Plant Intelligence: an Alternative Point of View

Annals of Botany 93: 345±351, 2004 doi:10.1093/aob/mch058, available online at www.aob.oupjournals.org VIEWPOINT Plant Intelligence: an Alternative Point of View RICHARD FIRN* Department of Biology, University of York, PO Box 373, York YO10 5YW, UK Received: 9 September 2003 Returned for revision: 24 October 2003 Accepted: 8 January 2003 The concept of plant intelligence has been advanced by Trewavas as a potentially useful framework to guide those seeking to understand plant growth and development. In this short critique, the validity of this concept is critically assessed. Central to this critique is the proposition that the concept of the individual, to which intelligence and behaviour are intimately linked, cannot usefully be applied to plants. It is argued that the adaptive responses of plants are best appreciated if the importance of the autonomy of the individual organs is acknow- ledged. Although Trewavas does acknowledge the autonomy of organs by describing an individual plant as being à democratic confederation', that terminology implies a complexity to the interaction between organs which would demand a cogitative ability beyond that actually demonstrated in plants. It may be more appropriate to consider a plant as operating normally as a simple economic federation of many specialized economies (organs and cells). Occasionally, there can be a dramatic, and sometimes complex, reshaping of the economic balances, with the result that the fate of some or many of the individual cells will change. However, such major changes in growth and development are driven by a few simple events in an individual organ and cells. These driving events are more akin to small local revolutions in individual states than they are to democratic decisions in a sophisticated confederation. ã 2004 Annals of Botany Company Key words: Phenotypic plasticity, adaptation, development, individuality, intelligence, plant behaviour. INTRODUCTION the overlaying of a very in¯exible pattern of growth and In a stimulating, thought-provoking and wonderfully wide- development with an extremely variable behaviour (both ranging article, Trewavas has argued that `the use of the `hard wired' and learned). (This short article focuses on term intelligence with regard to plant behaviour will lead to comparisons of unitary `higher' animals and plants while a better understanding of the complexity of plant signal recognizing that equally important comparisons might be transduction, the discrimination and sensitivity with which drawn between `lower' and colonial animals and plants.) In plants construct images of their environment and raise contrast, the concept of the individual in the case of a plant critical questions how plants respond at the whole plant is much harder to de®ne. It is easy to think of a very young level' (Trewavas, 2003). Trewavas argued that evidence of seedling (the commonest experimental object in plant learning and memory in plants, both considered necessary science) as being an individual, but which is the individual components of a truly intelligent system, has largely been bracken plant in a huge clonal patch of bracken? Are all ignored with the result that there is little appreciation of Cox's Orange apple trees the same individual? Maybe, intelligence in plants. While there is a danger that any along with the injudicious use of statistics and the excessive discussion about intelligence in plants becomes distracted constraints that tight experimental control impose on studies by semantics, beneath any such linguistic debate there are of plant functioning (Trewavas, 2003), we need to add that a important issues that need to be appreciated by anyone blinkered use of ìndividual' young seedlings as model attempting to understand how plants work. systems may also be misleading. Interestingly, the wide- spread adoption, in the 19th century, of the very young seedling as the model for much experimental work INTELLIGENCE IS A PROPERTY OF coincided with the exploration of the proposal that, as in INDIVIDUALS? animals, certain plant organs could control the growth and development of other parts of the individual (for some A key issue in discussing intelligence is the concept of history, see Went and Thimann, 1937). In a very young individuality. The word individual leads us to the ®rst seedling with only two, distinct elongating organs, each semantic trap. The word in English derives from Latin, in- possessing an apical region pioneering the exploration of meaning not and dividuus meaning divisible. However, their own very different environments, it is maybe reason- dictionary de®nitions (e.g. Chambers, 1959) stretch this able to consider the seedling as an individual. However, de®nition to encompass meanings from subsisting as one to having an independent existence. Animals are highly once the two young axes lose their monopolies when other individualistic in the sense of subsisting as one. Each organs grow and develop, the sense of what is the individual animal has an individual identity which is a consequence of becomes less clear. Consequently, while there are some general principles governing the ways in which plants grow * For correspondence. Fax 01904 328505, e-mail [email protected] and develop, principles that may be most easily identi®ed by Annals of Botany 93/4, ã Annals of Botany Company 2004; all rights reserved 346 Firn Ð Plant Intelligence: an Alternative Point of View studying very young seedlings, the experimentalist needs to response to a stimulus' and that allows the term to be be conscious of the need to explain how similar processes applied rather easily to plants. Plants do indeed show might be controlled in more complex, multi-organ plants. A responses to stimuli and clearly those responses are largely 4-d-old arabidopsis seedling might look like an individual adaptive, hence one comes to a point that Stenhouse's but a strawberry plant with attached runners, a coppiced de®nition of intelligence could be applied to plants. But has willow tree or a shallot plant present dif®culties for those this semantic exercise helped us identify new, productive seeking to identify the individual. Those experimentalists ways of observing, studying, manipulating or understanding who con®ne their studies to young seedlings are not plants? Several generations of scientists have never doubted confronted with one of the key differences between animals that all organisms have evolved to show some ability to and plants. In animals, growth and development is the adapt to their environmental circumstances. A bacterium enlargement and modi®cation of the individual. But, in can monitor its environment and instigate developmental plants, growth and development also includes the adding of processes appropriate to the prevailing circumstances, but is new members, or the discarding of some old members, of that intelligence? Such simple adaptation behaviour might what Trewavas calls the `democratic confederation'. This be bacterial intelligence but is clearly not animal intelli- key difference is least apparent in young seedlings; but even gence. Hence we have reached a de®nition of intelligence in young seedlings the main organs can be grown in that has no meaning unless combined with another word or isolation, hence in the short term such organs largely depend used in a precise context in a sentence. This is not a new on their neighbours in the `confederation' as suppliers problem, as shown by the debate about whether machines (McIntyre, 2001) rather than governors. The `confederation' can be intelligent. The term machine intelligence can mean has evolved with economic dependence being the main something other than the intelligence of a machine. We can driving force behind specialization, hence the seedling is certainly start using the term plant intelligence but only if it really an economic union rather than democratic confeder- is agreed that the term has nothing to do with intelligence ation. (Plant biologists might more usefully read Adam (the ability to discern, comprehend and choose) in the more Smith than Thomas Paine to appreciate their experimental widely accepted sense. (To add to the opportunity for subjects.) The capacity of the seedling, and more evidently confusion it should be pointed out that the term `plant the capacity of the mature plant, is largely the summed intelligence' is already in use to mean the utilization of capacity of the component parts, with many of those data about the performance of factories to optimize capacities being interdependent largely in èconomic' performanceÐbut plants could be considered as factories, terms. As will now be argued, any ìntelligence' that so maybe that is OK; http://www.gefanucautomation.com/ might be ascribed to `the plant' could only reside in organs, plantintelligence/default.asp.) However, why do we need a tissues or cells because the concept of the plant as an new term? If the discussion of a plant's adaptive responses individual is a misleading one. is less ambiguous than a discussion of the plant's intelligence, why adopt the new term? Indeed, might not the adoption of the term plant intelligence begin to distort, INTELLIGENCE rather than clarify, our perception of the way in which plants Ìntelligence is not a term commonly used when plants are function? To illustrate this danger, some of the key terms discussed' (Trewavas, 2003). Maybe this is because plants that are part of Trewavas's view of plant intelligence will are clearly not intelligent in the sense that most people

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