What Is Plant Behaviour?*

Plant, Cell and Environment (2009) 32, 606–616 doi: 10.1111/j.1365-3040.2009.01929.x What is plant behaviour?* ANTHONY TREWAVAS Institute of Molecular Plant Science, University of Edinburgh, Edinburgh EH9 3 JH, UK ABSTRACT ‘Among plants, form may be held to include something corresponding to behaviour in the zoological field. The The nature of plant behaviour is discussed, and it is con- animal can do things without inducing any essential change cluded that it is best described as what plants do. The in its bodily structure. When a bird uses its beak to pick up possibility that plant behaviour is simply signal-induced food, the beak remains unchanged. But for most, but not all, phenotypic plasticity is outlined, and some limitations of plants, the only available forms of action are either growth this assumption are considered. Natural environments or discarding of parts, both of which involve a change in present many challenges to growing plants, and the conse- the size and form of the organism’ (Arber 1950, p. 3). This quent signalling that plants perceive is becoming extremely statement identifies phenotypic plasticity as a form of complex. Plant behaviour is active, purposeful and inten- action in plants, that is, plant behaviour. The Latin word tional, and examples are discussed. Much plant behaviour, habere, from which the word behaviour is derived, means concerned with stress and herbivory, is also based on an ‘having’ or ‘being characterized by’.Arber’s statement indi- assessment of the future likelihood of further damaging cates that plant behaviour is action, that is, doing something. episodes and is therefore predictive. Plant behaviour Behaviour is then what a plant does, rather than something involves the acquisition and processing of information. it is characterized by or has. Informational terminology provides a suitable way of incorporating the concepts of learning, memory and intelligence into plant behaviour, capabilities that plants are Behaviour and plasticity rarely credited with. Finally, trade-offs, cost–benefit assess- In a seminal chapter, Silvertown & Gordon (1989) defined ments and decision making are common plant behavioural plant behaviour as the response to signals, and this, along attributes. It is suggested that intelligent assessments that with Arber’s description, equates plant behaviour with the involve the whole plant are essential to optimize these phenomenon of phenotypic plasticity (Trewavas 2003; adaptive capabilities. Sultan 2005; Karban 2008). Ecologists describe plasticity in terms of ‘norms of reaction’ that specify the boundaries of Key-words: communication network; intelligence; intention; plastic variation to individual signals (Schlichting & Pigli- purpose. ucci 1998; Sultan 2000). Not all tissues exhibit plastic responses (Bradshaw 1965). BEHAVIOUR IS WHAT PLANTS DO Phenotypic plasticity is not unique to plants however. Plant behaviour can, and indeed should, express a pheno- Defining plant behaviour typically local response to local signalling, but so can that The life cycle goal of any individual plant is optimal fitness, of other organisms. For example, human weightlifting spe- usually equated to maximum numbers of viable seedlings or cifically increases the development of the muscles most more conveniently, for experimental purposes, the numbers involved. The real difference between plant and animal of seeds. Seed yield is known to be dependent on lifetime behaviour was again indicated by Arber (1950, p. 136). acquired resources (carbohydrates, minerals and water, i.e. ‘The individuality of the mammalian body is of a much food), extent of predation and success in reproduction. more fixed character; that body consists of a limited Similar fitness requirements exist for animals – acquisition of number of organs which were once and for all marked out adequate food, avoidance of predators (or catching prey) in the embryo. With its parts arranged in an ordered hier- and successful reproduction. In animals, all these behav- archy there is no such thing as indefinite succession of ioural processes involve movement, and movement is limbs, of branches of limbs, numerically unfixed and liable recognized as the basis of animal behaviour. Higher plants to impede one another but this is what we find among spend their life cycle rooted in one position and,to the casual plants’. Movement is essential for the higher animal lif- observer, exhibit no movement, with only rare exceptions estyle. Only with accurate replication of limb numbers and like Mimosa. How then can plant behaviour be described? complex coordination among them could this be repro- ducibly achieved. Thus, crucial embryological tissue speci- Correspondence: A. Trewavas. Fax: +0131 650 5392; e-mail: fication is limited to the protected environments of the [email protected] egg or uterus, and subsequent plasticity is constrained to *This manuscript is part of the special issue on plant behaviour. more marginal changes in already specified organs. The © 2009 The Author 606 Journal compilation © 2009 Blackwell Publishing Ltd Plant behaviour 607 potential for plasticity is considered to have a genetic behaviour and (2) selected only a few individuals (geno- basis, but its realization must be epigenetic. types) for subsequent breeding out of a much greater range Most higher plants have a modular structure, and the of behavioural and genotypic variation (Lewontin 2001). plant body is plastically constructed from variable numbers But all phenotypes are constructed from a complex two- of leaves plus buds and branch roots. Plasticity enables the way conversation between genes and the total environ- phenotype to accurately occupy local space, change its phe- ment. Growth-room environments are perceived and used notype as it grows, forage accurately for resources, competi- to specify only one out of a range of phenotypes. All that tively exclude neighbours and construct, within genetic/ genes can ever do is specify a norm of reaction; they are environmental limitations, its own niche. The niche concept not invariant determinants of phenotype or behaviour involves little understood competitive and cooperative two- (Lewontin 2001). way signalling between individual and environment that is important in community structure (Muller-Landau 2003; Uriarte and Reeve 2003; Silvertown 2004; Donohue 2005; ENVIRONMENTAL SIGNALLING COMPLEXITY Kelly et al. 2008; Liebold 2008). Badri & Vivanco (2009) in AND BEHAVIOUR this issue reviewed recent information on root exudates Many signals are perceived that contribute to niche construction. Predation is inevitable for wild plants, but numerous What growth rooms cannot mimic is the enormous com- dormant meristems, regrowth and often extraordinary plexity of the external environment experienced by the wild regenerative capacities can diminish but not eliminate the plant. Behaviour is inextricably linked to environmental potential reduction in fitness. It is also the reason that plants signalling. Because plants are sessile organisms, they may do not place critical functions in one or two tissues as perceive more environmental signals and with greater sen- animals do with heart or kidneys. Such specialization would sitivity and discrimination than the roaming animal. ‘If make the individual extremely vulnerable to even slight etiolated seedlings are placed between two sources of light predation. However, the phenotype is holistically deter- differing so slightly that the differences cannot be detected mined. Excision of either a whole shoot or root inhibits by ordinary photometric methods, the seedling always further plasticity changes until regeneration of the lost bends promptly towards the source of the more intense organs is completed. Moreover, fitness itself is a function of light’ (Palladin 1918, p. 246) is certainly indicative. the integrated phenotype, not just the behaviour of indi- In this special issue on plant behaviour, many articles vidual tissues. deal with particular kinds of environmental signalling. Foraging is described as the behavioural alterations that Limitations to equating behaviour just to enhance the uptake of essential resources and De Kroon signal-induced changes et al. (2009) highlighted both the local and integrated signalling that underpins these vital processes. Mott (unpub- There are several problems with equating plant behaviour lished data) described the systems behaviour of complexes only with plasticity. The term ‘reproductive behaviour’ is of stomatal cells that are crucial for foraging for carbon often used to distinguish whether reproduction is sexual dioxide. Forde and Walch-Liu (2009) also reviewed the or vegetative without regard to plasticity changes. Some important role of amino acids and nitrate in constructing species do have separate male and female flowers, and the root phenotype. The shoot phenotype is dependent on environmental conditions can change the proportions of the presence, absence and crucially the identity of neigh- each, implicating plasticity, too (Trewavas 2007b). Tsvi bours (see pictures in Bazzaz 2000, p. 114), and these may Sachs objected to essential developmental processes like reflect the ubiquity of competition. Ballaré (2009) empha- germination being classed as behaviour (quoted in Silver- sized the critical role of phytochrome in both light forag- town 1998). On the other hand, there is certainly inherent ing, overall resource allocation, herbivore defence and thus plasticity in the germination phenotypes of almost any shoot phenotype construction.

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