First and foremost, when aiming to investigate emotions or feelings, the terms should be clearly defined an operationalized. In the relevant literature, different terms are being used to refer to emotion. Some researchers choose to use certain terms exclusively for humans, while other words are mostly used for other animals. Andrews (2020) stresses that if we invent new words for other species while keeping old words for human beings, we are throwing up unnecessary semantic barriers to comparing humans with other species. Interpreting behavior as associated with a particular feeling in humans and interpreting the same behavior as something else in animals thwarts comparative research, and consequently the progress of fundamental research into the proximate and ultimate causations of emotions.
Increasingly, researchers approach emotions as multifaceted states that include physiological, behavioral, and cognitive components that are measurable (Mendl et al., 2010; Paul et al., 2005; Massen et al., 2019). We believe that insight in emotion states can be gathered with various methods.
Numerous examples could be given, but just to make our case, we will cover a few here that combined relatively noninvasive methods in various species to compare behavioral and physiological measures of emotions. In a study using thermography, Nakayama et al. (2005) demonstrated a decrease in nasal skin temperature in rhesus macaques in response to a human dressed in a lab coat and holding a catching net. Along with this temperature drop, the monkeys frequently showed a silent bared-teeth face, staring open-mouth face, and lip-smacking, all expressions of negative emotions. Another example is the finding that in a touchscreen task, bonobos had an attentional bias towards emotional expressions of conspecifics. In addition, more “nose-wipes” were observed during trials where an emotional image had to be approached rather than avoided, indicative of emotional arousal (Kret et al., 2016). In an experiment with dogs, it was shown that when separated from their owner, dogs were more alert. They stood up, walked, or ran around and especially towards the door, while barking and whining. On the physiological level, a detailed analysis of their heart rate suggested a negative emotion (Katayama et al., 2016). Another study by combining behavioral and cardiac measurements suggests that sheep have negative emotions following negative events, and positive emotions following positive situations (Reefmann et al., 2009). Cardiac activity and salivary cortisol concentration were combined in a study with horses (Janczarek et al., 2019). The horses showed negative emotions in response to the presence of an audience in the arena. By measuring psychophysiological reactions, hormone levels, cognitive bias tasks or behavioral observations, emotions can be inferred.
Emotions are contagious: i.e., they easily spread throughout a social group. Various studies have shown basic forms of empathy in social species, from rodents to primates, such as mimicry of expressions of emotion, matching another’s emotional state, and responding to the distress of others with reassurance behavior or helping actions (reviewed by Preston & de Waal, 2002; de Waal & Preston, 2017). Some animals, such as ravens, not only match conspecifics’ emotions on a behavioral level (e.g., Osvath & Sima, 2014) but also match their judgement bias, which is interpreted as an emotional state, after having witnessed a conspecific react with apparent frustration to a negative manipulation (Adriaense et al., 2019). Chimpanzees show jealous reactions when their own valuable social bonds are under threat (Webb et al., 2020); long-tailed macaques relax (i.e., show a decrease in circulating cortisol) while cooperating with a friend (Stocker et al., 2020), and several species consider “the glass half full rather than half empty” in judgement- or cognitive bias tasks (Paul et al., 2020). In line with Panksepp’s argument, recent research incorporating the behavioral, physiological, and cognitive components of emotions, is thus suggesting that not only do animals show emotional behavioral responses, they also seem to experience them as well as those of conspecifics (Kret et al., 2020; Nieuwburg et al., 2021).
Emotions are embedded in a complex network of brain structures including both cortical and subcortical areas activated in close interplay with the body (Prochazkova & Kret, 2017). Recent neuroimaging research taps into emotions and their cognitive interpretation and shows that it’s too simple to state that “feelings are cortical.” Using ecologically valid paradigms involving risky decisions or social dilemmas to induce strong emotions, these studies have shown the pivotal role of ancient brain structures in human feelings of social exclusion, depression, and even suicidal tendencies (e.g., Cáceda et al., 2020). Other studies have demonstrated a close connection between the body and the brain. For example, a study put participants under high levels of stress while measuring bodily responses (heart rate, skin conductance, cortisol), self-reported stress levels, and brain activity via fMRI. Clear relationships were observed between the neural responses on the one hand and bodily responses and self-reported stress on the other (Orem et al., 2019).
Emotions even recruit the most ancient neural structures. The spinal cord rapidly activates in response to emotional stimuli (Smith & Kornelsen, 2011), and classical work by Hohmann (1966) has shown that a spinal cord lesion drastically impacts the feelings reported by patients. We are not saying here that all animals with a spinal cord have feelings. But the involvement of such structures, which are highly conserved among vertebrates (Leung & Shimeld, 2019), casts doubt on the emphasis on consciousness, language, cultural construction, and human uniqueness. Even the evolutionarily more “recent” neural architecture of humans is mostly shared with mammals and birds (e.g., Stacho et al., 2020). The human brain is hardly categorically distinct from other brains. That said, we don’t deny that the human brain may have features that other species lack (e.g., Koechlin, 2011; Preuss, 2011; Semendeferi et al., 2011) and that these unique structures may alter emotional experiences (LeDoux, 2017). At the same time, this is also true for other species since all species have unique brains. The difference is that there is a lot more unknown about the role of other species’ brain structures in emotions. Demonstrating parallel neural mechanisms involved in the emotions of humans and other animals, Panksepp (2011) saw no reason to postulate different emotional experiences, and we tend to agree with him on this point.
But even if we do put an emphasis on consciousness: Recent studies on mirror self-recognition (as a proxy for self-awareness), theory of mind, metacognition, and planning for the future (reviewed by de Waal, 2016) do suggest self-reflective capacities in animals, even if some other scientists remain skeptical (e.g., Heyes, 2017; Povinelli, 2020). For example, rhesus monkeys have “memory awareness” in that they know what they know or don’t know (Smith et al., 2013; Templer & Hampton, 2012); capuchin monkeys, California scrub jays, and Eurasian jays seem to not only grasp what others know, but also what others desire (Hattori, 2012; Ostojić et al., 2017), and chimpanzees take (false) beliefs of conspecifics into account (Krupenye et al., 2016). Given how ill-defined consciousness is and how widespread advanced cognitive traits seem to be in other species, we deem it premature to assume that said species have no consciousness of their emotions. From an evolutionary perspective, it is more logical to assume humanlike consciousness in species related to us rather than deny it, which means that we best adopt the former as a working hypothesis (de Waal, 2019).
Cognitive and Evolutionary Parsimony and Ethical Considerations
Imagine an animal that backs away from a harmful stimulus. We see a chimpanzee who, while staring at a snake and uttering soft alarm calls, carefully and slowly moves out of the way. The starting point of some scientists, for example, LeDoux, is that such behavior should be assumed to be unconsciously controlled and devoid of feelings unless proven otherwise. The rule of cognitive parsimony is applied here, which postulates the simplest possible cognitive process when it comes to interpretating behavior. Cognitive parsimony is important to consider when interpreting behaviors of many animal species. If in the example above we would have described the behavior of a fruit fly instead of a chimpanzee, we agree that this approach would be most correct. However, the example is about humans’ most closely living relative, a species that is well-studied and one that we have a lot of information on.
It is important to realize that the rule of cognitive parsimony is rarely applied to human behavior. When researchers suggest that human emotions rely on higher-order conscious cognitive processes, since humans verbally report their emotions, they risk postulating processes that may be unnecessary, hence violating Occam’s razor. Setting aside the discussion about the validity of self-report, feelings are best considered the consequence rather than the cause of emotional states (Anderson & Adolphs, 2014). Consequently, we think that feelings cannot inform us about the cognitive processes and complexity of the emotional state itself. In our view, this chimpanzee in the above example is feeling scared and is acting deliberately cautiously to minimize potential harm. This does not mean that that interpretation is all that should be reported. To get the picture complete, it should be accompanied with an objective description of the behavior so that this data remains accessible and open for future interpretation.
By looking to preserve cognitive parsimony at all costs, comparative psychologists may be disregarding evolutionary parsimony, which dictates that we should offer explanations that posit the fewest possible changes in the phylogenetic tree. Although cognitive parsimony can be important, we here would like to emphasize the biological stance of evolutionary parsimony, stating that when related species show similar behavior under similar circumstances, these are likely driven by similar psychological processes (de Waal, 1999). Until the contrary can be demonstrated, we must assume that similar behavior in these species is paired with similar emotions and in some cases similar feelings. This position is, of course, not entirely new. One of the first to advocate cross-specific uniformity in behavioral explanations was philosopher David Hume (1739, p. 226), who formulated the following touchstone well before we had a theory of evolution:
Tis from the resemblance of the external actions of animals to those we ourselves perform, that we judge their internal likewise to resemble ours; and the same principle of reasoning, carry'd one step further, will make us conclude that since our internal actions resemble each other, the causes, from which they are deriv'd, must also be resembling. When any hypothesis, therefore, is advanc'd to explain a mental operation, which is common to men and beasts, we must apply the same hypothesis to both.
Hume’s stance raises the question how far we can stretch the concept of similar states and how related two species should be for them to experience similar feelings. Whereas, given the ancient structures and mechanisms involved, we do expect some sort of emotional states in all animals, we are agnostic about feelings in distantly related species, such as invertebrates. Conversely, we argue that it is unreasonable to exclude the possibility of feelings in all animals and specifically in those that are closely related to us, hence similar in body and brain. We, furthermore, embrace the idea that feelings may have evolved convergently in multiple lineages and that the comparative study of these taxa will help us shed light on the selection pressures that may have shaped the evolution of both emotions and feelings (Fitch et al., 2010; Massen, 2020).
Finally, we would like to include a warning. Those who do not set emotions apart from feelings, and doubt the latter’s existence in animals, have a special obligation to produce convincing evidence when they deny the existence of animal feelings. This Cartesian position carries ethical implications. Humans experience a different sense of obligation towards entities with or without feelings, which is why the question of animal sentience is central to every current debate about the humane treatment of animals. This means that we need to proceed with the utmost care in this domain so as to avoid giving fodder to those who consider animals unworthy of moral consideration. We (including the authors of this opinion piece) have an obligation to be clear about what is a mere assumption and what is fact when it comes to animal feelings. At the same time, scientific evidence of animal emotions is needed to create a better understanding of the depth of their emotional lives. To that extent, the section below lists some important steps to be taken.
Where to Go from Here?
First, we should shift the focus from things we cannot measure to things that we can measure (Adolphs & Andler, 2018). For example, technological advances allow us to measure animal’s emotional facial expressions (e.g., the chimpanzee’s and other species’ FACS of Waller et al., 2020). We can also noninvasively measure bodily expressions and physiological arousal by using thermography, pupillometry, heartrate measurements, hormone levels, and measurements of neural activation (reviewed by Nieuwburg et al., 2021). Similarly, we study emotionally biased decision-making and the perception of emotions in experimental paradigms with techniques such as touchscreens and eyetrackers (e.g., Parr & Heintz, 2009; Kret et al., 2016). We acknowledge that the associated feelings still remain inaccessible but note that this also largely holds for humans. For this reason, our recommendation to focus on emotions’ measurable aspects extends to modern psychological research on humans, which thus far has concerned itself more with feelings than emotions. Doing so will facilitate comparisons between humans and other species and move us away from the unreliability of introspection (Baumeister et al., 2007). This is not to deny the importance of feelings, but there is debate (see above) about how essential they are to the way emotions work.
Second, the aim of human and comparative psychology is to understand psychological states or traits through experimentation, observation, and interview. We seek to understand behavior and assign meaning to what we see, often using hypotheses based in physiology, neuroscience, and/ or evolutionary theory. Whether postulated intervening variables are knowable or unknowable is not always the issue. We don’t ask astronomers not to invoke gravity, which is invisible, to explain planetary movements, or biologists not to invoke shared evolution, which is also invisible, to explain why chimpanzee hands are so strikingly similar to those of humans. Science is full of postulated intervening variables to make sense of observed phenomena. In the same way, the invisibility of animal feelings is not a good argument against them.
A third step forward, in our view, is to try to take the perspective of animals more when asking questions and designing studies. If we take a typically human phenomenon and ask the question whether, say, chimpanzees show it too, it is more likely that this behavior characterizes us better than them. The animal behavior literature is full of examples where we have misjudged animals based on human testing biases (de Waal, 2016). These biases often dictate the search for humanlike traits in animals, especially in those that are closely related to us, and in doing so overlooks the uniqueness of other species. We have trouble seeing a chimpanzee the way a conspecific does. Rather than focusing on humanlike emotions, we should consider the species-specific emotions of other animals as they have evolved in line with that species’ specific needs. We need a bottom-up approach that does not necessarily focus on predefined human emotions.
To conclude, in our view, if a species shows behavioral, neurophysiological, hormonal, or cognitive responses to valenced stimuli, we can speak of emotions until proven otherwise. In some instances, we might even speak of feelings. We advocate a multi-method rather than a single method approach and believe that the variety of species that we can study, with their unique brains and bodies, can give us new insights into emotions and feelings.