History and Epistemology of Plant Behaviour: a Pluralistic View?

Synthese (2021) 198:3625–3650 https://doi.org/10.1007/s11229-019-02303-9 BIOBEHAVIOUR

History and epistemology of plant behaviour: a pluralistic view?

Quentin Hiernaux1

Received: 8 June 2018 / Accepted: 24 June 2019 / Published online: 2 July 2019 © Springer Nature B.V. 2019

Abstract Some biologists now argue in favour of a pluralistic approach to plant activities, under- standable both from the classical perspective of physiological mechanisms and that of the biology of behaviour involving choices and decisions in relation to the environment. However, some do not hesitate to go further, such as plant “neurobiologists” or philosophers who today defend an intelligence, a mind or even a plant consciousness in a renewed perspective of these terms. To what extent can we then adhere to pluralism in the study of plant behaviour? How does this pluralism in the study and explanation of plant behaviour fit into, or even build itself up, in a broader history of science? Is it a revolutionary way of rethinking plant behaviour in the twenty-first century or is it an epistemological extension of an older attitude? By proposing a synthesis of the question of plant behaviour by selected elements of the history of botany, the objective is to show that the current plant biology is not unified on the question of behaviour, but that its different tendencies are in fact part of a long botanical tradition with contrasting postures. Two axes that are in fact historically linked will serve as a common thread. 1. Are there several ways of understanding or conceiving plant behaviour within plant sciences and their epistemology? 2. Can the behaviour of a plant be considered in the same way as that of an animal? The working hypothesis defended in this article consists in showing that the current opposition between growth, development and reductionist physiology on the one hand and the biology of behaviour involving sensitivity and choices in plant activity (i.e. agency) on the other hand has been built up through the history of botany.

Keywords Philosophy of biology · History of biology · Plant sciences · Behaviour · Botany

B Quentin Hiernaux [email protected]

1 Fonds National de la Recherche Scientiﬁque (FNRS), Centre de recherche en Philosophie (PHI), Université Libre de Bruxelles (ULB), 50 Avenue Roosevelt, 1050 Brussels, Belgium 123 3626 Synthese (2021) 198:3625–3650

1 Introduction

In her book The natural philosophy of plant form first published in 1950, the botanist, historian and philosopher of science Agnes Arber suggested that plant morphology could not be conceived solely as the static study of the plant’s external characteristics. Not only is the shape of a plant best understood in relation to its anatomy, but even more importantly “one can consider the [plant] shape as including something that corresponds to behaviour in the animal domain” (Arber 2012, p. 3). This idea, already present in a text by biologist E. S. Russell (1934) was not self-evident. In the last century, many biologists contested the very notion that plant behaviour existed. However, Arber’s idea is now being revived by plant biologists who have set themselves the task of elucidating the nature of plant behaviour (van Loon 2015). The special issues on plant behaviour in Plant, Cell & Environment (Ballaré and Trewavas 2009)orAoB Plants (Cahill 2015) bear witness to this endeavor. The relevance of this idea is such that it can even be found today in plant biology textbooks: “In plants, in fact, growth performs many functions that we group under the term ‘behaviour’ in animals”. (Raven et al. 2013, p. 539). The possession of a nervous system is no longer a necessary condition of behaviour (Silvertown and Gordon 1989; Cahill 2015). Some (Cvrcková et al. 2009, 2016) now argue in favour of a pluralistic approach to plant activities, framed both in terms of the classical perspective of physiological mechanisms and of the biology of behaviour involving choices and decisions (Hodge 2009) in relation to the environment, without necessarily appealing to the mind, intelligence or conscience.1 Behaviour is therefore understood here in a very particular biological sense that will have to be defined and that differs from the moral, psychological or social meaning of behaviour as seen from a human perspective. However, some do not hesitate to fray further into the biology of behaviour, such as plant “neurobiologists” or philosophers who today defend a plant intelligence (Mancuso and Viola 2015; Calvo and Baluška 2015;Trewavas2014), mind (Maher 2017) or even consciousness (Marder 2013)ina renewed understanding of these terms. What exactly does this pluralism tell us about the study and nature of plant behaviour? To summarize the two main alternatives, the classical biological approach focuses on elucidating the mechanisms and causes of plant reactions and functions. Its explanatory mode is rather reductionist or analytical in seeking to limit the study of functions to specific physico-chemical or adaptationnist explanations. The causes of a behaviour are generally multiple and can, for example, be studied in terms of phylogeny (e.g. particular genetic trait inherited determines a particular reaction), development (the flowering of a plant is determined by its growth stage) or mechanism (flowering depends on a particular hormone). In this perspective, behaviours that cannot be entirely reduced to physico-chemical causes are random or must have an unknown

1 “We propose defining behavior as “observable consequences of the choices a living entity makes in response to external or internal stimuli.” We emphasize that the word “choice” is used here in the sense of adopting one of at least two alternative fates or trajectories, in the state-space available to the living being in question, including, but not limited to, movement (or lack thereof) in the physical space. By no means does the use of this word imply involvement of a mind or consciousness. In our sense, flipping a metabolically or genetically wired switch also is a choice if its probability depends on outside stimuli and internal settings (previous history) of the biological system concerned” (Cvrcková et al. 2016). 123 Synthese (2021) 198:3625–3650 3627 evolutionary explanation. Historically speaking, this deterministic alternative can be associated with the traditional vision of plant behaviour as passive and mechanically determined by external physical causes. Conversely, biology of behaviour, also referred to as agentivist (on agency in biology see Walsh 2015; Moreno and Mossio 2015; Okasha 2018; Barandarian et al. 2009 and the special issue in the Journal of Adaptive Behavior), focuses on the synthetic study of behaviour according to its functions, goals and flexibility with respect to the organism as an integrated whole. This posture does not reduce the explanation of behaviour to its efficient causes (phylogeny, development or mechanism) but can invoke final causes that are justified by autonomy at the organism level. As long as a living being’s behaviour is not reducible to specific causes (physical, genetic, adaptationist), a margin of autonomy can be postulated in terms of its choices and decisions. Traditionally, agency is associated with “higher” animal (and human) behaviour. Sen- sitivity, movement and cognition make these animals autonomous, that is capable of undertaking certain actions spontaneously in their environment through internal—and not (only/always) mechanical—causality.2 Biologists now know that plants are also mobile as well as sensitive to their environment, although the question of how to interpret their behaviour in terms of cognition (mental states, intentions, representa- tions, memory, etc.) is debated (Dretske 1988; Maher 2017). In this sense, the growth behaviour of a stem or root in one direction rather than another (all other things being equal) can be described as the choice or strategy of the plant showing flexibility and goal-oriented3 behaviour (conversely, the reductionist posture, in the absence of a determining cause, will impute the behaviour as random). These two approaches are, to some extent, compatible. Indeed, the agentivist approach includes the physiological or adaptationist approaches, but does not reduce all behavioural patterns to their terms. The classical biological approach can thus be compatible with an agentivist posture even though it is rarely the case as we can see with biologists who state that any plant behaviour should in theory be reducible to a system of efficient causes and deny the organism’s ability to direct its own action or to choose between several situations (e.g. Firn 2004). We are therefore faced with an explanatory pluralism. Examples from the literature illustrating both approaches are discussed below. This article’s hypothesis is that biologists are more inclined to recognize even a minimal of agency in animals (as in humans) while, for philosophical but also historical reasons, they oppose it in the case of plants. So, how does the pluralism in the study and explanation of plant behaviour fit into, or even develop throughout, a broader history of plant science? Is the agentivist perspective a revolutionary way of rethinking plant behaviour in the twenty-first century or is it an epistemological extension of an older

2 Internal causality is what is speciﬁc to the organism and explains some of its behaviours. Historically it has been framed as the organism’s autonomy or its instinct as opposed to the external world’s physical constraints which are the external causes. However, this internal causality evolved to include genetic causality as an internal program of the organism. Internal causality is therefore not synonymous with autonomy but is broader. 3 Goal-oriented is not the same as Goal-directed. The goal-directed behaviour is directed towards a goal by a desire while the goal-oriented is directed towards a goal without necessarily having a desire: a programmed machine or a genetically determined behaviour for example (Dretske 1988, pp. 109–136). 123 3628 Synthese (2021) 198:3625–3650 but more marginal attitude? This article’s common thread is that the current pluralism between reductionist physiology, growth and development, on the one hand, and the biology of behaviour emphasizing autonomy, sensitivity and choices in plant activity, on the other hand, built itself up through the history of botany. By synthesizing the question of plant behaviour through selected elements of the history of botany, this article’s objective is to show that current plant biology is not uniﬁed on the question of behaviour and that its different tendencies are in fact part of a long botanical tradition comprised of contrasting postures. Two axes of inquiry that are in fact historically linked will serve as a common thread. 1. Were there several ways of understanding or conceiving plant behaviour within plant sciences and its epistemology? 2. Could a plant’s behaviour be considered in the same way as that of an animal? These questions are above all heuristic insofar as they are general enough to guide the historical investigation while at the same time revealing more precise issues and arguments in relation to contemporary debates.

2 Historical elements

There is no straightforward way of deﬁning behaviour, especially plant behaviour, unequivocally and consensually. There are now at least 25 operational deﬁnitions (Levitis et al. 2009). Rather than entering this contemporary theoretical debate, we use examples to approach the ways in which the notion has been constructed in context. To this end, we outline a historical synthesis based on elements advanced by botanists ranging from the Antiquity to the present day. This historical overview also aims to show that the idea of “purely” biological behaviour has philosophical links with a more anthropological or psychological tradition. Although phrasing plant activity in terms of “behaviour” is relatively recent, many relevant observations can be found throughout the history of botany as far back as Antiquity. They are all based on the fundamental idea of the plant’s sensitivity to its environment. Conversely, thinkers who have opposed the idea of plant behaviour have often sought to deny them any sensitivity. This opposition begs the question, however, of whether recognizing plant sensitivity necessarily implies an autonomous behaviour (i.e. agency) that could not be reduced to the expression of mechanical constraints or a genetic program.

2.1 Antiquity: the origins of plant study

Most Western thinkers based their attitude towards plants on animal reference models (i.e. zoocentrism) (Delaporte 2011). Indeed, a “vertebrate zoocentric bias” (Hull 1978, 1992; Hallé 1999;Hall2011) has persisted in the West since the Antiquity throughout the modern period and up until today. The biological and philosophical study of behaviour is no exception. This is due to the fact that, unlike animals, plants rarely exhibit behaviours that are immediately perceptible and have most often been considered passive and insensitive. Contrary to animal behaviour, which manifests

123 Synthese (2021) 198:3625–3650 3629 near-instant mobility and reactivity to stimulation, plants do not seem to move or exhibit sensitivity (Cvrcková et al. 2016). The archetype of this reasoning is found in Aristotle’s (384–322 BC) De Anima (On the Soul) whose writings constitute the origins of natural sciences in the West. Aristotle positioned himself against his predecessors and criticized their anthropocen- trism insofar as it defined life in terms of locomotion, sensitivity and breathing (403b) or even thought. Strikingly, the philosopher did not consider these characteristics as essential to the definition of living organisms precisely because they do not exist in plants (410b).4 Aristotle recognized that plants feed, grow, reproduce, age (degener- ate) and die like any other living being. He therefore considered these faculties to be the most fundamental to life (412a) and associated them with the vegetative soul. But in doing so, Aristotle established sensitivity as an ancillary faculty of the living which he reserved only for animals. Nor do plants have the faculty to desire, have goals and intentions related to the search for pleasure and the avoidance of pain. According to the philosopher, the possibility of experiencing pain and pleasure presupposes at least the sense of touch that even the most “imperfect” animals possess (unlike the other senses) (434a). But on what basis did Aristotle exclude the possibility of a minimal sense of touch in plants? Aristotle argued that while plants can undergo material changes (such as being heated or cut), they cannot feel these changes. It is unlikely that he made this argument based upon sound observations of plant behaviour and far more likely that it simply flowed from certain philosophical prejudices that prevented him from recognizing a potential plant sensitivity. In a reference to the metaphysics of the elements (i.e. fire, water, earth…), Aristotle explains that plants cannot have a sense of touch insofar as they are entirely made up of the earth element, just as our bones or our hair, which are the insensitive parts of our body. Furthermore, he asserts that it is not possible to possess touch without being an animal (435a–435b). However, this is paradoxical, if not incoherent, in that Aristotle asserted that plants share the nutritive faculty with other living beings (432a) and that this faculty was intrinsically linked to the sense of touch: “Touch is also the sense of nutrition” because it allows the qualities and properties of food to be tested (414a). As plants do have the faculty of nutrition, Aristotle could have legitimately considered that they at least had some minimal sense of touch. The ambiguity of plant life is all the more palpable because Aristotle twice compared the roots of plants to the mouth or head of animals through which they feed (412a–412b and 416a). But the philosopher, in his hierarchical conception of the living, linked sensitivity to the animal faculty of locomotion. By and large, this philosophical reasoning remained unquestioned for nearly two thousand years, mostly likely and in part because of Aristotle’s predominance within medieval and modern philosophical and scientific thought, reinforced by certain Christian theories on the “great chain of beings” (Lovejoy 1964;Hall2011; Mancuso and Viola 2015). If we follow Marder (2013, p. 21), or Calvo (2016), Western tradition has also retained local displacement (locomotion) as the only genuine movement which is a mark of sensitivity (neglecting growth and change of state as movements).

4 In Aristotle’s time it was thought that plants did not breathe. 123 3630 Synthese (2021) 198:3625–3650

While Aristotle’s disciple, Theophrastus (371–288 ACN), and Pliny the Elder (23–79), had already noted the ability of plants to move (Tassin 2016, p. 27), their observations were obviously not systematic or experimental in the contemporary sense. Considered to be the father of botany, Theophrastus nevertheless observed plant reactions, mainly through their growth. The subtlety of Theophrastus’ observations is worth emphasizing. After completing his master’s work on natural history through observations of animal behaviour recorded in seven long-lost books (Amigues 1988, p. 8), Theophrastus set out to methodically study the plant kingdom. He distinguished himself by insisting upon the importance of a plant’s relationship to its environment (HP, Book IV). However, his relative openness to plant life and its sensitivity, mani- fest in certain passages of his Inquiry into Plants (Historia plantarum), comes into to conﬂict with a causal and mechanistic conception inherited from Aristotle, which he sought to apply more systematically in his work On the Causes of Plants (De causis plantarum) (Amigues 2012). He took up Aristotle’s idea that “plants do not have, like animals, a character and activities” (I, 1, 1) while simultaneously critiquing him for a hasty assimilation of the plant world to the animal world at the expense of observation (Amigues 1988, p. 70). In Aristotle’s defense, the frame of thought of his time probably did not allow him to recognize plant sensitivity, which was difﬁcult to perceive. However, the perceptible only imperfectly overlaps with the observable. Although plants do not quickly move, it is clear that their growth movement and transformations could be indirectly observed as marks of their sensitivity, without it being directly perceived. The lack of measuring instruments, but more fundamentally our way of perceiving at a timescale different from that of plants, has hindered the recognition of their sensitivity and therefore their behaviour. The persistence of hierarchical models of living beings inherited from Aristotelian thought and Western religious tradition compounds this blindspot. Late Antiquity and Middle Ages observations of plants and their behaviour was almost totally eclipsed by pharmacology and astrological botany (Arber 1912, pp. 204–220, Greene 1983; Magnin-Gonze 2009). The practical use of plants competed with the theoretical study of their organization (Delaporte 2011, p. 21).

2.2 From the sixteenth to the eighteenth century: emergence of modern botany

In the sixteenth century, however, several botanists such as Valerius Cordus (1515–1544) and Garcia da Orta (1501–1568) began to describe and explain the movements of leaves of the Legumes (Fabaceae) (Davy de Virville and Leroy 1969). At the same time, Conrad Gesner (1516–1565), observed the nyctinastic5 and heliotropic6 movements of many plants (Greene 1983, p. 791). But how could such observations be understood under the prevailing assumption that plants are insensitive? The solution according to the accepted view of the time seems simple: the observed reactions do not result from any form plant sensitivity, but are merely physical and mechanical. A plant feeds itself like a sponge ﬁlls itself with water, it is attracted

5 Nyctinasty is the plant movement that accompanies the alternation of day and night and that is similar to a waking and sleeping behaviour of plants. 6 Heliotropism is the movement of a plant or parts of a plant towards the Sun. 123 Synthese (2021) 198:3625–3650 3631 by the Sun like iron is to a magnet. The causes of a plant’s actions are not internal, autonomous, but external. Thus, a fundamental epistemological difficulty emerges out of a conflict between philosophical assumptions (the insensitivity of the plant) and the absence of satisfactory physical explanations of plant activities in strictly mechanical terms (external causality). The botanist and philosopher Andrea Cesalpino (1519–1603) illustrated the paradox very clearly in his De Plantis libri (1583): “Plants, lacking all that is similar to sensation, cannot select their food, but extract moisture from the soil of the earth matter [in solution] in another way [than through senses], but what this other way can be is very difficult to see, since there is no other similar process in nature to which it can be connected. This cannot happen in the way a magnet attracts iron, because in this case it is a larger body that attracts a smaller one; so that in this hypothesis the soil would attract moisture out of the plant. Nor can we assume vacuum as the engine of force since the soil contains as much air as it does moisture, and there are plants whose stems contain more air than water. Are we in the case where certain substances, when dry, have the ability to absorb moisture?” (Cesalpino 1583, pp. 3–4).7 The modern alternative that Cesalpino illustrates is the following: either the plants are sensitive (like animals) and this explains the cause of their activities, or plants are indeed insensitive and strictly physical mechanistic causes must explain their activities. The overwhelming presupposition of the time was that plants were insensitive and yet, there were no convincing physical explanations for their activities. Despite the official dogma of plant insensitivity, Cesalpino was thus inclined to recognize that plants, particularly climbing plants, have a certain ability to perceive adjacent objects insofar as they seek them out and surround them (Arber 2012, p. 29). The idea of plant insensitivity will however be maintained in much of modern botany because of the combined hegemony of Aristotelianism and Christian ideology (Hall 2011; Delaporte 2011). Under the influence of Descartes’ philosophy (1596–1650), several seventeenth century plant “physiologists” such as Mariotte (1620–1689) undertook to study plant nutrition, growth and circulation of plant sap on a mechanistic basis, rejecting the idea of a vegetative soul. At that time, as in Antiquity, the soul was still considered as an explanatory principle of life, sensitivity and movement. It therefore played the role of a principle of autonomy of the living relatively to the physical world. With mechanicism however, it became possible to explain plant activity in terms of physical causes reducible to matter and movement.8 In the wake of the first advances in chemistry, Mariotte highlighted the composition of plant matter. He noted that these compounds were different from those taken from the soil and varied according to species (thus calling into question the Aristotelian idea that the plant would consist of earth). Other experimental research in botany followed, for example, with the study of stem phototropism or grafts by Robert Sharrock (1630–1684) in 1660. Plant respira- tion, growth and geotropism of the roots were studied by Denis Dodart (1634–1707)

7 De Plantis, quoted by Greene 1983, modified translation, p. 827. 8 As an explanatory register, animism therefore differs from the mechanicism (to which it is opposed or simply complementary if it is placed at a different metaphysical level from the physical level of the mechanism). 123 3632 Synthese (2021) 198:3625–3650 in 1700. In the same vein, John Ray (1627–1705), Stephen Hales (1677–1761) and Marcello Malpighi (1628–1694) studied sap circulation from an experimental point of view. The botanical historians Davy de Virville and Leroy (1969b, p. 679) refer to the seventeenth century as the century of Cartesian biology, in contrast with the following century when Leibniz’s influence was more pronounced. From this perspective, mechanistic determinism can be seen as a success insofar as the question of plant sensitivity (and the soul) becomes dispensable or avoidable and it could even be said to be incompatible with experimental advances. Seventieth century mechanicism considered all nature and organisms (animals and plants) as machines, which made it possible to study plants on the same theoretical level as animals (Delaporte 2011, p. 22). However, in practice, the difficulty was that, unlike in animals, the study of plant forms is not correlated with organs and therefore does not indicate the presence of functions. On the other hand, plants grow, reproduce and even move to some extent like animals. This overlap explains why animals, better known and understood, served as a scientific model to capture the unknown complexity of plants (Delaporte 2011, pp. 20–34). Prejudices about plants remain inseparable from the great chain of beings which was intended to reflect a hierarchical and immutable ranging from plants at the very bottom of the scale, to animals and humans at the top. The history of botany offers numerous illustrations of this gradation. As a case in point, let us simply quote Linnaeus (1707–1778), who began his Fundamentals of Botany (1736) by stating that natural entities are divided into three kingdoms: mineral, vegetable and animal and that “Minerals grow. Plants grow and live. Animals grow, live and feel” (Linnaeus 1736, aphorism 3). Linnaeus confirmed this insensitivity of plant life in his aphorism 133: “Although plants are devoid of sensations, they live as much as animals” (Linnaeus 2005). This Aristotelian reasoning was coupled with mechanicism in a philosopher- physician-botanist of modernity like La Mettrie (1709–1751) as he explicitly and intimately associated the faculty of movement not only with sensitivity, but moreover with the intelligence of organisms: “The more the bodies I’m mentioning take after plant nature, the less instinct they will have, the less discernment their operations will suppose. The more they will participate in animality, or will function similarly to us, the more generously they will be endowed with this precious gift. These common or mixed beings[polyps], whom I call so, because they are children of the two kingdoms, will have in one word all the more intelligence, as they will be obliged to give themselves greater movements to find their subsistence” (La Mettrie 2003, pp. 43–44). For most philosophers and botanists of La Mettrie’s time, plants were not only insensitive because they were incapable of movement, but, in addition, movement was understood as a condition for intellectual faculties. Therefore, plants could not be considered intelligent precisely because movement was associated with locomotion. For La Mettrie (2003), who radicalized the Cartesian mechanicism of his time, we do not need a soul to explain the growth of a plant any more than we need a soul to explain the slower growth of a stone. Plants may be alive, but they are only machines with automated reactions. He also contrasts plant operations with the animal instinct, which serves as the internal cause of some of their behaviours. Modern botany com- 123 Synthese (2021) 198:3625–3650 3633 bined with Descartes’ philosophy thus aims to make the determinism of the physical world triumph over plant life at all levels. As ecologist Jacques Tassin writes: “Renaissance thinkers, who see animals as little more than machines, discredit plants. From this succession of considerations, we have kept a deep imprint: plants remain in our eyes only a vague shivering of matter, a subregnum of the living, an unfinished outline of animals, and their destruction often leaves us unconcerned.” (Tassin 2016, p. 12). While some of Descartes’ contemporaries were already critical and skeptical of the idea that animals are merely insensitive machines with determined behaviour, it seems as though nobody seemed troubled by plants receiving the same theoretical treatment. However, as Delaporte (2011) explains, the question of plant sensitivity and irritability occupied an important place in debates between botanists, especially in the eighteenth century. The alternative between sensitivity and physical mechanism was not the result of a binary historical succession. On the contrary, during the modern period, a pluralism already existed when it came to explaining plant behaviour. Indeed, some naturalists such as Girtanner (1790), Brown (1792), Hooper (1797)orErasmus Darwin (1800) defended the idea of a true plant sensitivity. Moreover, it is worth remembering that the issue of plant sensitivity in modern times is not only scientific, but also moral. Then like now, those who denied plant sensitivity were at the same time seeking to eliminate the possible question of plant suffering and to legitimize their destruction by man. Conversely, thinkers who recognized plant sensitivity had to develop arguments in favour of a natural economy in which the destruction of plants was a necessary evil. In both cases though, it is always a question of preserving the privileged position of man within the hierarchy of Creation (Delaporte 2011, p. 193).

2.3 From the eighteenth to the nineteenth century: development of experimentation and the advent of plant physiology

In the nineteenth century the development of experimental plant physiology marked a turning point in the study of plant behaviour. Already in the eighteenth century, botanist Henri-Louis Duhamel du Monceau (1700–1782), like others before him (Web- ster 1966), had been struck by the sensitive plant (Mimosa pudica) and its ostentatious sensitivity. Indeed, this plant is capable of folding its leaflets in a few seconds following a stimulus (contact, shock, heat).9 A few years later, botanist R. L. Desfontaines (1750–1833) pushed the investigations further and was the first to highlight a habituation of the species, i.e. an ability to adapt its response to certain stimuli: “Desfontaines made an experiment that has often been repeated, and always with the same result. Having placed a sensitive in a cart, he saw it, as he should have expected, hurriedly close all its leaves as soon as it felt the shaking caused by the movement of the wheels. Soon however, he observed an extraordinary fact: despite the continuous movement of the car, the plant, recovering from its first fright, gradually reopened its leaves to keep them spread out as long as the cart

9 This type of movement is today called thigmonasty. 123 3634 Synthese (2021) 198:3625–3650

remained in motion. But when, after a pause, the cart started again, the sensitive closed all its leaves, and only reopened them when it had become accustomed again to the movement of the cart. (Boscowitz 1867, pp. 147–148).

The sensitivity of the Mimosa pudica seemed all the more real as the use of anesthetic substances inhibited its reactions (Boscowitz 1867, pp. 151–152). However, it would take several more years for plant sensitivity to be tested more systematically. Indeed, the sensitive was considered by many as an exception which does not make it possible to generalize the existence of sensitivity in other plants (Delaporte 2011, p. 163). Notwithstanding its exceptionality, this particular plant created a breach in the ideology of plant insensitivity (Webster 1966). Nevertheless, further steps were needed to open up the possibility of a generalisation of plant sensitivity. According to Delaporte (2011, p. 161), it was ﬁrst necessary to be familiar with nutrition (and the resulting growth) and generation issues in plants to seriously take into account the mobility of plant parts. Indeed, the study of nutrition had made some botanists recognize that plants might not be totally passive in their nutrition process. Moreover, plant sexuality was still difﬁcult to accept in the eighteenth century given how closely this function was linked to animal instinct related to sensitivity and locomotion.

“How just soever it may have been in a philosophical view, to consider the stamina and pistils, as answering to the respective functions of sex in the animal kingdom, it should not have been forgotten, that in animals, this process is voluntary, but that in vegetables, notwithstanding all that the ingenuity of the ancients and moderns have urged in defense of the sentient principle, we are not yet justiﬁed in referring this process to any other than what we are accustomed to call a mechanical cause” (Pultney 1790, t1, p. 345).

The absence of mating thus argued in favour of the absence of true sensitivity in plants. The absence of sexual instinct and copulation was considered as an absence of will. Reproduction, when admitted in plants, was therefore, at best, the result of a mechanical cause and plant sensitivity was superfluous for understanding such a function. Plants were passive, while animals were active. Even those who advocated for plant sexuality did so not because it was similar to the internal causality of animal instinct, but because it referred to a more universal mechanical process of perpetuating species. Within the context of the hierarchy of beings (and its correlate: the hierarchy of functional principles), assigning sexuality to plants was problematic since it was intimately connected to the sensitivity and even the desire and pleasure that guides animal reproductive instincts. This explains why stamen movements (Bonnet 1769) or phototropisms were only really studied experimentally from the middle of the eighteenth century (Delaporte 2011, p. 161). More generally, it was not until the end of the nineteenth century that plant sexuality was accepted and understood. More than 150 years will have been needed between Camerarius’ first experimental discoveries on fertilization in 1694 and the understanding of the double fertilization of angiosperms and the alternating phases in the life cycle of all plants (Crespi and Linskens 1999; Taiz and Taiz 2016). These difficulties are partly illuminated by the hypothesis of an explanatory pluralism that runs through history. The plant and its behaviour could not be explained a priori like the animal and its behaviour. We can therefore better 123 Synthese (2021) 198:3625–3650 3635 understand the vigour of the rejection of plant sexuality or the attempt of “sexualists” to reduce it to a pure mechanism of nature (Delaporte 2011, pp. 101–148). Augustin-Pyramus de Candolle’s (1778–1841) experiments on changing circadian rhythms marked an important turning point at the dawn of the nineteenth century. They helped extend the idea of habituation, and thus sensitivity, to all plants (beyond Mimosa pudica) (Candolle 1801; Guedes 1974). Candolle observed that nocturnal lighting and daytime darkness cause plants to adapt their waking and sleeping behaviour. In addition, the new habits acquired by plants persist for some time after the stimuli have stopped. A plant subjected successively to two diametrically opposed light sources, towards which it moves in turn, will preserve this back and forth movement for a certain time, even after this light alternation has ceased (Boscowitz 1867, pp. 130–131; Flourens 1842). According to botanist Leo Errera (1858–1905), these experiments testified to the idea that, in addition to sensitivity, plant habituation expresses a form of memory (Errera 1910, p. 321). However, these results regarding plant behaviour were problematic insofar as the structures and mechanisms with which they could be accounted for, remained unknown. Physiologists did not observe muscles or nerves that would give an explanatory basis to plant movements and sensitivity and even less a brain that would ensure the presence of memory. Indeed, for some naturalists such as Lamarck (1744–1829), the sensitivity model for living organisms is animal’s muscle (or organ) irritability, which a priori condemns any plant sensitivity:

“Plants are living bodies that are not irritable, incapable of instantly and itera- tively contracting any of their parts on themselves, and lacking the ability to act, as well as the ability to move” (Lamarck 1815, p. 124).

Two main hypotheses were then in conflict among those who did not outright reject the idea of plant sensitivity. Either plants have structures equivalent to nerves, or sensitivity is made possible by mechanisms totally different from those that exist in animals. In the nineteenth century, botanists such as Lorenz Oken (1779–1851) or Goethe (1749–1832) still defended the first position by arguing that the “spiral fibres” of plants play the role of nerves. Others, like James. P. Tupper (circa the second half of the 17th and the first half of the eighteenth century), Gustav Theodor Fechner (1801–1887) or Arnold Boscowitz (1826–Unknown date of death) considered that sensitivity is possible without the existence of nerves or the equivalent of the nervous system (Tupper 1811, Boscowitz 1867, pp. 158–163):

“Is it not obvious, in fact, that it is not the absence or presence of nerves that must decide whether a being possesses or does not possess the faculty of feeling, but rather some highlights of its existence, or all the manifestations of which his entire life is composed? […] One would be entitled to suppose it, even though the nerves would absolutely be missing. Now, when in the course of this study, we will have recognized these essential aptitudes in plants, without nevertheless discovering in them a nervous system, we will be led willy-nilly to admit the existence of sentient creatures, although devoid of nerves” (Boscowitz 1867, pp. 159–160). 123 3636 Synthese (2021) 198:3625–3650

Nerves are only a means of transmitting sensitivity and are not sensitivity itself. Since there are movements in plants, whether spontaneous (growth for example) or induced (Mimosa’s movement), plant physiology had to explain them as a reaction to certain stimuli (with mechanisms different from animals and their nerves). However, even if their effects were now clearly observable, the means of such sensitivity had yet to be established. The development of plant physiology and its laboratories in the second half of the nineteenth century allowed this fundamental issue to be addressed. This was accom- panied by institutional obstacles, since the very idea of a discipline such as plant physiology aroused the reticence of scientists until at least the early 20th century: “‘Physiology’ - in the general sense of the term - is the science that studies the lives of beings that move, feel, react to stimulants, quickly and suddenly. Plants are not known to present movements, have sensations, reactions, so the term ‘physiology’ usually applies to everything that lives except plants: plant physiology is not known, even by name” (Errera 1910, t IV, p. 315). Thus, until the end of the nineteenth century and notwithstanding places such as Germany, physiology applied mainly to animals as botany struggled to emerge from clichés of outdated herbaria to become an experimental discipline (Errera 1910). Plant physiology existed, but the prevalence of descriptive botany had long made it marginal: “For centuries, most botanical research focused on describing and classifying plants and studying their medicinal properties. Before~ 1850, the idea of studying the functioning of plants for itself hardly crossed scientists’minds, with the exception of a few remarkable pioneers. In one word, (as in a hundred), despite the existence of these brilliant precursors, plant physiology as an autonomous and organized scientific discipline still did not exist in the middle of the 19th century” (Bernier 2013, pp. 93–94). For various reasons, taxonomy developed more significantly in botany than it did in zoology. Economic and utilitarian first: plants are above all a source of remedies and materials. Secondly, for methodological reasons, plants can be observed and described more easily given their relative lack of mobility. Finally, in plants, the external structure is the most readable, while their anatomy and functioning remain unclear compared to those of animals. In contrast, physiology was modelled on animals, which have func- tionally specific internal organs. This model is then imported into botany. Physiologists explained the inferior by the superior under the regime of its functions (plants had to have a sexuality or a fluid circulation similar to that of animals). This relationship was reversed in the nineteenth century, the inferior became the model of the superior with cell theory (and subsequently genetics) developed from plants and it was no longer the function, but the identification of a common intimate structure, that served as a point of comparison. In addition, the existence of the cell wall and the chemical separation of plant cells have made observation and physiological experimentation easier in botany than in zoology (Delaporte 2011, pp. 201–205). It is especially thanks to the works of the German school of Julius von Sachs (1832–1897) and Wilhelm F. P. Pfeffer (1845–1920) (Sachs 1865, 1882;Pfeffer 1881; Kutschera 2015), but also, among others, Charles Darwin (1809–1882) (Dar- 123 Synthese (2021) 198:3625–3650 3637 win 1865, 1875) and his son Francis (1848–1925) (Darwin and Darwin 1880) and J. C Bose (1858–1937) (Bose 1907, 1913, 1925) that plant physiology truly progressed (Stalhberg 2006; Kutschera and Niklas 2009; Bernier 2013;Trewavas2014).10 With laboratory experiments, the first chemical mechanisms explaining plant behaviour (notably with auxin) are discovered. The sensitivity and movements of the growing coleoptiles, but especially of the root tips of plants studied by the Darwins, even led them to propose the analogical hypothesis of a root brain to the extent that plants seem to make decisions and adapt according to their underground environment.11

“The course pursued by the radicle in penetrating the ground must be determined by the tip; hence it has acquired such diverse kinds of sensitiveness. It is hardly an exaggeration to say that the tip of the radicle thus endowed, and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower organism; the brain being seated with the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements” (Darwin and Darwin 1880, p. 573).

In the same line of thinking as Charles Darwin’s work on the Venus flytrap (Dionaea muscipula), whose stimulation of the sensitive hairs induces the rapid closure of its trap on the insect that has imprudently ventured inside (Darwin 1875), one of his contemporaries, Burdon-Sanderson, discovered that the activation of the trap depends on an electrical signal (Burdon-Sanderson 1873, 1899). In 1901 Jagadish Chandra Bose noticed the same influence of electric current in the sensitive plant (Chamovitz 2012, chapter 3).12 The existence of chemical and electrical mechanisms of the action- potential type thus makes the reality of plant sensitivity and behaviour increasingly plausible. Botanist Gottlieb Haberlandt (1854–1945) also sought to highlight plants’ sense organs (Haberlandt 1890, 1901). At this period, more explicit connections were again attempted with the animal nervous system (Bose 1926). However, the detection of electrical impulses in plants without the presence of nerve structures made it difficult to accept the idea that a nervous system was needed to account for any form of sensitivity. The hypothesis of an equivalent to the animals’ nervous system to explain plant sensitivity became less obvious during the nineteenth century for at least two reasons. First, at the cellular level, the cellulosic walls of plant cells appeared (at the time) to interfere with electrical transmissions and constituted a physical barrier. Second, electrical communication is challenged by the discovery of hormonal chemical communication signals (Brenner et al. 2006). As Darwin wrote:

10 We have shown that there have been observations of the movement or sensitivity of certain plants before the 19th century, but their study was rarely experimental, systematic and generalizable to the whole plant kingdom. 11 This work gave rise to a heated controversy with Sachs, considered the father of plant physiology and the international reference in this field, both on the mechanisms and their interpretation (Bernier 2013, p. 93-104, Kutschera and Briggs 2009). 12 J. C. Bose (1858-1937) is at the origin of the discoveries and first major botanical experiments on the role of electricity in the communication of information, although the influence of electricity on plants was highlighted much earlier (cf. Boscowitz 1867, Davy de Virville et al. 1954). In 1783, Pierre Bertholon published a treatise entitled De l’électricité dans les végétaux [On Electricity in Plants]. 123 3638 Synthese (2021) 198:3625–3650

“Yet plants do not of course possess nerves or a central nervous system; and we may infer that with animals such structures serve only for the more perfect transmission of impressions, and for the more complete intercommunication between the several parts” (Darwin and Darwin 1880, p. 572).

While scientists like the Darwins did not seem to free themselves from the classical comparison of plants with animals in proposing the analogical hypothesis of the root brain, they did have the merit of inverting the way of thinking about plants which was no longer as degraded animals but rather of animals as perfected plants. This discrep- ancy was far from insigniﬁcant: it called into question the whole cultural tradition of the chain of beings; this about-turn was, moreover, coherent with the theory of natural selection and the idea of evolution developed by Darwin. To think of plants not as lacking when compared to animals, but as having their own speciﬁcities, opened perspectives, particularly that of a non-nervous sensitivity. If sensitivity and movement could be observed and demonstrated, then there was only one step to take to claim the existence of true plant behaviour. The underlying idea of these authors was that plants were more complex than previously imagined and therefore could not be considered fully programmed or physically determined. As plant physiology developed, the possibility of genuine plant autonomy was reactivated. This is what physiologist Julius von Sachs, citing botanist Alexander Braun (1805–1877), advanced:

“Are plants only a product of the activity of matter, and therefore beings without a personal life, generated by blind forces subject to the general laws of nature, or should they be considered as living beings of an independent and personal life whose source can be found in themselves? By virtue of the theories of physiologists, who, by discarding the principle of life force, explained certain phenomena of existence by the laws of physics and chemistry, life was stripped of the supernatural element it possessed, and which seemed to be, of all its acting forces, the most direct; the almost insurmountable difficulties which separated the study of organic life from that of inorganic life were ironed out. Since physical forces always seem to be closely related to matter, and since their results seem to be subject to strict laws, one has taken the risk of considering all natural phenomena as the result of original forces, whose fixed and determined actions are applied according to the laws of blind necessity, and has compared it to a mechanism that moves in the eternal circle of natural laws. Given this doctrine, one is obliged to assume that the fulfilment of eternal necessities has always taken place, and consequently, the doctrine in question, based on the principles of physics, makes any eventuality incomprehensible. Moreover, the purpose of movement remains an enigma that the doctrine of blind necessity is powerless to solve” (Sachs 1892: pp. 188–189).

This passage illustrates the explanatory pluralism of plant behaviour, dramatized by nineteenth century experimental physiology. On the one hand, physico-chemical reductionism made room for certain causal explanations of the mechanisms of plant life by rejecting vitalism. Yet, on the other hand, it was unsatisfactory for at least two reasons. First, from a nomological point of view: for an evolutionist like Sachs, if the living is subject to the laws of a blind and eternal physical necessity, how can we 123 Synthese (2021) 198:3625–3650 3639 explain the randomness of life and the contingency of living forms at the heart of the theory of evolution? Second, Sachs makes a more ethological argument: physical laws only make it possible to account for the mechanisms of behaviour according to their causes but do not make it possible to account for the effects and aims of plant movements, a fortiori when the vitalist explanation is rejected. The function or purpose of a behaviour is just as essential to its understanding (Tinbergen 1963). It is therefore reasonable to assume that Sachs was inclined to preserve pluralism in the study of plant behaviour by avoiding the alternative of pure physical reductionism as opposed to metaphysical vitalism. From the end of the nineteenth century, some botanists even proposed to overtly recognize a certain psychic life of plants in light of experimental discoveries on their memory or sensitive adaptations.13 These hypotheses were intended to give a more unified image of behaviour consistent with that of the animal world: “When we look at the facts related to plant nutrition as a whole; when we see plants showing perseverance in the search for their food, abandoning an arid land to move towards a more fertile land, we are almost tempted to admit that these efforts are spontaneous acts, and that the individual from whom they emanate must experience some sensation : just as one believes that he is allowed to see in the beast a sentient being, because it acts in a similar way, though in a different sphere” (Boscowitz 1867, p. 59). Errera (1910, t IV, p. 317) explained that the mental acts of animals were defined by two things: they fulfill a future purpose and are accomplished through chosen means. This is found in plants because they are, for example, able to grow towards a light source and to do so by various means, unlike the purely physical movement of the fall of a stone which allows only one trajectory. In plant growth, there appears to be a kind of choice in the sense that alternatives coexist (Cvrcková et al. 2016, see note 1). In addition, a plant’s actions can always be interpreted as planning for long-term goals in the interest of the plant’s life. As Darwin wrote: “In almost every case we can clearly perceive the final purpose or advantage of the several movements. Two, or perhaps more, of the exciting causes often act simultaneously […], and one conquers the other, no doubt in accordance with its importance for the life of the plant” (Darwin and Darwin 1880, p. 573). Like those of animals and unlike those of stones, plants’ actions can be explained in terms of purpose. In this respect, plants would be endowed with an autonomous behaviour or with what today is called agency (qualified as “soul” in the words of that time) (Errera 1910, IV, pp. 315–323). Boscowitz went one step further in his philosophical reflection by suggesting, against all mechanistic determinism, that plants can be said to be free, like animals, insofar as they can make decisions and act distinctly from their congeners, for “these phenomena of vegetation escape the laws of physics” (1867, pp. 74–80). In this sense, Boscowitz seemed to associate freedom with every

13 The recognition of a psychic life of plants is actually a much older philosophical idea present in Ancient Greece, some Hindu currents etc. (Hall 2011). We refer to 19th century botanists because they were the first scientists to defend this idea on the basis of experimental arguments in the same line as contemporary neurobiologists. 123 3640 Synthese (2021) 198:3625–3650 living being, since life is not entirely reducible to physical determinism (what Sachs called “blind necessity”). This could even be a fundamental epistemological principle implicit in the study of the living if we accept what the philosopher of science Georges Canguilhem (1904–1995) wrote in La connaissance de la vie: “The biological study of movement begins only with taking into consideration the orientation of movement, because it alone distinguishes vital movement from physical movement, tendency, from inertia” (Canguilhem 2015, p. 15). The question is therefore no longer whether plants are mobile or not—this is beyond doubt-, but the extent to which their sensitivity reveals a certain “psychic life”, an agency (or even an “intelligence”) at least expressed in the form of flexibility, orientation and goals. Plant movement demands justifications not only in terms of its causes but also of its purposes. In the evolutionary framework that emerged in the nineteenth century, the behaviour of organisms could be explained by way of their favourable selection in relation to their survival and reproduction goals. This is why all biologists can talk about the behaviour of plants (at least in some cases) but not that of stones. However, these ideas in favour of genuine agency of plant behaviour seemed to have once again become marginal after the first third of the twentieth century, probably because of the prevalence of a new deterministic paradigm influenced by advances in physics and, more importantly, genetics.

2.4 The twentieth century: genetics

The progressive achievements of nascent plant physiology, which opened the possibility of a genuine study of plant behaviour by highlighting its sensitivity, were often discredited in the twentieth century. Scientific work of the time explicitly took aim at what preceded them. For instance, the German philosopher Max Scheler (1874–1928), resting upon the work of botanist A. H. Blaauw, went so far as to reaffirm the Aris- totelian hierarchy of the living: “In plants, there are no specific tropisms, sensations, or even the smallest elements of a reflex arch, no conditioned association or reflex, and therefore no kind of ‘sensory organ’, as Haberlandt had tried to circumscribe them in detailed studies. Motor phenomena triggered by stimuli previously related to such things have been shown to be elements of general plant growth movements” (Scheler 1928[1951], p. 25). Critics of plant sensitivity therefore returned to the sledgehammer argument that what determined sensitivity was necessarily the presence of nerves, reflexes, brains and all the other characteristics animal sensitivity depends on. At that time, a form of regression or blockage was observed in relation to the discoveries of plant physiology which preceded and associated the modalities of plant growth with real autonomous behaviours. Plant growth and development were explicitly opposed to animal behaviour. The detection of electric current in all plants and the more precise study of the mechanisms of signal transmission in the vascular system would only be taken up again in the 1960s (Stalhberg 2006). In this period, plant electrophysiology, 123 Synthese (2021) 198:3625–3650 3641 which had been a scientific discipline for a hundred years (1870–1970), was actively terminated. The most used textbooks on plant physiology (Taiz and Zeiger 2010)did not cover the field and did not mention action potentials until very recently (in the sixth and last 2015 edition, there is only minor coverage of these subjects related to carnivorous plants). During the twentieth century, genetics were progressing. With the discovery of genes and their functioning, a new biological paradigm emerged. Fischer (1930) coined it “the genetic theory of natural selection”, which is a deterministic and quantitative approach of adaptive evolution understood as a change in allele frequencies (Sultan 2015, p. 142). It culminated in the discovery of the structure of DNA in 1953, which laid the foundations for the laws of heredity and, correlatively, reinforced the deterministic approach to plants. From this moment on, determinism was no longer physical or mechanistic determinism, but genetic (Fox Keller 1995, 2000). The development and even the behaviour of organisms, at least those considered to be the simplest, were seen as programmed by their genes. François Jacob (1965 Nobel Prize in Medicine) could thus explain in Le jeu des possibles (1981) that, in bacte- ria and other microorganisms, perceptions and reactions were rigorously determined by genes that only allow binary responses (p. 108). In lower invertebrates, sensory information could be converted into motor-nervous information, that is, into innate response mechanisms to stimuli. Finally, in birds or mammals, the information could be processed by the brain, which would produce a simplified representation of the outside world. The behaviour of organisms tends to blend into the specie’s genetic programme. In addition, it is likely that molecular biology and genetics also con- tributed to inhibiting the study of plant behaviour given its predominant focus on the cellular or sub-cellular level (Brenner et al. 2006). Indeed, at the time, there was no plant ethology capable of specifically undertaking the global study of plant activity, unlike animal ethology which had already been firmly developed (with authors such as Loeb, Jennings, von Uexküll, Fabre, Lorenz, Tinbergen, Pavlov, Skinner, etc.). By the end of the twentieth century, the study of plant behaviour (types of movement and excitability) remained partial and rarely taught (Simons 1992, p. 14). There was no structured and unified (experimentally and geographically) plant behaviour field. The idea that plant reactions were determined by the external environment’s physical factors was thus reinforced or even replaced by internal, genetic programming model, which presented itself as the ultimate causal response to everything that physical determinism could not explain in plant behaviour. The plant-machine made a strong comeback, ever more marginalising the possibility of a genuine study of the emergent properties of vegetable behaviour. It did not take long however, for plant ecologists to observe a phenotypic flexibility during the life of plants according to the constraints of the environment.

“Plant biologists, confronted with the dramatic and obvious effects of environment on individual development and ﬁtness, were explicitly exhorted to ignore these effects as meaningless variation (e.g. Stebbins 1980). Generally, traits known to be expressed differently in different conditions were consid- 123 3642 Synthese (2021) 198:3625–3650

ered at best ‘a group of interesting exceptions’ to the rule of rigid genetic control” (Sultan 2015, p. 18). Rather than using the term “behaviour”, plant biologists focused on the vocabulary and explanations of “developmental plasticity” or “adaptive or phenotypic plasticity” (Nettle and Bateson 2015;Varin2017) and renewed the border dispute with the animal world thanks to a vocabulary different from that of ethology. Meanwhile, this did not prevent other biologists and ecologists from continuing to record new discoveries on plant behaviour. In the early 1970s, scientists proposed to further explore the sensitivity of plants through the study of their tropisms and growth reactions. Behaviours such as shade avoidance or growth modification in response to contact (thigmomorphogenesis) were studied (Jaffe 1973; Braam and Davis 1990; Braam 2005, etc.). Discoveries on aerial and underground plant communication (Baldwin and Schultz 1983; Mahall and Callaway 1991; Baluška et al. 2006; Baldwin et al. 2006; Scott 2008, etc.) and subsequently on nutrient transfer through mycorrhizae (Garbaye 2013 for a synthesis of this topic) and plant memory followed (Thellier 2015 for an overview of this topic) in the 1980s. Nonetheless, the genetic model maintained its predominance well until the 1990s. Indeed certain behaviours of “simple” animals seemed to be quite strictly genetically determined, for example, the parasite cleaning behaviour of the hygienist bee (Rothenbuhler 1964). The “all genetic” paradigm began to show its limits however, even in “simple” organisms, at the end of the twentieth century. Indeed, it was pro- gressively shown that genetically programmed cases of behaviour are rare, more complex and less univocally determined than was imagined (Lapidge et al. 2002). The complexity of gene regulation, the discovery of epigenetics and the influence of interactions with the environment, the impossibility of predicting events in strictly genetic terms, were all elements that undermined the idea of entirely determined behaviour. It can be said that plants express their behaviour through their growth (mainly by tropisms), but this growth, unlike that of many animals, remains largely unde- termined from a genetic point of view. Beyond their basic architecture, plants show an impressive degree of developmental variability. In its very terminology, the concept of “developmental plasticity” revealed from the outset the difficulty for genetic determinism to account for plant behaviour. Indeed, if development were really determined in its entirety, there should be no room for the contingencies of plasticity. For example, the study of organ development within the root has now shown that the development of particular cell types such as absorbent hair is not entirely determined by the expression of the genetic program of the initial meristematic cells14 (Raven et al. 2014). It is rather the relative position of neighbouring cells that influences their fate: “It seems that the initials of the cortex, and perhaps all initials, depend on position information from more differentiated daughter cells in the same cell layer. In other words, the initials of the apical meristem of the root do not seem to possess

14 These are stem cells that are present in the buds of all plants and are renewed throughout their continuous growth. 123 Synthese (2021) 198:3625–3650 3643

any intrinsic information deﬁning their fate. This contradicts the traditional view that meristems are autonomous machines capable of producing differentiation plans on their own” (Raven et al. 2014, p. 574).

Plants therefore seem to be uniﬁed by a coherent behaviour if, by this, we mean their ability to choose within and through environmental interactions, and that we cannot entirely reduce these interactions to a genetic determinism or to the mechanism of each part which would function like the parts of a clock or a machine.

3 Discussion and conclusion

In the twenty-first century, the sensitivity and movements of plants are widely recognized, and the reality of plant behaviour is increasingly accepted. If from a historical point of view, the recognition of movement by botanists was a cru- cial step in attributing behaviour to plants, it would be inaccurate today to reduce plant behaviour to movement alone. In fact, in plants, behaviours are the responses of organisms to environmental problems, whether or not they involve movement. It is now accepted that plant behaviour is expressed in the most visible, but not necessarily only way through plant growth (Trewavas 2014,p.73).In addition, behaviour can be defined independently of any reference to the struc- tural mechanisms by which it is expressed (muscle movement or cell elongation) (Silvertown and Gordon 1989; Karban 2008; Cahill and McNickle 2011; Cahill 2015). Technical and scientific advances now offer numerous experimental studies highlighting electrical, chemical, hydraulic or hormonal signaling mechanisms relating to phenomena explainable in terms of defense, communication, memory and even learning in plants (Trewavas 2014; Chamovitz 2012; Lenne 2014; Mancuso and Viola 2015; Thellier 2015; Gagliano 2015; Abramson and Chicas- Mosier 2016; Tassin 2016). Again, all these terms are to be understood in a non-anthropomorphic sense, which does not mean they are totally alien to their traditional context. However, from an epistemological point of view, controversies have scarcely evolved. They continue to be more embedded in the way behaviour is named and interpreted than in the facts themselves. Recent debates about plant “intelligence” are emblematic at this level (Trewavas 2003, 2004, 2005, 2014;Firn2004;Alpi et al. 2007; Brenner et al. 2007; Cvrcková et al. 2009; Calvo and Baluška 2015). In a way, they replay and amplify recurring elements in controversies about abili- ties of plants to memorize, choose and learn (Gagliano et al. 2014). This is reflected in the recent discipline of “plant neurobiology” (Brenner et al. 2006;Barlow2008; Mancuso and Viola 2015), which has taken on the task of framing plant sensitivity by analogy with animal neurobiological processes. One of their main tenants, is that plant cells have all the features and capabilities of neurons (Baluška 2010). For example, current plant neurobiologists consider root apex navigation as a cognitive process and claim their affiliation with the theory of root apex brain proposed by Charles and Francis Darwin (Baluška et al. 2009;Barlow2010; Baluška and Mancuso 2018). They argue that roots are social, cognitive and behaviourally very 123 3644 Synthese (2021) 198:3625–3650 active plant organs (Gruntman and Novoplansky 2004; Falik et al. 2006; Hodges 2009; Baluška and Mancuso 2018). More generally, these scientists emphasize the active nature of plant behaviour, for example in the way they communicate with other plants or insects to achieve their goals (reproduction, defence against preda- tion, etc.). But for many of its detractors, it is simply impossible to speak of plant behaviour in neurobiological terms insofar as plants are devoid of brains and nerves. Certain scientists (Alpi et 35 al. 2007) believe that this is a misuse of language, an important source of bias in the way we approach plant reactions. Contemporary philosophers (Churchland 1986, p. 13, 2002, p. 70 commented by Calvo 2016; see Maher 2017, pp. 67–68 for other examples) and biologists (Wilkins 1995;Firn2004; Struik et al. 2008) deny any agency to plants and assume that plant behaviour is decentralized, passive and programmed, for example by comparing it to the mechanical regulation of a thermostat or a washing machine program that can neither choose nor learn (unlike animals). From this perspective, the passivity of plant behaviour is no longer due to insensitivity or lack of movement, but to selection and adaptation that would suffice to account for all their activities (without having to assume a unified organic intelligence). The analogy with modern history, its examples and arguments and the emergence of plant physiology in the nineteenth century is striking: intellectual blockages seem to have changed very little in 150 years of experimental plant study. Thus, the agentivist plant biologists defend a far more active model of plant behaviour similar to that of animals in terms of its effects, while plant neurobiologists go even further by emphasizing and reactivating analogies with structures such as those that would exist between plant cells and neurons or in terms of action-potential mechanisms that induce the movements of plant organs and animal muscles (and are hindered in both cases by the same anesthetic substances) (Yokawa et al. 2018, 2019). From this historical standpoint, plant neurobiology appears less revolutionary, or upsetting, than we might initially think. It can however, be credited for making more explicit the pluralism that has always underpinned the explanations of plant behaviour. For more than four centuries, two epistemological conceptions of plant behaviour have thus clashed within botany and plant biology: one is an entirely mechanistic and deterministic (physical then genetic and adaptationnist) approach to the actions of plants, the other recognizes a form of agency of plants that gives them a genuine form of perception and a certain variability in their modes of action. To simplify, the first approach compares the activities of plants with those of phenomena in the physico-chemical world, while the second seeks to compare them with the spontaneous activities of animals. These two explanatory approaches have their own vocabulary and perspectives. Below we have drawn up a non-exhaustive summary table:

123 Synthese (2021) 198:3625–3650 3645

Determinism Agency

Insensitivity (till the twentieth century) Sensitivity Machine/heteronomy Soul/autonomy Development Behaviour Object in a physical world Autonomous agent Physical necessity Biological contingency Mechanism Function Causality Purpose Physiology Biology of behaviour/Ethology/Plant neurobiology Reductionism Holistic approach (behavioural ecology) Randomness-Determinism Choice/decision Genetic traits Interactions (social or environmental) Programming Learning

This pedagogical presentation should not suggest that all the concepts of these two approaches are necessarily in opposition. In fact, rather than opposing these two explanatory approaches, some biologists of plant behaviour and philosophers are now seeking to reconcile this pluralism (Cvrcková et al. 2009, 2016). All biologists nowa- days admit, for example, that plants are sensitive organisms and that their genes have an influence on their behaviour. Many other concepts are shared and are not problematic (the fact that there is a selection pressure that shapes behaviour, that some behaviours are instinctive while others are learned, that epigenetics can link environmental interactions and genetic traits, etc.). Furthermore, our historical synthesis shows that it is misguided to hastily reduce behavioural determinism to external causality and agentivity to internal causality. Indeed, genetic determinism is a form of internalized causal reductionism and behavioural ecology does not conceive the agency of organisms independently of their interactions with the social group or the external environment—even if it does not reduce them to the necessity of a causal mechanism. It can thus be claimed that some of plants’ behavioural strategies exhibit forms of contingency and unpredictabil- ity (Cahill and McNickle 2011). One of the keys to understanding these phenomena probably lies in the ability of individual learning (Gagliano et al. 2014; Gagliano et al. 2016). Another approach is often favoured from a methodological point of view: epistemological neutrality regarding the interpretative choice mentioned above. This position is the one most often adopted in the study of plants where the very definition of the term “behaviour” poses specific problems. To the extent that neutrality is a practical position, which is rather inferred by the absence of an explicit position in favour of determinism or agency, it leaves many theoretical issues pending. In this way, answering questions such as the intentionality of behaviours, the unity of behaviour (must a behaviour be related to the unity of the organism or to infra- or supra-organic entities such as genes, cells, organs or populations?) or the possibility of a plant ethology, require positioning oneself with regard to the perspective adopted. This is also true for some evolutionary issues. For example, the agency of organisms involves them in the 123 3646 Synthese (2021) 198:3625–3650 evolution of their species and does not merely reduce them to products of a selection process (Walsh 2015; Okasha 2018). Behaviours involving niche construction go in this direction: by shaping their own environment (e.g. soil for plants), organisms themselves become active in certain environmental selection conditions15 (Sultan 2015). Nevertheless, the agentivist position is not free from criticism. Indeed, in practice, discerning which behaviours are actually determined and which behaviours are not entirely determined remains problematic, especially in organisms such as plants. This should make us aware that explanations in terms of deterministic causality or agentivity need not be mutually exclusive, but that most behaviours can be approached by both types of explanation. Moreover, from the moment the epistemological principle of parsimony is no longer respected in scientific explanations, with the introduction of philosophical concepts that cannot be directly demonstrated, one may fear a multiplication of such concepts and a form of anthropomorphic plant behaviour. A non-critical anthropomorphisation is also a source of bias, it can harm observations and interpretations of plant behaviour. The agentivist posture must thus provide new epistemological guarantees to the concepts it introduces into the biology of behaviour (Dennett 1983), for example by naturalizing them through scientific foundations (Walsh 2015, pp. 210–11; Barandarian et al. 2009; Di Paolo 2005; Ruiz-Mirazo and Moreno 2012; Ruiz-Mirazo et al. 2000) or more generally by showing the effects and new ways of thinking they pragmatically open up in terms of scientific hypotheses and experimental apparatus (Despret 2009, 2014). Although this goes beyond the epistemology of of plant behaviour, recognizing an agency in organisms that traditionally lacked it, such as plants, indirectly raises ethical questions. Indeed, going against the sensibilities, choices, directions and goals of an organism that is, to some extent, an actor of its own life, requires a minimum of awareness and respect of its behaviours. It is not a question of condemning all recourse to plant exploitation, but of having a more reasoned and respectful use of it. This last point should not a priori be discredited or underestimated, especially since it is complementary to many reflections on environmental ethics (Hall 2011). In conclusion, one perspective on plant behaviour is not in and of itself, in absolute terms, better than another. We have shown that the explanatory pluralism of behaviour has been constructed in history through a series of problems and concepts and that choosing between one or the other was as much a strategic question as it was an epistemological one. Contemporary sciences therefore inherit an array of approaches to plant behaviour. It is now time to balance the terms of the opposition that historically consisted in distinguishing animal behaviour from plant behaviour. The diversity of life forms, the evolutionary framework, but also recent experiences (Gagliano 2015, Trewavas 2014) invite us to adopt a more continuous and nuanced ontological and epistemological perspective on living organisms and their behaviour.

Acknowledgements I thank Professor Benoît Timmermans for his support, my colleague Dr. Tyler Reige- luth for his ﬁnal proofreading and the anonymous reviewers as well as the editors who allowed me to considerably improve this article.

15 Of course niche construction doesn’t imply a teleological view on evolution or a necessary intentional activity of the organism. 123 Synthese (2021) 198:3625–3650 3647

References

Abramson, C. I., & Chicas-Mosier, A. M. (2016). Learning in plants: Lessons from Mimosa pudica. Frontiers in Psychology, 7, 417. Alpi, A., et al. (2007). Plant neurobiology: No brain, no gain? Trends in Plant Science, 12, 135–136. Amigues, S. (1988). Théophraste. Recherches sur les plantes: à l’origine de la botanique, trad. fr. S. Amigues, Paris: Les Belles Lettres. Amigues, S. (2012). Théophraste. Les causes des phénomènes végétaux, trad. S. Amigues. Paris: Les Belles Lettres. Arber, A. (1912). Herbals, their origin and evolution, a chapter in the history of botany 1470–1670. Cambridge: Cambridge University Press. Arber, A. (2012). The natural Philosophy of plant form [1950]. Cambridge: Cambridge University Press. Baldwin, I. T., Halitschke, R., Paschold, A., von Dahl, C. C., & Preston, C. A. (2006). Volatile signaling in plant-plant interactions: “Talking trees” in the genomics era. Science, 311(5762), 812–815. Baldwin, I. T., & Schultz, J. C. (1983). Rapid changes in tree leaf chemistry induced by damage: Evidence for communication between plants. Science, 221, 227–279. Ballaré, C., & Trewavas, A. (2009). Plant behaviour special issue. Plant, Cell & Environment, 32(6), 605. Baluška, F. (2010). Recent surprising similarities between plant cells and neurons. Plant Signaling & Behavior, 5, 87–89. Baluška, F., & Mancuso, S. (2018). Plant cognition and behavior: from environmental awareness to synaptic circuits navigating root apices. In F. Baluška (Ed.), Memory and learning in plants (pp. 51–77). Berlin: Springer International Publishing. Baluška, F., Mancuso, S., & Volkmann, D. (Eds.). (2006). Communication in plants: Neuronal aspects of plant life. Dordrecht: Springer. Baluška, F., Mancuso, S., Volkmann, D., & Barlow, P. W. (2009). The ‘root-brain’ hypothesis of Charles and Francis Darwin: Revival after more than 125 years. Plant Signaling & Behavior, 4, 1121–1127. Barandarian, X., Di Paolo, E., & Rohde, M. (2009). Defining agency: Individuality, normativity, asymmetry and spatio-temporality in action. Journal of Adaptive Behavior., 10, 1–13. (Special Issue on Agency). Barlow, P. W. (2008). Reflections on ‘plant neurobiology’. BioSystems, 92(2), 132–147. Barlow, P. W. (2010). Plant roots: Autopoietic and cognitive constructions. Plant Root, 4, 40–52. Bernier, G. (2013). Darwin un pionnier de la physiologie végétale. L’apport de son fils Francis. Académie Royale de Belgique: Bruxelles. Bonnet, C. (1769). Contemplation de la nature (2nd ed.). Amsterdam: M.-M. Rey. Boscowitz, A. (1867). L’âme de la plante. Paris: Ducrocq. Bose, J. C. H. (1907). Plant response as a means of physiological investigation. London, New York: Longman, Green and Co. Bose, J. C. H. (1913). Researches on the irritability of plants. London: Longman, Green and Co. Bose, J. C. H. (1925). Physiological and anatomical investigations on Mimosa pudica. Proceedings of the Royal Society of London. Series B, B98, 280–299. Bose, J. C. H. (1926). The nervous mechanism of plants. London: Longman, Green and Co. Braam, J. (2005). In touch: Plant responses to mechanical stimuli. New Phytologist, 165, 373–389. Braam, J., & Davis, R. W. (1990). Rain-induced, wind-induced, and touch-induced expression of calmodulin and calmodulin related genes in Arabidopsis. Cell, 60, 357–364. Brenner, E. D., Stahlberg, R., Mancuso, S., Baluška, F., van Volkenburgh, E., (2007). Response to Alpi et al.: Plant neurobiology: The gain is more than the name, Trends in Plant Science, 12(7), 285–286. Brenner, E. D., Stahlberg, R., Mancuso, S., Vivanco, J., Baluška, F., & Volkenburg, E. (2006). Plant neurobiology: An integrated view of plant signalling. Trends in Plant Sciences, 11, 413–449. Brown, J. (1792). Elementa medicinae. Mediolani: J. Galealius. Burdon-Sanderson, J. (1873). Note on the electrical phenomena which accompany stimulation of leaf of Dionea muscipula. Proceedings of the Royal Society of London, 21, 495–496. Burdon-Sanderson, J. (1899). On the relation of motion in animals and plants to the electrical phenomena which are associated with it. Proceedings of the Royal Society of London, 65, 37–64. Cahill, J. F. (2015). Introduction to the special issue: Beyond traits: Integrating behaviour into plant ecology and biology. AoB PLANTS, 7: plv120 Cahill, J. F., & McNickle, G. G. (2011). The behavioral ecology of nutrient foraging by plants. Annual Review of Ecology Evolution and Systematics, 42, 289–311. Calvo, P. (2016). The philosophy of plant neurobiology: A manifesto. Synthese, 193(5), 1323–1343.

123 3648 Synthese (2021) 198:3625–3650

Calvo, P., & Baluška, F. (2015). Conditions for minimal intelligence across eukaryota: A cognitive science perspective. Frontiers in Psychology, 6, 1329. Canguilhem, G. (2015). La connaissance de la vie. Paris: Vrin. Cesalpino, A. (1583). De plantis libri. Florentia: Georgium Marescottum. Chamovitz, D. (2012). What a plant knows. Oxford: Oneworld Publications. Churchland, P. S. (1986). Neurophilosophy: Toward a unified science of the mind-brain. Cambridge, MA: MIT Press. Churchland, P. S. (2002). Brain-wise: Studies in neurophilosophy. Cambridge, MA: MIT Press. Crespi, M., & Linskens, H. F. (1999). The discovery of sexual reproduction in higher plants. Acta Biologica Cracoviensia, series Botanica, 41, 19–29. Cvrcková, F., Lipavská, H., & Žárský, V.(2009). Plant intelligence: Why, why not or where? Plant Signaling & Behavior, 4, 394–399. Cvrcková, F., Žárský, V., & Markoš, A. (2016). Plant studies may lead us to rethink the concept of behavior. Frontiers in Psychology, 7, 622. Darwin, E. (1800). Phytologia; or the philosophy of agriculture and gardening. London: J. Johnson. Darwin, C. (1865). On the movements and habits of climbing plants. Journal of the Linnean Society of London (Botany), 9, 1–118. Darwin, C. (1875). Insectivorous plants. London: John Murray. Darwin, C., & Darwin, F. (1880). The power of movement in plants. London: John Murray. Davy de Virville, A. (1954). Histoire de la botanique en France. Paris: SEDES. Davy de Virville, A., Leroy, J.-F. (1969). Botanique à la Renaissance. In: Taton R. (ed) et al., La science moderne de 1450 à 1800 (pp. 177–187). Paris: Presses Universitaires de France. Davy de Virville, A., Leroy, J.-F. (1969b). Botanique au XVIIIe siècle. In: Taton R. (ed) et al., La science moderne de 1450 à 1800 (pp. 677–697). Paris: Presses Universitaires de France. de Candolle, A.-P. (1801). Expériences relatives à l’influence de la lumière sur quelques végétaux. Journal de Physique, 52, 128. de La Mettrie, J. O. (2003). L’homme-plante [1748]. Paris: le Corridor bleu. de Lamarck, J.-B. C. (1815). Histoire naturelle des animaux sans vertèbres. Paris: Verdière. Delaporte, F. (2011). Le second règne de la nature [1979]. Paris: Editions des archives contemporaines. Dennett, D. C. (1983). Intentional systems in cognitive ethology: The ‘panglossian paradigm’ defended. The behavioral and brain Sciences, 6, 343–390. Despret, V. (2009). Penser comme un rat. Versailles: Quae. Despret, V. (2014). Que nous diraient les animaux si… on leur posait les bonnes questions ?. Paris: La Découverte. Di Paolo, E. (2005). Autopoiesis, adaptivity, teleology, agency. Phenomenology and the Cognitive Sciences, 4, 429–452. Dretske, F. (1988). Explaining behavior. Cambridge & London: MIT Press. Errera, L. (1910). Receuil d’œuvres. Physiologie générale, Philosophie. Bruxelles: Lamertin. Falik, O., de Kroon, H., & Novoplansky, A. (2006). Physiologically-mediated self/non-self root discrimination in Trifolium repens has mixed effects on plant performance. Plant Signaling & Behavior, 1, 116–121. Firn, R. (2004). Plant intelligence: An alternative point of view. Annals of Botany, 93, 345–351. Fisher, R. A. (1930). The genetical theory of natural selection. London: Oxford University Press. Flourens, M. J. P. (1842). Éloge historique de Pyramus de Candolle. Institut royal de France: Académie royale des Sciences. Fox Keller, E. (1995). Refiguring life: Metaphors of twentieth-century biology. The Wellek Library Lecture Series at the University of California, Irvine: Columbia University Press. Fox Keller, E. (2000). The century of the gene. Cambridge: Harvard University Press. Gagliano M. (2015). In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants. AoB Plants,7. Gagliano, M., Renton, M., Depczynski, M., & Mancuso, S. (2014). Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia, 175(1), 163–172. Gagliano, M., Vyazovskiy, V., Borbély, A. A., Grimonprez, M., & Depczynski, M. (2016). Learning by association in plants. Scientific Reports, 6, 38427. Garbaye, J. (2013). La symbiose mycorhizienne. Versailles: Quae. Girtanner, C. (1790). Mémoire sur l’irritabilité, considérée comme principe de vie dans la nature organisée. Journal de physique, 36, 422–440.

123 Synthese (2021) 198:3625–3650 3649

Greene, E. L. (1983). Landmarks of botanical history II. Stanford: Stanford University Press. Gruntman, M., & Novoplansky, A. (2004). Physiologically mediated self/non-self discrimination in roots. Proceedings of the National Academy of Sciences of the United States of America, 101, 3863–3867. Guédès, M. (1974). Augustin-Pyrame de Candolle et les mouvements des végétaux. In Histoire et nature, nouvelle série, fasc. 2. Haberlandt, G. (1890). Das reizleitende Gewebesystem der Sinnpflanze. Leipzig: Engelmann-Verlag. Haberlandt, G. (1901). Sinnesorgane im Pflanzenreich zur Perzeption mechanischer Reize. Leipzig: Verlag von Wilhelm Engelmann. Hall, M. (2011). Plants as persons a philosophical botany. Albany: State University of New York Press. Hallé, F. (1999). Éloge de la plante: Pour une nouvelle biologie. Paris: Seuil. Hodge, A. (2009). Root decisions. Plant, Cell and Environment, 32(6), 628–640. Hooper, R. (1797). Observation on the structure and economy of plants; to which is added the analogy between the animal and vegetable kingdom. Oxford: Fletcher and Co, Rivington, Murray and Highley. Hull, D. L. (1978). A matter of individuality. Philosophy of Science, 45, 335–360. Hull, D. L. (1992). Individual. In E. F. Keller & E. Lloyd (Eds.), Keywords in evolutionary biology (pp. 181–187). Cambridge: Harvard University Press. Jacob, F. (1981). Le jeu des possibles. Paris: Fayard. Jaffe, M. J. (1973). Thigmomorphogenesis: The response of plant growth and development to mechanical stimulation—with special reference to Bryonica dioica. Planta, 114, 143–157. Karban, R. (2008). Plant behaviour and communication. Ecology Letters, 11, 727–739. Kutschera, U. (2015). Basic versus applied research: Julius Sachs (1832–1897) and the experimental physiology of plants. Plant Signaling & Behavior, 10, 9. Kutschera, U., & Briggs, W. R. (2009). From Charles Darwin’s botanical country-house studies to modern plant biology. Plant Biol, 11, 785–795. Kutschera, U., & Niklas, K. J. (2009). Evolutionary plant physiology: Charles Darwin’s forgotten synthesis. Naturwissenschaften, 96, 1339–1354. Lapidge, K. L., Oldroyd, B. P., & Spivak, M. (2002). Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften, 89, 565–568. Lenne, C. (2014). Dans la peau d’une plante. Paris: Belin. Levitis, D. A., Lidicker, W. Z., & Freund, G. (2009). Behavioural biologists don’t agree on what constitutes behaviour. Animal Behaviour, 78, 103–110. Linnaeus, C. (2005), Fondements botaniques, qui, comme Prodrome à de plus amples travaux livrent la théorie de la science botanique par brefs aphorismes [1736], trad. fr. G. Dubos et T. Hoquet, Paris: Vuibert. Lovejoy A. (1964) [1936]. The great chain of being: A study of the history of an idea. Cambridge, Mas- sachusetts: Harvard University Press. Magnin-Gonze, J. (2009). Histoire de la botanique. Paris: Delachaux et Niestlé. Mahall, B. E., & Callaway, R. M. (1991). Root communication among desert shrubs. Proceedings of the National Academy of Sciences U.S.A., 88, 874–876. Maher, C. (2017). Plant minds: A philosophical defense. New York: Routledge. Mancuso, S., Viola, A. (2015). Brilliant Green. The surprising History and Science of Plant Intelligence, trad. J. Benham, Washington, Island Press. Marder, M. (2013). Plant-thinking a philosophy of vegetal life. New York: Columbia University Press. Moreno, A., & Mossio, M. (2015). Biological autonomy: A philosophical and theoretical enquiry.New York: Springer. Nettle, D., & Bateson, M. (2015). Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proc. R. Soc., B, 282: 20151005. Okasha, S. (2018). Agents and goals in evolution. Oxford: Oxford University Press. Pfeffer, W. (1881). Pflanzenphysiologie. Leipzig: Engelmann. Pultney, R. (1790). Historical and biographical sketches of the progress of Botany in England from its origin to the Linnean system. London: T. Cadell. Raven, P., Evert, R., & Eichorn, S. (2013). Biology of plants (8th ed.). New York: Freeman and Company Publishers. Raven, P., Evert, R., Eichorn, S. (2014). Biologie végétale, 3e éd., trad. fr. J. Bouharmont, Bruxelles: De Boeck. Rothenbuhler, W. C. (1964). Behavior genetics of nest cleaning in honey bees. Iv. Responses of F1 and backcross generations to disease-killed blood. American Zoologist, 45, 111–123.

123 3650 Synthese (2021) 198:3625–3650

Ruiz-Mirazo, K. J., & Moreno, A. (2012). Autonomy in evolution: From minimal to complex life. Synthese, 185, 21–52. Ruiz-Mirazo, K. J., et al. (2000). Organisms and their place in biology. Theory in Biosciences, 119, 209–223. Russell, E. S. (1934). The study of behaviour. Aberdeen: British Association for the Advancement of Science. Scheler, M. (1951). La situation de l’homme dans le monde [1928], trad. fr. M. Dupuy. Paris: Aubier. Scott, P. (2008). Physiology and behaviour of plants. Hoboken: John Wiley. Silvertown, J., & Gordon, D. M. (1989). A framework for plant behavior. Annual Review of Ecology and Systematics, 20, 349–366. Simons, P. (1992). The action plant. Oxford and Cambridge: Blackwell. Stalhberg, R. (2006). Historical overview on plant neurobiology. Plant Signaling & Behavior, 1(1), 6–8. Stebbins G. L. (1980). Botany and the synthetic theory of evolution. In E. Mayr & W. B. Provine (Eds.) The evolutionary synthesis (pp. 139–152). Cambridge: Harvard University Press. Struik, P. C., Yin, X., & Meinke, H. (2008). Plant neurobiology and green plant intelligence, science, metaphors and nonsense. Journal of the Science of Food and Agriculture, 88, 363–370. Sultan, S. E. (2015). Organism and environment. Oxford: Oxford University Press. Taiz, L., & Taiz, L. (2016). Flora unveiled: The discovery and denial of sex in plants. Oxford: Oxford University Press. Taiz, L., & Zeiger, E. (2010). Plant physiology. The Fifth Edition: Sinauer Associates. Tassin, J. (2016). À quoi pensent les plantes. Paris: Odile Jacob. Thellier, M. (2015). Les plantes ont-elles une mémoire?. Versailles: Quae. Tinbergen, N. (1963). On aims and methods of ethology. Z Tierpsychology, 20, 410–433. Trewavas, A. (2003). Aspects of plant intelligence. Annals of Botany, 92, 1–20. Trewavas, A. (2004). Aspects of plant intelligence: An answer to Firn. Annals of Botany, 93, 353–357. Trewavas, A. (2005). Green plants as intelligent organisms. Trends in Plant Sciences, 10(9), 413–419. Trewavas, A. (2014). Plant behaviour and intelligence. Oxford: Oxford University Press. Tupper, J. P. (1811). An essay on the probability of sensation in vegetables. London: Richard Taylor and co. van Loon, L. C. (2015). The intelligent behavior of plants. Trends in Plant Science, 21(4), 286–294. Varin, S. (2017). Plasticité et instabilité développementale. Concept en biologie. Exemple des végétaux, Paris: L’harmattan. von Sachs, J. (1865). Handbuch der Experimentalphysiologie der Pflanzen. Leipzig: W. Engelmann. von Sachs, J. (1882). Vorlesung über Pflanzen-Physiologie. Leipzig: W Engelmann. von Sachs, J. (1892). Histoire de la botanique (1530–1860), trad. fr. Henry de Varigny. Paris: Reinwald et cie. Walsh, D. M. (2015). Organisms, agency and evolution. Cambridge: Cambridge University Press. Webster, C. (1966). The recognition of plant sensitivity by English botanists in the seventeenth century. Isis, 57(187), 5–23. Wilkins, M. B. (1995). Are plants intelligent? In P. Day & C. Catlow (Eds.), Bycicling to utopia. Oxford: Oxford University Press. Yokawa, K., Kagenishi, T., & Baluška, F. (2019). Anesthetics, anesthesia, and plants. Trends in Plant Science, 24, 12–14. Yokawa, K., Kagenishi, T., Pavlovic, A., Gall, S., Weiland, M., Mancuso, S., et al. (2018). Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps. Annals of Botany, 122, 747–756.

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