacts local climate (Grimm et al. 2008), negatively impacting habitat quality for urban terrestrial and aquatic wildlife. This heat stress impacts wildlife welfare and resilience. Similarly, new lines of research are investigating the impact of urban artificial light at night (ALAN) on wildlife health. Experimental studies by Kernbach et al. (2020) found that ALAN reduced melatonin and increased West Nile virus (WNV)-induced mortality in house sparrows (Passer domesticus). Thus, despite house sparrows' obligate commensalism with humans, some of the ways that we alter environments in urban areas have negative effects on their welfare and health. This data on WNV, a disease shared between people and animals, makes it clear that we need a One Health approach to urban wildlife management to reduce the impact of urban environments on wildlife welfare and health which can directly impact that of people and domesticated animals. These three examples show that the Five Freedoms framework can help us understand the complex effects of urbanization on the welfare and health of the wild animals that live in our backyards. Additionally, by utilizing a One Health approach, we can recognize that these wildlife welfare issues also impact domesticated animals and human health because of our proximity to urban wildlife. Further efforts to integrate the welfare framework into assessments of urban wildlife population resilience and urban development planning will also benefit international sustainable development goals (SDGs 3, 11, 14, and 15; Opoku 2019) because urban wildlife welfare has networked social-ecological system effects that we are only just beginning to understand. The preceding talks explain what welfare is and how it relates to ecology in general and urban wildlife in particular. But how can we actually assess welfare in wild animals? When defined as the valenced mental experiences of an animal over time, welfare is a hidden (a.k.a. latent) variable, meaning that it is inaccessible to scientists for measurement. Hidden variables are common in science (e.g., phylogeny, existence, and characteristics of distant exoplanets) but challenging to assess. These challenges demand the development of reliable, measurable indicators. Hidden variables are not the only types of variables for which we use indicators: We can also use them for composite or construct variables like health, or variables that are simply too difficult or expensive to measure directly, like biodiversity. Indicators and target variables can have three types of relationships: effect indicators are directly impacted by the target variable; causal indicators directly impact the target variable; and correlational indicators are impacted by a cause that also impacts the target variable (i.e., they are correlated but do not directly impact each other). While there may be important reasons to choose indicators of one causal type or another, any indicator must first be validated to ensure that it changes in a consistent way with the target variable. Use evidence to diagram the causal relationships between the target variable, the indicator, and the independent variables of interest that are believed to impact the target variable. In the case of welfare indicators, we might have Internal and external conditions → welfare (inaccessible) → indicator(s) We used this method to perform a mini-validation to give us an idea of which welfare indicators might be worth pursuing for wild House Sparrows. We created interventions that briefly raised or lowered welfare and recorded vocalization, postures, and activities. The positive welfare interventions were providing abundant, preferred food and creating a cool space during hot weather. The negative welfare interventions were inducing competition for preferred food and introducing a mock predator. We performed these for 1 hour each for five House Sparrow flocks around northwest Houston, TX, USA. Although this procedure is not extensive enough to be a full validation, we will use the results to determine which potential indicator(s) are most promising, so that we can focus on more extensive validations of the promising indicators. Performing validations for welfare indicators builds a strong foundation for further research into the welfare of wild animals. It is important to set aside plenty of time to perform these validations, and to carefully consider the causal relationships between indicators and target variables. Additionally, because altering conditions is typically the most difficult part of this procedure, we encourage researchers to collect data on multiple types of potential indicators during validation—for example, both physiological and behavioral data to reduce the need to repeatedly vary conditions each time a different indicator needs to be validated. Currently, many wild animal welfare studies are limited due to a lack of validated indicators. Thus, performing validations of welfare indicators for wild animals builds a strong basis on which future ecologists can continue to integrate welfare into their understanding of animal ecology. Knowledge produced by ecological research is often used to determine wildlife management strategies. Understanding more about the welfare of animals in the wild will better equip wildlife managers to maintain positive welfare in the populations they manage. One tool for wild animal management is chemical contraception, a less invasive method of population control. Although nicarbazin (NCZ), the active ingredient in contraceptive-laced bait, was originally developed as a coccidiostat for poultry, it has been proven to be an effective contraceptive in urban pigeons. NCZ has also been found to reduce heat tolerance in poultry, but little research has been done on NCZ's impact on heat tolerance in pigeons or other physiological or behavioral effects, despite its use in wild urban populations. Jessica Wright-Lichter conducted a study to determine if there is a correlation between NCZ exposure and number of heat-mediating behaviors, such as gular fluttering, panting, and wing spreading. In the study, pigeons were maintained in a facility intended to mimic their urban habitat, with NCZ-laced bait offered along with other high nutrition feed. Heat assays were created to test the impact of NCZ on heat-mediating behaviors, and plasma samples were collected to ascertain NCZ levels sufficient for contraception. The study found that, due to the low palatability of NCZ-laced bait, and regardless of acclimation regime, pigeons did not consume sufficient doses of NCZ to produce a contraceptive effect. While NCZ levels were too low to allow for analysis of NCZ's effect on heat-mediating behaviors, the discovery that the North American formulation of NCZ bait is not palatable enough to work as a contraceptive is significant for wildlife management. Pigeons' subjective experiences of the taste of the bait are integral to the bait's effectiveness, particularly since pigeons have many food choices in urban settings. NCZ bait must be at least as desirable to them as any food they can forage for themselves. Wright-Lichter plans to test the desirability of the different formulations of NCZ bait currently available before conducting further tests on the impacts of NCZ on pigeon physiology and behavior, and to continue to develop methods of analyzing welfare markers that are less disturbing to the subjects under study. The research presented at this symposium demonstrates neglected synergies between ecology and wild animal welfare science. Tapping into the mental states of wild animals adds new depth to fitness-related traits such as foraging, aging, sociality, health, and reproduction on which current models of population and community ecology are based. Animal mental states have evolved because, on the whole, they enhance fitness, yet we know very little about how this nontrivial part of animal lives contributes to their survival and reproduction. The abundance of wild animals in our own backyards presents exciting and accessible opportunities to explore this research frontier, which ecologists have traditionally avoided, to gain a deeper and more informed understanding of the lives of wild animals. Doing so will not only advance understanding of human impacts on wild animal ecology and welfare, but also allow us to confront our responsibility of reducing the negative welfare effects that we might cause. We are grateful to Grey Fernandez for organizing this symposium. BFF thanks the Science and Strategy Teams at Wild Animal Initiative for their feedback on an early version of her presentation. Wild Animal Initiative provided the conference registration fee, travel, lodging, and meals for the four symposium presenters. DD and JWL's work described here was funded by grants from Wild Animal Initiative. BFF's work described here was funded by Charities Aid Foundation Canada. No data were collected for this article.