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Plant, Cell and Environment (2009) 32, 726–741 doi: 10.1111/j.1365-3040.2009.01979.x Picking battles wisely: plant behaviour under competition ARIEL NOVOPLANSKY* Mitrani Department of Desert Ecology, Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus 84990, Israel ABSTRACT Plants are limited in their ability to choose their neighbours, but they are able to orchestrate a wide spectrum of rational competitive behaviours that increase their prospects to prevail under various ecological settings. Through the perception of neighbours, plants are able to anticipate probable competitive interactions and modify their competitive behaviours to maximize their long-term gains. Specifically, plants can minimize competitive encounters by avoiding their neighbours; maximize their competitive effects by aggressively confronting their neighbours; or tolerate the competitive effects of their neighbours. However, the adaptive values of these non-mutually exclusive options are expected to depend strongly on the plants’ evolutionary background and to change dynamically according to their past development, and relative sizes and vigour. Additionally, the magnitude of competitive responsiveness is expected to be positively correlated with the reliability of the environmental information regarding the expected competitive interactions and the expected time left for further plastic modifications. Concurrent competition over external and internal resources and morphogenetic signals may enable some plants to increase their efficiency and external competitive performance by discriminately allocating limited resources to their more promising organs at the expense of failing or less successful organs. Key-words: avoidance; competitive behaviour; confrontation; environmental information; future perception; metaplasticity; phenotypic plasticity; self/non-self; somatic competition; tolerance. INTRODUCTION Starting at the earliest days of scientific thinking, competition has been recognized as one of the most important factors dictating the fate of individuals and the distribution of species. It was Aristotle who described and exemplified competition, territoriality and dominance in animals (Aristotle trans. 1965), and his successor Theophrastus who, Correspondence: A. Novoplansky. Fax: +972 8 6596821; e-mail: [email protected] *Present address: Section of Evolution and Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA. 726 for the first time, studied GxE interactions by transplanting plants to areas out of their natural ranges (Theophrastus 1916). Further attention by the fathers of the science of evolution (Lamarck 1809; Darwin 1859) have resulted in substantial theoretical and experimental efforts to understand the role of competition in shaping populations and communities (Tansley 1917; Clements 1929; Fisher 1930; Gause 1934; Hairston, Smith & Slobodkin 1960; Grime 1979; Tilman 1982, 1988; Connell 1983; Schoener 1983; Keddy 2001) and the evolution of competitive strategies and traits (MacArthur & Wilson 1967; Pianka 1970; Charlesworth 1971; Roughgarden 1971; Grace & Tilman 1990; Aarssen 1992; Stearns 1992; Silvertown, Franco & Harper 1997). However, plant competition has been traditionally studied on different sides of disciplinary gaps (Novoplansky 2002; Callaway, Penning & Richards 2003; Ackerly & Sultan 2006). While ecologists usually focus on population- and community-level implications of species’ differential abilities to prevail under competition for limited resources (Goldberg & Barton 1992; Goldberg 1996; Keddy et al. 2002; Fargione & Tilman 2006), plant physiologists traditionally study various traits that underlay these adaptations (e.g. Rao, Raghavendra & Reddy 2006). But perhaps not surprisingly, it was Charles Darwin himself who, with the help of his son, meticulously studied what we now call behavioural traits in plants (Darwin 1880), many of which are directly related to competition – perhaps the single most important ecological force underlying his epochmaking work (Darwin 1859). Stimulated by earlier work on the evolutionary ecology of phenotypic plasticity and life histories (e.g. Bradshaw 1965; Levins 1968; Schlichting 1986; Sultan 1987), recent work has been focusing on the ability of plants to make adaptive decisions about a myriad of challenges based on cues and signals they perceive from their environment (Silvertown & Gordon 1989; Sultan 2007). Due to their dynamic game-related nature, some of the more intricate and intriguing behaviours are related to biological interactions such as herbivory (e.g. Baldwin et al. 2006) and competition (Smith 1982; Silvertown & Gordon 1989; Aphalo & Ballare 1995; Callaway et al. 2003; Trewavas 2003; Karban 2008), where the adaptive value of any given behaviour inherently depends on the behaviours of others (e.g. Matsuda & Abrams 1994; Falster & Westoby 2003). When discussing the analogy between animal and plant behaviour, some prefer to delimit plant behaviour to reversible short-term responses that agree with the common © 2009 Blackwell Publishing Ltd Competitive behaviour in plants 727 definition of acclimation (Karban 2008, but see Silvertown & Gordon 1989; Novoplansky 2002; Sachs 2002). However, the very essence of being a plant means that their short-term responses to environmental changes commonly involve both immediate physiological and slower yet longer-to-last morphological modifications via the addition and abandonment of tissues and organs (Bradshaw 1965; Grime, Crick & Rincon 1986). Not surprisingly, these modifications usually take a longer absolute time when compared to movement of most motile animals. Using the conceptual framework of environmental grain (Levins 1968), the analogy between plants and animals might be better viewed in terms of the relative response time which might be depicted by the relation between the time scales of plant responses and the environmental changes that trigger them. This notion seems especially relevant to reciprocal competitive responses of plants that have comparable developmental response times. In addition, the fact that most plants leave behind a trail of cellulitic and ligneous ‘debris’ should not necessarily be interpreted as a reflection of irreversible development but possibly a manifestation of the low recycling value of these tissues to the plant. The current review, therefore, discusses plant competitive behaviour from a more inclusive point of view, with the hope to trigger discussion rather than a squabble over definitions. The discussion attempts to deal with the evolutionary and ecological rationales, and the mechanistic aspects of some plant behaviours, yet without the intention to comprehensively covering the existing knowledge of the field; this has been done in other excellent reviews (e.g. Silvertown & Gordon 1989; Hutchings & de Kroon 1994; Aphalo & Ballare 1995; Schlichting & Pigliucci 1998; Aphalo, Ballare & Scopel 1999; Schenk, Callaway & Mahall 1999; Callaway et al. 2003; de Kroon, Mommer & Nishiwaki 2003; Trewavas 2003; Sultan & Stearns 2005; Karban 2008). Frustratingly yet excitingly, despite the recent surge of interest, many aspects of this topic are still vague or even totally obscure. Thus, the following discussion unavoidably includes an imbalanced collection of examples and hypothetical notions that will hopefully be further corrected and moulded into a more substantial body of theory and knowledge in the future. Specifically, it discusses the types of information that plants require and acquire to make ‘educated’ competitive decisions, and the categories and hierarchies of their competitive behaviours under various ecological circumstances. INFORMATION Information, or its lack thereof, is key to decision making of any type, and its importance to fitness-determining processes such as survival, resource capturing and interference cannot be underemphasized (e.g. Cohen 1971; Charnov 1976; Smith 1982; Mangel 1990; Sih 1992; Aphalo & Ballare 1995; Maynard-Smith & Harper 1995; Aphalo et al. 1999; Wong & Ackerly 2005). While deterministic growth can be executed with little or no external cues, plastic development is invariably based on environmental information perceived by the responding organisms. The perception of neighbours and competitive behaviour in higher organisms is usually based on sophisticated central nervous systems (CNS) and information processing, yet information-acquisition systems dedicated to the perception of neighbours, resource availabilities and sophisticated communication are ubiquitous even among the oldest and most rudimentary life forms such as fungi (Hogan 2006), bacteria (Fuqua, Winans & Greenberg 1994) and viruses (Weitz et al. 2008). Plants are able to perceive their potential competitors based on minute temporal and spatial differences in electromagnetic radiation at various ranges, and metabolite concentrations and fluxes (Aphalo & Ballare 1995; Aphalo et al. 1999; Karban 2008).While some of the perceived information is directly related to the spatial and temporal distribution of essential resources such as light, water and minerals, the more elaborate and intriguing types of competitive-relevant information are related to the dynamics of resource levels and their proxies, and the specificity of their biotic determinants (Estabrook & Yoder 1998; Aphalo et al. 1999; Callaway 2002; Dudley & File 2007). Among the vectors used by plants to perceive their competitive environment are light fluxes and spectral composition (Smith 2000; Weinig 2002; Wada, Shimazaki & Iino 2005), volatile compounds (Ninkovic 2003; Pierik et al. 2004) and root exudates (e.g. Mahall & Callaway 1991; Schenk et al. 1999; de Kroon et al. 2003). However, any adaptive notion regarding information perception can only be understood in the context of future rather than the immediate environmental conditions. Since plastic responses – especially those related to development of new organs and resource allocation and translocation – require time, useful information must be relevant to the future environment that the responding plant eventually functions in (Ballaré et al. 1987; Novoplansky, Cohen & Sachs 1990a). This principle is ubiquitously important for any decision-making system, yet it is especially crucial in competitive settings where the behaviour of each party is inherently dependent on the responses of its counterparts (Maynard Smith 1982; Maina, Brown & Gersani 2002). Although environmental information is invariably based on past events and conditions, in many cases, it is correlated with and thus indicative of future conditions. Such correlations are ubiquitous in both natural and man-made systems; they are readily utilized in a wide spectrum of control systems where pre-emptive adaptation and action are advantageous (e.g. Blanke, Pourzanjani & Vukic 2000; Mangan, Zaslaver & Alon 2003). Perhaps, the most studied ecologically relevant forecasting system that is based on such feedforward correlations is the red/far-red (R/FR) spectral sensitivity that enables plants to perceive and respond to the presence of potentially competitive neighbours even before actual competition for light develops (Ballaré et al. 1987). The tight asymmetric nature of light competition (e.g. Schwinning & Weiner 1998) often dictates an aggressive arms race whereby plants are more sensitive and responsive to spectral cues that are indicative of future competition than they © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 728 A. Novoplansky are to the prevailing levels of photosynthetic light (Smith 1982; Ballaré et al. 1987; Casal, Sánchez & Deregibus 1987; Ballaré, Scopel & Sánchez 1990; Novoplansky et al. 1990a,b; Novoplansky 1991). Anticipatory competitive responses can also be based on correlations between early subacute and later severe stresses. For example, young seedlings of the small desert plant Scleropogon brevifolius drastically increase their root allocation under subacute competition with seedlings of Sporobolus airoides, a response that primes them to tolerate later competition for water and survive longer periods of severe drought (Novoplansky & Goldberg 2001a). Another relatively neglected yet potentially important source of information regarding anticipated competition is the spatial and temporal gradients of resources. Such gradients often exhibit predictable trajectories that can be informative of future conditions. For example, Calendula arvensis and Phlox glandiflora develop larger and produce more seeds when growing in increasing rooting volumes than in the largest yet constant rooting volume (Nyanumba 2007). Individual organs exhibit similar morphogenetic control: when different roots of the same Pisum sativum plants were grown in variable constant and dynamically changing nutrient levels, plants allocated more resources to the roots that experienced dynamically improving rather than deteriorating nutritional conditions, regardless of the absolute resource levels (Shemesh et al., unpublished data). The importance of anticipatory cues is expected to be positively correlated with the amount and proportion of time left for adaptive responses. Accordingly, young plants, whose life is mostly in the future, are expected to be more responsive to information related to their future competitive environment. The extreme of this notion is exemplified by seeds whose developmental decisions are invariably related to the future. In contrast, older, especially senescing plants, such as annuals at the end of their growth season, are expected to disregard anticipatory cues and be predominantly responsive to prevailing resource availabilities (Novoplansky et al. 1990a; Elazar 2005). Nevertheless, even when early cues and signals are tightly correlated with later competitive conditions, they are merely proxies. Accordingly, it is expected that when given sufficient developmental time and to the extent that early developmental moves do not limit later modifications (Diggle 1994; Novoplansky, Cohen & Sachs 1994; Watson, Geber & Jones 1995; Novoplansky 1996; Bell & Sultan 1999; Weinig & Delph 2001), responsiveness to anticipatory information is expected to be accompanied by continuous ‘verifications’ and corrections based on the prevailing competitive levels and resource availabilities (Novoplansky et al. 1990a; Cohen & Mangel 1999). Information specificity To what extent are cues and signals regarding the prevailing and future competition informative and usable? Overwhelmed by a myriad of internal and external cues, plants cannot and have no adaptive incentive to respond to them all. Although carrying information, some of the cues might be unreliable, contradictory or reflective of transient or inconsequential events. In addition, competitive cues might be generated by other parts of the same individual or neighbours belonging to the same genotype which would render competitive responses ecologically and evolutionary costly and damaging. It is, therefore, suggested that perception systems have been selected to enable plants to differentiate between meaningful and ‘junk’ information and, when possible, help plants to maximize their competitive responsiveness towards worthy targets while avoiding wasteful allocation to competition against self and kin, or wage hopeless battles against overwhelmingly superior competitors. In some cases, plants have demonstrated abilities to discriminate between their neighbours and to develop differentially in accordance with their species identity (Mahall & Callaway 1991; Krannitz & Caldwell 1995; Gersani et al. 2001; Semchenko, John & Hutchings 2007b), ecotypic background (Mahall & Callaway 1992, 1996), physiological integrity (Falik et al. 2003; Holzapfel & Alpert 2003; Gruntman & Novoplansky 2004) and even genetic relatedness (Kelly 1996; Donohue 2003; Dudley & File 2007); yet, the precise mechanisms responsible for the competitive discrimination are still obscure. Recognition and coordination Recent evidence suggests the involvement of specific self/ non-self recognition in competitive interactions between roots. The first report of such discrimination was by Mahall & Callaway (1991) who found that the desert shrub Ambrosia dumosa differentially avoids root elongation in the presence of roots of other Ambrosia individuals. Competitive kin discrimination was also demonstrated in a few studies that compared the performance of plants that grew in sibling- and non-sibling groups: while Triplasis purpurea had a higher fitness in mixed than in homogeneous groups, suggesting the involvement of resource partitioning (Cheplick & Kane 2004), Cakile edentula had a higher fitness (Donohue 2003) and lower root allocation in sibling groups than in non-sibling groups, implying kin selection (Dudley & File 2007). Similarly, in Miscanthus sinensis, root growth was hardly affected by contacts with roots belonging to an alien genotype but was significantly inhibited when contacting roots belonging to the same genotype (de Kroon et al. 2003). Yet, it is still unclear whether these behaviours are based on immune-like allorecognition, similar to selfincompatibility systems that enable plants to avoid inbreeding by self-pollination (Takayama & Isogai 2005). Interestingly, self/non-self discrimination need not necessarily be based on allorecognition. In a growing number of cases, plants have been demonstrated to avoid competition between roots of the same plant (Gersani et al. 2001; Falik et al. 2003; Holzapfel & Alpert 2003; Gruntman & Novoplansky 2004; Falik, de Kroon & Novoplansky 2006). Specifically, plants grow fewer and shorter roots in the vicinity and, in some cases, towards other roots that belong © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 Competitive behaviour in plants 729 to the same intact plant (Falik et al. 2003; Semchenko et al. 2007b), and increase their root allocation in the vicinity of alien plants at the expense of reproduction (Maina et al. 2002; O’Brien, Gersani & Brown 2005). In Buchloe dactyloides, separating cuttings that originate from the same node cause their becoming progressively alienated from each other and eventually relate to each other as genetic aliens (Gruntman & Novoplansky 2004). Although the methods used in some of these studies have been challenged (Schenk 2006; Hess & de Kroon 2007; Semchenko, Hutchings & John 2007a) and debated over (O’Brien & Brown 2008), it is clear that at least in some of the reported cases competitive discrimination between self and non-self neighbours is based on physiological coordination among roots that belong to the same intact plant rather than allogenetic recognition (Falik et al. 2003; Holzapfel & Alpert 2003; Gruntman & Novoplansky 2004). Probabilistic information All plants, especially those belonging to the same species, use the same resources in very similar ways (Goldberg 1990). In the case of light, plants that grow under the same conditions are expected to leave similar shade signatures of lowered photosynthetic light and R/FR ratios. However, some plants have been demonstrated to respond differently to shade of different neighbouring species (Marcuvitz & Turkington 2000; Weinig 2000a; Semchenko & Zobel 2007). Can plants use generic shade signals to differentiate between their competitor’s and their own shade? For light signals to be informative of the identity of the competitor, they must relay on probabilities of being generated by self and non-self neighbours. It is known that the relative position of leaves and branches within the plant’s canopy strongly affects the probability of self-shading (Ackerly & Bazzaz 1995; Valladares & Pearcy 1998). For example, leaves positioned near the stem apex have a significantly lower probability of encountering self-shading compared with lower leaves (Yamada et al. 2000). In Ocimum basilicum, shading of the uppermost part of the seminal shoot which has the lowest probability of being shaded by other parts of the same plant, triggered significant stem elongation, while identical shading of lateral branches, whose probability of being shaded by other branches of the same individual is high, triggered little to no elongation (Raz 2005). Another possible source of information regarding shade identity is the relative direction of shade. The seminal shoots of young Portulaca oleracea plants were subjected to directional vegetative shading immediately after the plants become recumbent. While plants that were shaded from their periphery (greater probability of non-self-encounter) changed their orientation and increased the elongation of their laterals away from the shade, no such responses were observed when the shade was directed from the inner parts of the plant outwards (greater probability of self-shading) (Raz 2005). Another source of such information could be the diurnal timing of shade interception. Shade reaching plants during the earliest and latest periods of the day has a relatively greater probability of being generated by non-self neighbours (Novoplansky et al. 1990a; Novoplansky 1991). In contrast, midday shade has a greater probability of being cast by higher foliage of the same individual or much taller neighbours (Weinig 2000a; see ‘COMPETITIVE BEHAVIOURS’ below). Indeed, end-of-day shade signals are known to have significant effects on plant physiology and morphology (e.g. Tso, Kasperbauer & Sorokin 1970; Kasperbauer 1971; Aphalo, Gibson & Di Benedetto 1991; Peer, Briggs & Langenheim 1999; Marcuvitz & Turkington 2000) and shade avoidance was found to be consistent with stronger effects of end-of-day red/far-red reductions in field set-ups (Kasperbauer 1971). However, more detailed testing of the effects of R/FR signals throughout the photoperiod presented no support for this hypothesis (Casal & Smith 1989; Raz 2005); consistent with the notion that the rapid and often noisy decline in R/FR ratios towards the end of the day would be less reliable compared with the integration of these cues throughout the entire photoperiod (Casal & Smith 1989). How strong are the competitors? Perhaps the most useful information a plant can have regarding its potential competitors is related to the probability of competing with them successfully. Rather than waging war indiscriminately, plants, as any other rational system, are expected to take advantage of such information to pick winnable and avoid hopeless battles (see ‘COMPETITIVE BEHAVIOURS’ for a detailed discussion). More specifically, such information should be related to the relative competitive ability of the responding plant and its neighbours. Besides the inherent information regarding their general capabilities to pre-empt resources and interfere with their neighbours (MacArthur & Wilson 1967; Grime 1979; Morgan & Smith 1979; Stearns 1992; Dudley & Schmitt 1996), plants are expected to be particularly sensitive and responsive to dynamic changes in their own abilities to acquire resources and withstand the competitive effects of their neighbours. A simple candidate mechanism that may enable plants to acquire such information could be based on an embedded positive feedback whereby the plant allocates resources to competitive behaviours only as long as they are sustainably beneficial. For example, plants are expected to allocate resources to stem elongation as long as the resulting photosynthetic returns are positive. Interestingly, such control would also ensure that branches do not overshoot above the height of their neighbours, which would not only fail to confer greater gains (Schmitt, McCormac & Smith 1995; Weinig 2000a), but could also result in significant costs and risks (e.g. Anten et al. 2009). A candidate source of such information is the trajectories of resource gradients discussed earlier. For example, in Hydrocotyle vulgaris and Trifolium repens, plants develop longer petioles when subjected to vertically improving light gradients than when under homogeneous shade (Leeflang, During & Werger 1998; Weijschedé et al. 2006). Interestingly, these results are at odds with the expected inverse © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 730 A. Novoplansky correlation between shoot elongation and light availability, which supports the notion that plants are able to integrate cues over temporal and spatial gradients in ways that may increase their competitive performance (Nyanumba 2007; Shemesh et al., unpublished data). Contingent contexts Although absolutely essential, neighbour perception alone cannot suffice. The execution of adaptive and efficient competitive responses must take into account a myriad of contexts that may dictate very different responses to the same cues under different circumstances. For example, the same shade signals are expected to trigger stronger competitive responses in plants that experience relatively weaker root than light competition (Bloom, Chapin & Mooney 1985), as in the case of later successional stages (Tilman 1988). When young Portulaca seedlings were subjected to various intensities of photosynthetic light and R/FR ratios from opposite directions, they became recumbent preferentially towards the direction of the lower FR light, even when it meant growing towards filters that absorbed 20 times more photosynthetic light. A preference for the direction with higher photosynthetic light over lower FR was also found, but only under more extreme light differences. Such contextdependent responses enable plants to take advantage of local competitive opportunities rather than merely growing where conditions are ‘appropriate’ (Novoplansky, Cohen & Sachs 1989; Novoplansky 1991). In general, acting upon cues of prevailing and especially future competition is expected to depend on numerous additional factors such as overall resource availability (e.g. Weijschedé et al. 2006), germination time, phenological stage (Weinig 2000a), expected time available for the execution of the competitive response (Novoplansky et al. 1994; Weinig 2000b), quantity of stored nutrients and carbohydrates, probability of future damage, various abiotic stresses and catastrophic disturbances (Grime 1979), most of which are yet to be explored (see ‘COMPETITIVE BEHAVIOURS’ below). COMPETITIVE BEHAVIOURS Several questions arise regarding the ability of plants to utilize the above-mentioned environmental information: Can plants pick their competitive battles?; What are the behavioural alternatives that plants can employ when engaged in competition?; To what extent are plants able to make adaptive competitive decisions based on relevant environmental information? The current state of our knowledge does not allow for satisfactory answers to these questions and their daunting complexity might prevent even their adequate presentation in a short overview. In the following section, I briefly present a few aspects of the possible ecological rationale and mechanisms of competitive behaviour in plants. The great costs and hazards of competition imply that, in most cases, plants are expected to simply avoid it. However, more often than not, plants are bound to engage in fierce competitive matches with their neighbours, potentially at great consequential reductions in fitness (e.g. Novoplansky et al. 1990b; O’Brien et al. 2005). Accordingly, plants are expected to possess not only various adaptations that maximize resource capturing, but also perception mechanisms that enable them – when possible and given sufficient reliable information – to decide whether to avoid, confront or tolerate their neighbours. In the following section, I describe a few distinctive, although usually not mutually exclusive, categories of competitive behaviours followed by a short discussion of their possible adaptive implications under various ecological circumstances. Behavioural categories It is suggested that most competitive behaviours belong to one or more of the following functional categories. Competitive avoidance Behaviours that minimize competitive interactions. Excellent examples for avoidance behaviours are provided by plants whose germination is increased under lower probabilities of competition. For example, dispersal and germination of some plants are significantly enhanced by exposure to smoke or high temperatures, typical to natural fires (e.g. Clarke & French 2005) that are tightly correlated with the removal of large competitors. Some studies suggest that sibling competition is avoided by increased maternal-induced dormancy following good years after which competition is expected to be high (Phillipi 1993; Tielbörger & Valleriani 2005). Interestingly, vertical stem elongation, the hallmark of the ‘shade avoidance syndrome’, simultaneously increases competitive responses (avoidance) and effects (see ‘Competitive confrontation’ below). However, shade avoidance need not necessarily be accompanied by confrontational behaviour. For example, Psychotria limonensis plants avoid self-shading by reorienting their leaves in response to R/FR cues (Galvez & Pearcy 2003). Young P. oleracea plants become recumbent and avoid developing branches that face neighbouring plants or sources of high FR (Novoplansky et al. 1990a; Novoplansky 1991). When Pinanga coronata plants grow larger, their leaf blades become longer and narrower, while their petioles increasingly elongate further away from the stem (Kimura & Simbolon 2002). It should be noted, however, avoidance behaviours can only be adaptive as long as resource patches or pulses are not challenged by too many plants (Kalisz et al. 1999; Ronce 2007). Although such conditions may be common in highly disturbed or abiotically stressed environments – where plants often grow in predictably sparse stands (Novoplansky et al. 1990a) – more commonly, plants grow in relatively high densities thus bound to confront their neighbours. Competitive confrontation Behaviours that maximize the negative influences of plants upon the performance of their neighbours, namely © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 Competitive behaviour in plants 731 promote both direct and indirect ‘competitive effects’ (sensu Goldberg 1990). Such behaviours promote resource uptake or allelopathic activity in plants that are subjected to competition or cues of expected competition. Aboveground confrontational competition involves, among other responses, increased shoot allocation and elongation in response to shade, shade signals and volatile cues (see‘INFORMATION’ above).Similarly,belowground confrontation involves increased root allocation in response to competition for water and minerals (e.g. Wilson 1988; Sachs 2005). The potentially high production costs of noxious metabolites and their potential self-retarding effects suggest the possible existence of competitively induced allelopathy. However, although conceivable, direct evidence for its existence is still missing. Support for this possibility comes from evidence for allelopathy that is induced by volatiles such as methyl jasmonate and methyl salicylate which are chiefly known for their inductive effects on plant defences against insect herbivores and microbial pathogens (e.g. Bi et al. 2007). Confrontation behaviours typically characterize dense stands in relatively productive habitats where plants are often engaged in a tight and fierce arms race for the domination of limited resources. However, under such competitive conditions, a large proportion of the plants, and typically also most of the biomass of the few lucky dominant individuals grow under increasing resource limitations (e.g. Weiner et al. 2001). Growing under such chronically poor conditions might trigger subordinate individuals and organs to assume various tolerance behaviours. Competitive tolerance Behaviours that maximize the performance of plants under the worsened conditions caused by their neighbours. Such behaviours are compatible, although do not totally overlap, with the scope of ‘competitive response’ (Goldberg 1990). This category includes behaviours that increase survival and resource acquisition under shade (Henry & Aarssen 1997; Valladares & Niinemets 2008) and neighbour-induced drought (Garaua et al. 2008), nutrient depravation (e.g. Liancourt, Corcket & Michalet 2005) and allelopathic effects (e.g. Friebe, Wieland & Schulz 1996). For example, shade tolerance could involve increases in the efficiencies of sunfleck utilization (Kuppers et al. 1996; Valladares, Allen & Pearcy 1997) and the minimization of respiration costs (Givnish 1988) and CO2 losses (Walters & Reich 1996; Craine & Reich 2005). Similarly, drought tolerance involves morphological (e.g. Bell & Sultan 1999) and physiological (Heschel et al. 2002; Bacon 2004; Golluscio & Oesterheld 2007) modifications that increase water-use efficiency and minimize water loss. Therefore, tolerance behaviours might foster competitive dominance where plastic modifications allow longer survival during periods of or patches of resource deficiency (Grime & Mackey 2002), and more opportunities to take advantage of ephemeral resource pulses or patches (Goldberg & Novoplansky 1997; Novoplansky & Goldberg 2001a,b; Sher, Goldberg & Novoplansky 2004). Organizational hierarchies Regardless of their functional type, probably all plants are able to exhibit foraging behaviours that increase their ability to acquire resources at various spatial and temporal scales, contrasts, magnitudes and predictabilities (Bradshaw 1965; Levins 1968; Drew & Saker 1978; Crick & Grime 1987; Caldwell & Pearcy 1994; Hutchings & de Kroon 1994; Alpert & Stuefer 1997; Sachs & Novoplansky 1997; Herben et al. 2003; Mágori et al. 2003; Hodge 2004; Hutchings & Wijesinghe 2008; Kembel et al. 2008). While morphological responses allow plants to take advantage of large opportunities, they are more costly, less reversible and take longer. In contrast, lower-level physiological and biochemical responses are less costly, swifter, more reversible and expected to be more efficient in exploiting smaller, shorterlasting and less predictable opportunities (Bradshaw 1965; Grime & Mackey 2002; Table 1).Whether or not plant strategies are dictated by tradeoffs between different plastic adaptations is still under a heated debate (Kembel & Cahill 2005; Grime 2007; Kembel et al. 2008) and is beyond the scope of the present discussion. However, it is suggested that plants are able to refine the magnitude and resolution of their foraging and competitive responses by utilizing plastic responses at variable scales within each of the mentioned organizational levels and competitive categories (Table 1). Although large-scale responses usually include syndromes that involve responses at multiple categories and hierarchies (e.g. Smith 2000; Farnsworth 2004), responses at smaller scales and magnitudes might only involve behaviours that belong to some categories or lower organizational levels (Table 1). At the morphological level, when presented with sufficient resources and time, plants are expected to develop larger infrastructural branches that allow an efficient addition of lower-ordered laterals at a later stage. In contrast, smaller or less predictable opportunities are expected to invoke slower risk-averse growth of single leaves on existing branches, or smaller and less costly ephemeral roots on already existing structural roots. At the physiological level, longer and predictable exposures to high or low light levels might trigger substantial and longer-to-last changes in e.g. ribulose 1·5-bisphosphate carboxylase/oxygenase (Rubisco) content, while more ephemeral changes are expected to invoke faster and more reversible modifications in e.g. electron transport rates (Table 1; Valladares & Niinemets 2008). Metaplasticity The plethora of behavioural categories, organizational levels and scales demonstrates the sophistication of the ‘plastic toolbox’ that plants utilize to cope with the everchanging competitive challenges they are presented with. However, the sheer complexity and high operative costs of these plastic systems (DeWitt, Sih & Wilson 1998; Givnish 2002; Van Kleunen & Fischer 2005; Bell & Galloway 2008) present an acute need for higher-order control and coordination. Because each low-level behaviour is in itself a © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 Shift b Shifts Shift c Combinations Tolerance Confrontation Increased resource and time allocation; reduced reversibility Syndrome 2 Syndrome 1 High chlorophyll concentration, high quantum yield Large thin leaves, sparse stomata Low leaf clumping and apical dominance High rubisco content Small thick leaves, dense stomata Tree-like, increased shoot/root ratio Photo-and spectro-tropisms away from shade and sources of far-red light Elongated stems, sparse leaves Asymmetrical branching away from shade or expected shade Avoidance Category manifestation of phenotypic plasticity, a higher-level plastic control of such behaviours may be defined as metaplasticity (Abraham & Bear 1996). More specifically, to be affective and efficient, the context, timing and extent of specific plastic behaviours are expected to depend on contingent factors that are related to the specific state of the plant and the multiple challenges it is faced with. Metaplastic control might include a variety of internal morphogenetic contingencies that are related to the plant’s deeper developmental history (e.g. Jones & Watson 2001), maternal and current physiological state (e.g. Lundgren & Sultan 2005), ontogenetic stage (Diggle 1994; Bell & Sultan 1999), size, phenology and various external cues that are related to current and anticipated stresses, disturbances, biotic interactions and the time left for plastic modifications of variable magnitudes (Novoplansky et al. 1994; Pigliucci et al. 1996). Given sufficient reliable information, plants might shift metaplastically between behavioural categories and hierarchies according to their expected gains. For example, Abutilon theophrasti elongates in response to shade and shade cues when competing with similarly statured plants in dense weedy stands or soybean fields. However, when grown in corn fields, this plant elongates only as long as it is not overtopped by much taller neighbours (Weinig 2000a). Competitive behaviours might metaplastically interact with each other. In A. theophrasti, early confrontational elongation limits shade responses later in the season (Weinig & Delph 2001). However, early competitive interactions might also prime plants to tolerate later competitive and abiotic stresses and prevail in later competitive stand-offs (e.g. Novoplansky & Goldberg 2001a). Metaplastic shifts between competitive categories are demonstrated in postfire succession in Mediterranean habitats that commonly involves long-lasting war-of-attrition stand-offs between pines and oaks (e.g. Gracia, Retana & Roig 2002). Typically, the more fire-resistant oaks take advantage of the high light, post-fire periods, during which they actively compete for light with similar-statured trees and shrubs. Yet, once overtopped by the faster-growing pine saplings, the oaks avoid further competitive confrontation. During pinedominated phases and until the following fire, the oaks exhibit shade tolerance behaviours that include plastic modifications in morphological characters such as leaf size and lobation, and the photosynthetic system (Valladares et al. 2002; Valladares & Niinemets 2008). The effects of relative size and density Level Architecture Morphology Physiology and lower levels Shift a Table 1. Examples of competitive behaviours at different categories and hierarchies. Depending on various contingencies, plants are able to utilize and shift between various behavioural combinations. The comparison between syndrome 1 and 2 exemplifies responses to large and predictable vs small and unpredictable changes in the competitive environment, respectively. The behavioural shifts correspond to the scenarios depicted in Fig. 1 732 A. Novoplansky Plants are concurrently engaged in variable competitive interactions that take place under continuously changing densities and resource availabilities. Thus, plants are expected to demonstrate a mosaic of competitive behaviours that may belong to different categories for the same or different resources. Living in crowded stands usually means that avoiding competition with certain neighbours eventually results in confrontation with others. Accordingly, the need to ‘pick battles’ is expected to increase with density © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 Competitive behaviour in plants 733 (b) (a) C (c) C C ity ns e D A T A A T T Figure 1. Examples for metaplastic competitive shifts under increasing density. Triangle corners represent theoretical extreme behaviours: A – avoidance; C – confrontation; T – tolerance. Plants or plant organs may assume various combinations of competitive behaviours based on their developmental state and ecological context. (a) Similarly sized dominant individuals; (b) increasing dominance and size hierarchies; (c) chronic subordinate individuals that, e.g. germinate late or belong to relatively small taxa. but vary with the relative size of the responding plant and its evolutionary background. At very low densities, plants are expected to mainly avoid competition among their own organs and demonstrate little interactions with their neighbours. At slightly higher densities, through the perception of anticipatory cues, plants are expected to avoid their neighbours and take advantage of open patches and gaps (Fig. 1a). However, this behaviour is expected to mainly characterize plants of open and disturbed habitats where unoccupied patches are long lasting and relatively predictable (Novoplansky et al. 1990a). In contrast, avoidance behaviour is expected to be unstable strategy under higher densities, where open gaps are short-lived, and their occupation might come at the expense of lowered confrontation efficiency (Novoplansky 1996). At high densities, similarly statured plants are expected to shift from avoidance to confrontation, which often involves fierce arms race and tragedy of the commons, whereby the plants allocate increasingly greater proportions of their resources to competitive functions and structures at the expense of reproduction (Fig. 1a; O’Brien et al. 2005). However, initial stochastic differences in size are commonly amplified gradually and result in a few dominants and a large number of subordinates, a process that is more emphasized under asymmetric competition (e.g. Weiner et al. 2001). While the dominant individuals are bound to continue their aggressive confrontation, the subordinates might, according to their evolutionary background (Morgan & Smith 1979; Dudley & Schmitt 1996), either continue to confront their dominant counterparts at great costs and little gain, or metaplastically ‘give in’ and switch to tolerance behaviours (Fig. 1b; Weinig 2000a; Valladares et al. 2002; Valladares & Niinemets 2008). Being hardly affected by their subordinates, dominant individuals are expected to express no avoidance and relatively moderate degree of confrontational behaviour towards them. In contrast, under increased density, the subordinates are expected to shift from avoidance to tolerance (Fig. 1b,c), a transition that may be accelerated in response to the rapidly dwindling resource availabilities resulted by the fierce confrontation between their dominant neighbours. Interestingly, concurrent multi-level competitive interactions between same- and different-statured plants means that even dominant individuals could also compete with larger and often unbeatable competitors of another species or life form. Such plants are expected to demonstrate confrontational behaviours towards their similarly sized peers but to avoid or tolerate their much larger counterparts. For example, although forest understorey plants are known to be less responsive to shade cues and should avoid confrontation with tall canopy trees (Morgan & Smith 1979; Schmitt et al. 2003), they still have a clear incentive to confront their similarly statured understorey neighbours. Naturally, such responses must depend on the plant’s ability to differentiate between shade and shade cues generated by tall trees and short neighbours (Semchenko & Zobel 2007; see ‘Probabilistic information’). Finally, the ability of plants to metaplastically shift their behaviour among and within different behavioural categories and organizational hierarchies implies that ‘fixity’, or the apparent absence of phenotypic variability that results from direct natural selection – such as in the case of canalization (Waddington 1953, 1956; Schlichting & Pigliucci 1998) – or lack of selection for plasticity, has to be judged with caution. More often than not, fixity at a certain behavioural category or organizational level is based on interactions with others (Table 1). Accordingly, the magnitude of plasticity can only be judged at the level of specific individual characters and behaviours (Novoplansky 2002). Somatic competition Being genetically identical (but see Klekowski 1988), organs that belong to the same plant are expected to avoid overlapping between their depletion zones, which in turn results in greater probability for non-self encounters and confrontation (Schenk et al. 1999; Falik et al. 2003; Holzapfel & Alpert 2003; Semchenko et al. 2007b). Confrontation between redundant organs on the same plant may occur in two, not mutually exclusive, settings. The first situation occurs when the plant undergoes growth spurts following dormancy or major damages. At the initial stage, many similarly statured buds, young branches or roots grow side by side and gradually develop size asymmetry, whereby a © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 734 A. Novoplansky few become dominant, while others cease growing or even die (Sachs 1966; Jones & Harper 1987; Marcelis et al. 2004). Depending on the plant’s developmental history and external competitive challenges, such ‘somatic self-thinning’ might result in the coexistence of a few co-dominant organs (e.g. multi-trunk trees; Sachs & Novoplansky 1995), or the dominance of a single organ, e.g. a single shoot in a shaded understory climber. A second type of confrontation occurs between organs that develop under different growth conditions which often results in the domination of the more successful organs at the expense of their less fortunate counterparts (Sachs & Novoplansky 1997). Similarly to the population-level interactions (Fig. 1), intensified competition means that some of the plant’s organs develop under, at times self-imposed, poorer growth conditions. The gain from further allocation to less fortunate organs is expected to be dependent on the evolutionary background, probabilistic and realized degree and resolution of resource heterogeneity (Hutchings & de Kroon 1994; Alpert & Stuefer 1997; Ikegami, Whigham & Werger 2008) and the physiological status of the plant (McIntyre 2001; Benner 1988; Novoplansky et al. 1989; Cline 1991). Such smaller or slower modules may (1) grow further and confront the neighbours based on the support of other modules on the same plant; (2) adapt to and tolerate the poorer conditions (Fig. 1b,c); or (3) become overpowered and lose their resources to more successful modules on the same plant (e.g. Souza & Válio 1999). Somatic confrontation takes place at two complementary levels. The first is internal: in shoots, high performance is coupled with increased auxin synthesis in the young developing leaves and its polar transport towards the roots, which in turn induces the differentiation of additional vascular elements towards the growing branch and enhances root formation (Sachs 1981, 1991). By the same token, high root performance is coupled with greater synthesis of cytokinins (Matthyse & Scott 1984; Sachs 1991; Beck 1996) and possibly other hormones (Jackson 2002; Takayama & Sakagami 2002). The faster the roots develop, the more carbohydrates and auxin they receive and catabolize (Jiang & Feldman 2002), thus enhancing further shoot development. The second type of competition is for external resources (e.g. Jones & Harper 1987). Interestingly, because the relative performance of any given organ also affects its hormone formation, most likely internal and external competitions depend on the same signals. The larger a branch and the faster it develops, the more auxin it forms, which in turn induces the development of additional vascular strands that connect it with the roots and allows it to dominate larger sectors of the cambium (Sachs 1981). Accordingly, the formation of auxin, and possibly other hormones, serve as a self-perpetuating mechanism in which further support and allocation to developing organs are based on positive feedback between their past performance and continued success (Sachs & Novoplansky 1997). To the extent that plant growth is resource limited, the increased success of certain organs necessarily comes at the expense of less fortunate organs on the same plant (Snow 1931; Novoplansky et al. 1989). Accordingly, somatic integration and coordination allow plants to not merely support less successful organs (e.g. Saitoh, Seiwa & Nishiwaki 2006), they are also able to ‘hold their organs accountable’ for their relative performance. Accordingly, the development of individual roots or shoots is expected to be enhanced only when their development proves beneficial to the entire plant in the long run (Novoplansky et al. 1989; Gersani & Sachs 1992; Sachs, Novoplansky & Cohen 1993; Sachs 2005). However, internal competition is only possible among anatomically connected and physiologically integrated organs. These stipulations are not fulfilled in many adult desert and Mediterranean shrubs that exhibit axis splitting (Fahn 1964; Schenk 1999), and in clonal plants that are comprised of multiple potentially independent modules (Hutchings & de Kroon 1994). Interestingly, the morphogenetic controls underlying somatic competition and other correlative phenomena such as apical dominance (Cline 1991) and adaptive control of shoot/root ratios (Iwasa & Roughgarden 1984; Sachs 2005) could also account for physiologically mediated self/nonself discrimination (see ‘Recognition and coordination’). Tight accountability of individual organs of different orders to the rest of the plant means that self/non-self discrimination could be facilitated without any specific recognition or external communication among potentially competing organs. A positive feedback, whereby further allocation to developing organs depends on their past and expected contribution to the rest of the plant, means that allocation to organs whose development interferes with the performance of other organs on the same plant sector should result in decreased or even ceased support by the rest of the plant to that sector. Such generic morphogenetic control may account for discriminative behaviours, whereby plants prefer to avoid competition with organs that belong to the same coordinated individual and confront others that belong to detached neighbours, regardless of their genetic identity (Gersani et al. 2001; Maina et al. 2002; Falik et al. 2003; O’Brien et al. 2005; Raz 2005). CONCLUSIONS Can plants pick their battles? Perhaps the most quoted rationale for the accentuated expression of phenotypic plasticity in plants is their limited mobility. However, although most plants cannot choose their neighbours, the present discussion suggests that they are able to utilize a wide spectrum of competitive behaviours that fit their prospects to compete or withstand the competition of their neighbours. Plants and individual organs can avoid, confront and tolerate their neighbours at different spatial and temporal scales and magnitudes (Table 1). The multiplicity of competitive behaviours and their differential activation implies the involvement of various higher level metaplastic controls (Novoplansky et al., unpublished data). But what could be the meta- cues and signals that are involved in the dynamic shifting between different categories and hierarchies of © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 Competitive behaviour in plants 735 competitive behaviours? Such meta- cues and signals should reflect the real-time absolute and relative prospective benefits of the alternative behaviours. It is speculated that a source of such information could be the higher-order derivatives of lower-level cues and signals that trigger the corresponding lower-level plasticities. For example, although R/FR ratios usually provide reliable information regarding the presence of neighbours and the probability of their future competitive effects, alone they provide little information regarding the prospects of confrontation with these neighbours. However, temporal changes in light and R/FR levels could provide indications for the probability of confronting their neighbours successfully. Accordingly, increasing light and R/FR gradients could indicate ‘optimistic’ prospects and increase the incentive for further growth and confrontation (Leeflang et al. 1998; Weijschedé et al. 2006; Nyanumba 2007). In contrast, constant shade or, worse yet, deteriorating light and R/FR ratios indicate poor prospects for further confrontation and may trigger a shift to tolerance behaviour (Fig. 1b,c). However, anticipatory information is merely indicatory of the probabilities and prospects of future competitive interactions. Later modifications are expected to depend on actual performance of organs and their contribution to the entire plant (see ‘COMPETITIVE BEHAVIOURS’). Further allocation to less successful organs is expected to vary according to existing alternatives. Plants may support less fortunate organs if their poorer performance is expected to be passing in space or time or if they help spanning over poor patches (Hutchings & de Kroon 1994). However, if other organs on the same plant perform better, or if the entire plant stands little prospects of prevailing, the growth of such organs is expected to stop. In addition, allocation to the entire shoot or root will be augmented when they are expected to alleviate relative shortages in carbohydrates and various soil resources, respectively (Bloom et al. 1985; Sachs 2005). The inherent interplay between anticipatory information and materialized performance is a common theme in any plastic response. Whether it is the differentiation of new vascular strands from a growing bud (Sachs 1981), somatic competition between redundant organs, dynamic modifications of shoot/root ratios, or shade responses, all plastic responses can be described as ‘educated exploratory endeavours’. They are initially triggered by anticipatory cues and signals and, given time and need, modified based on the materialized eventualities and updated anticipatory information (Novoplansky et al. 1990a). Naturally, the precise behavioural combination assumed by any given plant may depend on intricate contingencies related to their evolutionary background, developmental past and operational tradeoffs. Of particular importance in this context is the time available for the execution of further plastic modifications. Insufficient time is expected to strongly limit plasticity, especially when larger-scale behavioural changes are involved (Novoplansky et al. 1994; Novoplansky 1996; Pigliucci et al. 1996). Accordingly, it is expected that short-living plants or organs will only demonstrate large plastic modifications at the beginning of their lives and will exhibit increasingly smaller and swifter behaviours (Table 1) as they get older and closer to their death or when under less predictable growth conditions. Large metaplastic shifts are expected to be more common and apparent in perennial plants that are engaged in longlasting war-of-attrition battles (see ‘Metaplasticity’). Some open questions and future directions Competitive behaviour in plants is naturally too wide and diverse a topic to cover in a short overview. The following is a partial and rather subjective list of topics and open questions that might be worthwhile tackling by future work. Higher-level implications Besides demonstrating the amazing abilities of CNS-less organisms to perform rational behaviours, the study of competitive behaviour in plants is hoped to be constructive in understanding processes at larger ecological scales. Similarly to the ways biophysical information is scaled up from the basic level of the individual leaf to that of the entire ecosystem (e.g. Van Wijk 2007), studying the consequences of physiological and individual-level behaviours is expected to improve our understanding of processes that underlay higher-level phenomena such as species interactions and distributions (Grime & Mackey 2002; Callaway et al. 2003; Hodge 2004; Kembel et al. 2008), productivity (SorrensenCothern, Ford & Sprugel 1993; Schwinning & Weiner 1998), spatial patterning (e.g. Gilad, Shachak & Meron 2007; Herben & Novoplansky 2008), diversity (e.g. Chesson and Rosenzwieg 1991; Chesson et al. 2004; Lepik, Liira & Zobel 2005) and evolution (West-Eberhard 2003; Pigliucci, Murren & Schlichting 2006). Perhaps, the most pressing is the study of large-scale implications at the level of entire ecosystems. It is increasingly acknowledged that competitive behaviours play important roles in invasive processes (Bloom et al. 1985; Poorter & Lambers 1986; Sultan 2001). In addition, it is hypothesized that competitive behaviours belonging to different hierarchies and categories affect ecosystem attributes through their differential affects on photosynthetic efficiency and respiration rates, water-use efficiency (e.g. Lucero, Grieu & Guckert 2000) and nutrient cycling. Competitive metaplasticity The present discussion suggests the need for better understanding of higher-level metaplastic interactions between various hierarchies and categories of competitive behaviours, including their possible costs, horizontal and vertical controls, signals, syndromes and cascades, operational tradeoffs and ecological implications. Allelopathic behaviour? In spite of traditional scepticism, evidence for direct competitive interference in various forms of allelopathy seems © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741 736 A. Novoplansky clear and convincing (Schenk et al. 1999; Hierro & Callaway 2003; de Kroon et al. 2003). Although a few studies have demonstrated dual defensive-allelopathic effects of various inducible plant metabolites (Lovett & Hoult 1995; Tang et al. 1995; Callaway, DeLuca & Belliveau 1999), to the best of my knowledge, allelopathic plasticity that is directly induced by root competition is yet to be demonstrated. It is expected that exploring this possibility will not only yield interesting findings but also improve our understanding of population-, community- and maybe even ecosystem-level phenomena (Callaway et al. 2003). Facilitative behaviours? In spite of the importance of facilitation in dictating various population- and community-level processes (e.g. Lortie 2007), to the best of my knowledge, so far, there are no studies that have demonstrated induced facilitative behaviours in plants. It is conceivable that plants express induced facilitative responses toward siblings and kin (see ‘Recognition and coordination’), or establish ad-hoc cooperation when unrelated individuals are faced by large common challenges whose potential negative effects are expected to exceed losses due to competition between them. Competition and storage behaviour Storage of carbohydrates and minerals has profound effects on plant survival and performance (e.g. Poorter & Kitajima 2007). Given sufficient reliable information, plants are expected to not merely store when alternative challenges are relaxed (e.g. Tripler et al. 2002) but possibly also preempt competitive interactions and plastically divert more minerals and carbohydrates to storage when competitive interactions are anticipated. This hypothesis only exemplifies the potential complexity of the interesting and yet to be explored interactions between competitive and storage behaviours. ACKNOWLEDGMENTS I thank Tomáš Herben, Hagai Shemesh, Rick Karban, Eliah Malka, Omer Falik Stefano Mancuso and two anonymous reviewers for the constructive suggestions. Special thanks are due to Danny Cohen and the late Tsvi Sachs for their close personal friendship, scientific partnership and the innumerable discussions that helped shape many of the concepts that appear here and to Tony Trewavas and Carlos Ballaré for the encouragement and patience. 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