the mechanisms and consequences of interspecific competition among plants - aschehoug...

ES47CH12-Aschehoug ARI 16 August 2016 13:55

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The Mechanisms andConsequences of InterspecificCompetition Among PlantsErik T. Aschehoug,1 Rob Brooker,2 Daniel Z. Atwater,3

John L. Maron,4 and Ragan M. Callaway4,5

1Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803;email: [email protected] James Hutton Institute, Aberdeen AB15 8QH, Scotland, United Kingdom3Department of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Instituteand State University, Blacksburg, Virginia 240614Division of Biological Sciences, The University of Montana, Missoula, Montana 598125The Institute on Ecosystems, The University of Montana, Missoula, Montana 59812

Annu. Rev. Ecol. Evol. Syst. 2016. 47:263–81

The Annual Review of Ecology, Evolution, andSystematics is online at ecolsys.annualreviews.org

This article’s doi:10.1146/annurev-ecolsys-121415-032123

Copyright c© 2016 by Annual Reviews.All rights reserved

Keywords

conditionality, demography, indirect effects, biogeography, plantcompetition, resource competition

Abstract

During the past 100 years, studies spanning thousands of taxa across almostall biomes have demonstrated that competition has powerful negative effectson the performance of individuals and can affect the composition of plantcommunities, the evolution of traits, and the functioning of whole ecosys-tems. In this review, we highlight new and important developments thathave the potential to greatly improve our understanding of how plants com-pete and the consequences of competition from individuals to communitiesin the following major areas of research: (a) mechanisms of competition,(b) competitive effect and response, (c) direct and indirect effects of compe-tition, (d ) population-level effects of competition, (e) biogeographical dif-ferences in competition, and ( f ) conditionality of competition. Ecologistshave discovered much about competition, but the mechanisms of competi-tion and how competition affects the organization of communities in naturestill require both theoretical and empirical exploration.

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Review in Advance first posted online on August 24, 2016. (Changes may still occur before final publication online and in print.)

Changes may still occur before final publication online and in print

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INTRODUCTION

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 theoryof the last century. There have been a number of broad reviews of plant competition (Connell1983, Schoener 1983, Grace & Tilman 1990, Goldberg & Barton 1992) and many more focusedsummaries of specific topics such as belowground competition (Casper & Jackson 1997), theinfluence of competition on evolution (Thorpe et al. 2011), and methods related to the study ofcompetition (Gibson et al. 1999). We know from a long history of study that plant competitionis ubiquitous and often has strong impacts on individual fitness and the ways species assembleinto communities. Rather than a comprehensive review of the enormous breadth of work onplant competition, we highlight advances and new insights within the major areas in which workhas focused: (a) mechanisms of competition, (b) competitive effect and response, (c) direct andindirect effects of competition, (d) population-level outcomes of competition, (e) biogeographicaldifferences in competition, and (f ) conditionality of competition. Given past confusion and debate(Harper 1977, Grace 1991) regarding how competition is defined, particularly with respect tomechanisms (species level traits) versus outcomes (fitness effects), here we define plant competitionas the ability of individuals to usurp resources or otherwise suppress their neighbor’s fitness andinclude 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 captureresources and monopolize space. Therefore, understanding the mechanisms that enable plants tocompete for limiting resources can foster better predictions regarding competitive outcomes andthe consequences of competition.

Resource Competition

Resource competition can be considered sensu stricto “the capture of essential resources from acommon, finite pool by neighboring individuals” (Trinder et al. 2013, p. 919). Importantly, thisdefinition includes the direct use of common resources, the indirect effect of one plant on theavailability of a resource to its neighbor (Goldberg 1990), and processes such as resource supplypreemption. 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 ofcompetition: (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 highestdemand, resulting in trade-offs (e.g., greater shoot growth at the expense of root growth) that canaffect their ability to obtain other resources and compete. In this section we focus on new advancesin understanding the mechanisms by which plants compete for light, water, and soil nutrients andhow these mechanisms affect competitive ability.

Light. Competition for light is perhaps the simplest form of resource competition because light isunidirectional and highly predictable in supply compared with water and soil nutrients. Preemp-tion of light (Craine & Dybzinski 2013) is achieved by a plant positioning its leaves between itsneighbors and the light source by growing taller, earlier, faster, or all three. Therefore, key traitsfor light competition include phenology, height, and relative growth rate. Light competition is

264 Aschehoug et al.


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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 inareas 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 redratio, are signaled through plant phytochrome photoreceptors (Pierik et al. 2013), which initiateelongation of hypocotyls, internodes, and petioles through cell expansion and cell division. Ulti-mately, SAS enables shaded leaves to be positioned in patches of improved light quality and leadsto increased competition for light among neighbors. Light competition can also affect competitiveability. The need to preempt light in the face of competition selects not only for taller plants butalso for a greater investment in leaf area than is needed to maximize light collection when notin competition (Craine & Dybzinski 2013). Increased height and leaf area results in reduced netcarbon gain per individual plant but allows the plant to suppress its neighbors. Greater investmentin stems and leaves and reduced potential carbon gain driven by the need to preempt light captureby neighbors may also reduce a plant’s ability to acquire water and soil nutrients and result in adiminished overall competitive ability.

Water. Although low water availability strongly limits productivity in most ecosystems, our un-derstanding of the mechanisms of competition for water remain relatively poor. Generally, plantshave two strategies for dealing with competition for water: (a) invest in traits that minimize com-petition through rapid uptake (low water use efficiency) and preemption, and (b) increase wateruse efficiency to increase competitive ability.

Plant species from semiarid and arid regions minimize competition for water via temporaland spatial niche partitioning (Fowler 1986, Casper & Jackson 1997). For example, woody andgraminoid species often access water from different depths (Ehleringer et al. 1991), and rootingdepth or placement may be more important than the overall size of the root system when a plantcompetes for water (Padilla & Pugnaire 2007). In savannas, more shallowly rooted grass speciespreempt water pulses from reaching more deeply rooted tree or shrub species (Fowler 1986 andreferences therein), but competition between deep- and shallow-rooting species can increase whendeep-level water reserves are not replenished (McIntyre et al. 1997). The ability to use soil waterrapidly 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 maintainuptake rates even when soils are dry (Casper & Jackson 1997).

High water use efficiency and the capacity to tolerate low soil water availability are thought tobe key traits involved in drought tolerance. However, intense competition for water resources mayalso select for higher water use efficiency (Craine & Dybzinski 2013) because it allows individualsto competitively exclude neighbors (DeLucia et al. 1988). But increasing water use efficiencyalso reduces water uptake and flow through the soil, which affects the uptake of other limitingresources such as soluble soil nutrients (Herron et al. 2010) and the photosynthetic capture ofcarbon (Huxman et al. 2008), which in turn affects overall competitive ability.

Soil nutrients. Competition for soil nutrients is more complex than competition for light orwater, 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 haslow diffusion rates and is not acquired via mass flow. Preemption of soil nutrients requires active

www.annualreviews.org • Competition Among Plants 265


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proliferation of fine roots and root hairs into resource patches (Kembel & Cahill 2005) in order tomonopolize the resource pool (Hodge & Fitter 2013, Pierik et al. 2013). High root density increasesthe 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 Vuurenet al. (1996) found that isolated Triticum aestivum growing in a 15N-enriched patch acquired mostN 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 capturerelationship does not appear to be simply size dependent. This point is important because itchallenges previous assumptions about the predominance of size-asymmetric competition.

Interactions among different mechanisms of resource uptake. Most research has focusedon how plants compete for a single resource; consequently, exploring the interactive effects ofsimultaneous competition for multiple resources is an important challenge for ecologists. For ex-ample, 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 bio-diversity because of greater light competition. Cahill (1999) found complex relationships betweenabove- and belowground competition depending on the availability of soil resources. Similarly, theuptake of water, nutrients, and CO2 can also be tightly coupled (Schwinning & Kelly 2013) withreduced 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 nutrientdiffusion (Tinker & Nye 2000) and uptake processes mediated by soil communities (Herron et al.2010). These examples demonstrate that competitive mechanisms and their general effects arelikely to interact.

New approaches to resource competition. A major mechanistic issue to address in competitionresearch is the direct measurement of resource capture. A better understanding of the relationshipbetween 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 com-petition (Trinder et al. 2013), which improve insight into both which species are more competitiveand why. Isotope pool dilution and the use of radioisotopes may be difficult to apply, but there arenew techniques to track plant nutrient uptake and changes in resource pools and to assess plantresponses to competition. For example, Pierik et al. (2013) noted that next-generation sequencingmakes it feasible to move from studies of nutrient dynamics and competition in Arabidopsis tospecies with other life histories and traits also important for competition. These techniques wouldallow us to assess resource limitation and capture with a much greater temporal resolution andperhaps in a nondestructive manner.

Interference Competition

Interference competition among plants occurs when plants directly inhibit their neighbor’s abil-ity to acquire resources or grow. Territoriality is well studied in animals, but only recently haveecologists investigated territoriality among plants. The most widely studied mechanism for in-terference is allelopathy, or biochemically mediated interactions among plants. The study ofallelopathy 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 impactindividual 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-studiedsystems, 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 electrontransport (Dayan et al. 2010), resulting in reduced competitive ability in neighbors. Sorgoleoneis produced and compartmentalized in and exuded from root hairs, where it can accumulate invery high concentrations (Dayan et al. 2010), but how the roots of other species take it up isunclear (Dayan et al. 2009). Thus, how the allelochemical moves to leaves and enters chloroplastsof adult plants remains a mystery. Furthermore, conditionality in the effects of sorgoleone canoccur because of its highly hydrophobic nature, its adsorption to soil particles, and the effect ofmicroorganisms (Dayan et al. 2010).

Species in the genus Juglans (walnut trees) have been thought to poison other plant speciesfor millennia (Willis 2000). Some species of Juglans contain large amounts of juglone, a naphtho-quinone, which is perhaps the most commonly studied allelopathic chemical in ecology. Manystudies show that juglone inhibits germination and the growth of other plants (Willis 2000). Afascinating aspect of juglone-based interactions is the conditionality of its effects, including vari-ation among Juglans species in production, seasonal differences in concentration, species-specificresponse to the compounds, and effects that correspond with different soil conditions and light.

A more complete understanding of allelopathic interactions, unlike for general competitiveeffects defined above, is limited by weak links between the excellent information on biochemistryin lab experiments and the actual function and relative importance of individual or suites ofbiochemicals in the field.

COMPETITIVE EFFECT AND RESPONSE

Competitive ability in plants has two components: (a) the ability to suppress a neighbor, or com-petitive effects, and (b) the ability to tolerate a neighbor’s competitive effects, or competitiveresponse (Goldberg 1990). When two plants interact, the effect and response abilities of bothcompetitors determine the outcome of competition, measured as the overall performance of eachspecies (Gibson et al. 1999).

Our understanding of how functional traits influence competitive effect and response is stillin its infancy. Strong competitive effects have been linked to high growth rate, production ofharmful 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 seedsize, although correlative links between traits and competitive response have often been incon-sistent. The difficulty in connecting functional traits to variation in competitive response maybe because competitive response is more contingent on abiotic conditions and neighbor identitythan competitive effect (Wang et al. 2010). A better linking of particular mechanisms of compe-tition to competitive effects and responses could yield large dividends for further understandingcompetitive outcomes.

Resource competition models have generally predicted a positive correlation between thetraits that improve resource capture and competitive effect and responses (Chesson 2000). Inother words, plants good at acquiring resources are also good all-around competitors. But othertheoretical models predict that tolerance and suppression will be negatively correlated: Traitsthat 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 tol-erance and suppression, with some reporting positive correlations (e.g., Willis et al. 2010) andothers 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 inde-pendent components of competitive ability they can respond separately to natural selection anddrive much more complex ecological consequences. Classic views of competitive effect and re-sponse posit that when competition occurs between competitors of equal size, effect and responsecontribute equally to overall competitive ability (Goldberg 1990). However, this perspective oncompetitive 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 interactionsamong all competitors favors tolerance over suppression because when a plant tolerates compe-tition, 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 otherindividuals competing nearby. This finding raises a new and crucial dimension to competitiveability: Natural selection may favor response over effect when plants compete in complex multi-species assemblages (Atwater 2012). MacDougall & Turkington (2004) found that the ability of aspecies to tolerate competition is a better predictor of field performance than the ability to sup-press neighbors. Furthermore, selection caused by competitors appears to improve the responseof one species to another but not the effects on neighbors (Rowe & Leger 2011)—a finding thatis 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 abil-ity? (b) How do effect and response separately influence community dynamics? (c) What traits drivecompetitive effect versus response? and (d ) Can effect and response evolve independently? Answersto these questions could substantially improve our overall understanding of competitive dynamics.

DIRECT AND INDIRECT EFFECTS OF COMPETITION

Historically, most research on competition among plants has focused on individuals and thenegative direct effects of competition. For example, community assembly theory (Weiher & Keddy1999) seeks to predict how direct competitive interactions among species influence the structureand 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 amongall species in a given pool. The major conceptual outcome of hierarchical assembly rules is thatthe best competitor in the hierarchy eventually competitively excludes all other. This is onlyavoided under nonequilibrium conditions, such as disturbance, or when consumers or abioticheterogeneity limit competitive dominance.

Because plants typically interact in a multispecies neighborhood with many individuals, thepotential exists for indirect interactions to be an underappreciated but important driver of com-petitive outcomes (Miller 1994, Aschehoug & Callaway 2015). Indirect interactions occur whenthe impact of one species on another is mediated by a third species (Wootton 1994) and thereforeoccur only among groups of species. Indirect interactions can be important because they may leadto nontransitive competition, which is an alternative to hierarchical assembly rules. Indirect inter-actions 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-casepairwise 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 positiveeffect on species B through a direct negative effect on species A (Figure 1a). Competitive loops canvary in length and intensity and can be nested among groups of species, all factors that influencethe overall impact of nontransitive competition on community structure (Laird & Schamp 2006).Importantly, nontransitive competition can counter the competitive exclusion principle.



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a b

Figure 1(a) Nontransitive interaction and (b) indirect facilitative interaction. Solid arrows represent directinteractions, and dashed arrows indicate indirect interactions. Black arrows represent negative, competitiveinteractions, and red arrows represent positive, facilitative interactions. Redrawn from Aschehoug &Callaway (2015). c© 2015, The University of Chicago Press.

Nontransitive competition and its effect on plant community assembly has strong theoreticalsupport. For example, models indicate that nontransitive interactions among groups of competitorscreate 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 theprevalence of nontransitive competition in natural communities. Their results suggest that non-transitive competition is likely to be widespread and common but largely dependent on temporalabiotic heterogeneity. Thus, nontransitive competition among plants may be a product of theconditionality of ecological interactions and not the strict competitive ability of individual species.Despite strong theoretical support, very little experimental support for nontransitive interactionsamong plants has been found (although see Lankau et al. 2011). This lack of support may simplybe 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 assembleinto communities.

Competitive interactions among groups of species can also result in positive indirect effectswithout the formation of competitive loops. The last 30 years have seen a developing body of theoryhighlighting 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 afriend of mine”). For example, Levine (1999) found that Carex nudata had direct negative effectson Conocephalum conicum when they were competing in pairs, but this reversed to a net positiveeffect via indirect facilitation when a third species, Mimulus guttatus, was present. In a large-scale, community-level test of indirect effects, Aschehoug & Callaway (2015) built experimentalcommunities of species in a replacement series design that allowed comparison of competitionintensity 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 highlyattenuated when species competed simultaneously in groups because of the presence of indirectfacilitation. 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 competitionto be strong and frequent, but competition between species when in complex groups was weakand infrequent. This suggests two things: (a) that pairwise interactions greatly overestimate thecompetitive effects of species and (b) that competition among species in complex communitiesmay promote coexistence rather than lead to competitive exclusion.

This disconnect between competition in pairs and competition in communities may result fromadditive effects. That is, competition between species when in multispecies groups may be the sumof 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 effectsin multispecies communities are additive. Yield density models suggested that competitive intensityin most multispecies assemblages could be predicted by pairwise interaction outcomes. However,certain combinations of species showed significant deviations from the predictions of the modelgenerated from pairwise interactions. But when nonadditive parameters were added to the model,the predictive power of the model increased significantly, indicating that indirect interactionsamong specific combinations of species can establish nonadditive effects that are difficult to predictfrom pairwise-derived models. Dormann & Roxburgh (2005) found that Lotka-Volterra (LV) typemodels built from pairwise outcomes did not accurately predict biomass and coexistence for three-species mixtures in five out of the six combinations grown. Similarly, LV models did not predictbiomass 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 matchedexperimental outcomes.

Despite the fact that indirect effects resulting from competition appear to be ubiquitous amongplants, theory incorporating indirect effects into community assembly theory is not well devel-oped. The pervasive and cascading effects of indirect interactions challenge our foundationalideas on competition, such as the competitive exclusion principle and the need for niche separa-tion for stable coexistence in communities. To advance our understanding of how competitiongoverns community assembly, a more complete understanding of when indirect effects are im-portant (e.g., low- versus high-productivity systems) is required. In addition, the ability to ac-curately predict the role of competition in communities using models hinges on an improvedunderstanding of when the indirect effects of competition are additive versus nonadditive. Toachieve this, future tests of competition need to move beyond the simplistic view that plants in-teract in pairs to a more holistic view of the suite of interactions plants experience in species-richcommunities.

IMPACTS OF COMPETITION ON PLANT POPULATIONS

Hundreds of studies have examined the impacts of interspecific competition on the performanceof individual plants, but these studies have told us little about how such competitive effects ramifyto populations. Studies of plant competition typically assess how competition influences individualplant performance. Biomass is typically the response variable in these experiments because it isconvenient to measure and because biomass is strongly correlated with plant reproduction andoverall 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 competitiveimpacts 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 tocompetition often occur over a very small range of biomass values relative to what plants can achievein 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 influencethe number of individuals in a population in future generations. Lastly, concomitant decreases indensity-dependent interactions can compensate for reduction in survival in any one year. For thesereasons, the most informative studies on the population-level impacts of competition are thosethat either empirically evaluate how competition influences plant abundance across generationsor examine competitive effects on all life stages so that future abundance can be forecast usingdemographic models. The few studies that have taken this approach have made important advancesin 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 competitionon the demography of a target species across life stages. Demographic data are used to param-eterize 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 acrossall life stages. Another is that it enables one to forecast longer-term effects of competition acrossgenerations. Finally, one can gain insight into which demographic component is influenced bycompetition and which most influences competitive impacts on future population growth. Usingthis approach, Freville et al. (2005) performed two different experiments, one to measure effectsof competition on germination rate and another to examine how competition influenced all othervital rates. Combining data from these two experiments, they estimated that interspecific compe-tition reduced asymptotic population growth (λ) for three focal species by more than 90%. Thedifference in growth rate due to competition was driven by the fact that competition dramaticallyreduced fecundity (Freville et al. 2005). Studies using a similar approach have forecast how exoticspecies competitively influence native plant population growth (Thomson 2005) and how compe-tition and herbivory jointly influence native versus exotic thistle population growth (Tenhumberget al. 2015).

Experiments, demographic data, and stage-based models have been broadly used to examineeffects of other interactions, such as herbivory, on populations (Maron & Crone 2006). Morework of this type is needed to better understand plant–plant interactions (Maron et al. 2010) andto better generalize how competition varies in its population impacts across species, functionaltypes, and systems. Such approaches can be especially valuable in studies of competitive effects onlong-lived plants.

Effects of Competition on Plant Distribution

If competitive effects are strong enough, some species can be competitively excluded from particu-lar habitats. For example, Gurevitch (1986) found that the perennial bunchgrass Stipa neomexicanawas severely limited in distribution by competition for water with other grass species along a gra-dient. Other studies have shown that competition with perennial grasses in seasonally flooded sitescan restrict a shrub species to drier areas (Sanchez & Peco 2004) and that grasses in resource-richmoist meadows are competitively excluded from nearby resource-poor dry meadows (Theodose& Bowman 1997). Shrubs on resource-rich andesitic soils were found to competitively excludePinus ponderosa seedlings that occurred naturally on adjacent resource-poor andesite soils (Callawayet 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 toprevent 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 influencingplant distributions at relatively small spatial scales, but whether this is true at regional scales isunclear. Theory has long posited that competition is important in limiting geographic rangesof species (Price & Kirkpatrick 2009), and competition may influence how plants adjust theirdistributions in response to future climate change (Tylianakis et al. 2008). Although studies haveevaluated 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 examinedin relation to other biotic interactions, facilitation appears more important than competition inaffecting plant distributions (Stanton-Geddes et al. 2012).

Competition can also influence community composition and the relative abundance of com-ponent species if it significantly regulates recruitment into communities (see Weiher & Keddy1999). Competition can act as a local filter, which can influence variation in the relative ratesof recruitment among component species, thereby affecting community structure. Seed additionstudies indicate that the removal of competitors (by a disturbance treatment) enhances recruit-ment of new species (Maron et al. 2012), suggesting that competition at the local scale can be animportant determinant of community composition.

By monopolizing microsites, resident vegetation can competitively limit the recruitment ofconspecifics and other species. But are these effects species specific? A few studies indicate thatremoval of the same amount of dominant versus subdominant or rare residents results in differentcompetitive effects on recruitment. Thus, removal of many rare species and the presumed openingof a broader suite of niches may reduce competitive resistance to colonization more than removinga dominant species would. Gilbert et al. (2009) examined this possibility by adding seedlings toplots and found that resident competitive effects against added seedlings were caused by onedominant species instead of many rarer species combined. In a similar experiment that involvedadding seeds rather than seedlings to plots, Pinto et al. (2014) found that removing dominantplant biomass or an equal amount of biomass across several rarer species had similar impacts onthe diversity of added species. Finally, Lyons & Schwartz (2001) found that by removing lesscommon species, assemblages became more invasible, suggesting that competitive interactionsinvolving rare species limited recruitment of new colonists. Although dominant species are oftenconsidered the superior competitors (Facelli & Temby 2002), based in part on mass effects, thecombined effects of subordinate or even rare species in affecting recruitment into local assemblagesare 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 tolonger-term effects on plant dynamics and community composition.

The Need for a Population-Level Perspective

Many models extrapolate the impacts of interspecific competition to populations, but few empiricalstudies have directly measured the effects of competition on population-level parameters such asfitness and recruitment. Importantly, broad themes in plant competition, for example, understand-ing how the strength of competition varies across gradients in productivity, would benefit from apopulation perspective rather than focusing only on individual responses. Long-term, population-level impact studies have been central to our understanding of how other interactions involvingplants, 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 questionsregarding the population-level impacts of competition remain. For example, highly abundantspecies are often considered superior competitors to less abundant species (Grime 2001), butemerging work suggests that rare species can have surprisingly large impacts on ecosystems(Mariotte 2014). Therefore, it is of increasing interest to understand competitive dynamicsamong species that differ in relative abundance and how this, in turn, affects reproduction andrecruitment within communities.

INVASIVE SPECIES AND BIOGEOGRAPHIC DIFFERENCESIN COMPETITION

Plant species that establish in new, non-native ranges offer a unique opportunity to understandcompetition within the context of the long-term evolutionary trajectories of communities. Thefact that some species competitively dominate new recipient communities in ways that differ dra-matically from their native range raises the question of whether evolutionary history can drivethe competitive interactions between native and invasive species. A great deal of work has focusedon whether escape from specialist natural enemies helps tip the competitive balance in favor ofinvasive species, but so far, only a few field studies have explored whether escape from plant com-petition explains the change in performance of an invasive species in its introduced versus nativerange. Callaway et al. (2011) found that removal of surrounding plants in Europe increased thebiomass and reproduction of resident spotted knapweed (Centaurea stoebe) individuals, indicatingstrong competitive effects on knapweed in areas where it is native. In contrast, removal of sur-rounding vegetation in North America had no significant effects on knapweed performance, aresult consistent with greenhouse experiments (Sun et al. 2014). Further, the notion that invadersmay gain an advantage from competitor escape was tested in a diversity–invasibility field experi-ment performed by Sun et al. (2015). They assembled native grassland communities in Switzerlandthat varied in native plant diversity, in a manner consistent with a similar experiment conductedin knapweed’s nonnative range in Montana (Maron & Marler 2008). Both experiments addedspotted knapweed seeds to plots varying in native diversity. In Montana, knapweed prolificallyinvaded species-poor assemblages, but competition reduced knapweed’s ability to colonize di-verse assemblages. In Switzerland, where knapweed is native, however, knapweed failed to invadeany assemblage regardless of community diversity, indicating far greater competitive resistancein the native range. Moreover, all levels of diversity had powerful negative effects on the growthof knapweed seedlings (Sun et al. 2015). Thus, unlike in the introduced range, even low-diversitycommunities in knapweed’s native range offered substantial competitive resistance to knapweedcolonization.

Just as the impact of surrounding vegetation on invasives may differ biogeographically, sotoo may the competitive impact of invaders on natives differ. For example, some studies haveshown 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 arecorrelative, they suggest that some invasives have greater competitive impacts (on a per capita orpercentage cover basis) in introduced ranges than in native ranges.

The mechanisms that drive these biogeographic effects of competition remain obscure. There-fore, future work that examines interactions between exotics and natives in a biogeographic contexthas a great deal of potential to expand our understanding of both the mechanisms of competitionand the role evolution plays in dictating the outcomes of competition.



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CONDITIONALITY AND COMPETITION

One of the primary difficulties in scaling competition between individual plants up to populationsand communities is strong conditionality in competitive outcomes. Biotic and abiotic contextsaffect the strength and direction of competition, and understanding such conditionality is crucialfor predicting when, where, and how competition affects the distribution and abundance of speciesand organization of communities (Brooker et al. 2005, Chamberlain et al. 2014).

Previously, we explored how additional competitors may alter the outcome of competitiveinteractions through indirect effects—a form of biotic conditionality. Other factors, such as her-bivory and abiotic heterogeneity, are also well studied and have strong effects on competitiveoutcomes. For example, when consumers prefer some species to others, competitive interactionscan be altered (Louda et al. 1990). Additionally, as resource supply changes in space and time, theoutcome of competitive interactions can also change (Rebele 2000, Besaw et al. 2011). In this sec-tion, we restrict our assessment of the literature to recent or overlooked advances in understandingcompetitive conditionality.

Environmental Gradients: The Importance and Intensity of Competition

The use of environmental gradients in plant ecology has contributed to understanding the contra-dictory 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 environmentalgradients, although the focal resource may vary. In contrast, life history trade-off theory (Grime2001) predicts that competition should be strong in high-productivity, low-stress areas and weakin low-productivity, high-stress areas. Environmental gradients provide a good opportunity totest these predictions experimentally.

To our knowledge, the first relevant experimental test of these ideas found that competitionat the high-productivity end of a topographic gradient excluded S. neomexicana and limited thespecies to the more stressful, low-productivity ridges (Gurevitch 1986). A number of other studieshave 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, Readeret al. (1994), comparing the growth of Poa pratensis with and without neighbors over a gradientof productivity, concluded that competition did not significantly decrease with decreasing pro-ductivity, 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 focuson the intensity (absolute impact) versus the importance (impact relative to the total environ-ment) 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 fromexperimental studies relating environmental gradients to the role of competition, and thereforesupport for either theory, depend on whether metrics of intensity or importance are used. Re-analyzing Reader and colleagues’ (1994) data, Brooker et al. (2005) found that the importance ofcompetition, in contrast to the intensity, declined substantially with decreasing productivity andthat importance and intensity do not always correlate. Clearly delineating between importanceand 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 canbe highly context dependent and may shift from mutualist to parasitic relationships based onenvironment (Saikkonen et al. 1998). Such dramatic changes in plant–microbe relationshipsare likely to have equally dramatic effects on a plant’s competitive ability. For example, someplant species that are not highly dependent on arbuscular mycorrhizal fungi can exhibit strongercompetitive 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 reducingthe distance between roots required for allelopathic compound deposition and increasing thetotal concentration of chemical exudates in root tissues (Barto et al. 2011), resulting in reducedcompetitive ability for plants with mycorrhizal mutualists.

Fungal endophytes can increase the competitive ability of plants, most commonly in cool-season 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, Aschehouget al. (2012) found that two fungal endophyte phylotypes enhanced the competitive effects ofC. stoebe on North American grass species. One endophyte increased the competitive ability ofC. stoebe without increasing its size, suggesting that the effects of mutualists on competitive abilityare not necessarily related to their direct effects on hosts. Other studies have found that endophyteinfection can increase the intensity of a species’ competitive effects (Saari & Faeth 2012), whereasothers have found that endophytes affect plant traits in ways that may reduce their competitiveability (Faeth et al. 2004).

Soil biota contain consumers and mutualists but are often treated holistically because theireffects on plants cannot be easily reduced to a single taxa (see Callaway et al. 2011) and manyof the microbes are not culturable. Plant–soil feedbacks are pervasive, can strongly influenceplant performance, and have the potential to either increase or decrease competitive interactionsamong plant species. Most feedbacks between soil and plants in native systems have negativeconsequences for plants (Kulmatiski et al. 2008); thus, species that are relatively more susceptibleto negative feedbacks are likely to be at a competitive disadvantage. However, the few studies thathave taken an integrated approach to these fundamentally important interactions have found awide range of results. Bever (1994) found that competition was not affected by negative plant–soilfeedbacks, whereas other work has shown that negative feedbacks can be stronger when plants arecompeting 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 forthree 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 competitioneliminated feedback effects expressed in the absence of competition for Sorghastrum nutans, andSchizachyrium scoparium did not experience feedbacks with soil biota. Hendriks et al. (2015) foundthat each of the four plant species they tested experienced negative soil feedbacks, expressed as adecrease 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 inferiorcompetitors. However, all competition–feedback interactions were expressed only belowground.Finally, Callaway et al. (2004) found that plant–soil feedback outcomes for the invasive C. stoebewere highly negative in native European soils and positive in North American soils, the nonnativerange. Further, feedbacks for North American and European Festuca species were negative intheir native soils. However, in competition these plant–soil feedbacks changed. When grown withC. stoebe, the European Festuca ovina grew larger in European soils trained by C. stoebe than insoils 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 soilstrained 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 ecologistshave only scratched the surface of these complex, context-dependent interactions.

Trait-Mediated Interactions

Plants can be highly plastic in an array of morphological, developmental, physiological, and bio-chemical traits (de Kroon et al. 2005, Metlen et al. 2009), suggesting that competitive ability is alsoplastic. Variation in phenotype has important implications for how a species acclimates or adaptsto a local environment and the potential to create tremendous conditionality in the way individualsinteract. The ecological ramifications of plant phenotypic plasticity are poorly understood but arean emerging field of research in community ecology (see review by Aschehoug & Callaway 2012).

Trait-mediated interactions arise when phenotypic plasticity affects the direct competitiveinteractions of individuals (Callaway et al. 2003). No studies have explicitly examined the effects ofplasticity on direct competition between plant species. However, evidence can be pieced togetherfrom previous work. For example, two Haplopappus species appeared to adjust the depth of theirroot systems in response to belowground competition from Carpobrotus edulis (D’Antonio & Mahall1991). 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 & Callaway2012). Aschehoug & Callaway (2014) found that variation in the root morphology of Quercus dou-glasii in response to access to water resulted in two remarkably different outcomes of competitionamong understory plants. When Q. douglasii trees have deep-rooted morphologies, nonnative an-nual grasses in the understory are directly facilitated, and in turn they competitively exclude thenative perennial grass Stipa pulchra. However, trees with a shallow-rooted morphology reversed theinteraction by suppressing nonnative annual grasses and indirectly facilitating S. pulchra. Changesin root morphology created conditionality in the outcome of the interactions, such that indirectinteractions promoted the coexistence of species and increased community diversity. This study isthe only known test of plasticity and indirect effects of competition. However, its striking resultsdemonstrate that further research on this topic has the potential to greatly improve our under-standing of the conditionality of plant–plant interactions, especially in the context of changingenvironments.

CONCLUSIONS

We have focused on how each of our selected topics has contributed new ideas to competitionamong plants. However, several general themes have emerged frequently and warrant explicitattention.

First, methods matter. Across all major types of plant competition studies, pairwise tests ofcompetition are the most common (Gibson et al. 1999). Although pairwise experiments are easyto implement and allow for fine-scale evaluations of mechanisms and individual performance, theyhave proven to be poor predictors of competition in communities. Future studies must incorporategreater complexity in experiments in order to move beyond simplistic views of competition.

Second, timescales matter. Most competition studies tend to focus on short-term responseparameters such as within-season biomass. This focus may be suitable for assessing the outcomesof competition for annual plants, but understanding the outcomes of competition in multispeciesand perennial plant communities requires a broader perspective (Trinder et al. 2013). This is par-ticularly 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 relativelyshort duration, meaning little is known about how competition impacts recruitment, patternsof community development, and relative abundance—something that can be achieved only bylong-term studies.

And third, context matters. It is important to keep in mind the relative strength of competitioncompared with other local processes that influence community structure, especially environment.Clearly, plant competition is an important determinant of community structure, but withoutcontext that evaluates other factors, we are likely to overestimate the role competition plays in theassembly of communities.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

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