In his 1872 book The Expression of the Emotions in Man and Animals, Darwin proposed that insects might express basic forms of emotion through the stridulation of their wings. Despite this early suggestion, the study of emotions in invertebrates has been a subject of both intrigue and scepticism. These organisms are often considered as simple reflex machines due to their relatively less complex nervous systems compared to vertebrates. However, emerging and convincing evidence suggests that despite their relatively simple neural architectures, they have remarkable cognitive abilities that build upon associative learning, enabling flexible and adaptive behavior (Giurfa, 2013). The view of invertebrates as cognitively sophisticated organisms is slowly changing the perspective on their emotional life too, opening the proposal that they might be capable of experiencing states resembling human-like emotions. While challenging our anthropocentric notions, the investigation of emotions in invertebrates promises to broaden the understanding of the evolutionary origins and adaptive functions of these phenomena across the animal kingdom.

Defining Emotion

From a biological and evolutionary point of view, emotions are defined as neurological survival mechanisms that enable organisms to prioritize and coordinate responses to environmental challenges. However, this definition provides no insight into their nature. Fundamentally, and from a human perspective, an emotion can be considered as a private, subjective and transient state that can be communicated to others through verbal and non-verbal behaviour (e.g., facial expressions). Over the years, this definition has been enriched through the study of multiple correlates of the emotional experience, including physiological markers, somatic manifestations, and cognitive processes. This broader definition has enabled scientists to assess emotions in phylogenetically distant species, such as invertebrates, where emotional manifestations might not have evolved from the same ancestral origin (i.e., they may not be homologous) while still appearing similar (analogous) to those in humans (Mendl, Burman and Paul, 2010; Anderson and Adolphs, 2014; Perry and Baciadonna, 2017).

The study of emotions in phylogenetically distant species is also based on the proposal that they may share fundamental properties, i.e., building blocks, that are conserved across species and that are common to different emotional states. Some of these building blocks include properties, such as persistence (emotional states lasting beyond the immediate presence of a stimulus), scalability (the proportionality of the response to the intensity of the salient stimulus), valence (the quality of the emotional response, whether positive or negative), and generalization (the transfer of an emotional response to stimuli that are similar but not identical to the original elicitor). The study of the building blocks of emotions can help differentiate emotional responses from simple reflexes and can highlight their fundamental role in adaptive behaviour. In other words, it can bypass the dichotomous dilemma as to which species are capable of emotions, and open new avenues on the understanding of their underlying, shared and unique mechanisms (Anderson and Adolphs, 2014).

Evidence of emotions in invertebrates

Several studies have demonstrated that invertebrates exhibit behaviours that resemble the building blocks of emotional states. One of the earliest and most astonishing evidence of this, is Kandel’s study on the sea slug (Aplysia californica), which demonstrated that the ability to predict aversive events through learning the association between a neutral stimulus and an aversive one (also defined as “classical conditioning") is not only present in mammals, but also in “simpler” species (20000 neurons). Kandel and colleagues proved that the simple presentation of a shrimp extract previously paired with an electric shock induced defensive responses, such as withdrawal, inking, escape, and reduced feeding, also and importantly in the absence of the electric shock. This pioneering work contributed to Kandel’s impressive research on the neurobiology of learning and memory, which was recognized with the attribution of the Nobel Prize in 2000 and paved the way for more investigations of this kind (Kandel, 2006).

For instance, recent controlled studies have shown that bees exposed to predators (i.e., Asian hornets, Vespa velutina) modify a range of behaviours in response (Dong et al., 2023). These include spending less time near the predator, moving more quickly in its presence, and retreating faster when threatened. At the colony level, when hornets appear at food sources, foragers retreat into the nest, reduce their recruitment dancing, and emit specific sounds known as stop signals, which further inhibit dancing. These inhibitory stop signals also decrease levels of the neurochemical dopamine in the bees' heads, which could potentially reduce their perception of food quality. These findings highlight the profound systemic effects that predators have on bee behaviour, sensory processing, and colony dynamics. If the experience of putative negative emotions in invertebrates can seem somehow unsurprising, due to its role in promoting survival, the experience of possible positive emotions is perhaps even more remarkable. Positive emotions too play a crucial role in species survival. They promote the approach of valuable stimuli and can help mitigate the impact of stressors. For example, bumblebees receiving a small drop of sucrose (a rewarding stimulus) started foraging faster after a simulated predator attack compared to a control group that did not receive a reward, suggesting that the small pre-test reward helped mitigate the impact of a stressful experience (Solvi, Baciadonna and Chittka, 2016).

These studies have demonstrated the existence of emotion-like states in simpler animals by observing behaviours, biological and physiological responses during learning paradigms (e.g., classical conditioning) or following the induction of specific stressor. Another set of paradigms has been used to test the existence of emotional experiences across taxa. These paradigms assess how emotions can influence cognition (e.g., decision-making). Pioneering work by Mike Mendl and collaborators demonstrated that unpredictable housing conditions, a stressful event, can lead to judgment biases in rats, suggesting a link between emotional states and cognitive processing. (Harding, Paul and Mendl, 2004). The use of the judgment bias tests was inspired by multiple lines of research in human clinical psychology, which suggest that individuals experiencing negative emotional states, such as anxiety or depression, tend to make negative judgments about ambiguous stimuli. A well-known example to illustrate this, is a study conducted by Eysenck et al. (1991). In this study, participants were presented with an ambiguous sentence, such as "The doctor examined little Emily’s growth." Individuals diagnosed with generalized anxiety disorder interpreted the sentence negatively, as if Emily had some disease. In contrast, control participants and people recovered from anxiety interpreted the statement as neutral, assuming that Emily was growing normally in height and weight.

In the seminal study mentioned above (Harding, Paul and Mendl, 2004), rats were trained to press a lever in response to a tone predicting a food reward and to avoid pressing it in response to a tone predicting an aversive white noise. Once they mastered this discrimination, they were subjected to an unpredictable and detrimental housing condition, designed to induce a negative state, or to a predictable good housing condition. When exposed to ambiguous tones with intermediate frequencies, rats in the unpredictable housing condition responded more slowly and less frequently than controls, suggesting reduced anticipation of a positive outcome. This response pattern closely resembles behaviours observed in depressed or anxious humans, where interpretations of ambiguous situations tend to be negatively biased. The judgement bias test has since been applied to various species, including honeybees and bumble bees. In honeybees, exposure to stressors, such as shaking, induced a negative cognitive bias (Bateson et al., 2011). Bees shaked for 60 seconds were less likely to respond to ambiguous odour cues associated with punishment. On the other hand, Solvi and colleagues (2016) demonstrated that bumblebees, when given a small pre-test sucrose reward, exhibited a positive cognitive bias, showing faster responses to ambiguous cues. More recently, a novel application investigated how physical stressors can impact cognition in bumblebees using what is called an active choice paradigm. Unlike the classical go/no-go paradigm described above, where individuals either approach or suppress an action, the active choice paradigm requires bumblebees to make a choice, allowing them to directly indicate their interpretation of ambiguous stimuli. This approach has been useful to address potential confounding factors, such as motivation and attention, otherwise not controlled for in the go/no-go paradigm (Procenko, Read and Nityananda, 2024).

So far, this evidence supports the claim that invertebrates have states that fit the criteria used to define emotions.

Why we care: ethical implications and impact

The proposal that invertebrates are capable of emotion-like states has significant ethical implications for their treatment and welfare, including regulations as to how humans should interact with them. To establish whether invertebrates are capable of sentience, significant efforts have been made to develop an empirical and scientific framework that includes neurobiological and behavioural criteria (Birch et al., 2021; Crump et al., 2022). Based on these criteria, for example, it has been concluded that cephalopods and decapods are indeed sentient beings; evidence that resulted in the adoption of the UK’s Animal Welfare (Sentience) Act in 2022.¹

The adoption of these criteria across six insect orders has been used to argue that at least two of them, Blattodea (cockroaches and termites) and Diptera (flies and mosquitoes), might be sentient too. To date, studies investigating sentience in the Hymenoptera (bees, ants, wasps) order are scarce, compared to other others (Gibbon et al., 2022). Therefore, further research is needed to assess whether they meet the established neurobiological and behavioral criteria for sentience. Expanding our understanding of their cognitive and emotional capacities could have profound implications for their ethical treatment and welfare regulations.

Conclusion

The study of emotions in invertebrates is an exciting and rapidly evolving field. Evidence from behavioural, cognitive, and neurophysiological studies support the idea that invertebrates exhibit emotion-like states, albeit in forms that may differ from those of vertebrates. These findings not only expand our understanding of invertebrate biology but also prompt a revision of the evolutionary origins and ethical dimensions of emotion. As research advances, our understanding of invertebrate emotions is likely to deepen, reshaping our perspective on the emotional lives of animals.

References

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