نقش ادراک حسی گیاه در تعاملات گیاهان و حیوانات Role of plant sensory perception in plant–animal interactions

Introduction Humans necessarily view all living things through the lens of our own experience, and this unavoidable conceptual bias has been a frequent source of confusion in biology. It gives rise to a natural tendency, among scientists and non-scientists alike, to anthropomorphize non-human species, with sometimes unfortunate consequences (Abelson, 1974; Kennedy, 1992). But it can also lead us to overlook underlying similarities between humans and other organisms, whose ways of living may seem at first glance to be utterly different from our own. Not surprisingly, both types of error have been amply represented in the study of plants, and perhaps nowhere more so than in relation to plants’ perceptual and sensory capabilities. On one hand, plants’ sedentary lifestyle tends to obscure the myriad ways in which they actively perceive and respond to their environments, as the responses frequently entail changes in internal physiology—such as leaf or phloem chemistry—that are relatively imperceptible (to humans), as well as changes in growth and development that are more readily apparent, but which unfold on timescales too slow to be seen by casual observation. Indeed Aristotle, who arguably founded the systematic study of biology, thought that plants lacked the capacity for sensory perception and that this absence set them apart from animals and humans, arguing that ‘plants live without sensation, and it is by sensation that we distinguish animal from what is not animal’ (Aristotle, 1984). On the other hand, humans are almost invariably fascinated by examples of plants that exhibit ‘animal-like’ sensory responses and behaviours, such as the rapid movements exhibited by some carnivorous plant species. This fascination may have deep roots in human psychology, as the salience of anthropomorphic and other counterfactual and supernatural concepts has been attributed to the violation of intuitive ontological categories that humans recognise from the earliest stages of cognitive development (Boyer, 1996, 2001). And it may explain why fanciful and empirically unsupported claims about the purportedly complex inner lives of plants have often gained a prominent and, as discussed below, occasionally problematic, place in the public imagination. The apogee of botanical pseudoscience probably arrived in the mid-1970s, marked by the publication of ‘The Secret Life of Plants: A Fascinating Account of the Physical, Emotional and Spiritual Relations Between Plants and Men’ (Tomkins and Bird, 1973), which summarized a wide range of ‘research’ purporting to address plants’ perceptual, psychological, and emotional capacities. This book—a New York Times bestseller that has been translated into several foreign languages and remains in print to this date—also inspired a 1979 documentary film of the same name. It prominently featured the work of Cleve Backster, a former CIA interrogation specialist who used polygraph equipment to measure changes in the electrical resistance of plant leaves and claimed to record patterns revealing emotional responses to various experimental conditions, including threats of harm against the plant or other nearby organisms. Backster also claimed to show that plants were capable of extra-sensory ‘primary perception’ of human emotional states, as well as stress in other organisms (Backster, 1968). A second book published the same year, ‘The Sound of Music and Plants’ (Retallack, 1973), described experiments exploring the effects of different styles of music on plant growth and wellbeing (Retallack’s plants reportedly preferred classical music to rock, but were largely indifferent to country and western). Despite a rather obvious lack of scientific rigour (i.e. evidence presented in peer-reviewed studies published in mainstream scientific journals) work such as that described above received considerable public attention and popular press coverage, to the point that many reputable scientists felt compelled to respond (e.g. Abelson, 1974; Galston, 1975; Galston and Slayman, 1979). The leading research journal Science published a test of the primary perception hypothesis (Backster, 1968) that replicated the techniques of one of Backster’s most prominent experiments but, rather unsurprisingly, found no discernable plant response to the mass death (by boiling) of brine shrimp (Horowitz et al., 1975). Meanwhile, a panel of biologists at the 1975 annual meeting of the American Association for the Advancement of Science explored claims regarding plant sentience and deemed them scientifically unsupportable, with one member lamenting a ‘gap between what scientists believe and what the lay public believes’ (St. Petersburg Times, 1975). From the perspective of the present day, it may provoke some amusement to think of leading scientists and academic journals of the 1970s devoting significant time and space to debunking absurd claims about the emotional psychology of houseplants. But this attention was the product of legitimate concern about the widespread public dissemination of unfounded pseudoscientific claims. Furthermore, there is little doubt that the widespread attention paid to this debate by the general scientific community influenced the perception of legitimate scientific research on the sensory and perceptual abilities of plants, with scepticism about the topic sometimes hindering scientific advances in this area (as discussed below). This history also provides important context for recent and ongoing debates about whether plants may in some sense be said to exhibit “intelligent” behaviour or even some rudimentary form of “consciousness”. These debates play out within the context of legitimate scientific inquiry and argument— and, frankly, often pivot on semantic and interpretive points rather than substantive differences about underlying scientific facts—with investigators on one side intent on emphasizing the real complexity and sophistication that plants manifest in their responses to environmental conditions (e.g. Trewavas, 2002, 2003; Brenner et al., 2006; Trewavas and Baluška, 2011), while others urge caution against overreaching or sensational claims and the use of terminology that may lead to misinterpretation (e.g. Alpi et al., 2007; Struik et al., 2008; Olsson and Forkman, 2012). It seems clear that the perceptual capabilities of plants lie somewhere between the extremes identified above. Plants are not the emotional adepts of Cleve Baxter’s imagination, but nor are they the senseless automatons that Aristotle and others may have believed them to be. Indeed, unlike the vast majority of animal species, which are capable of self-directed movement during at least some stage of their life cycles and are thus able to seek out favourable environments or flee adverse conditions, the growing stages of plants must adapt themselves to the conditions that prevail in the particular location where they are rooted and contend with the full range of environmental variability occurring at that location over the course of their lifetime. Consequently, plants respond to environmental variability largely through plasticity in growth and development, and they frequently exhibit plasticity in their morphology and physiology far exceeding that typically exhibited by animals. Such adaptability depends critically on an ability to detect, or anticipate, changing environmental conditions and respond accordingly (Casal et al., 2004). Thus, it is hardly surprising that recent and ongoing advances in the study of plant biology are yielding an increased appreciation for the complexity and sophistication of plants’ perceptual abilities. As a comprehensive account of these abilities lies beyond the scope of the current work, the remainder of this paper will focus more narrowly on summarizing current knowledge about the role of plant sensory perception in mediating interactions among plants and animals, including insect herbivores, which represent one of the most significant biotic stressors encountered by plants in most terrestrial ecosystems, and which are particularly well studied because of their relevance for human agriculture.