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ES47CH12-Aschehoug ARI V I E W Review in Advance first posted online on August 24, 2016. (Changes may still occur before final publication online and in print.) N I N A Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 13:55 C E S R E 16 August 2016 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. 263 Changes may still occur before final publication online and in print ES47CH12-Aschehoug ARI 16 August 2016 13:55 INTRODUCTION Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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 264 Aschehoug et al. Changes may still occur before final publication online and in print Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. ES47CH12-Aschehoug ARI 16 August 2016 13:55 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 www.annualreviews.org • Competition Among Plants Changes may still occur before final publication online and in print 265 ES47CH12-Aschehoug ARI 16 August 2016 13:55 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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 266 Aschehoug et al. Changes may still occur before final publication online and in print Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. ES47CH12-Aschehoug ARI 16 August 2016 13:55 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). www.annualreviews.org • Competition Among Plants Changes may still occur before final publication online and in print 267 ARI 16 August 2016 13:55 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. ES47CH12-Aschehoug 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. 268 Aschehoug et al. Changes may still occur before final publication online and in print ES47CH12-Aschehoug Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. a ARI 16 August 2016 13:55 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 www.annualreviews.org • Competition Among Plants Changes may still occur before final publication online and in print 269 ARI 16 August 2016 13:55 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. ES47CH12-Aschehoug 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 270 Aschehoug et al. Changes may still occur before final publication online and in print ES47CH12-Aschehoug ARI 16 August 2016 13:55 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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 www.annualreviews.org • Competition Among Plants Changes may still occur before final publication online and in print 271 ARI 16 August 2016 13:55 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. ES47CH12-Aschehoug 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 272 Aschehoug et al. Changes may still occur before final publication online and in print ES47CH12-Aschehoug ARI 16 August 2016 13:55 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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. www.annualreviews.org • Competition Among Plants Changes may still occur before final publication online and in print 273 ES47CH12-Aschehoug ARI 16 August 2016 13:55 CONDITIONALITY AND COMPETITION Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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 274 Aschehoug et al. Changes may still occur before final publication online and in print Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. ES47CH12-Aschehoug ARI 16 August 2016 13:55 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 www.annualreviews.org • Competition Among Plants Changes may still occur before final publication online and in print 275 ES47CH12-Aschehoug ARI 16 August 2016 13:55 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 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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 276 Aschehoug et al. Changes may still occur before final publication online and in print ES47CH12-Aschehoug ARI 16 August 2016 13:55 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Louisiana State University - Baton Rouge on 08/31/16. For personal use only. 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. 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