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. species. Volatile (gaseous) chemicals are increasingly seen as A further complication is the potential lack of reversibil- important in plasticity. Well-established information has ity in phenotypic responses raised in this issue by Metlen, already reported the phenotypic alterations induced by Aschehoug & Callaway (2009).As they pointed out, behav- humidity (water vapour), carbon dioxide, oxygen (in flood- ioural plasticity in secondary metabolite production is ing responses and 10% oxygen environments), ethylene, reversible. But in contrast, abscission can be used to sub- ozone and, more recently, nitric oxide. But as Galis et al. stantially reverse phenotypic changes, and innate animal (2009) and Dicke (2009) reviewed here, signalling via behaviour certainly appears irreversible. volatile chemicals is of crucial importance in herbivory A further issue is whether there is an intrinsic control resistance. Particular combinations of volatiles overcome phenotype, generated in the absence of signalling and often vascular constraints on systemic signalling (Frost et al. assumed to be a growth-room phenotype. This perception 2007), while other combinations signal adjacent plants is compounded by the relatively uniform appearance of (Karban 2008). Different groups of volatiles again can be many field crops, a situation that has arisen because crop herbivore specific, attracting predatory, parasitoid wasps plant breeders have (1) eliminated much signal-induced (De Moraes et al. 1998). Dodder, a parasitic plant, also © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 608 A. Trewavas homes in on its host by detecting stem-released volatiles BEHAVIOUR, MOVEMENT, PURPOSE (Runyon, Mescher & De Moraes 2006), observations criti- AND INTENTION cal to understanding how Dodder maximizes the energy McDougall (1924) described behaviour in the following gained from the host while minimizing its energy invest- way. Animals are behaving if they actively resist the push ment in coiling and haustoria formation (Kelly 1992).Apart and pull of the environment, exhibit persistence of activity from ethylene, specific receptors for these volatiles await independently of the impression (signal) that may have characterization. initiated it and exhibit variation in the direction of persis- Other kinds of signalling have been detected, but their tent movements. This definition would characterize plant current molecular basis remains unknown. As both Hodge behaviour, too. (2009) and Novoplansky (2009), again in this issue, indicated, root systems are not only able to sense the soil volume in which they grow but can recognize and discrimi- Movement and behaviour nate against the roots of adjacent conspecifics and thus possess self-recognition. [Astonishingly bacteria have self- Movement would seem to be the simplest criterion of behav- recognition (Gibbs, Urbanowski & Greenberg 2008), indi- iour, and movement has always been an essential cating perhaps the ubiquity of self-recognition processes.] part of the animal lifestyle to find food, avoid predators (or Potentially, the roots of any individual plant avoid each catch prey) and find mates. Predator–prey relations among other as far as possible to improve the extent of soil space animals accelerated the evolutionary specialization of occupied and exhibit a kind of territoriality (Schenk, Calla- sensory organs and muscles to respond to signals. The way & Mahall 1999). Furthermore, the root system exhibits nervous tissue, a rapid information transmission system, holistic responses to the patchy environment experienced. then evolved, to link these two together. The faster the These observations do imply complex signalling below prey responded and moved,the faster any effective predator ground; could these root signals be presently unknown had to evolve in turn.Animal behaviour tends to be equated volatiles, too (Erb et al. 2008)? with movement because we ourselves are animals, because Other biotic signalling results from competition for soil our perception/response system works at the rate of trans- resources, from mycorrhizal and cooperative bacterial inter- mission of the nervous system (like most other animals) and actions and from allelopathic chemicals, disease, mutualism, because we regard our own movement as behaviour. trampling and, finally, plant cooperation (Kelly et al. 2008). Multicellular organisms that lack a nervous system can be Some of these signals, like disease and bacterial coopera- expected to operate on a very different timescale,and higher tion, are relatively well understood; the others are less well plants are no exception. This change of timescale creates characterized. problems for recognition of behaviour. Pfeffer (1906, What makes for much greater complexity is that many p. 2) early on recognized the problem. ‘The fact that in of these signals arrive coincidentally. Decisions among large plants the power of growth and movement are often conflicting signals have to be made and priorities not strikingly evident has caused plants to be popularly determined on phenotypic change. Leyser (2009), in this regarded as still life.Hence,the rapid movements of Mimosa issue, described the role of auxin in leaf and branch ini- pudica were regarded as extraordinary for a plant, and the tiation in which a coherent model is beginning to emerge. same applies to the spontaneous movements performed by The abiotic signals of light, gravity, mechanical signals, soil Hedysarum gyrans (telegraph plant).If mankind from youth structure and composition, minerals and water availability upwards were accustomed to view nature under a magnifi- add to the difficulties for the growing plant because each, cation of 100 to 1000 times (seeing streaming or lower plant like the biotic signals, varies in direction, length of signal- sperm swimming) or to perceive the activities of weeks or ling and intensity. This enormous complexity of signalling months in a minute as is possible by the aid of a kinemato- ensures that no plant behavioural response is autonomic, a graph, this erroneous idea would be entirely dispelled’. kind of behaviour that requires complete replication Pfeffer (1906) thus predicted time-lapse facilities that brings under all environmental circumstances. Selection will plant behaviour, in some sense, to a more familiar human favour individuals that can best assess the probabilities of timescale. The web site (http://plantsinmotion.bio.indiana. particular kinds of behavioural action and optimize their edu/plantmotion/starthere.html) constructed by Roger fitness. Hangartner contains many excellent time-lapse examples This enormous signalling/environmental complexity is that show behaviour that complies with the aforementioned best conceived by the reader as a complex but changing McDougall (1924) definition. One fundamental difference topological surface composed of hills and valleys, and the between plant and animal behaviours is therefore in their successful plant (from seed to flower) must navigate its respective time frames. way through this topological and hazardous environmental The real value of time-lapse records is to uncover behav- terrain, which keeps changing in structure, with minimal iour either difficult to record or missed by previous record- expenditure of energy. Bazzaz (2000, pp. 91, 168) illustrated ing procedures. For example, the Attenborough (1995) striking, complex topological surfaces involving the influ- time-lapse films record a kind of rapid vertical/horizontal ences of only two environmental parameters. How much shaking behaviour by a growing bramble stem that so far more complex with 20 or more? has no explanation. Other revealing time-lapse movies are © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 Plant behaviour 609 to be found in Massa & Gilroy (2003) on root behaviour goal-directed behaviour is clearly dependent on growth encountering soil obstructions and Runyon et al. (2006) on substance involvement (auxin, ethylene, etc.) that is only Dodder locating its prey by detecting host volatiles. Time- partly understood. lapse recording needs to be focused on the behaviour of Certain forms of purposeful behaviour seem overwhelm- wild plants as well, because the timescale difference with ingly controlled by one signal; the extreme sensitivity of human observers implies that much novel behaviour may etiolated seedlings to unidirectional blue light that can simply have never been seen. override opposing gravity signals is an obvious example. The most obvious purposeful behaviour, however, arises Purposeful behaviour from an integration of different signals. Charles Darwin (1880) showed experimentally how seedling roots sensed In a seminal paper, Aphalo & Ballare (1995) indicated how the signals of touch, light, moisture and gravity simulta- plants were commonly perceived as ‘passive organisms’ neously resulting in sensory integration (Trewavas 2007c). undergoing a predetermined programme whose culmina- Furthermore, he showed that growing roots could distin- tion was occasionally slowed by poor environments. They guish between these signals and decide which was the most argued instead that plant behaviour is both active and pre- crucial to respond to. Both touch and humidity can override dictive. The ‘passive plant’ attitude almost certainly results the gravitational signal if applied in a different direction from experimental experience of plants in which signals are (Eapen et al. 2003; Massa & Gilroy 2003), in a recent excel- imposed by the investigator to make plants perform in con- lent expansion of Darwin’s observations on soil obstruc- trolled conditions, perhaps, similar to the way circus animals tions, indicating how the root response is integrated are made to perform. But in the wild, it is plants that must between touch and gravity. Natural soil is very heterog- compile environmental information and make active deci- enous both in texture and in the distribution of resources sions to change development, in order to optimize life cycle (Bell & Lechowicz 1994). Signal integration is therefore behaviour and eventual fitness. necessary. The successful plant must more correctly assess Active behaviour may be more simply defined as a the probabilities of appropriate action in constructing the dependence on metabolic energy (Rosenblueth, Weiner & root phenotype. Bigelow 1943). True passive behaviour is then simply limited to processes, like the explosive distribution of seeds, Intentional behaviour that depend only on unequal drying of dead tissue or the floating of seeds in the wind. Piaget (1979,p.1) described behaviour as follows:‘By behav- Active behaviour is most easily defined as purposeful iour, I refer to all the actions directed toward the outside when it is goal oriented (Rosenblueth et al. 1943; Russell world in order to change conditions therein or to change 1946). The goal is often achieved by some complex form of their own situation in relation to these surroundings’. This negative feedback, and obvious examples (out of many) are definition is equally applicable to plant behaviour but the adaptive responses of tropic bending to gravity or light. implies intention, usually defined as goal-directed behav- In negative feedback, an information loop is constructed iour. Do plants intend to resist herbivores; do they intend to from the signal to the responding cells to indicate the respond to gravity; do they intend to resist the common margin of error from the goal and adjust behaviour accord- stresses they experience? The description of the behaviour ingly (Trewavas 2007a).The clearest indications of a kind of of individual root systems as growing to actively deny negative feedback control are the damped oscillations resources to competitors certainly implies intention (Maina, around the goal that can sometimes be observed in tropic Brown & Gersani 2002; Gruntmann & Novoplansky 2004). bending (Trewavas 2003). The issue of intentional behaviour was raised and dis- Other examples of more complex and less understood, cussed at length by Scott-Turner (2007) in the context of purposeful (goal-directed) behaviour are (1) the stem thick- social insect colony behaviour. Relatively simple interac- ening that accompanies wind sway; (2) leaf abscission that tions between the individual insect organisms construct a rebalances the water relations of a whole plant when water communication network with complex and some, recogniz- supplies are diminished; (3) the (indeterminate?) elonga- ably, intentional properties. In analogous fashion, the com- tion of the leaf petiole in water plants like Nymphaea, munication network of cells and tissues that construct the which only stops when the leaf breaks surface; and (4) individual plant may be the mechanistic basis of intention in the seasonal, average tree-leaf temperature that remains plant behaviour. remarkably uniform at about 21 °C from trees ranging Does intention imply cognitive involvement? Both Mat- from the subtropical to the arboreal (Helliker & Richter urana and Varela (1980) and Bateson (1985) indicated that 2008). This unusual form of long-term homeostasis, which cognition, defined as the act of knowing, is implicit in all life, undoubtedly benefits photosynthetic processes, is suggested constructed as it is from complex hierarchical network to result from an interaction among internal leaf cooling, structures (Trewavas 2007a).These authors stated that even leaf structure, branch structure and leaf distribution among organisms such as plants without nervous systems perceive, others, all important behavioural traits that have clearly respond and thus know about their environment; they are been optimized. Russell (1946) included several other good therefore capable of cognition. ‘It is not too much to say plant examples. The molecular mechanism underpinning that a plant is capable of cognition in much the same way © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 610 A. Trewavas that a human being is. The plant gathers information about no information. GTP-binding proteins are commonly used its surroundings, combines this with internal information by cells to ‘time’ the lengths of protein–protein interactions. about its internal state and makes decisions that reconcile Only if the protein–protein interaction lasts longer than the its well-being with its environment’ [Trewavas 2005a; modi- hydrolysis rate of GTP, do cells regard the interaction as fied from an original social insect quote by Seeley & Levien providing a high quality of information. It is in part for these (1987)]. reasons that Nurse (2008) called for much greater research The notion of intentional behaviour might also conflict emphasis on how information is gathered, processed, stored with the Neo-Darwinist view of natural selection that sug- and used, and how this generates higher-level phenomena. gests organisms as passive in the face of random selection. The alternative to simple selection from a systems frame- Information terms for learning, memory and work and permitting intention is powerfully argued by intelligent behaviour Gould (2002, p. 614 onwards). In informational language, memory is simply information stored for later use, learning is simply acquisition of infor- MEMORY, LEARNING AND mation and intelligent behaviour is the assessment of infor- INTELLIGENT BEHAVIOUR mation that leads to adaptive, problem-solving responses. The quality of biological information is Figure 1 indicates the various kinds of information catego- determined by constraint ries that underpin plant behaviour with their different but equivalent terminologies. The value of using information Information theory was first posed by Shannon & Weaver terminology is that there is no implication concerning the (1949). However, their concept of information based on mechanisms involved in transmitting information (Box 1). entropy has been difficult to apply to biology (Trewavas Nervous systems process information by mainly different 2007a). Biological information can be equated to meaning- mechanisms to those used by cells of all kinds, but the ful communication. This definition of information implies analogous learning, memory and intelligence behaviours that the quality of information gained is proportional to the can be recognized in cells, tissues, whole plants and other constraint with which it is sensed and transduced. organisms. Meaningful plant signals (properly called semeotics) are first distinguished by specific receptors; the greater the Memory selectivity exerted by the receptor, the higher the quality of information conveyed to the cell. However, single receptors Memory has been described by authors as contributing to a can do little more than provide an all-or-nothing signal to variety of plant behavioural situations. Memory is probably the cell. To provide further essential information on the time length of the signal and its direction for example, other Box 1. Common misconceptions of the use of related receptors are needed.Thus, families of receptors are words involved in information processing common, for example, the phytochromes, cryptochromes, nitrate reductases, auxin receptors, calmodulins (calcium Bruce et al. (2007) suggested that the use of the term receptors) and so on. Holistic integration of the information ‘memory’ in plants implies a cognitive function. provided by the receptor families and integrated with other However, neither learning, memory nor indeed intelli- families helps provide a kind of ‘three-dimensional’ signal gence are words limited to biological, let alone, cognitive perception in both space and time. processes. For example, computers possess memory, and Constraint is equally important during signal transduc- the more advanced ones can learn. Some molecules tion chains that depend on protein–protein interactions. and steels are described as possessing a shape memory Cell cytoplasms contain anywhere from 20 to 40% protein, induced by a particular annealing regime (e.g. Sehitoglu and some membranes, such as the mitochondrial mem- et al. 2001). Intelligence has been used to refer to many brane, are 80% protein. Protein–protein interactions of all biological processes and organisms (Trewavas 2005b) kinds will therefore be common and without some discrimi- and machines. Plant biology has borrowed many words nation, cellular responses will simply be destroyed by infor- that were originally designed to describe purely human mational noise. Transduction sequences are constructed characteristics because the botanical process examined from proteins whose adjacent members exhibit comple- was analogous. The plant ‘vascular system’ containing mentary surface topologies often induced by a prior signal. ‘veins’ and ‘vessels’ is analogous in function to the For example, signal-induced changes in the surface topol- human vascular system, but the mechanisms whereby ogy of protein kinases may now enable specific interaction each works are entirely different. Hairs, stress, arms race, with a protein substrate. Specific surface interactions battles, pathways, cross talk and foraging are a few other between these proteins, when they occur, will exhibit rela- borrowed words, and there are many more. However, tively strong binding and will last a relatively long period, when defined in information terms, memory, learning and information exchange will be high, as a result of con- and intelligence are suitable terms for any organism straint. In contrast, noisy interactions although frequent, regardless of the precise mechanisms involved. will be only weakly binding, short-lived and convey little or © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 Plant behaviour 611

Network Molecules, cells, tissue, whole plant Orchestration of information flow [downward causation]

Information storage [memory] Meaningful Information Information information out [signal (meaningful acquisition [adaptive behaviour, information), cue] [learning] response, problem solving] Information assessment [intelligence]

Loop

Figure 1. Information flow through biological networks that initiates eventual behavioural changes. Biological networks are hierarchical; they are constructed starting with cellular molecules, cells, tissues, individual plant (genet), population, niche or community. Each of these levels in the hierarchy forms a network in its right. However, these networks differ markedly in the strength of connections that hold them together, reflecting probably the fidelity with which information is perceived and interpreted between the constituents of the network and the increasing noisiness of the information communication channels. The connections are strongest inside plant cells and then weaken progressively: molecules > cells > tissues > plant > population > niche > communities. As the connection strengths weaken, greater plasticity is experienced, but even in communities, there is some fidelity in communicated information. The psychologist Schull (1990) argued strongly for a species population to express intelligent behaviour. The figure is presented in informational terms, and alternative commoner words that describe analogous processes are indicated in brackets. However, one less than usual feature in individual plants is the loop (earlier indicated as niche construction) that connects the adaptive response back to subsequent signalling. As plants grow, they continually modify their own environment and the characteristics of future perceived signals. essential in all plant behaviours. Only a few examples are Park 2003) but memory of some can also be passed to indicated here. subsequent generations (Durrant 1962; Molinier et al. Several weeks of cold temperature can create a mitoti- 2006). The effect of previous plant neighbours on pheno- cally stable memory (vernalization) that can last for 300 d. typic development can be remembered for up to a year Chromatin remodelling may be the molecular underpin of after transplantation elsewhere (Turkington, Hamilton & memory here (Goodrich & Tweedie 2002; Amasino 2004; Gliddon 1991). In contrast, hypo-osmotic shock memory Sung & Amasino 2004), and phosphorylation pathways in can last about 20 min (Takahashi et al. 1997). Finally, the animals lead to chromatin remodelling (Stipanovich et al. Venus flytrap requires stimulation of two hairs to effect 2008). Herbivory establishes a long-term memory of previ- closure; these have to be stimulated within 40 s of each ous attacks that primes defence mechanisms, increasing other (Shepherd 2005). One stimulation of a single hair is resistance against further attacks (Karban and Niiho 1995; thus remembered for 40 s. Baldwin & Schmelz 1996; Ruuhola et al. 2007; Karban No wild plant could survive without some memory of its 2008). Priming can last for years. Targeted illumination current perceived signals or without a cumulative memory generates a spatial memory of phototropic signals lasting that collates its past information experience and integrates several hours that can override a shorter-term gravitropic it with present conditions so that the probabilities of poten- memory interpolated before or after illumination (Nick, tial futures could be assessed. The mentioned examples Sailer & Schafer 1990). The memory of mechanical stimu- indicate memory lasting from seconds to minutes, to hours, lation and mineral imbalance can last for many days after to days, years or even longer. These surely reflect, in part the signal has ceased (Desbiez et al. 1984;Verdus,Thellier & and rather crudely, the various known stages of many signal Ripoli 1997). Tendril coiling requires both coincident blue transduction pathways. Generally, the earliest intracellular light and mechanical signals, but either signal, given sepa- events are ion flux changes and protein phosphorylation rately, can be remembered for several hours (Trewavas modification (seconds, minutes, hours); slower events are 2005b). Stress effects from numerous treatments [cold, heat, modification of gene expression and transacting factors salinity, drought, ultraviolet (UV) light, mineral imbalance, (hours, days). Even longer-term events are intercellular sig- disease, etc., including, surprisingly, ABA] can be remem- nalling modifications (hours, days or even months and bered and influence not only a later response (Goh, Nam & years) and, finally, chromatin remodelling (days to years). © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 612 A. Trewavas

Each signal leaves an imprint specific both to the charac- regulatory, molecular-design circuits can produce graded teristics of the signal and the current state of the intracel- responses as well as complete conversion (Becskei, lular molecular network, thus modifying the topology of the Seraphin & Serreano 2001). network. Additional signals within the appropriate time An alternative mechanism is the possibility that the pro- frame are thus interpreted differently as information flows gressive nature of the response may simply reflect the through the modified structure. numbers of cells that have passed a threshold in an all- or-nothing response to the stress. On this basis, as the stimulus is increased, more cells would undergo this all- Learning or-nothing change. This mechanism implies a substantial variation in sensitivity of individual cells to the mentioned Information storage, (memory) cannot be constructed stress signals. A possible indicant of such cell sensitivity without information acquisition first (learning). Learning variation is to be found in guard cell closure. Whereas can be simple; for example, heliotropic plants learn the some guard cells close with very low concentrations of optimal direction of the sun and maintain that position of ABA, a closure of over 90% required four to five orders leaf orientation. More complex learning involves reinforce- of magnitude increase in ABA concentration (Trewavas ment, and good examples are the plant responses to what 2003). Variation to the mentioned stress signals between are commonly called the stress conditions of cold, drought, individual plants might also generate the progressive heat, heavy metals, soil minerals, salinity, wind sway, flood- nature when results are expressed as averages if again ing, excess/UV light, oxidative stress, herbicides, herbivory, there is a plant all-or-nothing response. disease and even ABA (McKersie & Leshem 1994; Knight, Brandt & Knight 1998; Goh et al. 2003; Trewavas 2005b; Bohnert 2007; Dinenny et al. 2008; Frost et al. 2008;Voesink COST–BENEFIT ASSESSMENT, DECISION & Pierik 2008). In all these cases, eventual resistance to a MAKING AND INTELLIGENCE severely damaging stress can be gained by a progressive Intelligence is the capacity for problem solving application of a milder but increasing strength of stress.This learning response enables a quicker, more aggressive, adap- What is meant by intelligence? For historical reasons only, tive resistance to subsequent stress episodes. This is clearly some mistakenly identify intelligent behaviour as being a a kind of trial-and-error learning (often called Thorndikean uniquely human characteristic. This perception has arisen learning) and has been called priming in the case of her- because of the importance of intelligence in education and bivory and disease. Priming is, however, straightforward the dominance of educational psychologists in discussion of learning leading to a long-term memory that can last for intelligent behaviour from 1900 onwards. Psychology is, by months (Frost et al. 2008).Another term applied only to the its nature, concerned predominantly with human behav- abiotic stress stimuli is acclimation, a term that reflects the iour, but it is quite clear that many,if not most psychologists, passive (laboratory) control of plant behaviour and ignores do not think that intelligence is something limited to human the clearly active role played by the wild plant in assessment beings or indeed organisms with brains. Fitness and natural and response. selection are the arbiters of all kinds of organism behaviour The behavioural responses to an increasing imposition of with the sole exception possibly of recent mankind. It is stress, indicate that in the wild, this is really predictive the failure to recognize this crucial point that leads to all behaviour – a preparation for likely, more severe episodes kinds of controversies as to the nature of human intelli- in the future. The progressive nature of the learning indi- gent behaviour among psychologists. Intelligent behaviour cates that there is a trade-off between a commitment to a evolved to increase fitness. full-blown resistance mechanism, which can be costly, bal- Sternberg, a psychologist who has written more exten- anced against an assessed probability that further episodes sively than others on intelligence (e.g. Sternberg 2006, Cian- might recur in the near future and ensuring a quicker colo & Sternberg 2004 and references in these), solicited the response if it does. The emphasis here is on probability; opinions of some 20 psychologists as to the meaning of certainty only occurs in the laboratory.The skill with which intelligence (Sternberg & Detterman 1986). This was a these cost–benefit assessments can be made contributes repeat of an investigation first carried out in 1921. In his directly to ultimate fitness and requires an intelligent analysis of these articles, Sternberg (1986) indicated that assessment. Prediction of future loss of photosynthetic light descriptions involving cognition or adaptation were equally leading to shade-avoidance phenotypes is well established acceptable and identified problem solving as the common- (Aphalo & Ballare 1995). est descriptor. The well-known IQ test is simply an adapta- The basis of this kind of learning (priming) in plants is not tion to the presented situation of the test. Warwick (2001), understood, but in molecular terms multiple, interlinked, an Artificial Intelligence expert, generalized intelligent positive feedback loops might offer the least cost of a long- behaviour to be the capacity for problem solving and term memory (Ingolis & Murray 2002; Bisjman & Grois- emphasized that intelligent behaviour in organisms other man 2003; Xiong & Ferrell 2003; Acar, Becskei & Van than humans must be judged in terms of the capabilities of Oudenaarden 2005; Brandman et al. 2005). Learning would the organism in question.To do otherwise is to be subjective involve the construction of these feedback processes. Such and anthropocentric. Sternberg (1986) himself identified © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 Plant behaviour 613 intelligence as existing between species, within species, will almost certainly diminish the capability to respond to within organisms, etc., and therefore broadly present in life another. The multitude of problems requires intelligent, itself. Gardener (1983) and Steinhardt (2001) indicated that adaptive responses. even in humans, intelligence is a whole organism property. Psychologists therefore do not limit intelligent behaviour to humans or other advanced animals or even to cognitive A potential mechanism for plant intelligence; a processes (Stenhouse 1974; Griffin 1976; Sternberg 1986; communication network Schull 1990; Warwick 2001). ‘Plants have evolved an integrated complex of hormonal Intelligent behaviour cannot be divorced from the situa- systems – a coordinated but non-centralized intelligence tion that elicits it. All wild organisms face highly variable system . . . that manages bioenergetic resources’ (La Cerra situations in which they must attempt to optimize their & Bingham 2002, p. 11). An adaptive representational survival and produce the maximal numbers of siblings. network has also been proposed to underpin intelligent The capacity to solve the environmental problems that responses (Trewavas 2005a) and is also suggested for bac- vary enormously and threaten the optimization of fitness terial learning (Tagkopoulos, Liu & Tavazoie 2008). requires intelligent solutions. The key term that underpins Although the interactions among the seven or eight known intelligent behaviour is assessment. Optimal assessment hormones are beginning to be understood, these on their using stored information, interacting with the stage of own may not provide a sufficiently complex network to deal development and current acquired information, leads to with the variety of presented problems experienced by wild problem solving, successful adaptive responses and thus plants. The communication network may be made more increased fitness. Plant intelligence, like plant behaviour complex by including other molecules such as proteins, pep- itself, has suffered from an inability of easy human obser- tides, nucleic acids, small RNA’s oligosaccharides, sugars, vation, leading to a common assumption that both must be minerals, etc., that are known to move between cells (Tre- absent. wavas 2003).As such networks must self-assemble, they will also self-orchestrate, seeking their most stable configura- tion (Trewavas 2007a). Orchestration is commonly called Problem solving and trade-offs downward causation (Trewavas 2007a); an alternative term is circular causality (Scott Kelso 1995). The importance of In the attempts by plants to optimize fitness, numerous downward causation in biological networks is also discussed problems interfere. The individual plant has to accommo- at length by Noble (2006) and Kauffman (2008). date the uneven distribution of light, minerals, soil structure Changes in orchestration will be continuous as the indi- and water, competition, along with variation in rainfall, vidual plant progresses from seed to flower and accommo- wind and damage by disease pests and herbivores. Flowers dates a changing panoply of signals that elicits adaptive need to be positioned where pollination is optimal. The behaviour. Any signal, as information, contributes to its costs and benefits of any behavioural change in growth and own orchestration.Assessment of any signal arises naturally development and the resources to back it up require assess- from the present whole network structure that is itself a ment (Bazzaz 2000; De Jong and Klinkhamer 2005). Deci- compilation of present and past environmental and devel- sions need to be made about how best to redistribute the opmental history. Intelligent behaviour (adaptive problem- limited internal resources among competing tissues to try solving behaviour) is thus a property of the whole plant and and provide ultimate success. As resource limitation not individual tissues. increases, it becomes increasingly crucial to make the right Plants that can place a root or shoot in the best position decisions to increase the probability of success. The mecha- to gain resources, as against indifferent or resource-absent nisms used in decision making and trade-offs are currently places, act intelligently. Those plants that most quickly esti- only weakly understood, and most research still uses well- mate which branches or leaves no longer provide adequate nourished laboratory plants. Selection, however, will not resource-gathering potential and block them from further allow such decisions to be made at random! root resource access, have a higher capacity for problem Trade-offs of resources are known to occur between root solving.Those plants that more accurately predict the future and shoot, between different shoots, roots, branches or resource availability or herbivore damage and decide on leaves, between vegetative and reproductive growth and resource distribution appropriately are smarter than others, between vegetative growth and herbivore/disease resis- and the reward is a likely gain in fitness. tance (Hutchings 1997; Lerdau & Gershenzon 1997; Bazzaz 2000; Weaver & Amasino 2001; De Jong and Klinkhamer 2005; Trewavas 2005a, 2007a; Frost et al. 2008). Natural pes- CONCLUSIONS ticide levels in wild plants occupy 1–5% of their dry weight, sufficient to reduce both growth and seed yield; any Plant behaviour is best described as what a plant does – increased synthesis as a result of attack will diminish growth doing rather than having.The commonest misapprehension further.There will also be trade-offs in resources devoted to about higher plants is that they are simple organisms. The different abiotic stress conditions that will need careful ‘still life’ description indicated by Pfeffer (1906) is undoubt- assessment because an excess resistance response to one edly the major cause of that perception. In complexity of © 2009 The Author Journal compilation © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 606–616 614 A. Trewavas signalling and problem solving within their own environ- De Jong T.J. & Klinkhamer P.G.L. (2005) Evolutionary Ecology of mental context, plants lack nothing compared with animals Plant Reproductive Strategies. Cambridge University Press, in skill and behavioural complexity. There is an undoubted Cambridge, UK. De Kroon H., Visser E.J.W., Huber H. & Hutchings M.J. (2009) A need for plant biologists to investigate the design charac- modular concept of plant foraging behaviour: the interplay teristics of plant cell protein and phosphorylation networks between local responses and systemic control. Plant, Cell & and how these generate purposeful and potentially inten- Environment 32, 704–712. tional goal-directed behaviour. While plant gene identifica- De Moraes C.M., Lewis W.J., Parc P.W., Alborn H.T. & Tumlinson tion has been very successful, systems design is presently J.H. (1998) Herbivore-infested plants selectively attract parasi- under-investigated. Ecologists and molecular biologists are toids. Nature 393, 570–573. needed to construct fruitful interactions centred around Desbiez M.O., Kergosein Y., Champagnant P. & Thellier M. (1984) Memorisation and delayed expression of regulatory message in wild behaviour, trade-off assessments, communication plants. Planta 160, 392–399. networks, assessment and thus intelligence. Dicke M. (2009) Behavioural and community ecology of plants that cry of help. Plant, Cell & Environment 32, 654–665. REFERENCES Dinenny J.R., Long T.A., Wang J.Y., Jung J.W., Mace D., Pointer S., Barron C., Brady S.M., Scheifelbein J. & Benfey P.N. (2008) Cell Acar M., Becskei A. & Van Oudenaarden A. (2005) Enhancement identity mediates the response of Arabidopsis roots to abiotic of cellular memory by reducing stochastic transitions. Nature stress. Science 320, 942–945. 435, 228–232. Donohue K. (2005) Niche construction through phenological plas- Amasino R. (2004) Vernalisation, competence and the epigenic ticity: life history dynamics and ecological consequences. New memory of winter. The Plant Cell 16, 2553–2559. Phytologist 166, 83–92. Aphalo P.J. & Ballare C.L. (1995) On the importance of informa- Durrant A. (1962) The environmental induction of heritable tion acquiring systems in plant–plant interactions. Functional change in Linum. Heredity 17, 27–61. Ecology 9, 5–14. Eapen D., Barroso M.L., Campos M.E., Ponce G., Corkidi G., Arber A. (1950) The Natural Philosophy of Plant Form. Cambridge Dubrovsky J.G. & Casab G.I. (2003) A no hydrotropic response University Press, Cambridge, UK. root mutant that responds positively to gravitropism in Arabi- Attenborough D. (1995) The private life of plants. BBC Natural dopsis. Plant Physiology 131, 536–546. History Unit. A BBC TV Production in association with Turner Erb M., Ton J., Degenhardt J. & Turlings T.C.J. (2008) Interactions Broadcasting Systems, Inc. between arthropod-induced aboveground and belowground Badri D.V. & Vivanco J.M. (2009) Regulation and function of root defenses in plants. Plant Physiology 146, 867–874. exudates. Plant, Cell & Environment 32, 666–681. Forde B.G. & Walch-Liu P. (2009) Nitrate and glutamate cues for Baldwin I.T. & Schmelz E.A. (1996) Immunological memory in the behavioural responses in plant roots. Plant, Cell & Environment induced accumulation of nicotine in wild tobacco. Ecology 77, 32, 682–693. 236–246. Frost C.J., Appel H.A., Carlson J.E., De Moraes C.M., Mescher Ballaré C.L. (2009) Illuminated behaviour. Phytochrome as a key M.C. & Schultz J.C. (2007) Within plant signalling via volatiles regulator of light foraging and plant herbivore defense. Plant, overcomes vascular constraints on systemic signalling and Cell & Environment 32, 713–725. primes responses against herbivores. Ecology Letters 10, 490– Bateson G. (1985) Mind and Nature. A Necessary Unity. Fontana, 498. London, UK. Frost C.J., Mescher M.C., Carlson J.E. & De Moraes C.M. (2008) Bazzaz F.A. (2000) Plants in a Changing Environment. Cambridge Plant defence priming against herbivores: getting ready for a University Press, Cambridge, UK. different battle. Plant Physiology 146, 818–824. Becskei A., Seraphin B. & Serreano L. (2001) Positive feedback in Galis I., Gaquerel E., Pandey S.P. & Baldwin I. (2009) Molecular eukaryotic gene networks; cell differentiation by graded to mechanisms underlying plant memory in JA-mediated defense binary response conversion. EMBO Journal 20, 2528–2535. responses. Plant, Cell & Environment 32, 617–627. Bell G. & Lechowicz M.J. (1994) Spatial heterogeneity at small Gardener H. (1983) Frames of Mind. The Theory of Multiple Intel- scales and how plants respond to it. In Exploitation of Environ- ligences. Basic Books Publishers, New York, NY, USA. mental Heterogeneity by Plants (eds M.M. Caldwell & R.W. Gibbs K.A., Urbanowski M.L. & Greenberg E.P. (2008) Genetic Pearcy) pp. 391–411. Academic Press, New York, NY, USA. determinants of self-identity and social recognition in bacteria. Bisjman J.J.E. & Groisman E.A. (2003) Making informed deci- Science 321, 256–259. sions: regulatory interactions between two component systems. Goh C.H., Nam H.G. & Park Y.S. (2003) Stress memory in plants: Trends in Microbiology 11, 359–366. a negative regulation of stomatal response and transient induc- Bohnert H.J. (2007) Abiotic stress. In Encyclopedia of Life Sci- tion of rd22 gene to light in abscisic acid-entrained Arabidopsis ences, pp. 1–9. John Wiley and Sons Ltd, London, UK. plants. The Plant Journal 36, 240–255. Bradshaw A.D. (1965) Evolutionary significance of phenotypic Goodrich J. & Tweedie S. (2002) Remembrance of things past; plasticity in plants. Advances in Genetics 13, 115–155. chromatin remodelling in plant development. Annual Review of Brandman O., Ferrell J.E., Li R. & Meyer T. (2005) Interlinked fast Cell Developmental Biology 18, 707–746. and slow feedback loops drive reliable cell decisions. Science 310, Gould S.J. (2002) The Structure of Evolutionary Theory. Harvard 496–498. University Press, Cambridge, MA, USA. Bruce T.J.A., Matthes M.C., Napier J. & Pickett J.A. (2007) Stress- Griffin D.R. (1976) The Question of Animal Awareness. Evolution- ful memories of plants: evidence and possible mechanisms. Plant ary Continuity of Mental Experience. The Rockefeller University Science 173, 603–608. Press, New York, NY, USA. Ciancolo A.T. & Sternberg R.J. (2004) Intelligence; a Brief History. Gruntmann M. & Novoplansky A. (2004) Physiologically mediated Blackwell Publishing, Oxford, UK. self/non-self discrimination mechanism. Proceedings of the Darwin C. (1880) The Power of Movement in Plants. John Murray, National Academy of Sciences of the United States of America London, UK. 101, 3863–3867.

Helliker B.R. & Richter S.L. (2008) Subtropical to boreal conver- Novoplansky A. (2009) Picking battles wisely: plant behaviour gence of tree-leaf temperatures. Nature 454, 511–514. under competition. Plant, cell & Environment 32, 726–741. Hodge A. (2009) Root decisions. Plant, Cell & Environment 32, Nurse P. (2008) Life, logic and information. Nature 454, 424–426. 628–640. Palladin P.I. (1918) Plant Physiology. Blakiston Son and Co., Hutchings M.J. (1997) Resource allocation patterns in clonal herbs Philadelphia, PA, USA. and their consequences for growth. In Plant Resource Allocation Pfeffer W. (1906) The Physiology of Plants, Vol. 3 (translated by (eds F.A. Bazzaz & J. Grace) pp. 161–190. Academic Press, A.J. Ewart). Clarendon Press, Oxford, UK. London, UK. Piaget J. (1979) Behaviour and Evolution. Routledge and Kegan Ingolis N.T. & Murray A.W. (2002) History matters. Science 297, Paul, London, UK. 948–949. Rosenblueth A., Weiner N. & Bigelow J. (1943) Behaviour, purpose Karban R. (2008) Plant behaviour and communication. Ecology and teleology. Philosophy of Science 10, 18–24. Letters 11, 1–13. Runyon J.B., Mescher M.C. & De Moraes C.M. (2006) Volatile Karban R. & Niiho C. (1995) Induced resistance and susceptibility chemical cues guide host location and host selection by parasitic to herbivory. Plant memory and altered development. Ecology plants. Science 313, 1964–1967. 76, 1220–1225. Russell E.S. (1946) The Directiveness of Organic Activities. Cam- Kauffman S.A. (2008) Reinventing the Sacred. Basic Books, New bridge University Press, Cambridge, UK. York, NY, USA. Ruuhola T., Salminen J.P., Haviola S., Yang S. & Rantala M.J. Kelly C.L. (1992) Resource choice in Cuscuta europea. Proceedings (2007) Immunological memory of mountain birches: effects of of the National Academy of Sciences of the United States of phenolics on performance of the autumnal moth depend on America 89, 12194–12197. herbivory history of trees. Journal of Chemical Ecology 33, 1160– Kelly C.L., Bowler M.G., Pybus O. & Harvey P.H. (2008) Phylog- 1176. eny, niches and relative abundance in natural communities. Schenk H.J., Callaway R.M. & Mahall B.E. (1999) Spatial root Ecology 89, 962–970. segregation: are plants territorial? Advances in Ecological Knight H., Brandt S. & Knight M.R. (1998) A history of stress Research 28, 145–180. alters drought calcium signalling pathways in Arabidopsis. The Schlichting C.D. & Pigliucci M. (1998) Phenotypic Evolution: A Plant Journal 16, 681–687. Reaction Norm Perspective. Sinauer Associates Inc., Sunderland, La Cerra P. & Bingham R. (2002) The Origin of Minds. Harmony MA, USA. Press, New York, NY, USA. Schull J. (1990) Are species intelligent? Behavior and Brain Science Lerdau M. & Gershenzon J. (1997) Allocation theory and chemical 13, 63–108. defence. In Plant Resource Allocation (eds F.A. Bazzaz & J. Scott Kelso J.A. (1995) Dynamic Patterns; the Self-organisation of Grace) pp. 265–278. Academic Press, London, UK. Brain and Behavior. MIT Press, Cambridge, MA, USA. Lewontin R.C. (2001) Gene, organism and environment: a new Scott-Turner J. (2007) The Tinkerer’s Accomplice. Harvard Univer- introduction. In Cycles of Contingency (eds S. Oyama, P.E. sity Press, Cambridge, MA, USA. Griffiths & R.D. Gray) pp. 55–67. MIT Press, Cambridge, MA, Seeley T.D. & Levien R.A. (1987) A colony of mind.The beehive as USA. thinking machine. Sciences 27, 38–43. Leyser O. (2009) The control of shoot branching: an example of Sehitoglu H., Karaman I., Zhang X., Kim H., Chumlyakov Y., plant information processing. Plant, Cell & Environment 32, 694– Maier H.J. & Kireeva I. (2001) Deformation of NiTiCu shape 703. memory single crystals in compression. Metallurgical and Mate- Liebold M.A. (2008) Return of the niche. Nature 454, 39–41. rials Transactions A 32, 477–489. McDougall W. (1924) An Outline of Psychology. Methuen, Shannon C.E. & Weaver W. (1949) The Mathematical Theory London, UK. of Communication. University of Illinois Press, Urban, McKersie B.D. & Leshem Y.Y. (1994) Stress and Stress Coping IL, USA. in Cultivated Plants. Kluwer Academic Publishing, Dordrecht, Shepherd V.A. (2005) From semi-conductors to the rhythms of the Netherlands. sensitive plants: the research of J.C. Bose. Cellular and Molecular Maina G.G., Brown J.S. & Gersani M. (2002) Intra-plant Biology 51, 607–619. versus inter-plant competition in beans: avoidance resource Silvertown J. (1998) Plant phenotypic plasticity and non-cognitive matching or tragedy of the commons? Plant Ecology 160, 235– behaviour. Trends in Ecology and Evolution 13, 255–256. 247. Silvertown J. (2004) Plant coexistence and the niche. Trends in Massa G.D. & Gilroy S. (2003) Touch modulates gravity sensing to Ecology and Evolution 19, 605–611. regulate the growth of primary roots of Arabidopsis thaliana. Silvertown J. & Gordon G.M. (1989) A framework for plant behav- The Plant Journal 33, 435–445. ior. Annual Review of Ecology and Systematics 20, 349–366. Maturana H.R. & Varela F.J. (1980) Autopoiesis and Cognition.D. Steinhardt E. (2001) Person versus brains; biological intelligence in Reidel Publishing Company, Dordrecht, the Netherlands. human organisms. Biology and Philosophy 16, 3–27. Metlen K.L., Aschehoug E.T. & Callaway R.M. (2009) Plant Stenhouse D. (1974) The Evolution of Intelligence – A General behavioural ecology: dynamic plasticity in secondary metabo- Theory and Some of Its Implications. George Allen and Unwin, lites. Plant, Cell & Environment 32, 641–653. London, UK. Molinier J., Ries G., Zipfel C. & Hohn B. (2006) Transgeneration Sternberg R.C. (2006) Cognitive Psychology, 4th edn. Thomson memory of stress in plants. Nature 442, 1046–1049. Wadsworth, Belmont, CA, USA. Muller-Landau H.C. (2003) Seeds of understanding of plant diver- Sternberg R.J. (1986) A framework for understanding conceptions sity. Proceedings of the National Academy of Sciences of the of intelligence. In What Is Intelligence? Contemporary View- United States of America 100, 1469–1471. points on Its Nature and Definition (eds R.J. Sternberg & D.K. Nick P., Sailer K. & Schafer E. (1990) On the relation between Detterman) pp. 5–19. Ablex Publishing Corporation, Norwood, photo- and gravitropically induced spatial memory in maize NJ, USA. coleoptiles. Planta 181, 385–392. Sternberg R.J. & Detterman D.K. (1986) What Is Intelligence? Noble D. (2006) The Music of Life. Biology beyond the Genome. Contemporary Viewpoints on Its Nature and Definition. Ablex Oxford University Press, Oxford, UK. Publishing Corporation, Norwood, NJ, USA.

Stipanovich A., Valjient E., Matamales M., et al. (2008) A phos- Trewavas A.J. (2007c) Response to Alpi et al: plant neurobiology – phatase cascade by which rewarding stimuli control nucleosomal all metaphors have value. Trends in Plant Science 12, 231–233. response. Nature 453, 879–884. Turkington R., Hamilton R.S. & Gliddon C. (1991) Within- Sultan S. (2000) Phenotypic plasticity for plant development. population variation in localised and integrated responses of Trends in Plant Science 5, 537–542. Trifolium repens to biotically patchy environments. Oecologia Sultan S. (2005) An emerging focus on plant ecological develop- 86, 183–192. ment. New Phytologist 166, 1–5. Uriarte M. & Reeve H.K. (2003) Matchmaking and species mar- Sung S. & Amasino R.M. (2004) Molecular genetic study of the riage: a game theory model of community assembly. Proceedings memory of winter. Journal of Experimental Botany 57, 3369– of the National Academy of Sciences of the United States of 3377. America 100, 1787–1792. Tagkopoulos I., Liu Y.-C. & Tavazoie S. (2008) Predictive behav- Verdus M.C., Thellier M. & Ripoli C. (1997) Storage of environ- iour within microbial genetic networks. Science 320, 1313–1317. mental signals in ﬂax: their morphogenetic effects as enabled by Takahashi K., Isobe M., Knight M.R., Trewavas A.J. & Muto S. a transient depletion of calcium. The Plant Journal 12, 1399– (1997) Hypo-osmotic shock induces increases in cytosolic free 1410. calcium in tobacco suspension culture cells. Plant Physiology Voesink L.A.C.J. & Pierik R. (2008) Plant stress proﬁles. Science 113, 587–594. 320, 880–881. Trewavas A. (2003) Aspects of plant intelligence. Annals of Botany Warwick K. (2001) The Quest for Intelligence. Judy Piatkus, 92, 1–20. London, UK. Trewavas A. (2005a) Green plants as intelligent organisms. Trends Weaver L.M. & Amasino R.M. (2001) Senescence is induced in in Plant Science 10, 414–419. individually darkened Arabidopsis leaves but inhibited in whole Trewavas A. (2005b) Plant intelligence. Naturwissenschaften 92, darkened plants. Plant Physiology 127, 876–886. 401–413. Xiong W. & Ferrell J.E. (2003) A positive feedback-based bistable Trewavas A. (2007a) A brief history of systems biology. The Plant memory module that governs a cell fate decision. Nature 426, Cell 18, 2420–2430. 460–465. Trewavas A.J. (2007b) Plant behavioural ecology. In Encyclopedia of Life Sciences, pp. 1–8. John Wiley and Sons Ltd, London, Received 7 August 2008; received in revised form 9 December 2008; UK. accepted for publication 11 December 2008