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D V A
The Mechanisms and
Consequences of Interspecific
Competition Among Plants
Erik T. Aschehoug,1 Rob Brooker,2 Daniel Z. Atwater,3
John L. Maron,4 and Ragan M. Callaway4,5
1
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803;
email: [email protected]
2
The James Hutton Institute, Aberdeen AB15 8QH, Scotland, United Kingdom
3
Department of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Institute
and State University, Blacksburg, Virginia 24061
4
Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
5
The Institute on Ecosystems, The University of Montana, Missoula, Montana 59812
Annu. Rev. Ecol. Evol. Syst. 2016. 47:263–81
Keywords
The Annual Review of Ecology, Evolution, and
Systematics is online at ecolsys.annualreviews.org
conditionality, demography, indirect effects, biogeography, plant
competition, resource competition
This article’s doi:
10.1146/annurev-ecolsys-121415-032123
c 2016 by Annual Reviews.
Copyright All rights reserved
Abstract
During the past 100 years, studies spanning thousands of taxa across almost
all biomes have demonstrated that competition has powerful negative effects
on the performance of individuals and can affect the composition of plant
communities, the evolution of traits, and the functioning of whole ecosystems. In this review, we highlight new and important developments that
have the potential to greatly improve our understanding of how plants compete and the consequences of competition from individuals to communities
in the following major areas of research: (a) mechanisms of competition,
(b) competitive effect and response, (c) direct and indirect effects of competition, (d ) population-level effects of competition, (e) biogeographical differences in competition, and ( f ) conditionality of competition. Ecologists
have discovered much about competition, but the mechanisms of competition and how competition affects the organization of communities in nature
still require both theoretical and empirical exploration.
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INTRODUCTION
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Competition is fundamental to community formation (Gause 1934), evolution (Hutchinson 1959),
and ecosystem function (Tilman et al. 2014) and underpins much of the major ecological theory
of the last century. There have been a number of broad reviews of plant competition (Connell
1983, Schoener 1983, Grace & Tilman 1990, Goldberg & Barton 1992) and many more focused
summaries of specific topics such as belowground competition (Casper & Jackson 1997), the
influence of competition on evolution (Thorpe et al. 2011), and methods related to the study of
competition (Gibson et al. 1999). We know from a long history of study that plant competition
is ubiquitous and often has strong impacts on individual fitness and the ways species assemble
into communities. Rather than a comprehensive review of the enormous breadth of work on
plant competition, we highlight advances and new insights within the major areas in which work
has focused: (a) mechanisms of competition, (b) competitive effect and response, (c) direct and
indirect effects of competition, (d) population-level outcomes of competition, (e) biogeographical
differences in competition, and (f ) conditionality of competition. Given past confusion and debate
(Harper 1977, Grace 1991) regarding how competition is defined, particularly with respect to
mechanisms (species level traits) versus outcomes (fitness effects), here we define plant competition
as the ability of individuals to usurp resources or otherwise suppress their neighbor’s fitness and
include both resource and interference competition.
MECHANISMS OF COMPETITION
At its most basic level, competition between plants is driven by the traits that allow plants to capture
resources and monopolize space. Therefore, understanding the mechanisms that enable plants to
compete for limiting resources can foster better predictions regarding competitive outcomes and
the consequences of competition.
Resource Competition
Resource competition can be considered sensu stricto “the capture of essential resources from a
common, finite pool by neighboring individuals” (Trinder et al. 2013, p. 919). Importantly, this
definition includes the direct use of common resources, the indirect effect of one plant on the
availability of a resource to its neighbor (Goldberg 1990), and processes such as resource supply
preemption. This defines resource competition as a process driven by particular mechanisms
(Trinder et al. 2013), and in turn this process has distinct outcomes such as reduced biomass,
reproduction, and persistence. Commonalities to all resource capture strategies exist in the face of
competition: (a) plants generally attempt to capture resources before their neighbors (preempt),
and (b) plants preferentially invest in structures that enable capture of the resources in highest
demand, resulting in trade-offs (e.g., greater shoot growth at the expense of root growth) that can
affect their ability to obtain other resources and compete. In this section we focus on new advances
in understanding the mechanisms by which plants compete for light, water, and soil nutrients and
how these mechanisms affect competitive ability.
Light. Competition for light is perhaps the simplest form of resource competition because light is
unidirectional and highly predictable in supply compared with water and soil nutrients. Preemption of light (Craine & Dybzinski 2013) is achieved by a plant positioning its leaves between its
neighbors and the light source by growing taller, earlier, faster, or all three. Therefore, key traits
for light competition include phenology, height, and relative growth rate. Light competition is
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also size asymmetric because larger plants get a disproportionately greater share of available light
(Hautier et al. 2009).
However, competition for light can be surprisingly complex. Recent research has shown that in
areas where productivity is high, shading by competitors can induce a shade avoidance syndrome
(SAS) (Pierik et al. 2013). Changes in the quality of light reaching leaves, such as the red:far red
ratio, are signaled through plant phytochrome photoreceptors (Pierik et al. 2013), which initiate
elongation of hypocotyls, internodes, and petioles through cell expansion and cell division. Ultimately, SAS enables shaded leaves to be positioned in patches of improved light quality and leads
to increased competition for light among neighbors. Light competition can also affect competitive
ability. The need to preempt light in the face of competition selects not only for taller plants but
also for a greater investment in leaf area than is needed to maximize light collection when not
in competition (Craine & Dybzinski 2013). Increased height and leaf area results in reduced net
carbon gain per individual plant but allows the plant to suppress its neighbors. Greater investment
in stems and leaves and reduced potential carbon gain driven by the need to preempt light capture
by neighbors may also reduce a plant’s ability to acquire water and soil nutrients and result in a
diminished overall competitive ability.
Water. Although low water availability strongly limits productivity in most ecosystems, our understanding of the mechanisms of competition for water remain relatively poor. Generally, plants
have two strategies for dealing with competition for water: (a) invest in traits that minimize competition through rapid uptake (low water use efficiency) and preemption, and (b) increase water
use efficiency to increase competitive ability.
Plant species from semiarid and arid regions minimize competition for water via temporal
and spatial niche partitioning (Fowler 1986, Casper & Jackson 1997). For example, woody and
graminoid species often access water from different depths (Ehleringer et al. 1991), and rooting
depth or placement may be more important than the overall size of the root system when a plant
competes for water (Padilla & Pugnaire 2007). In savannas, more shallowly rooted grass species
preempt water pulses from reaching more deeply rooted tree or shrub species (Fowler 1986 and
references therein), but competition between deep- and shallow-rooting species can increase when
deep-level water reserves are not replenished (McIntyre et al. 1997). The ability to use soil water
rapidly appears to provide substantial competitive advantages (DeLucia et al. 1988, Callaway et al.
1996). In addition to rapid uptake, osmoregulation that lowers cell water potentials can maintain
uptake rates even when soils are dry (Casper & Jackson 1997).
High water use efficiency and the capacity to tolerate low soil water availability are thought to
be key traits involved in drought tolerance. However, intense competition for water resources may
also select for higher water use efficiency (Craine & Dybzinski 2013) because it allows individuals
to competitively exclude neighbors (DeLucia et al. 1988). But increasing water use efficiency
also reduces water uptake and flow through the soil, which affects the uptake of other limiting
resources such as soluble soil nutrients (Herron et al. 2010) and the photosynthetic capture of
carbon (Huxman et al. 2008), which in turn affects overall competitive ability.
Soil nutrients. Competition for soil nutrients is more complex than competition for light or
water, because each nutrient has a particular dynamic that varies with soil properties. Therefore,
this section provides a brief overview of a complex topic; for more detail see works by Casper &
Jackson (1997), Cahill & McNickle (2011), Pierik et al. (2013), and Hodge & Fitter (2013).
Acquiring soil nutrients creates depletion zones around roots (Tinker & Nye 2000). This root–
soil interface is critical for soil resource acquisition, particularly for nutrients such as P, which has
low diffusion rates and is not acquired via mass flow. Preemption of soil nutrients requires active
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proliferation of fine roots and root hairs into resource patches (Kembel & Cahill 2005) in order to
monopolize the resource pool (Hodge & Fitter 2013, Pierik et al. 2013). High root density increases
the root–soil interface of a species and can provide competitive advantages (Hodge et al. 1999).
However, competition for nutrients may not simply be a race to grow more roots. Van Vuuren
et al. (1996) found that isolated Triticum aestivum growing in a 15 N-enriched patch acquired most
N before full root proliferation. Likewise, in a study of P uptake in sagebrush steppe, Caldwell et al.
(1991) found that root abundance alone did not explain the level of nutrient uptake by individuals.
Root development and patch exploitation can also be regulated by whole-plant nutrient status
(Pierik et al. 2013 and references therein), and so the root proliferation–resource pool capture
relationship does not appear to be simply size dependent. This point is important because it
challenges previous assumptions about the predominance of size-asymmetric competition.
Interactions among different mechanisms of resource uptake. Most research has focused
on how plants compete for a single resource; consequently, exploring the interactive effects of
simultaneous competition for multiple resources is an important challenge for ecologists. For example, acquisition of one specific resource can affect the need for, or availability of, other resources.
Hautier et al. (2009) found that eutrophication of species-rich European grasslands decreased biodiversity because of greater light competition. Cahill (1999) found complex relationships between
above- and belowground competition depending on the availability of soil resources. Similarly, the
uptake of water, nutrients, and CO2 can also be tightly coupled (Schwinning & Kelly 2013) with
reduced availability of water, leading to stomatal closure and reduced CO2 movement into the leaf.
In addition, reduced water availability may affect nutrient uptake rates because of slower nutrient
diffusion (Tinker & Nye 2000) and uptake processes mediated by soil communities (Herron et al.
2010). These examples demonstrate that competitive mechanisms and their general effects are
likely to interact.
New approaches to resource competition. A major mechanistic issue to address in competition
research is the direct measurement of resource capture. A better understanding of the relationship
between the mechanisms and outcomes of competition, a problem raised by Casper & Jackson
(1997), needs to be developed. In this context, little is known about the temporal dynamics of competition (Trinder et al. 2013), which improve insight into both which species are more competitive
and why. Isotope pool dilution and the use of radioisotopes may be difficult to apply, but there are
new techniques to track plant nutrient uptake and changes in resource pools and to assess plant
responses to competition. For example, Pierik et al. (2013) noted that next-generation sequencing
makes it feasible to move from studies of nutrient dynamics and competition in Arabidopsis to
species with other life histories and traits also important for competition. These techniques would
allow us to assess resource limitation and capture with a much greater temporal resolution and
perhaps in a nondestructive manner.
Interference Competition
Interference competition among plants occurs when plants directly inhibit their neighbor’s ability to acquire resources or grow. Territoriality is well studied in animals, but only recently have
ecologists investigated territoriality among plants. The most widely studied mechanism for interference is allelopathy, or biochemically mediated interactions among plants. The study of
allelopathy in plants during the last 20 years has led to an accumulation of robust evidence that
(a) plants chemically interact with their neighbors and (b) these interactions can greatly impact
individual performance and community structure (Reigosa Roger et al. 2006). Some of the best
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mechanistic insights for how allelochemicals are produced and used come from two well-studied
systems, Sorghum and Juglans (walnut trees).
Sorgoleone is a major component of root exudates from sorghum species (e.g., Sorghum bicolor,
Sorghum halepense) that impairs several molecular target sites, including photosynthetic electron
transport (Dayan et al. 2010), resulting in reduced competitive ability in neighbors. Sorgoleone
is produced and compartmentalized in and exuded from root hairs, where it can accumulate in
very high concentrations (Dayan et al. 2010), but how the roots of other species take it up is
unclear (Dayan et al. 2009). Thus, how the allelochemical moves to leaves and enters chloroplasts
of adult plants remains a mystery. Furthermore, conditionality in the effects of sorgoleone can
occur because of its highly hydrophobic nature, its adsorption to soil particles, and the effect of
microorganisms (Dayan et al. 2010).
Species in the genus Juglans (walnut trees) have been thought to poison other plant species
for millennia (Willis 2000). Some species of Juglans contain large amounts of juglone, a naphthoquinone, which is perhaps the most commonly studied allelopathic chemical in ecology. Many
studies show that juglone inhibits germination and the growth of other plants (Willis 2000). A
fascinating aspect of juglone-based interactions is the conditionality of its effects, including variation among Juglans species in production, seasonal differences in concentration, species-specific
response to the compounds, and effects that correspond with different soil conditions and light.
A more complete understanding of allelopathic interactions, unlike for general competitive
effects defined above, is limited by weak links between the excellent information on biochemistry
in lab experiments and the actual function and relative importance of individual or suites of
biochemicals in the field.
COMPETITIVE EFFECT AND RESPONSE
Competitive ability in plants has two components: (a) the ability to suppress a neighbor, or competitive effects, and (b) the ability to tolerate a neighbor’s competitive effects, or competitive
response (Goldberg 1990). When two plants interact, the effect and response abilities of both
competitors determine the outcome of competition, measured as the overall performance of each
species (Gibson et al. 1999).
Our understanding of how functional traits influence competitive effect and response is still
in its infancy. Strong competitive effects have been linked to high growth rate, production of
harmful litter and allelochemicals, and most importantly, size (Goldberg 1996, Wang et al. 2010).
Strong competitive responses have been associated with traits such as root development and seed
size, although correlative links between traits and competitive response have often been inconsistent. The difficulty in connecting functional traits to variation in competitive response may
be because competitive response is more contingent on abiotic conditions and neighbor identity
than competitive effect (Wang et al. 2010). A better linking of particular mechanisms of competition to competitive effects and responses could yield large dividends for further understanding
competitive outcomes.
Resource competition models have generally predicted a positive correlation between the
traits that improve resource capture and competitive effect and responses (Chesson 2000). In
other words, plants good at acquiring resources are also good all-around competitors. But other
theoretical models predict that tolerance and suppression will be negatively correlated: Traits
that improve tolerance of competition reduce the ability of a plant to suppress its neighbors
(Goldberg 1996). Empirical studies have not been able to resolve the relationship between tolerance and suppression, with some reporting positive correlations (e.g., Willis et al. 2010) and
others no correlation (e.g., Cahill et al. 2005, Wang et al. 2010).
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Whether competitive effect and response are correlated is important because if they are independent components of competitive ability they can respond separately to natural selection and
drive much more complex ecological consequences. Classic views of competitive effect and response posit that when competition occurs between competitors of equal size, effect and response
contribute equally to overall competitive ability (Goldberg 1990). However, this perspective on
competitive ability may be true only when competition is between two individuals (Atwater 2012).
Instead, when many individuals compete at the same time, the increased number of interactions
among all competitors favors tolerance over suppression because when a plant tolerates competition, the benefit of the competitive response is reserved entirely for that individual. However,
when a plant suppresses a neighbor, the benefit of the competitive effect is shared among all other
individuals competing nearby. This finding raises a new and crucial dimension to competitive
ability: Natural selection may favor response over effect when plants compete in complex multispecies assemblages (Atwater 2012). MacDougall & Turkington (2004) found that the ability of a
species to tolerate competition is a better predictor of field performance than the ability to suppress neighbors. Furthermore, selection caused by competitors appears to improve the response
of one species to another but not the effects on neighbors (Rowe & Leger 2011)—a finding that
is also supported by simulation models (Atwater 2012).
When one focuses on competitive effect and response as two distinct aspects of competition,
several key questions emerge: (a) How do effect and response contribute to overall competitive ability? (b) How do effect and response separately influence community dynamics? (c) What traits drive
competitive effect versus response? and (d ) Can effect and response evolve independently? Answers
to these questions could substantially improve our overall understanding of competitive dynamics.
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DIRECT AND INDIRECT EFFECTS OF COMPETITION
Historically, most research on competition among plants has focused on individuals and the
negative direct effects of competition. For example, community assembly theory (Weiher & Keddy
1999) seeks to predict how direct competitive interactions among species influence the structure
and dynamics of communities. Much of this theory assumes that plant competition is transitive
(Keddy & Shipley 1989), which means that there is a strict hierarchy in competitive ability among
all species in a given pool. The major conceptual outcome of hierarchical assembly rules is that
the best competitor in the hierarchy eventually competitively excludes all other. This is only
avoided under nonequilibrium conditions, such as disturbance, or when consumers or abiotic
heterogeneity limit competitive dominance.
Because plants typically interact in a multispecies neighborhood with many individuals, the
potential exists for indirect interactions to be an underappreciated but important driver of competitive outcomes (Miller 1994, Aschehoug & Callaway 2015). Indirect interactions occur when
the impact of one species on another is mediated by a third species (Wootton 1994) and therefore
occur only among groups of species. Indirect interactions can be important because they may lead
to nontransitive competition, which is an alternative to hierarchical assembly rules. Indirect interactions can occur within or across trophic levels and can have positive or negative effects on species
[reviewed by Wootton (1994)]. Nontransitive competition arises through a series of special-case
pairwise interactions that form a competitive loop (e.g., rock-paper-scissors). Competitive loops,
described mathematically as A > B, B > C, but C > A, result in species C having an indirect positive
effect on species B through a direct negative effect on species A (Figure 1a). Competitive loops can
vary in length and intensity and can be nested among groups of species, all factors that influence
the overall impact of nontransitive competition on community structure (Laird & Schamp 2006).
Importantly, nontransitive competition can counter the competitive exclusion principle.
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b
Figure 1
(a) Nontransitive interaction and (b) indirect facilitative interaction. Solid arrows represent direct
interactions, and dashed arrows indicate indirect interactions. Black arrows represent negative, competitive
interactions, and red arrows represent positive, facilitative interactions. Redrawn from Aschehoug &
c 2015, The University of Chicago Press.
Callaway (2015). Nontransitive competition and its effect on plant community assembly has strong theoretical
support. For example, models indicate that nontransitive interactions among groups of competitors
create a form of indirect facilitation that can promote or sustain coexistence among competitors
(Laird & Schamp 2006). Soliveres et al. (2015) used species co-occurrence patterns to estimate the
prevalence of nontransitive competition in natural communities. Their results suggest that nontransitive competition is likely to be widespread and common but largely dependent on temporal
abiotic heterogeneity. Thus, nontransitive competition among plants may be a product of the
conditionality of ecological interactions and not the strict competitive ability of individual species.
Despite strong theoretical support, very little experimental support for nontransitive interactions
among plants has been found (although see Lankau et al. 2011). This lack of support may simply
be because of the inherent difficulty of measuring such complex interactions in nature. Regardless,
nontransitive competition has the potential to have dramatic effects on the way plants assemble
into communities.
Competitive interactions among groups of species can also result in positive indirect effects
without the formation of competitive loops. The last 30 years have seen a developing body of theory
highlighting the importance of indirect facilitative interactions (Figure 1b) (Stone & Roberts 1991,
Miller 1994, Aschehoug & Callaway 2015). In these and other studies, shared competitors dampen,
or even reverse, the negative impact of one species on another (i.e., “an enemy of my enemy is a
friend of mine”). For example, Levine (1999) found that Carex nudata had direct negative effects
on Conocephalum conicum when they were competing in pairs, but this reversed to a net positive
effect via indirect facilitation when a third species, Mimulus guttatus, was present. In a largescale, community-level test of indirect effects, Aschehoug & Callaway (2015) built experimental
communities of species in a replacement series design that allowed comparison of competition
intensity among species when they were interacting in pairwise and multispecies assemblages. They
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found that the strong direct negative effects of competition between pairs of species was highly
attenuated when species competed simultaneously in groups because of the presence of indirect
facilitation. When species were competing in pairs, 8 of 16 interactions were significantly negative,
but when species were competing in groups of species, only 4 of 16 interactions were significant.
Null model comparisons of the number of significant interactions found pairwise competition
to be strong and frequent, but competition between species when in complex groups was weak
and infrequent. This suggests two things: (a) that pairwise interactions greatly overestimate the
competitive effects of species and (b) that competition among species in complex communities
may promote coexistence rather than lead to competitive exclusion.
This disconnect between competition in pairs and competition in communities may result from
additive effects. That is, competition between species when in multispecies groups may be the sum
of all of the interactions (direct and indirect). Weigelt et al. (2007) measured the effect of one-, two-,
and three-species neighborhoods on a target species to test the assumption that competitive effects
in multispecies communities are additive. Yield density models suggested that competitive intensity
in most multispecies assemblages could be predicted by pairwise interaction outcomes. However,
certain combinations of species showed significant deviations from the predictions of the model
generated from pairwise interactions. But when nonadditive parameters were added to the model,
the predictive power of the model increased significantly, indicating that indirect interactions
among specific combinations of species can establish nonadditive effects that are difficult to predict
from pairwise-derived models. Dormann & Roxburgh (2005) found that Lotka-Volterra (LV) type
models built from pairwise outcomes did not accurately predict biomass and coexistence for threespecies mixtures in five out of the six combinations grown. Similarly, LV models did not predict
biomass and coexistence in an experimental seven-species mixture. However, when a nonadditive,
or higher order, competition coefficient was added to the model, predictions more closely matched
experimental outcomes.
Despite the fact that indirect effects resulting from competition appear to be ubiquitous among
plants, theory incorporating indirect effects into community assembly theory is not well developed. The pervasive and cascading effects of indirect interactions challenge our foundational
ideas on competition, such as the competitive exclusion principle and the need for niche separation for stable coexistence in communities. To advance our understanding of how competition
governs community assembly, a more complete understanding of when indirect effects are important (e.g., low- versus high-productivity systems) is required. In addition, the ability to accurately predict the role of competition in communities using models hinges on an improved
understanding of when the indirect effects of competition are additive versus nonadditive. To
achieve this, future tests of competition need to move beyond the simplistic view that plants interact in pairs to a more holistic view of the suite of interactions plants experience in species-rich
communities.
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IMPACTS OF COMPETITION ON PLANT POPULATIONS
Hundreds of studies have examined the impacts of interspecific competition on the performance
of individual plants, but these studies have told us little about how such competitive effects ramify
to populations. Studies of plant competition typically assess how competition influences individual
plant performance. Biomass is typically the response variable in these experiments because it is
convenient to measure and because biomass is strongly correlated with plant reproduction and
overall fitness. Furthermore, for clonal species, changes in biomass directly reflect plant abundance.
Yet for nonclonal species, several reasons explain why these short-term measures of competitive
impacts on plant biomass do not easily extrapolate to effects of competition on plant abundance
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or population dynamics. First, in short-term experiments, the reductions in plant biomass due to
competition often occur over a very small range of biomass values relative to what plants can achieve
in the field and might not translate to realistic effects on plant survival or reproduction. Second,
even competitive effects that substantially reduce plant biomass or fecundity might not influence
the number of individuals in a population in future generations. Lastly, concomitant decreases in
density-dependent interactions can compensate for reduction in survival in any one year. For these
reasons, the most informative studies on the population-level impacts of competition are those
that either empirically evaluate how competition influences plant abundance across generations
or examine competitive effects on all life stages so that future abundance can be forecast using
demographic models. The few studies that have taken this approach have made important advances
in how we understand the ecology of competition.
Demographic Models and Competition Across Life Stages
Experiments combined with stage-based population models can evaluate the effects of competition
on the demography of a target species across life stages. Demographic data are used to parameterize population models to forecast the consequences of competition for population growth.
One advantage of this approach is that it allows integration of the impacts of competition across
all life stages. Another is that it enables one to forecast longer-term effects of competition across
generations. Finally, one can gain insight into which demographic component is influenced by
competition and which most influences competitive impacts on future population growth. Using
this approach, Fréville et al. (2005) performed two different experiments, one to measure effects
of competition on germination rate and another to examine how competition influenced all other
vital rates. Combining data from these two experiments, they estimated that interspecific competition reduced asymptotic population growth (λ) for three focal species by more than 90%. The
difference in growth rate due to competition was driven by the fact that competition dramatically
reduced fecundity (Fréville et al. 2005). Studies using a similar approach have forecast how exotic
species competitively influence native plant population growth (Thomson 2005) and how competition and herbivory jointly influence native versus exotic thistle population growth (Tenhumberg
et al. 2015).
Experiments, demographic data, and stage-based models have been broadly used to examine
effects of other interactions, such as herbivory, on populations (Maron & Crone 2006). More
work of this type is needed to better understand plant–plant interactions (Maron et al. 2010) and
to better generalize how competition varies in its population impacts across species, functional
types, and systems. Such approaches can be especially valuable in studies of competitive effects on
long-lived plants.
Effects of Competition on Plant Distribution
If competitive effects are strong enough, some species can be competitively excluded from particular habitats. For example, Gurevitch (1986) found that the perennial bunchgrass Stipa neomexicana
was severely limited in distribution by competition for water with other grass species along a gradient. Other studies have shown that competition with perennial grasses in seasonally flooded sites
can restrict a shrub species to drier areas (Sánchez & Peco 2004) and that grasses in resource-rich
moist meadows are competitively excluded from nearby resource-poor dry meadows (Theodose
& Bowman 1997). Shrubs on resource-rich andesitic soils were found to competitively exclude
Pinus ponderosa seedlings that occurred naturally on adjacent resource-poor andesite soils (Callaway
et al. 1996). Other studies have found that competition can influence the distributional patterns of
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plant species in tidal salt marshes (Pennings et al. 2005), and interspecific competition is thought to
prevent plants adapted to serpentine soils from colonizing nearby nonserpentine soil communities
(Brady et al. 2005).
These examples indicate that competitive interactions can play an important role in influencing
plant distributions at relatively small spatial scales, but whether this is true at regional scales is
unclear. Theory has long posited that competition is important in limiting geographic ranges
of species (Price & Kirkpatrick 2009), and competition may influence how plants adjust their
distributions in response to future climate change (Tylianakis et al. 2008). Although studies have
evaluated the extent to which interspecific competition might limit distributional patterns of plants
(Sexton et al. 2009), more experimental tests are needed. Where competition has been examined
in relation to other biotic interactions, facilitation appears more important than competition in
affecting plant distributions (Stanton-Geddes et al. 2012).
Competition can also influence community composition and the relative abundance of component species if it significantly regulates recruitment into communities (see Weiher & Keddy
1999). Competition can act as a local filter, which can influence variation in the relative rates
of recruitment among component species, thereby affecting community structure. Seed addition
studies indicate that the removal of competitors (by a disturbance treatment) enhances recruitment of new species (Maron et al. 2012), suggesting that competition at the local scale can be an
important determinant of community composition.
By monopolizing microsites, resident vegetation can competitively limit the recruitment of
conspecifics and other species. But are these effects species specific? A few studies indicate that
removal of the same amount of dominant versus subdominant or rare residents results in different
competitive effects on recruitment. Thus, removal of many rare species and the presumed opening
of a broader suite of niches may reduce competitive resistance to colonization more than removing
a dominant species would. Gilbert et al. (2009) examined this possibility by adding seedlings to
plots and found that resident competitive effects against added seedlings were caused by one
dominant species instead of many rarer species combined. In a similar experiment that involved
adding seeds rather than seedlings to plots, Pinto et al. (2014) found that removing dominant
plant biomass or an equal amount of biomass across several rarer species had similar impacts on
the diversity of added species. Finally, Lyons & Schwartz (2001) found that by removing less
common species, assemblages became more invasible, suggesting that competitive interactions
involving rare species limited recruitment of new colonists. Although dominant species are often
considered the superior competitors (Facelli & Temby 2002), based in part on mass effects, the
combined effects of subordinate or even rare species in affecting recruitment into local assemblages
are still unclear. Furthermore, most seed addition experiments are of relatively short duration,
leaving open the question of how patterns of recruitment, as affected by competition, translate to
longer-term effects on plant dynamics and community composition.
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The Need for a Population-Level Perspective
Many models extrapolate the impacts of interspecific competition to populations, but few empirical
studies have directly measured the effects of competition on population-level parameters such as
fitness and recruitment. Importantly, broad themes in plant competition, for example, understanding how the strength of competition varies across gradients in productivity, would benefit from a
population perspective rather than focusing only on individual responses. Long-term, populationlevel impact studies have been central to our understanding of how other interactions involving
plants, such as herbivory, influence plant dynamics (Maron & Crone 2006), but these sorts of
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experiments do not have strong parallels in the competition literature. Thus, many questions
regarding the population-level impacts of competition remain. For example, highly abundant
species are often considered superior competitors to less abundant species (Grime 2001), but
emerging work suggests that rare species can have surprisingly large impacts on ecosystems
(Mariotte 2014). Therefore, it is of increasing interest to understand competitive dynamics
among species that differ in relative abundance and how this, in turn, affects reproduction and
recruitment within communities.
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INVASIVE SPECIES AND BIOGEOGRAPHIC DIFFERENCES
IN COMPETITION
Plant species that establish in new, non-native ranges offer a unique opportunity to understand
competition within the context of the long-term evolutionary trajectories of communities. The
fact that some species competitively dominate new recipient communities in ways that differ dramatically from their native range raises the question of whether evolutionary history can drive
the competitive interactions between native and invasive species. A great deal of work has focused
on whether escape from specialist natural enemies helps tip the competitive balance in favor of
invasive species, but so far, only a few field studies have explored whether escape from plant competition explains the change in performance of an invasive species in its introduced versus native
range. Callaway et al. (2011) found that removal of surrounding plants in Europe increased the
biomass and reproduction of resident spotted knapweed (Centaurea stoebe) individuals, indicating
strong competitive effects on knapweed in areas where it is native. In contrast, removal of surrounding vegetation in North America had no significant effects on knapweed performance, a
result consistent with greenhouse experiments (Sun et al. 2014). Further, the notion that invaders
may gain an advantage from competitor escape was tested in a diversity–invasibility field experiment performed by Sun et al. (2015). They assembled native grassland communities in Switzerland
that varied in native plant diversity, in a manner consistent with a similar experiment conducted
in knapweed’s nonnative range in Montana (Maron & Marler 2008). Both experiments added
spotted knapweed seeds to plots varying in native diversity. In Montana, knapweed prolifically
invaded species-poor assemblages, but competition reduced knapweed’s ability to colonize diverse assemblages. In Switzerland, where knapweed is native, however, knapweed failed to invade
any assemblage regardless of community diversity, indicating far greater competitive resistance
in the native range. Moreover, all levels of diversity had powerful negative effects on the growth
of knapweed seedlings (Sun et al. 2015). Thus, unlike in the introduced range, even low-diversity
communities in knapweed’s native range offered substantial competitive resistance to knapweed
colonization.
Just as the impact of surrounding vegetation on invasives may differ biogeographically, so
too may the competitive impact of invaders on natives differ. For example, some studies have
shown that a similar amount of exotic cover leads to greater reductions in native cover (Ni et al.
2010, Callaway et al. 2012), native richness (Kaur et al. 2012, Ledger et al. 2015), and diversity
(Ledger et al. 2015) in nonnative compared with native communities. Although these studies are
correlative, they suggest that some invasives have greater competitive impacts (on a per capita or
percentage cover basis) in introduced ranges than in native ranges.
The mechanisms that drive these biogeographic effects of competition remain obscure. Therefore, future work that examines interactions between exotics and natives in a biogeographic context
has a great deal of potential to expand our understanding of both the mechanisms of competition
and the role evolution plays in dictating the outcomes of competition.
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CONDITIONALITY AND COMPETITION
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One of the primary difficulties in scaling competition between individual plants up to populations
and communities is strong conditionality in competitive outcomes. Biotic and abiotic contexts
affect the strength and direction of competition, and understanding such conditionality is crucial
for predicting when, where, and how competition affects the distribution and abundance of species
and organization of communities (Brooker et al. 2005, Chamberlain et al. 2014).
Previously, we explored how additional competitors may alter the outcome of competitive
interactions through indirect effects—a form of biotic conditionality. Other factors, such as herbivory and abiotic heterogeneity, are also well studied and have strong effects on competitive
outcomes. For example, when consumers prefer some species to others, competitive interactions
can be altered (Louda et al. 1990). Additionally, as resource supply changes in space and time, the
outcome of competitive interactions can also change (Rebele 2000, Besaw et al. 2011). In this section, we restrict our assessment of the literature to recent or overlooked advances in understanding
competitive conditionality.
Environmental Gradients: The Importance and Intensity of Competition
The use of environmental gradients in plant ecology has contributed to understanding the contradictory predictions of the two major theories of competition among plants. Resource ratio theory
(Tilman 1982) predicts that the role of competition should remain constant across environmental
gradients, although the focal resource may vary. In contrast, life history trade-off theory (Grime
2001) predicts that competition should be strong in high-productivity, low-stress areas and weak
in low-productivity, high-stress areas. Environmental gradients provide a good opportunity to
test these predictions experimentally.
To our knowledge, the first relevant experimental test of these ideas found that competition
at the high-productivity end of a topographic gradient excluded S. neomexicana and limited the
species to the more stressful, low-productivity ridges (Gurevitch 1986). A number of other studies
have found similar increases in competition with increasing productivity (e.g., Twolan-Strutt &
Keddy 1996), and all of these studies support the predictions of Grime (2001). In contrast, Reader
et al. (1994), comparing the growth of Poa pratensis with and without neighbors over a gradient
of productivity, concluded that competition did not significantly decrease with decreasing productivity, thereby supporting the predictions of Tilman (1982). However, Brooker et al. (2005)
argued that the fundamental distinction between Tilman’s theory and Grime’s theory was a focus
on the intensity (absolute impact) versus the importance (impact relative to the total environment) of competition. They proposed that Grime’s theory focused on competition’s importance,
whereas Tilman’s focused on its intensity, and that these need not be correlated. The results from
experimental studies relating environmental gradients to the role of competition, and therefore
support for either theory, depend on whether metrics of intensity or importance are used. Reanalyzing Reader and colleagues’ (1994) data, Brooker et al. (2005) found that the importance of
competition, in contrast to the intensity, declined substantially with decreasing productivity and
that importance and intensity do not always correlate. Clearly delineating between importance
and intensity may help reconcile important paradigms for how competition varies in nature.
Effects of Fungal Mutualists and Soil Biota on Competition
Fungal mutualists may improve the competitive ability of a species (Harnett et al. 1993)
through mechanisms such as increased nutrient capture ( Johnson et al. 2010) and more intense
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interference (Aschehoug et al. 2014). However, the relationship between plants and fungi can
be highly context dependent and may shift from mutualist to parasitic relationships based on
environment (Saikkonen et al. 1998). Such dramatic changes in plant–microbe relationships
are likely to have equally dramatic effects on a plant’s competitive ability. For example, some
plant species that are not highly dependent on arbuscular mycorrhizal fungi can exhibit stronger
competitive effects without the mutualist compared with when it is present (Marler et al. 1999).
In addition, mycorrhizal networks can increase the negative effects of allelopathy by reducing
the distance between roots required for allelopathic compound deposition and increasing the
total concentration of chemical exudates in root tissues (Barto et al. 2011), resulting in reduced
competitive ability for plants with mycorrhizal mutualists.
Fungal endophytes can increase the competitive ability of plants, most commonly in coolseason grasses (e.g., Clay & Holah 1999) but also in forbs (Aschehoug et al. 2012). For example,
in a test of only a tiny fraction of the endophytic fungal taxa that infect C. stoebe, Aschehoug
et al. (2012) found that two fungal endophyte phylotypes enhanced the competitive effects of
C. stoebe on North American grass species. One endophyte increased the competitive ability of
C. stoebe without increasing its size, suggesting that the effects of mutualists on competitive ability
are not necessarily related to their direct effects on hosts. Other studies have found that endophyte
infection can increase the intensity of a species’ competitive effects (Saari & Faeth 2012), whereas
others have found that endophytes affect plant traits in ways that may reduce their competitive
ability (Faeth et al. 2004).
Soil biota contain consumers and mutualists but are often treated holistically because their
effects on plants cannot be easily reduced to a single taxa (see Callaway et al. 2011) and many
of the microbes are not culturable. Plant–soil feedbacks are pervasive, can strongly influence
plant performance, and have the potential to either increase or decrease competitive interactions
among plant species. Most feedbacks between soil and plants in native systems have negative
consequences for plants (Kulmatiski et al. 2008); thus, species that are relatively more susceptible
to negative feedbacks are likely to be at a competitive disadvantage. However, the few studies that
have taken an integrated approach to these fundamentally important interactions have found a
wide range of results. Bever (1994) found that competition was not affected by negative plant–soil
feedbacks, whereas other work has shown that negative feedbacks can be stronger when plants are
competing than when they grow alone (Pendergast et al. 2013). Even within a single experiment,
Casper & Castelli (2007) found almost the same range of feedback–competition interactions for
three species of C4 grasses that has been reported in the literature as a whole. For example,
Andropogon gerardii exhibited negative feedback when in competition, interspecific competition
eliminated feedback effects expressed in the absence of competition for Sorghastrum nutans, and
Schizachyrium scoparium did not experience feedbacks with soil biota. Hendriks et al. (2015) found
that each of the four plant species they tested experienced negative soil feedbacks, expressed as a
decrease in root growth in soil trained by conspecifics relative to soil trained by heterospecifics.
They also found that this reduced root growth by more dominant competitors favored inferior
competitors. However, all competition–feedback interactions were expressed only belowground.
Finally, Callaway et al. (2004) found that plant–soil feedback outcomes for the invasive C. stoebe
were highly negative in native European soils and positive in North American soils, the nonnative
range. Further, feedbacks for North American and European Festuca species were negative in
their native soils. However, in competition these plant–soil feedbacks changed. When grown with
C. stoebe, the European Festuca ovina grew larger in European soils trained by C. stoebe than in
soils conditioned by conspecifics, probably because of negative soil feedback effects on C. stoebe.
But the North American Festuca idahoensis grew better in soils trained by conspecifics than in soils
trained by C. stoebe, perhaps because of the positive plant–soil feedbacks experienced by C. stoebe
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in North American soil. Clearly, plant–soil feedbacks and competition can interact, but ecologists
have only scratched the surface of these complex, context-dependent interactions.
Trait-Mediated Interactions
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Plants can be highly plastic in an array of morphological, developmental, physiological, and biochemical traits (de Kroon et al. 2005, Metlen et al. 2009), suggesting that competitive ability is also
plastic. Variation in phenotype has important implications for how a species acclimates or adapts
to a local environment and the potential to create tremendous conditionality in the way individuals
interact. The ecological ramifications of plant phenotypic plasticity are poorly understood but are
an emerging field of research in community ecology (see review by Aschehoug & Callaway 2012).
Trait-mediated interactions arise when phenotypic plasticity affects the direct competitive
interactions of individuals (Callaway et al. 2003). No studies have explicitly examined the effects of
plasticity on direct competition between plant species. However, evidence can be pieced together
from previous work. For example, two Haplopappus species appeared to adjust the depth of their
root systems in response to belowground competition from Carpobrotus edulis (D’Antonio & Mahall
1991). This adjustment not only results in diminished access to belowground resources (Ho et al.
2005) but also allows for continued coexistence among the species.
Trait variation may also lead to important trait-mediated indirect interactions among species,
resulting in cascading interactive effects on plant community dynamics (Aschehoug & Callaway
2012). Aschehoug & Callaway (2014) found that variation in the root morphology of Quercus douglasii in response to access to water resulted in two remarkably different outcomes of competition
among understory plants. When Q. douglasii trees have deep-rooted morphologies, nonnative annual grasses in the understory are directly facilitated, and in turn they competitively exclude the
native perennial grass Stipa pulchra. However, trees with a shallow-rooted morphology reversed the
interaction by suppressing nonnative annual grasses and indirectly facilitating S. pulchra. Changes
in root morphology created conditionality in the outcome of the interactions, such that indirect
interactions promoted the coexistence of species and increased community diversity. This study is
the only known test of plasticity and indirect effects of competition. However, its striking results
demonstrate that further research on this topic has the potential to greatly improve our understanding of the conditionality of plant–plant interactions, especially in the context of changing
environments.
CONCLUSIONS
We have focused on how each of our selected topics has contributed new ideas to competition
among plants. However, several general themes have emerged frequently and warrant explicit
attention.
First, methods matter. Across all major types of plant competition studies, pairwise tests of
competition are the most common (Gibson et al. 1999). Although pairwise experiments are easy
to implement and allow for fine-scale evaluations of mechanisms and individual performance, they
have proven to be poor predictors of competition in communities. Future studies must incorporate
greater complexity in experiments in order to move beyond simplistic views of competition.
Second, timescales matter. Most competition studies tend to focus on short-term response
parameters such as within-season biomass. This focus may be suitable for assessing the outcomes
of competition for annual plants, but understanding the outcomes of competition in multispecies
and perennial plant communities requires a broader perspective (Trinder et al. 2013). This is particularly true given the well-known variation in competitive outcomes that depend on the growth
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stage and response variable measured. In addition, most seed-addition studies are of relatively
short duration, meaning little is known about how competition impacts recruitment, patterns
of community development, and relative abundance—something that can be achieved only by
long-term studies.
And third, context matters. It is important to keep in mind the relative strength of competition
compared with other local processes that influence community structure, especially environment.
Clearly, plant competition is an important determinant of community structure, but without
context that evaluates other factors, we are likely to overestimate the role competition plays in the
assembly of communities.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
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