Picking Battles Wisely: Plant Behaviour Under Competition

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 for the first time, studied GxE interactions by transplanting plants to areas out of their natural ranges (Theophrastus Plants are limited in their ability to choose their neigh- 1916). Further attention by the fathers of the science of bours, but they are able to orchestrate a wide spectrum of evolution (Lamarck 1809; Darwin 1859) have resulted in rational competitive behaviours that increase their pros- substantial theoretical and experimental efforts to under- pects to prevail under various ecological settings. Through stand the role of competition in shaping populations and the perception of neighbours, plants are able to anticipate communities (Tansley 1917; Clements 1929; Fisher 1930; probable competitive interactions and modify their com- Gause 1934; Hairston, Smith & Slobodkin 1960; Grime petitive behaviours to maximize their long-term gains. 1979; Tilman 1982, 1988; Connell 1983; Schoener 1983; Specifically, plants can minimize competitive encounters Keddy 2001) and the evolution of competitive strategies by avoiding their neighbours; maximize their competitive and traits (MacArthur & Wilson 1967; Pianka 1970; Char- effects by aggressively confronting their neighbours; or tol- lesworth 1971; Roughgarden 1971; Grace & Tilman 1990; erate the competitive effects of their neighbours. However, Aarssen 1992; Stearns 1992; Silvertown, Franco & Harper the adaptive values of these non-mutually exclusive options 1997). However, plant competition has been traditionally are expected to depend strongly on the plants’ evolutionary studied on different sides of disciplinary gaps (Novoplansky background and to change dynamically according to their 2002; Callaway, Penning & Richards 2003;Ackerly & Sultan past development, and relative sizes and vigour. Addi- 2006). While ecologists usually focus on population- and tionally, the magnitude of competitive responsiveness is community-level implications of species’ differential abili- expected to be positively correlated with the reliability ties to prevail under competition for limited resources of the environmental information regarding the expected (Goldberg & Barton 1992; Goldberg 1996; Keddy et al. competitive interactions and the expected time left for 2002; Fargione & Tilman 2006), plant physiologists tradi- further plastic modifications. Concurrent competition over tionally study various traits that underlay these adaptations external and internal resources and morphogenetic signals (e.g. Rao, Raghavendra & Reddy 2006). But perhaps not may enable some plants to increase their efficiency and surprisingly, it was Charles Darwin himself who, with the external competitive performance by discriminately allo- help of his son, meticulously studied what we now call cating limited resources to their more promising organs at behavioural traits in plants (Darwin 1880), many of which the expense of failing or less successful organs. are directly related to competition – perhaps the single most important ecological force underlying his epoch- Key-words: avoidance; competitive behaviour; confronta- making work (Darwin 1859). tion; environmental information; future perception; Stimulated by earlier work on the evolutionary ecology metaplasticity; phenotypic plasticity; self/non-self; somatic of phenotypic plasticity and life histories (e.g. Bradshaw competition; tolerance. 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 INTRODUCTION cues and signals they perceive from their environment (Silvertown & Gordon 1989; Sultan 2007). Due to their Starting at the earliest days of scientific thinking, competi- dynamic game-related nature, some of the more intricate tion has been recognized as one of the most important and intriguing behaviours are related to biological interac- factors dictating the fate of individuals and the distribution tions such as herbivory (e.g. Baldwin et al. 2006) and com- of species. It was Aristotle who described and exemplified petition (Smith 1982; Silvertown & Gordon 1989;Aphalo & competition, territoriality and dominance in animals Ballare 1995; Callaway et al. 2003; Trewavas 2003; Karban (Aristotle trans. 1965), and his successor Theophrastus who, 2008), where the adaptive value of any given behaviour inherently depends on the behaviours of others (e.g. Correspondence: A. Novoplansky. Fax: +972 8 6596821; e-mail: Matsuda & Abrams 1994; Falster & Westoby 2003). [email protected] When discussing the analogy between animal and plant *Present address: Section of Evolution and Ecology, University of behaviour, some prefer to delimit plant behaviour to revers- California, One Shields Avenue, Davis, CA 95616, USA. ible short-term responses that agree with the common 726 © 2009 Blackwell Publishing Ltd Competitive behaviour in plants 727 definition of acclimation (Karban 2008, but see Silvertown by the responding organisms. The perception of neighbours & Gordon 1989; Novoplansky 2002; Sachs 2002). How- and competitive behaviour in higher organisms is usually ever, the very essence of being a plant means that their based on sophisticated central nervous systems (CNS) and short-term responses to environmental changes commonly information processing, yet information-acquisition sys- involve both immediate physiological and slower yet tems dedicated to the perception of neighbours, resource longer-to-last morphological modifications via the addition availabilities and sophisticated communication are ubiqui- and abandonment of tissues and organs (Bradshaw 1965; tous even among the oldest and most rudimentary life Grime, Crick & Rincon 1986). Not surprisingly, these forms such as fungi (Hogan 2006), bacteria (Fuqua, Winans modifications usually take a longer absolute time when & Greenberg 1994) and viruses (Weitz et al. 2008). compared to movement of most motile animals. Using Plants are able to perceive their potential competitors the conceptual framework of environmental grain (Levins based on minute temporal and spatial differences in elec- 1968), the analogy between plants and animals might be tromagnetic radiation at various ranges, and metabolite better viewed in terms of the relative response time which concentrations and fluxes (Aphalo & Ballare 1995; Aphalo might be depicted by the relation between the time scales of et al. 1999; Karban 2008).While some of the perceived infor- plant responses and the environmental changes that trigger mation is directly related to the spatial and temporal them. This notion seems especially relevant to reciprocal distribution of essential resources such as light, water competitive responses of plants that have comparable and minerals, the more elaborate and intriguing types of developmental response times. In addition, the fact that competitive-relevant information are related to the dynam- most plants leave behind a trail of cellulitic and ligneous ics of resource levels and their proxies, and the specificity of ‘debris’ should not necessarily be interpreted as a reflection their biotic determinants (Estabrook & Yoder 1998;Aphalo of irreversible development but possibly a manifestation et al. 1999; Callaway 2002; Dudley & File 2007). Among the of the low recycling value of these tissues to the plant. vectors used by plants to perceive their competitive envi- The current review, therefore, discusses plant competitive ronment are light fluxes and spectral composition (Smith behaviour from a more inclusive point of view, with the 2000; Weinig 2002; Wada, Shimazaki & Iino 2005), volatile hope to trigger discussion rather than a squabble over defi- compounds (Ninkovic 2003; Pierik et al. 2004) and root exu- nitions. The discussion attempts to deal with the evolution- dates (e.g. Mahall & Callaway 1991; Schenk et al. 1999; ary and ecological rationales, and the mechanistic aspects of de Kroon et al. 2003). some plant behaviours, yet without the intention to com- However, any adaptive notion regarding information prehensively covering the existing knowledge of the field; perception can only be understood in the context of future this has been done in other excellent reviews (e.g. Silver- rather than the immediate environmental conditions. Since town & Gordon 1989; Hutchings & de Kroon 1994; Aphalo plastic responses – especially those related to development & Ballare 1995; Schlichting & Pigliucci 1998; Aphalo, of new organs and resource allocation and translocation – Ballare & Scopel 1999; Schenk, Callaway & Mahall 1999; require time, useful information must be relevant to the Callaway et al. 2003; de Kroon, Mommer & Nishiwaki 2003; future environment that the responding plant eventually Trewavas 2003; Sultan & Stearns 2005; Karban 2008). functions in (Ballaré et al. 1987; Novoplansky, Cohen & Frustratingly yet excitingly, despite the recent surge of Sachs 1990a). This principle is ubiquitously important for interest, many aspects of this topic are still vague any decision-making system, yet it is especially crucial in or even totally obscure. Thus, the following discussion competitive settings where the behaviour of each party is unavoidably includes an imbalanced collection of examples inherently dependent on the responses of its counterparts and hypothetical notions that will hopefully be further cor- (Maynard Smith 1982; Maina, Brown & Gersani 2002). rected and moulded into a more substantial body of theory Although environmental information is invariably based and knowledge in the future. Specifically, it discusses the on past events and conditions, in many cases, it is correlated types of information that plants require and acquire to with and thus indicative of future conditions. Such correla- make ‘educated’ competitive decisions, and the categories tions are ubiquitous in both natural and man-made systems; and hierarchies of their competitive behaviours under they are readily utilized in a wide spectrum of control various ecological circumstances. systems where pre-emptive adaptation and action are advantageous (e.g. Blanke, Pourzanjani & Vukic 2000; Mangan, Zaslaver & Alon 2003). INFORMATION Perhaps, the most studied ecologically relevant forecast- Information, or its lack thereof, is key to decision making of ing system that is based on such feedforward correlations any type, and its importance to fitness-determining pro- is the red/far-red (R/FR) spectral sensitivity that enables cesses such as survival, resource capturing and interference plants to perceive and respond to the presence of poten- cannot be underemphasized (e.g. Cohen 1971; Charnov tially competitive neighbours even before actual competi- 1976; Smith 1982; Mangel 1990; Sih 1992; Aphalo & Ballare tion for light develops (Ballaré et al. 1987). The tight 1995; Maynard-Smith & Harper 1995; Aphalo et al. 1999; asymmetric nature of light competition (e.g. Schwinning Wong & Ackerly 2005). While deterministic growth can be & Weiner 1998) often dictates an aggressive arms race executed with little or no external cues, plastic development whereby plants are more sensitive and responsive to spec- is invariably based on environmental information perceived tral 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 all. Although carrying information, some of the cues might 1982; Ballaré et al. 1987; Casal, Sánchez & Deregibus 1987; be unreliable, contradictory or reflective of transient or Ballaré, Scopel & Sánchez 1990; Novoplansky et al. 1990a,b; inconsequential events. In addition, competitive cues might Novoplansky 1991). be generated by other parts of the same individual or neigh- Anticipatory competitive responses can also be based bours belonging to the same genotype which would render on correlations between early subacute and later severe competitive responses ecologically and evolutionary costly stresses. For example, young seedlings of the small desert and damaging. It is, therefore, suggested that perception plant Scleropogon brevifolius drastically increase their root systems have been selected to enable plants to differentiate allocation under subacute competition with seedlings of between meaningful and ‘junk’ information and, when Sporobolus airoides, a response that primes them to toler- possible, help plants to maximize their competitive ate later competition for water and survive longer periods responsiveness towards worthy targets while avoiding of severe drought (Novoplansky & Goldberg 2001a). wasteful allocation to competition against self and kin, or Another relatively neglected yet potentially important wage hopeless battles against overwhelmingly superior source of information regarding anticipated competition is competitors. the spatial and temporal gradients of resources. Such gra- In some cases, plants have demonstrated abilities to dis- dients often exhibit predictable trajectories that can be criminate between their neighbours and to develop differ- informative of future conditions. For example, Calendula entially in accordance with their species identity (Mahall & arvensis and Phlox glandiflora develop larger and produce Callaway 1991; Krannitz & Caldwell 1995; Gersani et al. more seeds when growing in increasing rooting volumes 2001; Semchenko, John & Hutchings 2007b), ecotypic back- than in the largest yet constant rooting volume (Nyanumba ground (Mahall & Callaway 1992, 1996), physiological 2007). Individual organs exhibit similar morphogenetic integrity (Falik et al. 2003; Holzapfel & Alpert 2003; Grunt- control: when different roots of the same Pisum sativum man & Novoplansky 2004) and even genetic relatedness plants were grown in variable constant and dynamically (Kelly 1996; Donohue 2003; Dudley & File 2007); yet, the changing nutrient levels, plants allocated more resources to precise mechanisms responsible for the competitive dis- the roots that experienced dynamically improving rather crimination are still obscure. than deteriorating nutritional conditions, regardless of the absolute resource levels (Shemesh et al., unpublished data). The importance of anticipatory cues is expected to be Recognition and coordination positively correlated with the amount and proportion of Recent evidence suggests the involvement of specific self/ time left for adaptive responses. Accordingly, young plants, non-self recognition in competitive interactions between whose life is mostly in the future, are expected to be more roots. The first report of such discrimination was by Mahall responsive to information related to their future competi- & Callaway (1991) who found that the desert shrub Ambro- tive environment. The extreme of this notion is exemplified sia dumosa differentially avoids root elongation in the pres- by seeds whose developmental decisions are invariably ence of roots of other Ambrosia individuals. Competitive related to the future. In contrast, older, especially senescing kin discrimination was also demonstrated in a few studies plants, such as annuals at the end of their growth season, are that compared the performance of plants that grew in expected to disregard anticipatory cues and be predomi- sibling- and non-sibling groups: while Triplasis purpurea nantly responsive to prevailing resource availabilities had a higher fitness in mixed than in homogeneous groups, (Novoplansky et al. 1990a; Elazar 2005). suggesting the involvement of resource partitioning (Chep- Nevertheless, even when early cues and signals are tightly lick & Kane 2004), Cakile edentula had a higher fitness correlated with later competitive conditions, they are (Donohue 2003) and lower root allocation in sibling groups merely proxies. Accordingly, it is expected that when given than in non-sibling groups, implying kin selection (Dudley sufficient developmental time and to the extent that early & File 2007). Similarly, in Miscanthus sinensis, root growth developmental moves do not limit later modifications was hardly affected by contacts with roots belonging to an (Diggle 1994; Novoplansky, Cohen & Sachs 1994; Watson, alien genotype but was significantly inhibited when con- Geber & Jones 1995; Novoplansky 1996; Bell & Sultan 1999; tacting roots belonging to the same genotype (de Kroon Weinig & Delph 2001), responsiveness to anticipatory et al. 2003). Yet, it is still unclear whether these behaviours information is expected to be accompanied by continuous are based on immune-like allorecognition, similar to self- ‘verifications’ and corrections based on the prevailing incompatibility systems that enable plants to avoid inbreed- competitive levels and resource availabilities (Novoplansky ing by self-pollination (Takayama & Isogai 2005). et al. 1990a; Cohen & Mangel 1999). Interestingly, self/non-self discrimination need not necessarily be based on allorecognition. In a growing number of Information specificity cases, plants have been demonstrated to avoid competition between roots of the same plant (Gersani et al. 2001; To what extent are cues and signals regarding the prevailing Falik et al. 2003; Holzapfel & Alpert 2003; Gruntman & and future competition informative and usable? Over- Novoplansky 2004; Falik, de Kroon & Novoplansky 2006). whelmed by a myriad of internal and external cues, plants Specifically, plants grow fewer and shorter roots in the cannot and have no adaptive incentive to respond to them 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. relatively greater probability of being generated by non-self 2007b), and increase their root allocation in the vicinity of neighbours (Novoplansky et al. 1990a; Novoplansky 1991). alien plants at the expense of reproduction (Maina et al. In contrast, midday shade has a greater probability of being 2002; O’Brien, Gersani & Brown 2005). In Buchloe dacty- cast by higher foliage of the same individual or much taller loides, separating cuttings that originate from the same neighbours (Weinig 2000a; see ‘COMPETITIVE BEHAV- node cause their becoming progressively alienated from IOURS’ below). Indeed, end-of-day shade signals are each other and eventually relate to each other as genetic known to have significant effects on plant physiology and aliens (Gruntman & Novoplansky 2004). Although the morphology (e.g. Tso, Kasperbauer & Sorokin 1970; methods used in some of these studies have been chal- Kasperbauer 1971; Aphalo, Gibson & Di Benedetto 1991; lenged (Schenk 2006; Hess & de Kroon 2007; Semchenko, Peer, Briggs & Langenheim 1999; Marcuvitz & Turkington Hutchings & John 2007a) and debated over (O’Brien & 2000) and shade avoidance was found to be consistent with Brown 2008), it is clear that at least in some of the reported stronger effects of end-of-day red/far-red reductions in cases competitive discrimination between self and non-self field set-ups (Kasperbauer 1971). However, more detailed neighbours is based on physiological coordination among testing of the effects of R/FR signals throughout the pho- roots that belong to the same intact plant rather than allo- toperiod presented no support for this hypothesis (Casal & genetic recognition (Falik et al. 2003; Holzapfel & Alpert Smith 1989; Raz 2005); consistent with the notion that the 2003; Gruntman & Novoplansky 2004). 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 Probabilistic information (Casal & Smith 1989). All plants, especially those belonging to the same species, use the same resources in very similar ways (Goldberg How strong are the competitors? 1990). In the case of light, plants that grow under the same conditions are expected to leave similar shade signatures of Perhaps the most useful information a plant can have lowered photosynthetic light and R/FR ratios. However, regarding its potential competitors is related to the probabil- some plants have been demonstrated to respond differently ity of competing with them successfully.Rather than waging to shade of different neighbouring species (Marcuvitz & war indiscriminately, plants, as any other rational system, Turkington 2000; Weinig 2000a; Semchenko & Zobel 2007). are expected to take advantage of such information to pick Can plants use generic shade signals to differentiate winnable and avoid hopeless battles (see ‘COMPETITIVE between their competitor’s and their own shade? For light BEHAVIOURS’ for a detailed discussion). More specifi- signals to be informative of the identity of the competitor, cally, such information should be related to the relative they must relay on probabilities of being generated by self competitive ability of the responding plant and its neigh- and non-self neighbours. It is known that the relative posi- bours. Besides the inherent information regarding their tion of leaves and branches within the plant’s canopy general capabilities to pre-empt resources and interfere with strongly affects the probability of self-shading (Ackerly & their neighbours (MacArthur & Wilson 1967; Grime 1979; Bazzaz 1995; Valladares & Pearcy 1998). For example, Morgan & Smith 1979; Stearns 1992; Dudley & Schmitt leaves positioned near the stem apex have a significantly 1996), plants are expected to be particularly sensitive and lower probability of encountering self-shading compared responsive to dynamic changes in their own abilities to with lower leaves (Yamada et al. 2000). In Ocimum basili- acquire resources and withstand the competitive effects of cum, shading of the uppermost part of the seminal shoot their neighbours. A simple candidate mechanism that may which has the lowest probability of being shaded by other enable plants to acquire such information could be based on parts of the same plant, triggered significant stem elonga- an embedded positive feedback whereby the plant allocates tion, while identical shading of lateral branches, whose resources to competitive behaviours only as long as they are probability of being shaded by other branches of the same sustainably beneficial. For example, plants are expected to individual is high, triggered little to no elongation (Raz allocate resources to stem elongation as long as the result- 2005). Another possible source of information regarding ing photosynthetic returns are positive. Interestingly, such shade identity is the relative direction of shade.The seminal control would also ensure that branches do not overshoot shoots of young Portulaca oleracea plants were subjected to above the height of their neighbours, which would not only directional vegetative shading immediately after the plants fail to confer greater gains (Schmitt, McCormac & Smith become recumbent. While plants that were shaded from 1995;Weinig 2000a), but could also result in significant costs their periphery (greater probability of non-self-encounter) and risks (e.g. Anten et al. 2009). changed their orientation and increased the elongation of A candidate source of such information is the trajectories their laterals away from the shade, no such responses were of resource gradients discussed earlier. For example, in observed when the shade was directed from the inner parts Hydrocotyle vulgaris and Trifolium repens, plants develop of the plant outwards (greater probability of self-shading) longer petioles when subjected to vertically improving light (Raz 2005). Another source of such information could be gradients than when under homogeneous shade (Leeflang, the diurnal timing of shade interception. Shade reaching During & Werger 1998; Weijschedé et al. 2006). Interest- plants during the earliest and latest periods of the day has a ingly, 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, fierce competitive matches with their neighbours, poten- which supports the notion that plants are able to integrate tially at great consequential reductions in fitness (e.g. cues over temporal and spatial gradients in ways that may Novoplansky et al. 1990b; O’Brien et al. 2005). Accordingly, increase their competitive performance (Nyanumba 2007; plants are expected to possess not only various adaptations Shemesh et al., unpublished data). that maximize resource capturing, but also perception mechanisms that enable them – when possible and given Contingent contexts sufficient reliable information – to decide whether to avoid, confront or tolerate their neighbours. In the following Although absolutely essential, neighbour perception alone section, I describe a few distinctive, although usually not cannot suffice. The execution of adaptive and efficient com- mutually exclusive, categories of competitive behaviours petitive responses must take into account a myriad of con- followed by a short discussion of their possible adaptive texts that may dictate very different responses to the same implications under various ecological circumstances. cues under different circumstances. For example, the same shade signals are expected to trigger stronger competitive Behavioural categories responses in plants that experience relatively weaker root It is suggested that most competitive behaviours belong to than light competition (Bloom, Chapin & Mooney 1985), as one or more of the following functional categories. in the case of later successional stages (Tilman 1988). When young Portulaca seedlings were subjected to various inten- Competitive avoidance sities of photosynthetic light and R/FR ratios from opposite directions, they became recumbent preferentially towards Behaviours that minimize competitive interactions. Excel- the direction of the lower FR light, even when it meant lent examples for avoidance behaviours are provided by growing towards filters that absorbed 20 times more photo- plants whose germination is increased under lower prob- synthetic light. A preference for the direction with higher abilities of competition. For example, dispersal and germi- photosynthetic light over lower FR was also found, but nation of some plants are significantly enhanced by only under more extreme light differences. Such context- exposure to smoke or high temperatures, typical to natural dependent responses enable plants to take advantage of fires (e.g. Clarke & French 2005) that are tightly corre- local competitive opportunities rather than merely growing lated with the removal of large competitors. Some studies where conditions are ‘appropriate’ (Novoplansky, Cohen & suggest that sibling competition is avoided by increased Sachs 1989; Novoplansky 1991). In general, acting upon maternal-induced dormancy following good years after cues of prevailing and especially future competition is which competition is expected to be high (Phillipi 1993; expected to depend on numerous additional factors such as Tielbörger & Valleriani 2005). Interestingly, vertical stem overall resource availability (e.g. Weijschedé et al. 2006), elongation, the hallmark of the ‘shade avoidance syn- germination time, phenological stage (Weinig 2000a), drome’, simultaneously increases competitive responses expected time available for the execution of the competi- (avoidance) and effects (see ‘Competitive confrontation’ tive response (Novoplansky et al. 1994; Weinig 2000b), below). However, shade avoidance need not necessarily be quantity of stored nutrients and carbohydrates, probability accompanied by confrontational behaviour. For example, of future damage, various abiotic stresses and catastrophic Psychotria limonensis plants avoid self-shading by reori- disturbances (Grime 1979), most of which are yet to be enting their leaves in response to R/FR cues (Galvez & explored (see ‘COMPETITIVE BEHAVIOURS’ below). 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; COMPETITIVE BEHAVIOURS Novoplansky 1991). When Pinanga coronata plants grow Several questions arise regarding the ability of plants to larger, their leaf blades become longer and narrower, utilize the above-mentioned environmental information: while their petioles increasingly elongate further away Can plants pick their competitive battles?; What are the from the stem (Kimura & Simbolon 2002). It should be behavioural alternatives that plants can employ when noted, however, avoidance behaviours can only be adap- engaged in competition?; To what extent are plants able to tive as long as resource patches or pulses are not chal- make adaptive competitive decisions based on relevant lenged by too many plants (Kalisz et al. 1999; Ronce environmental information? The current state of our 2007). Although such conditions may be common in highly knowledge does not allow for satisfactory answers to these disturbed or abiotically stressed environments – where questions and their daunting complexity might prevent plants often grow in predictably sparse stands (Novoplan- even their adequate presentation in a short overview. In the sky et al. 1990a) – more commonly, plants grow in following section, I briefly present a few aspects of the relatively high densities thus bound to confront their possible ecological rationale and mechanisms of competi- neighbours. tive behaviour in plants. The great costs and hazards of competition imply that, Competitive confrontation in most cases, plants are expected to simply avoid it. How- Behaviours that maximize the negative influences of ever, more often than not, plants are bound to engage in 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’ Organizational hierarchies (sensu Goldberg 1990). Such behaviours promote re- Regardless of their functional type, probably all plants are source uptake or allelopathic activity in plants that are able to exhibit foraging behaviours that increase their subjected to competition or cues of expected competi- ability to acquire resources at various spatial and temporal tion. Aboveground confrontational competition involves, scales, contrasts, magnitudes and predictabilities (Bradshaw among other responses, increased shoot allocation and elon- 1965; Levins 1968; Drew & Saker 1978; Crick & Grime 1987; gation in response to shade, shade signals and volatile cues Caldwell & Pearcy 1994; Hutchings & de Kroon 1994; (see‘INFORMATION’ above).Similarly,belowground con- Alpert & Stuefer 1997; Sachs & Novoplansky 1997; Herben frontation involves increased root allocation in response et al. 2003; Mágori et al. 2003; Hodge 2004; Hutchings & to competition for water and minerals (e.g. Wilson 1988; Wijesinghe 2008; Kembel et al. 2008). While morphological Sachs 2005). The potentially high production costs of responses allow plants to take advantage of large opportu- noxious metabolites and their potential self-retarding effects nities, they are more costly, less reversible and take longer. suggest the possible existence of competitively induced alle- In contrast, lower-level physiological and biochemical lopathy. However, although conceivable, direct evidence for responses are less costly, swifter, more reversible and its existence is still missing.Support for this possibility comes expected to be more efficient in exploiting smaller, shorter- from evidence for allelopathy that is induced by volatiles lasting and less predictable opportunities (Bradshaw 1965; such as methyl jasmonate and methyl salicylate which are Grime & Mackey 2002; Table 1).Whether or not plant strat- chiefly known for their inductive effects on plant defences egies are dictated by tradeoffs between different plastic against insect herbivores and microbial pathogens (e.g. Bi adaptations is still under a heated debate (Kembel & Cahill et al. 2007). Confrontation behaviours typically characterize 2005; Grime 2007; Kembel et al. 2008) and is beyond the dense stands in relatively productive habitats where plants scope of the present discussion. However, it is suggested are often engaged in a tight and fierce arms race for the that plants are able to refine the magnitude and resolution domination of limited resources. However, under such com- of their foraging and competitive responses by utilizing petitive conditions, a large proportion of the plants, and plastic responses at variable scales within each of the typically also most of the biomass of the few lucky dominant mentioned organizational levels and competitive categories individuals grow under increasing resource limitations (e.g. (Table 1). Although large-scale responses usually include Weiner et al. 2001). Growing under such chronically poor syndromes that involve responses at multiple cate- conditions might trigger subordinate individuals and organs gories and hierarchies (e.g. Smith 2000; Farnsworth 2004), to assume various tolerance behaviours. responses at smaller scales and magnitudes might only involve behaviours that belong to some categories or lower Competitive tolerance organizational levels (Table 1). At the morphological level, Behaviours that maximize the performance of plants under when presented with sufficient resources and time, plants the worsened conditions caused by their neighbours. Such are expected to develop larger infrastructural branches that behaviours are compatible, although do not totally overlap, allow an efficient addition of lower-ordered laterals at a with the scope of ‘competitive response’ (Goldberg 1990). later stage. In contrast, smaller or less predictable opportu- This category includes behaviours that increase survival nities are expected to invoke slower risk-averse growth of and resource acquisition under shade (Henry & Aarssen single leaves on existing branches, or smaller and less costly 1997;Valladares & Niinemets 2008) and neighbour-induced ephemeral roots on already existing structural roots. At drought (Garaua et al. 2008), nutrient depravation (e.g. the physiological level, longer and predictable exposures Liancourt, Corcket & Michalet 2005) and allelopathic to high or low light levels might trigger substantial effects (e.g. Friebe, Wieland & Schulz 1996). For example, and longer-to-last changes in e.g. ribulose 1·5-bisphosphate shade tolerance could involve increases in the efficiencies of carboxylase/oxygenase (Rubisco) content, while more sunfleck utilization (Kuppers et al. 1996;Valladares,Allen & ephemeral changes are expected to invoke faster and more Pearcy 1997) and the minimization of respiration costs reversible modifications in e.g. electron transport rates (Table 1; Valladares & Niinemets 2008). (Givnish 1988) and CO2 losses (Walters & Reich 1996; Craine & Reich 2005). Similarly, drought tolerance involves morphological (e.g. Bell & Sultan 1999) and physiological Metaplasticity (Heschel et al. 2002; Bacon 2004; Golluscio & Oesterheld 2007) modifications that increase water-use efficiency and The plethora of behavioural categories, organizational minimize water loss. Therefore, tolerance behaviours might levels and scales demonstrates the sophistication of the foster competitive dominance where plastic modifications ‘plastic toolbox’ that plants utilize to cope with the ever- allow longer survival during periods of or patches of changing competitive challenges they are presented with. resource deficiency (Grime & Mackey 2002), and more However, the sheer complexity and high operative costs of opportunities to take advantage of ephemeral resource these plastic systems (DeWitt, Sih & Wilson 1998; Givnish pulses or patches (Goldberg & Novoplansky 1997; 2002; Van Kleunen & Fischer 2005; Bell & Galloway 2008) Novoplansky & Goldberg 2001a,b; Sher, Goldberg & present an acute need for higher-order control and coordi- Novoplansky 2004). nation. Because each low-level behaviour is in itself a © 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741

732 A. Novoplansky

hift c hift S 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 s

hift b hift S and efﬁcient, the context, timing and extent of speciﬁc

hift plastic behaviours are expected to depend on contingent S

hift a hift S 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 contin-

ht gencies that are related to the plant’s deeper developmental g history (e.g. Jones & Watson 2001), maternal and current ft between various behavioural s itive environment, respectively. physiological state (e.g. Lundgren & Sultan 2005), ontoge- el

v netic stage (Diggle 1994; Bell & Sultan 1999), size, phenol- away s

m ogy and various external cues that are related to current s of far-red li

s and anticipated stresses, disturbances, biotic interactions and the time left for plastic modiﬁcations of variable mag-

ource nitudes (Novoplansky et al. 1994; Pigliucci et al. 1996). s Given sufﬁcient reliable information, plants might shift y and lower le pectro-tropi g s

co content metaplastically between behavioural categories and hierar- ibility s s chies according to their expected gains. For example, iolo er hade and s v s Abutilon theophrasti elongates in response to shade and h chlorophyll concentration, h rubi h quantum yield g g

g shade cues when competing with similarly statured plants Phy from hi Photo-and Hi Hi in dense weedy stands or soybean ﬁelds. However, when grown in corn ﬁelds, this plant elongates only as long as it is

s not overtopped by much taller neighbours (Weinig 2000a). reduced re e ;

v Competitive behaviours might metaplastically interact with tomata s yndrome 1

e each other. In A. theophrasti, early confrontational elonga- e S e lea s s s

y tion limits shade responses later in the season (Weinig & g par par s

, den Delph 2001). However, early competitive interactions s , s , s e s

e might also prime plants to tolerate later competitive and v v abiotic stresses and prevail in later competitive stand-offs tem s (e.g. Novoplansky & Goldberg 2001a). Metaplastic shifts Morpholo between competitive categories are demonstrated in post- ated yndrome 2 g e thin lea S

g ﬁre succession in Mediterranean habitats that commonly mall thick lea tomata involves long-lasting war-of-attrition stand-offs between Elon S s Lar ource and time allocation

s pines and oaks (e.g. Gracia, Retana & Roig 2002).Typically, the more ﬁre-resistant oaks take advantage of the high

ed re light, post-ﬁre periods, during which they actively compete s for light with similar-statured trees and shrubs. Yet, once overtopped by the faster-growing pine saplings, the oaks hade away s Increa g avoid further competitive confrontation. During pine- hoot/root ratio

s dominated phases and until the following ﬁre, the oaks and apical g ed exhibit shade tolerance behaviours that include plastic pected s x modiﬁcations in morphological characters such as leaf size and lobation, and the photosynthetic system (Valladares

Architecture et al. 2002; Valladares & Niinemets 2008). hade or e s ymmetrical branchin s A from Low leaf clumpin dominance Tree-like, increa The effects of relative size and density Plants are concurrently engaged in variable competitive

Level interactions that take place under continuously changing

s 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 Examples of competitive behaviours at different categories and hierarchies. Depending on various contingencies, plants are able to utilize and shi

ory different resources. Living in crowded stands usually means g

oidance that avoiding competition with certain neighbours eventu- v onfrontation ombination ally results in confrontation with others. Accordingly, the C Tolerance C A Cate Table 1. combinations. The comparison between syndromeThe 1 behavioural and shifts 2 correspond exempliﬁes to responses the to scenarios large depicted and in predictable Fig. vs 1 small and unpredictable changes in the compet 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

(a) (b) (c)

C C C

ity ns De A T A T A 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 Interestingly, concurrent multi-level competitive interac- its evolutionary background. tions between same- and different-statured plants means At very low densities, plants are expected to mainly that even dominant individuals could also compete with avoid competition among their own organs and demon- larger and often unbeatable competitors of another species strate little interactions with their neighbours. At slightly or life form. Such plants are expected to demonstrate con- higher densities, through the perception of anticipatory frontational behaviours towards their similarly sized peers cues, plants are expected to avoid their neighbours and but to avoid or tolerate their much larger counterparts. For take advantage of open patches and gaps (Fig. 1a). example, although forest understorey plants are known However, this behaviour is expected to mainly character- to be less responsive to shade cues and should avoid con- ize plants of open and disturbed habitats where unoccu- frontation with tall canopy trees (Morgan & Smith 1979; pied patches are long lasting and relatively predictable Schmitt et al. 2003), they still have a clear incentive to con- (Novoplansky et al. 1990a). In contrast, avoidance behav- front their similarly statured understorey neighbours. Natu- iour is expected to be unstable strategy under higher rally, such responses must depend on the plant’s ability to densities, where open gaps are short-lived, and their occu- differentiate between shade and shade cues generated by pation might come at the expense of lowered confron- tall trees and short neighbours (Semchenko & Zobel 2007; tation efficiency (Novoplansky 1996). At high densities, see ‘Probabilistic information’). similarly statured plants are expected to shift from avoid- Finally, the ability of plants to metaplastically shift their ance to confrontation, which often involves fierce arms behaviour among and within different behavioural catego- race and tragedy of the commons, whereby the plants allo- ries and organizational hierarchies implies that ‘fixity’, or cate increasingly greater proportions of their resources to the apparent absence of phenotypic variability that results competitive functions and structures at the expense of from direct natural selection – such as in the case of canali- reproduction (Fig. 1a; O’Brien et al. 2005). However, initial zation (Waddington 1953, 1956; Schlichting & Pigliucci stochastic differences in size are commonly amplified 1998) – or lack of selection for plasticity, has to be judged gradually and result in a few dominants and a large with caution. More often than not, fixity at a certain behav- number of subordinates, a process that is more empha- ioural category or organizational level is based on interac- sized under asymmetric competition (e.g. Weiner et al. tions with others (Table 1). Accordingly, the magnitude of 2001). While the dominant individuals are bound to plasticity can only be judged at the level of specific indi- continue their aggressive confrontation, the subor- vidual characters and behaviours (Novoplansky 2002). dinates might, according to their evolutionary background (Morgan & Smith 1979; Dudley & Schmitt 1996), either Somatic competition continue to confront their dominant counterparts at great costs and little gain, or metaplastically ‘give in’ and Being genetically identical (but see Klekowski 1988), switch to tolerance behaviours (Fig. 1b; Weinig 2000a; organs that belong to the same plant are expected to avoid Valladares et al. 2002; Valladares & Niinemets 2008). overlapping between their depletion zones, which in turn Being hardly affected by their subordinates, dominant results in greater probability for non-self encounters and individuals are expected to express no avoidance and confrontation (Schenk et al. 1999; Falik et al. 2003; Holza- relatively moderate degree of confrontational behaviour pfel & Alpert 2003; Semchenko et al. 2007b). Confrontation towards them. In contrast, under increased density, the between redundant organs on the same plant may occur in subordinates are expected to shift from avoidance to tol- two, not mutually exclusive, settings. The first situation erance (Fig. 1b,c), a transition that may be accelerated in occurs when the plant undergoes growth spurts following response to the rapidly dwindling resource availabilities dormancy or major damages. At the initial stage, many resulted by the fierce confrontation between their domi- similarly statured buds, young branches or roots grow side nant neighbours. 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 1989). Accordingly, somatic integration and coordination die (Sachs 1966; Jones & Harper 1987; Marcelis et al. 2004). allow plants to not merely support less successful organs Depending on the plant’s developmental history and exter- (e.g. Saitoh, Seiwa & Nishiwaki 2006), they are also able to nal competitive challenges, such ‘somatic self-thinning’ ‘hold their organs accountable’ for their relative perfor- might result in the coexistence of a few co-dominant organs mance. Accordingly, the development of individual roots or (e.g. multi-trunk trees; Sachs & Novoplansky 1995), or the shoots is expected to be enhanced only when their devel- dominance of a single organ, e.g. a single shoot in a shaded opment proves beneficial to the entire plant in the long run understory climber. (Novoplansky et al. 1989; Gersani & Sachs 1992; Sachs, A second type of confrontation occurs between organs Novoplansky & Cohen 1993; Sachs 2005). However, inter- that develop under different growth conditions which often nal competition is only possible among anatomically results in the domination of the more successful organs at connected and physiologically integrated organs. These the expense of their less fortunate counterparts (Sachs & stipulations are not fulfilled in many adult desert and Medi- Novoplansky 1997). Similarly to the population-level inter- terranean shrubs that exhibit axis splitting (Fahn 1964; actions (Fig. 1), intensified competition means that some of Schenk 1999), and in clonal plants that are comprised of the plant’s organs develop under, at times self-imposed, multiple potentially independent modules (Hutchings & de poorer growth conditions. The gain from further allocation Kroon 1994). to less fortunate organs is expected to be dependent on the Interestingly, the morphogenetic controls underlying evolutionary background, probabilistic and realized degree somatic competition and other correlative phenomena such and resolution of resource heterogeneity (Hutchings & de as apical dominance (Cline 1991) and adaptive control of Kroon 1994; Alpert & Stuefer 1997; Ikegami, Whigham shoot/root ratios (Iwasa & Roughgarden 1984; Sachs 2005) & Werger 2008) and the physiological status of the plant could also account for physiologically mediated self/non- (McIntyre 2001; Benner 1988; Novoplansky et al. 1989; self discrimination (see ‘Recognition and coordination’). Cline 1991). Such smaller or slower modules may (1) grow Tight accountability of individual organs of different further and confront the neighbours based on the support orders to the rest of the plant means that self/non-self of other modules on the same plant; (2) adapt to and toler- discrimination could be facilitated without any specific ate the poorer conditions (Fig. 1b,c); or (3) become over- recognition or external communication among potentially powered and lose their resources to more successful competing organs. A positive feedback, whereby further modules on the same plant (e.g. Souza & Válio 1999). allocation to developing organs depends on their past and Somatic confrontation takes place at two complementary expected contribution to the rest of the plant, means that levels. The first is internal: in shoots, high performance is allocation to organs whose development interferes with coupled with increased auxin synthesis in the young devel- the performance of other organs on the same plant sector oping leaves and its polar transport towards the roots, which should result in decreased or even ceased support by the in turn induces the differentiation of additional vascular rest of the plant to that sector. Such generic morphogenetic elements towards the growing branch and enhances root control may account for discriminative behaviours, whereby formation (Sachs 1981, 1991). By the same token, high root plants prefer to avoid competition with organs that belong performance is coupled with greater synthesis of cytokinins to the same coordinated individual and confront others that (Matthyse & Scott 1984; Sachs 1991; Beck 1996) and possi- belong to detached neighbours, regardless of their genetic bly other hormones (Jackson 2002; Takayama & Sakagami identity (Gersani et al. 2001; Maina et al. 2002; Falik et al. 2002).The faster the roots develop, the more carbohydrates 2003; O’Brien et al. 2005; Raz 2005). and auxin they receive and catabolize (Jiang & Feldman 2002), thus enhancing further shoot development. The CONCLUSIONS second type of competition is for external resources (e.g. Jones & Harper 1987). Interestingly, because the relative Can plants pick their battles? Perhaps the most quoted performance of any given organ also affects its hormone rationale for the accentuated expression of phenotypic formation, most likely internal and external competitions plasticity in plants is their limited mobility. However, depend on the same signals. The larger a branch and the although most plants cannot choose their neighbours, the faster it develops, the more auxin it forms, which in turn present discussion suggests that they are able to utilize a induces the development of additional vascular strands that wide spectrum of competitive behaviours that fit their connect it with the roots and allows it to dominate larger prospects to compete or withstand the competition of their sectors of the cambium (Sachs 1981). Accordingly, the for- neighbours. mation of auxin, and possibly other hormones, serve as a Plants and individual organs can avoid, confront and tol- self-perpetuating mechanism in which further support and erate their neighbours at different spatial and temporal allocation to developing organs are based on positive feed- scales and magnitudes (Table 1). The multiplicity of com- back between their past performance and continued success petitive behaviours and their differential activation implies (Sachs & Novoplansky 1997). To the extent that plant the involvement of various higher level metaplastic controls growth is resource limited, the increased success of certain (Novoplansky et al., unpublished data). But what could be organs necessarily comes at the expense of less fortunate the meta- cues and signals that are involved in the dynamic organs on the same plant (Snow 1931; Novoplansky et al. 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 lives and will exhibit increasingly smaller and swifter behav- should reflect the real-time absolute and relative prospec- iours (Table 1) as they get older and closer to their death tive benefits of the alternative behaviours. It is speculated or when under less predictable growth conditions. Large that a source of such information could be the higher-order metaplastic shifts are expected to be more common and derivatives of lower-level cues and signals that trigger apparent in perennial plants that are engaged in long- the corresponding lower-level plasticities. For example, lasting war-of-attrition battles (see ‘Metaplasticity’). although R/FR ratios usually provide reliable information regarding the presence of neighbours and the probability Some open questions and future directions of their future competitive effects, alone they provide little information regarding the prospects of confrontation with Competitive behaviour in plants is naturally too wide and these neighbours. However, temporal changes in light and diverse a topic to cover in a short overview.The following is R/FR levels could provide indications for the probability a partial and rather subjective list of topics and open ques- of confronting their neighbours successfully. Accordingly, tions that might be worthwhile tackling by future work. increasing light and R/FR gradients could indicate ‘optimis- tic’ prospects and increase the incentive for further growth and confrontation (Leeflang et al. 1998; Weijschedé et al. Higher-level implications 2006; Nyanumba 2007). In contrast, constant shade or, Besides demonstrating the amazing abilities of CNS-less worse yet, deteriorating light and R/FR ratios indicate poor organisms to perform rational behaviours, the study of com- prospects for further confrontation and may trigger a shift petitive behaviour in plants is hoped to be constructive in to tolerance behaviour (Fig. 1b,c). However, anticipatory understanding processes at larger ecological scales. Simi- information is merely indicatory of the probabilities and larly to the ways biophysical information is scaled up from prospects of future competitive interactions. Later modifi- the basic level of the individual leaf to that of the entire cations are expected to depend on actual performance of ecosystem (e.g. Van Wijk 2007), studying the consequences organs and their contribution to the entire plant (see of physiological and individual-level behaviours is expected ‘COMPETITIVE BEHAVIOURS’). Further allocation to to improve our understanding of processes that underlay less successful organs is expected to vary according to exist- higher-level phenomena such as species interactions and ing alternatives. Plants may support less fortunate organs if distributions (Grime & Mackey 2002; Callaway et al. 2003; their poorer performance is expected to be passing in space Hodge 2004; Kembel et al. 2008), productivity (Sorrensen- or time or if they help spanning over poor patches (Hutch- Cothern, Ford & Sprugel 1993; Schwinning & Weiner 1998), ings & de Kroon 1994). However, if other organs on the spatial patterning (e.g. Gilad, Shachak & Meron 2007; same plant perform better, or if the entire plant stands little Herben & Novoplansky 2008), diversity (e.g. Chesson prospects of prevailing, the growth of such organs is and Rosenzwieg 1991; Chesson et al. 2004; Lepik, Liira & expected to stop. In addition, allocation to the entire shoot Zobel 2005) and evolution (West-Eberhard 2003; Pigliucci, or root will be augmented when they are expected to alle- Murren & Schlichting 2006). Perhaps, the most pressing is viate relative shortages in carbohydrates and various soil the study of large-scale implications at the level of entire resources, respectively (Bloom et al. 1985; Sachs 2005). ecosystems. It is increasingly acknowledged that competi- The inherent interplay between anticipatory information tive behaviours play important roles in invasive processes and materialized performance is a common theme in any (Bloom et al. 1985; Poorter & Lambers 1986; Sultan 2001). plastic response. Whether it is the differentiation of new In addition, it is hypothesized that competitive behaviours vascular strands from a growing bud (Sachs 1981), somatic belonging to different hierarchies and categories affect competition between redundant organs, dynamic modifica- ecosystem attributes through their differential affects on tions of shoot/root ratios, or shade responses, all plastic photosynthetic efficiency and respiration rates, water-use responses can be described as ‘educated exploratory efficiency (e.g. Lucero, Grieu & Guckert 2000) and nutrient endeavours’. They are initially triggered by anticipatory cycling. cues and signals and, given time and need, modified based on the materialized eventualities and updated anticipatory information (Novoplansky et al. 1990a). Competitive metaplasticity Naturally, the precise behavioural combination assumed The present discussion suggests the need for better under- by any given plant may depend on intricate contingencies standing of higher-level metaplastic interactions between related to their evolutionary background, developmental various hierarchies and categories of competitive behav- past and operational tradeoffs. Of particular importance iours, including their possible costs, horizontal and vertical in this context is the time available for the execution of controls, signals, syndromes and cascades, operational further plastic modifications. Insufficient time is expected tradeoffs and ecological implications. 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 Allelopathic behaviour? expected that short-living plants or organs will only demon- In spite of traditional scepticism, evidence for direct com- strate large plastic modifications at the beginning of their petitive 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 Abraham W.C. & Bear M.F. (1996) Metaplasticity: the plasticity of 2003; de Kroon et al. 2003). Although a few studies have synaptic plasticity. Trends in Neuroscience 19, 126–130. demonstrated dual defensive-allelopathic effects of various Ackerly D. & Bazzaz F.A. (1995) Leaf dynamics, self-shading and carbon gain in seedlings of a tropical pioneer tree. Oecologia inducible plant metabolites (Lovett & Hoult 1995; Tang 101, 289–298. et al. 1995; Callaway, DeLuca & Belliveau 1999), to the best Ackerly D. & Sultan S.E. 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