Download 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
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
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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
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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
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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
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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. The study was supported in part by a research
grant from the Israel Science Foundation. This is publication no. 638 of the Mitrani Department of Desert Ecology.
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Received 16 February 2009; received in revised form 25 February
2009; accepted for publication 25 February 2009
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 726–741