Plant sentience? Between romanticism and denial: Science

A growing number of non-human animal species are being seriously considered as candidates for sentience, but plants are either forgotten or explicitly excluded from these debates. In our view, this is based on the belief that plant behavior is hardwired and inflexible and on an underestimation of the role of plant electrophysiology. We weigh such assumptions against the evidence to suggest that it is time to take seriously the hypothesis that plants, too, might be sentient. We hope this target article will serve as an invitation to investigate sentience in plants with the same rigor as in nonhuman animals. Miguel Segundo-Ortin is a postdoctoral fellow in the Department of Philosophy and member of the Minimal Intelligence Laboratory at the University of Murcia (Spain). His research is in the philosophy of the cognitive sciences, particularly embodied cognition, comparative cognition, and human agency. Website Paco Calvo is Professor of Philosophy of Science and PI of the Minimal Intelligence Laboratory at the University of Murcia (Spain). His research is on (the philosophy of) plant neurobiology, ecological psychology and embodied cognitive science. He is co-author with Natalie Lawrence of Planta Sapiens (Little, Brown (UK); Norton (US)). Website 1. Comparative cognition and the study of sentience in plants: An overview of the debate ‘Sentience’ refers to the capacity of an individual to have felt states, including sensory experiences, external or internal. Although the interest in studying sentience in nonhuman organisms is increasing, this research remains, in our view, remarkably Call for Commentary: Animal Sentience publishes Open Peer Commentary on all accepted target articles. Target articles are peer-reviewed. Commentary articles are editorially reviewed. There are submitted commentaries as well as invited commentaries. Commentary articles appear as soon as they have been reviewed, revised and accepted. Target article authors may respond to their commentaries individually or in a joint response to multiple commentaries. Instructions: http://animalstudiesrepository.org/animsent/guidelines.html Animal Sentience 2023.455: Segundo-Ortin & Calvo on Plant Sentience 2 zoocentric (Calvo 2018a; Calvo and Lawrence, 2023). We hope to redress this tendency, inviting scientists and philosophers to address the question of whether plants, too, may be sentient. Our hope is to convince researchers that this possibility is worth exploring scientifically (Segundo‐Ortin & Calvo, 2022; Raja & Segundo-Ortin, 2021). Scientific study of non-human sentience (animal or non-animal) is particularly challenging because direct evidence is lacking. Pearce (2008, p. 221) questions the very possibility of determining whether a non-human animal is conscious because we cannot “observe directly the mental states of an animal.” Echoing this view, Shettleworth (2010, p. 7) writes that “the point of most researchers studying animal cognition is that how animals process information can and should be analyzed without making any assumptions about what their private experiences are like.” Researchers must hence rely on indirect evidence, whether overt behavioral markers or correlated electrochemical activity. This “leap from observable behavior and physiological processes to conjectures about private conscious experiences” (Mazor et al., 2022, p. 3) requires some justification. Andrews (2020, Chapter 4) points out that most researchers rely on reasoning by analogy. If a behavior that occurs when humans experience pain is also observed in other species, we might infer that there too it is accompanied by the experience of pain. We can never be sure that the analogous behavior is accompanied by a subjective experience. The response to a damaging stimulus, for example, could be caused by insentient nociception (damage-detection) rather than pain. Moreover, analogy might be convincing with members of the ape clade and some other non-hominid mammals but it loses its strength as the target species becomes more distant from our own. What kind of behavior should we take as indicative of sentience in fruit flies? “If there are conscious entities that do not behave like humans, and if there is consciousness that we cannot perceive, then those entities will be unjustly excluded. Quite different beings may fail to meet those criteria while still being conscious” (Andrews 2020, p. 93). The same rationale applies to neurophysiological evidence. There is no principled reason to deny that radically different neural structures could give rise to felt states (Chittka 2017; Pagàn 2019; Solé et al. 2019). Sentience is nevertheless being increasingly recognized in many animal species, from apes, mammals, birds, reptiles and fishes, to octopuses and other invertebrates (Andrews, 2020; Crump et al., 2022; Mikhalevich & Powell, 2020). Based on behavioral and electrophysiological studies in invertebrates, Barron and Klein (2016; Klein & Barron, 2016) argue that some insects may have the capacity for sentience: Even though they are very different from the brain structures thought to support sentience in vertebrates, insects’ cephalic ganglia produce integrated neural representations of the world. Barron & Klein suggest that such representations are indicative of sentience, akin to those produced in vertebrates’ midbrains, with the cephalic ganglion of insects functionally equivalent to the midbrain. More skepticism is found when we move beyond the animal kingdom to the possibility that non-animal organisms, such as plants, can feel. Some authors have tried to argue against this skepticism. The “Cellular Basis of Consciousness” (CBC) theory (Baluška, Animal Sentience 2023.455: Segundo-Ortin & Calvo on Plant Sentience 3 Miller & Reber, 2021; Baluška & Reber, 2020, 2021; Reber & Baluška, 2020) proposes a bottom-up, evolutionary view of sentience. According to CBC, sentience emerged as an inherent feature of the first life-forms, including prokaryotes, and all biological taxa are equipped with some degree of feeling (Reber, 2019). “[A]ll adaptive functioning organisms, from the earliest on, must be sentient [...]. A non-sentient organism [...] would be an evolutionary dead-end” (Baluška & Reber, 2019, p. 1). According to CBC, sentience emerged to facilitate flexible adaptation to the environment; its complexity depends on the specific needs of each species and the characteristics of its ecological niche. Other researchers have argued that, contrary to CBC, current scientific knowledge does not provide serious support for investigating plant sentience (Mallatt et al., 2020; Taiz et al., 2019; we elaborate on these arguments in section 3). We agree that there is still much to be discussed before it can be accepted that plants feel, but we would disagree with those who would rather deny the possibility of plant sentience altogether. Regarding plant cognition (rather than sentience) current empirical findings strongly suggest that plants can perform many putatively cognitive abilities once thought to be unique to animals (Segundo-Ortin & Calvo, 2019). These abilities include the capacity to communicate with the plant’s biotic local environment (Arimura & Pearse, 2017; Karban, 2015); to distinguish kin from non-kin and modify behavior accordingly (Bilas et al., 2021); to make flexible decisions about multiple options and trade-offs (Karban & Orrock, 2018; Lee et al., Submitted); and even to learn from and remember past experiences (Baluška et al. 2018). Nevertheless, even if plants have surprising cognitive abilities, it remains debatable whether this is evidence that they feel, any more than similar abilities in robots and neural networks imply that they feel. A series of striking functional analogies between the nervous system of animals and the non-neural vascular system of higher plants has also been reported (see section 3 below). These similarities have motivated some researchers to broaden the definition of a ‘nervous’ system to include plants for “a better understanding of how evolution has driven the features of signal generation, transmission and processing in multicellular beings” (Miguel-Tomé & Llinás, 2021). Calvo (2017) has argued that the emerging field of plant neurobiology (Baluška et al. 2006; Brenner et al. 2006) offers new ways to investigate how plants integrate information from different parameters. In what follows we review the current evidence on plant cognitive activity and its electrophysiological substrate. Section 2 examines plant cognition. Section 3 reviews electrophysiological processes that may underlie plant cognition and sentience. We conclude with some general remarks about the implications of these findings. Animal Sentience 2023.455: Segundo-Ortin & Calvo on Plant Sentience