Welfare and physiology: a complicated relationship

This research note is an extension of Physiology Researcher Michaël Beaulieu's paper, Capturing wild animal welfare: a physiological perspective, which was published August 27, 2023, by Biological Reviews online.

Short-term emotions and long-term moods correspond to affective states that, depending on the time scale being considered, determine how an animal experiences their life (Crump et al. 2018). In vertebrates, the generation of affective states depends on the relative levels of neurotransmitters (e.g. dopamine, serotonin, etc.) in specific regions of the brain (Lövheim 2012). Despite very different neural organization, most of these neurotransmitters are also found in invertebrates (with or without a central nervous system), in which they also appear to be involved in the expression of affective states (Bateson et al. 2011; Fossat et al. 2014; Perry et al. 2016). 

The production of neurotransmitters responsible for related affective states is triggered by external stimuli and requires information processing (e.g., exposure to predators triggering fear) and can, in turn, affect the whole peripheral physiology of the individual. In vertebrates, the transmission of affective states from central neural structures to the periphery of the individual occurs through the modulation of the autonomic nervous system and the hypothalamo-pituitary-adrenal axis (Stiedl et al. 2010; Keifer et al. 2015; Zhang 2021). Rapid transmission of affective states to the periphery is expected to be highly adaptive, as it likely helps animals to adopt the most relevant physiological and/or behavioral response (fight/flight vs. rest/digest) to the conditions they encounter. For instance, if an individual experiences fear because of the presence of a predator, adopting a fight or flight strategy is likely to promote survival, assuming they have the capacity for combat or escape (Doherty & Ruehle 2020). Such a response is associated with a sudden increase in energetic requirements and is expected to be accompanied: (1) At the physiological level, by the breakdown of stored macromolecules (e.g. glycogen, triglycerides, lipids) into usable smaller molecules (e.g. glucose, fatty acids, glycerol), their release into the bloodstream, and the inhibition of glucose uptake by peripheral organs; (2) At the functional level, by faster heart and respiratory rates, higher core temperature, and the redistribution of blood flow to priority organs (e.g. heart, brain, etc.).

Peripheral physiological and functional changes may themselves also affect the expression of affective states. For instance, laboratory mice for whom heart rate has been experimentally increased can experience anxiety-like states in risky contexts (Hsueh et al. 2023). Such peripheral effects on the expression of affective states may be mediated by a variety of physiological factors (e.g. hormones, inflammatory factors crossing the blood-brain barrier) and likely contribute to interoceptive processes (i.e., experiencing  the physiological condition of the body, such as temperature or pulse; Chen et al. 2021). Therefore the connection between the affective states experienced by animals and their peripheral physiology is bidirectional. In other words, the affective states experienced by animals (e.g. anxiety) can affect their peripheral physiology (e.g., heart function) and, conversely, their peripheral physiology can also affect their subjective experience. Importantly, affective states and peripheral physiological markers (i.e. ‘measurable indicators of the body’s physiological status’; Jesuthasan et al. 2022) may theoretically covary even in the absence of direct interactions between them if they are both affected by the same external factors. Peripheral physiological parameters may therefore reflect affective states both in a causal and in a correlative way.

The challenge of using physiological markers as welfare indicators

In the same way that wildlife biologists measuring physiological markers in other disciplines (e.g. ecophysiology, conservation physiology) have access only to peripheral physiological markers, biologists wishing to use physiological markers to assess the welfare of animals in the wild are also typically limited to peripheral measurements. This results from both limited availability of suitable techniques and limitations of the techniques currently available for directly measuring physiological processes that are occurring in the brain of free-ranging animals, the use of which would also raise important ethical concerns (Gaidica & Dantzer 2022). Peripheral physiological markers can also be measured in other tissues besides those that can be sampled directly from animals that have been captured (e.g. blood, muscles), including peripheral structures (e.g. hair, feathers) and excretory material (e.g. feces) left by animals in their environment. 

Because of the bidirectional relationship between affective states and physiology described above, any peripheral physiological marker affected by and/or affecting the expression of affective states could theoretically be used as an indicator to assess the welfare of wild animals. However, peripheral physiological parameters are not only involved in the expression of affective states but also in other processes, such as the regulation of homeostasis (i.e., “a self-regulating process by which biological systems maintain stability while adjusting to changing external conditions”; Bilman 2020). Importantly, homeostatic changes may be but are not necessarily related to changes in affective states. For instance, being dehydrated leads both to physiological changes aiming at correcting this imbalance (e.g., production of antidiuretic hormone) and to thirst (i.e., an affective state motivating water intake). In contrast, when the conditions with which the organism has to cope require an immediate response without interpretation by animals, peripheral physiological processes aiming at correcting homeostasis may be activated independently of any emotional processes when (e.g., hypoglycaemia; Herman & Culliman 1997). Hence, most peripheral physiological parameters likely reflect to some extent both the emotional and the homeostatic states of the organism, which are intermingled but not necessarily interconnected. Finally, because peripheral physiological functions constantly interact with each other, the relationship between a given peripheral physiological marker and a given affective state is likely to be blurred by the interactions that this specific physiological marker has with other physiological functions (themselves affected or not by emotional and/or homeostatic conditions). This complexity points to the need to develop methodological approaches to validate the use of physiological parameters as robust indicators of animal welfare.

Validating physiological markers as welfare indicators in the wild

Most wildlife biologists already measuring physiological markers appear to select markers based on their own knowledge, background, and experience. For example, in the field of ecophysiology or conservation physiology, plasma glucocorticoids are traditionally (rightly or wrongly) measured to assess how vertebrates cope with challenging conditions because of their implication in the stress response (Beaulieu & Costantini 2014, MacDougall-Shackleton et al. 2019). Assuming that glucocorticoid levels also reflect certain affective states, the choice to measure glucocorticoids in welfare studies would imply that (1) the considered affective states and glucocorticoids vary on the same time scale (Gormally & Romero 2020), and (2) the relationship between given affective states and glucocorticoids is predominant over any homeostatic influences affecting glucocorticoid levels. Typically these assumptions (and the choice of glucocorticoids) in welfare studies are not well justified, which has presumably contributed to question the relevance of using such markers to assess animal welfare despite their direct relationship with centrally-generated affective states (Ralph & Tilbrook 2016). The widespread use of glucocorticoids without clear evidence of the mechanisms and how to interpret results clearly demonstrates that peripheral physiological markers need to be validated before being convincingly used as welfare indicators. 

Based on Browning 2023, the validation process for peripheral physiological markers as welfare indicators could be divided into three consecutive steps: 

1. Formulating and articulating assumptions about the valence and arousal value of the affective states experienced by animals under certain conditions (e.g. a negative valence and an increased arousal assumed to result from predator exposure);

2. Measuring whether these conditions are associated with a change in the peripheral physiology of animals (e.g. higher glucocorticoid levels observed in animals exposed to a predator);

3. Ensuring that this peripheral physiological change is consistent across a variety of conditions assumed to affect welfare in a similar fashion (e.g. increased glucocorticoid levels observed irrespective of the nature of the predator and in socially-isolated or restrained animals). 

If a given physiological marker consistently varies across conditions all assumed to be associated with the same valence and arousal, then it could be considered as a robust indicator of welfare (as its variation is independent of the condition causing the assumed welfare change). 

Even though the proposed validation process may appear quite intuitive and simple, it may be difficult to put into practice, especially in the wild. Indeed, the last validation step implies the use of a replication approach based on the examination of different populations exposed to different conditions or the same populations sequentially exposed to different conditions (as recommended in ecological studies; Filazzola & Cahill 2021). This rigorous scientific approach may, however, be impracticable in the wild because of the associated increased costs, workload, and the potential disturbance generated by multiple animal manipulations. This limitation points to the need during the validation process to first consider the feasibility of including  collection of biological samples, and adopting a replication approach.

To facilitate this validation process, it might also be possible to apply it first to non-wild animals who might be better amenable to replication approaches, and for whom the conditions they experience can be better controlled. In that case, it might be possible to work with individuals of the same species as the species of interest in the wild, or those of a closely-related species — typically the subjects of laboratory studies (e.g. rodents, fruit flies) or among the many species kept in zoos. Researchers, who choose to apply the validation process to non-wild animals first before applying the results in the wild, must nevertheless be mindful that the physiology and behavior of non-wild animals may not necessarily be comparable to that of wild animals (Crates et al. 2023). At the very least, non-wild individuals may still be studied for the analytical, physiological and biological validation of particular physiological measurements (Palme 2019). Moreover, non-wild individuals could also be studied to examine the relationship between specific physiological markers and behavioral welfare indicators that have been previously established based on sophisticated behavioral approaches to directly reflect emotional valence. Such sophisticated behavioral approaches would be difficult or even impossible to use in the wild (e.g. cognitive biases; Crump et al. 2018).

Conclusion

The relationship between welfare and physiology is highly complex because it can be causal/correlational, direct/indirect, and bidirectional, which makes the use of peripheral physiological markers to assess wild animal welfare challenging. Even without knowing the exact nature of the relationship between peripheral physiological markers and affective states, it is still possible to apply a validation process to examine whether physiological markers can be used as reliable welfare indicators. By determining consistent relationships between markers and affective states across conditions, it is indeed possible to establish them as robust welfare indicators that could then be combined with other validated markers to obtain a more thorough welfare profile.

Many welfare biologists could be discouraged from applying the proposed validation process because it is based on various initial assumptions and requires such a demanding replication approach. Nevertheless, this challenge may be overcome by collaborations between welfare biologists and physiologists, wildlife biologists, or zoo practitioners. Importantly, once validated, physiological markers have several advantages for assessing wild animal welfare that may convince welfare biologists to use them:

• Physiological measurements are generally considered to be highly objective and straightforward. 

• Physiological responses can occur in the absence of any observable behavioral response.

• Physiological responses can be measurable in some tissues at a later time, following an event that affects welfare, thereby possibly reflecting affective states across time. 

• Finite physiological responses with pleiotropic (or multiple) effects on behavior, although variable, are likely to be more consistent than behavioral responses between species, thereby facilitating comparative welfare studies. 

As such, welfare biologists would benefit from adding validated physiological measures to their toolbox, as this may help them to draw a more holistic picture of the affective states experienced by animals in the wild.

Wildlife contraception and welfare

Contraception as a promising tool for welfare improvements

When resources are scarce, wild animals sometimes die of starvation (Gordon et al. 1988), dehydration, or exposure due to a lack of suitable shelters (Sibly & Hone 2002, Hill et al. 2019), all of which cause significant suffering (Gregory 2008). In many species, the competition for resources is especially strong among juvenile animals (Sol et al. 1998, Ward et al. 2006). Naively, making more resources available seems like it would solve the resource scarcity problem, but increasing the amount of available resources will often lead to higher fertility rates and juvenile survival rates, which eventually leads to larger populations instead (Prevedello et al. 2013, Ruffino et al. 2014), such that the competition for resources does not decrease in the long term.

One simple approach to find out how many animals are negatively affected by resource scarcity is to measure the fraction of deaths that are directly attributed to starvation. However, such an approach plausibly underestimates the pervasiveness of resource scarcity, due to interactions among different types of causes of death. For example, predation appears to be the most common cause of death for several taxa and life stages (Hill et al. 2019, Collins & Kays 2011), but whilst it is the proximate or final cause when it happens, it may not always be the ultimate cause — the underlying reason the lethal event occurred. For example, an animal that is starving may be prone to taking risks (Anholt & Werner 1995), or too weak to run away, which causes them to be more exposed to predators, making them more likely to be eaten. Therefore, even for some proximate causes of death that do not seem to be related to resource scarcity, there could be an underlying scarcity-related risk factor. In that case, a reduction of one cause of mortality (e.g. predation) might be partially or fully ‘compensated’ by the increase of another cause of mortality (e.g. starvation) such that life expectancy doesn’t change, known as compensatory mortality (Bergman et al. 2015). If everyone who is starving is eaten by a predator just before they would otherwise die of starvation, it would superficially appear like starvation wasn’t a problem at all, if we base our judgment solely on the proximate cause of death (predation in this case). Nevertheless, resource scarcity does appear to be a fairly common phenomenon (Prevedello et al. 2013), and irrespective of the ultimate cause of death, living a life of near starvation is a negative experience and of welfare concern. However, since resource limitations often are restraining population sizes (Prevedello et al. 2013), many populations will simply grow in response to increased resource availability, resulting in a larger population with similar levels of starvation.

Contraception provides one mechanism by which resource scarcity could be reduced, without inducing a corresponding increase in population size (Hecht 2021). Moreover, contraception may improve individual well-being through the alleviation of resource scarcity in other ways as well. For example, contraception could improve the welfare of the offspring by reducing sibling competition for resources (Mendl 1988, Andersen et al. 2011, Hudson et al. 2011). It could also reduce the burden of gestation and childrearing for some parents by allowing them to save energy and invest more in maintaining body condition (Kirkwood 1977, Kirkwood & Rose 1991, Lemaître et al. 2015). The cost of parental care, and thus benefits of reducing it, are dependent on the species and sex of the individual (Goldberg et al. 2020, Santos & Nakagawa 2012), which will cause additional variation in the net welfare effect of contraception.

There are several studies in which the effects of contraceptives on proxies for welfare have been investigated in wild animals (see Supplementary Table 2 in the review by Gray & Cameron 2010), and they seem to show both negative and positive welfare effects. The negative effects that were detected for some species/methods are related to maladaptive social behavior and inflammation at injection sites, among other things (Gray & Cameron 2010). The plausibly positive effects that have been found are related to survival and body weight, which are the types of benefits that we would predict given the model outlined in the previous paragraph. Several of the studies on survival detected increases (see for instance: Twigg et al. 2001, Turner & Kirkpatrick 2002, Williams et al. 2007), but one of them found no effect (Saunders et al. 2002), and two of them observed mixed results (Ransom et al. 2013 and Bromley & Gese 2001). Many studies have looked for changes in body weight, and several of them have found increases in treated females (see Table S2 in Gray & Cameron 2010). Such increases in body weight could serve as a proxy for welfare through improved nutritional status, but it could also be a reflection of changes in satiety and the foraging risk-reward trade off, where the ultimate effect on welfare is less clear. Many studies have had very small sample sizes, lacked control groups, and focused on a narrow set of welfare relevant traits, so it is hard to draw any strong conclusions. However, it seems very likely that the type, target and delivery mechanism of contraceptives have contributed to the observed differences in welfare-related outcomes among studies.

It is important to note though, that wildlife contraceptives haven’t been developed or applied with the goal of improving wild animal welfare by alleviating resource scarcity. As an analogy: even though a squirt gun is ineffective at putting out large fires — it was never intended for that use — water delivered in the right way is nonetheless very useful when there is a fire. Similarly, it is perhaps no surprise that the currently available evidence on the welfare effects is inconclusive, if no one has intentionally tried to improve wild animal welfare with it. It is the compelling theoretical potential that wildlife contraception offers for significant welfare improvement for large numbers of individuals that makes us excited to see further research in this area.

A very brief history of wildlife contraception research

As of 2011 (Kirkpatrick et al. 2011), wildlife contraception had been developed and successfully tested in 85 species of animals (mostly mammals), and work on different forms of wildlife contraception have continued since then (Asa & Moresco 2019). There are several different forms of contraceptives available for wild animals. Vaccine-based contraceptives (so-called immunocontraceptives) like the porcine zona pellucida (PZP) vaccine and the gonadotropin-releasing hormone (GnRH) vaccine were developed for feral horses and other wild mammals in the 1980s, and are still being used today (Asa & Moresco 2019). Steroid hormonal contraception methods have also been investigated, although high costs, toxicity, and problems with delivery (Kirkpatrick et al. 2011) have caused these methods to mostly be abandoned. Surgical sterilization has also been used to reduce fertility in wild populations of animals (Denicola & Denicola 2021), but because of the invasiveness of the procedure, it is likely more detrimental to animal welfare than other methods (Hampton 2017). It is also oftentimes more expensive per treated animal (Kirkpatrick et al. 2011). More recently, contraceptives have been developed for birds (Nicarbazin), such as pigeons and geese, and 4-vinylcyclohexene diepoxide (VCD) developed for rats (See box). These contraceptives prevent fertilization (in the case of Nicarbazin) or development of germ cells (in the case of VCD), and have only recently become available as commercial products. Products like these open up the potential for large-scale application of wildlife contraceptives, given the abundance of pigeons and rats in the world, and the potential for use in other related species.

Future research

Although scientists have conducted wildlife contraception research for decades, the focus of this research has largely not been on the welfare impacts of contraception, most likely because the primary goal has been to reduce population sizes of pest or managed species, rather than to improve welfare. Consequently, more research is needed to address the many unanswered questions regarding the possible connection between contraception and welfare. Examples of such questions include: can we expect better or worse welfare outcomes in certain taxa? If there is strong interspecific competition, will contraception lead to compensatory population growth and resource use by competitor species, eliminating the potential positive effects?

In addition to ecological considerations of contraceptive use, each of the methods requires additional scrutiny. How do different delivery methods, such as oral baits, injections and surgical sterilizations differ in their welfare effects? What are the welfare related side-effects, and in what contexts do they outweigh the possible positive welfare benefits? What are the long-term welfare effects to the treated animals? What are the indirect effects from changes in population sizes on the welfare of individuals belonging to other species?

Finally, the inter-individual dynamics of different animal populations generate additional research questions. For example, do the effects of contraception on welfare differ between solitary and social species? One reason we might expect different welfare outcomes in social and solitary species is that for social species, fewer offspring could affect the collective gathering of resources or protection from outside threats. A smaller group could be suboptimal relative to a larger social group, and contraception could therefore reduce the group size below its optimum and have negative welfare implications. Conversely, individuals of solitary species might mostly experience competitive interactions with conspecifics, where a smaller population size would be more likely to have positive welfare effects through reduced competition.

We outline a few potential projects that could help answer some of the questions regarding the welfare aspects of wildlife contraception:

• Project idea 1: Empirically test the welfare effects of a contraceptive agent, with a focus on both the direct and indirect effects on individuals within the population. See an example for such a project on pigeons. Another target could be rodents (using, for example, the product ContraPest) or other species that have high fertility (with potential to improve the welfare of many individuals).

• Project idea 2: Empirically or theoretically test whether and how sociality interacts with the potential welfare effects of contraception.

• Project idea 3: Empirically test whether different delivery methods have different average welfare outcomes, and whether it is possible to predict which method will suit different types of species.

• Project idea 4: Empirically explore the factors that determine perceptions of wildlife contraceptives, and determine public support for making improvements beyond the ‘natural’ welfare-level as opposed to just minimizing harms.

For all of the possible projects mentioned above, studying both adults and juveniles would be highly valuable when possible, given that we expect somewhat different mechanisms to mediate the welfare effects in adults compared to the welfare effects on juveniles. For instance, we would expect any reduction in sibling competition to primarily affect juvenile welfare.

Box 1

When looking for ways to test hypotheses about the welfare effects of contraceptives on wild animals, we want to look for projects where there is a potential for improvement to a lot of individuals. Rats (Rattus spp.) seem highly promising in that regard, given that they have high fertility rates. The reproductive strategy of rats results in a large number of ‘excess’ individuals who will most likely die before they reproduce. By reducing competition, contraception might increase the fraction of juveniles surviving to reproductive maturity, even if there is no change in the size of the adult population. Humans are also already exploring contraceptive interventions for them. ContraPest (developed by SenesTech) is a type of contraceptive that can be used for rats and other rodents in the United States. Testing the welfare effects of ContraPest on rodents, or indeed trying to further cut costs or develop additional types of contraceptives for rodents, seem like very promising avenues for further research.

Pigeons (Columba livia) are another promising target species for studying the welfare effects of wildlife contraceptives, as they are also very common, and there is a commercially available contraceptive for them (OvoControl, produced by Innolytics). The fertility rate of pigeons is lower than the fertility rate of rats, which therefore likely affects the potential for juvenile welfare improvement. Nevertheless, the available contraceptive for pigeons appears to be somewhat cheaper than for rats, as is indicated by my rough cost estimate for applying OvoControl and ContraPest to populations of pigeons and rats, respectively. In addition, public support for pigeon welfare (and other bird species) improvements is likely to be greater than for rats (Jaeger & Wilks 2021), so studying the welfare effects of OvoControl might have greater potential for widespread implementation. Hence, studying the welfare effects of pigeon contraception might be the most promising option, in order to eventually achieve welfare improvements for wild animals through contraception.

While currently available data does not clearly demonstrate welfare improvements from contraceptive applications, there are good theoretical reasons to expect that contraception could be extremely effective under the right conditions. Therefore, if we explicitly try to use contraception to improve wild animal welfare, it has the potential to improve the living conditions of many wild animals, especially in populations where resource scarcity is pervasive. Wildlife contraception holds great potential to improve wild animal welfare, and research to address the key theoretical and empirical questions should be a priority.

Summary of “What is the value of wild animal welfare for restoration ecology?”

This piece was published in the March 2020 issue of Restoration Ecology.

Why discuss wild animal welfare in restoration ecology? 

Research and outreach disrupts status quo narratives, such as the perception that wild animal welfare and environmental management must operate under mutually-exclusive values, metrics, or models. Writing peer-reviewed articles in environmental science journals builds a common academic language to address environmental problems. It also catalyzes interdisciplinary thinking by considering pluralistic, alternative ethics of environmental stewardship. These two steps both bring us closer to generating solutions for improving the lives of wild animals. 

Our overall thinking is that proponents of wild animal welfare and restoration ecology share, to some extent, a non-anthropocentric worldview and a desire to collaborate to help wild animals. Yet the virtues and consequences of “respect and responsibility for wild animals” are viewed through a different lens by ecologists and proponents of wild animal welfare. 

The research in a nutshell

To build common ground toward solutions for improving the lives of wild animals, we provided a window into the animal welfare community for restoration ecologists, particularly wild animal welfare’s ethical positions and research priorities. We also acknowledged that people may differentially prioritize welfare- and conservation-oriented objectives. Yet, wild animal welfare is relevant, regardless, because of the instrumental value of providing for the needs of individual animals. 

To further frame our argument around animal ethics and morality, we blended our instrumental arguments around the moral foundations of conservation ethics, established in Aldo Leopold’s land ethic. We highlighted that the land ethic includes moral concern for individual, “fellow-members” of the landscape. Despite the value the land ethic places on animals, the management community has not resolved how to support individual animals while maintaining their ecosystem. It also does not sufficiently account for diverse ethical perspectives regarding what constitutes good environmental stewardship, nor take advantage of the information-value of animal welfare, as animal well-being depends on a host of behavioral, physiological, and environmental factors. 

Key takeaways

Our manuscript illustrates three ways that the perspective of wild animal welfare augments restoration ecology. 

1. Strengthening relationships between people and nonhuman animals. Restoration ecology could engage with wild animal welfare to advance a human-nature relationship infused with empathy and altruism.

2. Supporting multidimensional ecosystem health. It is possible to simultaneously improve ecosystem function and animals’ well-being. Synergistic interventions would concurrently support individuals and ecosystems, with the added benefit of encompassing multiple ethical and moral stances regarding what is good environmental stewardship.

3. Reducing uncertainty about interventions. Several aspects of animal welfare, such as health, physiology, behavior, and cognition, can modify species, communities, and ecosystems. A greater understanding of these relationships can reduce uncertainty regarding the outcomes of interventions for wildlife collectives or individuals. 

Next steps

An essential challenge ties together proponents of environmental management and wild animal welfare: resolving ethical and ecological conflicts on an increasingly complex and interconnected planet. The challenge for the wild animal welfare movement is to illustrate the ways that wild animal welfare is important and viable. Future work on these topics continues at Wild Animal Initiative to reorient animal advocacy and environmental science with a view of wild animals as morally-relevant subjects, who are entitled to a good life, and to catalyze evidence-based solutions for modern environmental problems on behalf of wild animals.