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Competitive Ability and Species Coexistence: A 'Plant's-Eye' View Author(s): Lonnie W. Aarssen Source: Oikos, Vol. 56, No. 3, (Nov., 1989), pp. 386-401 Published by: Blackwell Publishing on behalf of Nordic Society Oikos Stable URL: http://www.jstor.org/stable/3565625 Accessed: 08/04/2008 03:26 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=black. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We enable the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. http://www.jstor.org OIKOS56: 386401. Copenhagen1989 Competitive ability and species coexistence: a 'plant's-eye' view Lonnie W. Aarssen Aarssen, L. W. 1989. Competitiveability and species coexistence:a 'plant's-eye' view. - Oikos 56: 386-401. Plant species coexist by avoiding competitive exclusion. This paper develops a 'plant's-eye'view of avoidingcompetitiveexclusionwhich interpretscoexistenceat the species level as a consequenceof ongoing selection resultingfrom geneticallybased differencesin competitiveabilitieswithinlocal neighborhoods.That competitive abilitymay changeas a consequenceof selectionis supportedby resultsfrom a multi-generationcompetition experimentinvolving Senecio vulgarisand Phleum pratense.The potentialevolutionaryconsequencesof suchselectionoperatingwithin a communityof several species is then explored. The approachdeveloped here assumesthat resourcesupply/demandratio is sufficientlylow and that the extent to whichdemandsare madeon the same resourceunitsis sufficientlygreatfor plantsof differentspecies to competeintensely.It also assumeshoweverthat, severalgeneticallyvariableattributescombineto definethe competitiveabilityof a plantandthat the resultinggenotypicvariabilityin competitiveabilityis no greaterbetweenspecies than within species. This forms the basis of the competitivecombiningabilityhypothesis for species coexistence in which competitiveexclusion is avoided at the whole populationlevel because no populationcontainseven one genotype that is competitivelysuperior to all other genotypes belonging to any other coexisting population.One mechanismunderthis hypothesisassumesthat competitiveabilities are intransitiveat the genotypelevel. If this intransitivenetworkspansacrosstaxonomic boundaries,then those genotypeswith the best competitiveabilitieswithin local neighbourhoodsare just as likely to belong to one species as to another.The major implicationof this hypothesisrelates to its role in helping to explain the conflictingtruismsthat competitionwithinplant communitiesis intense and should thereforehave importantevolutionaryconsequences,but that plant species coexist with apparentlylittle differentiationpermittinginteractionavoidance. L. W. Aarssen, Dept of Biology, Queen's Univ., Kingston, Ontario, Canada K7L 3N6. prevent competitive exclusion, but none provide for the possibility of indefinite coexistence. Given that as many "Thefact thatorganismslivingin differentplacesare different as 99% of all species known to have ever existed are is easy to explainby Wallacianforces. The questionof how so manysortsof organismsare ableto persisttogetherin the same thought to be now extinct (Mayr 1970), species coexis'place' is much more difficult to answer, is much more in- tence has invariably been transient. Any species, given teresting;it demandsa biotic interpretationand a Darwinian enough time, will be excluded for reasons which need solution." not involve competition, and the probability of excluHarper(1977:750) sion increases as the spatial scale decreases and the temporal scale increases. As an operational definition The subject of coexistence has particular relevance for here, coexistence on the same trophic level (e.g. among species on the same trophic level, such as plants, where plants) will imply interaction without competitive exclucompetitive exclusion is often predicted from theory sion on the temporal and spatial scales appropriate to based on Gause's principle. Several mechanisms may the populations concerned. Two species coexist thereIntroduction Accepted 20 June 1989 ? OIKOS 386 OIKOS 56:3 (1989) fore, when at least some individualsof one population respondin some way, at least some of the time, to the presenceof individualsof the other populationwithout either species being competitivelyexcluded. Salisbury(1936: 47) wrote, "Thatcompetitionis severe in the plant world, no one can deny and this is operativeat all phasesof development."Ecologistsand especially plant ecologists it seems, have often taken competitionfor granted- so 'obvious'as to be almost exempt from the need for experimentaldemonstration of its importance.Even Darwin,who stressedcompetition as the major force of natural selection, devoted virtuallynone of his experimentsexplicitlyto the study of competition. "It is the doctrineof Malthusapplied with manifoldforce to the whole animaland vegetable kingdoms"(Darwin1859:63). Knowledgeof the inherent potentialfor all organismsto over-populatehas had an overwhelmingtendency to invoke justificationfor the assumption that competition should be virtually everywhererelentlessand inescapable. Thisconfidencein the importanceof competitionmet with a growingoppositionin the 1970s, mostly among ecologistsstudyinganimals,and an acrimoniousdebate has flooded the literatureover the past decade (e.g. Connell 1980, Haila 1982, Simberloff1982, Schoener 1982, 1983, Harvey and Silvertown1983, Lewin 1983, Salt 1984, Strong et al. 1984, Connor and Simberloff 1986). The debate forced a re-evaluationof the literature and one of the most importantthingsto emerge is that, while there are plenty of studiesthat demonstrate the occurrenceof competition,there is far less evidence indicating that it has important evolutionary consequences. The main conceptual issue of the debate hingesprimarilyon the widelyacceptedGaussian-based assumptionthat differentiationprovidingopportunity to avoid some criticallevel of interaction(e.g. by making demands on different resource units) is the only evolutionaryconsequenceof competitionthat permits species coexistence;e.g. "...competitioncan lead only to characterdivergence"(Lundbergand Stenseth1985: 105). Evidence for such differentiationis not, in itself, evidence for the importanceof past competitionas a selection pressure (Connell 1980). The crucial point howeveris this: lack of evidence for differentiationallowing a significant level of interaction avoidance amongcoexistingspeciesis, accordingto this Gaussianbased assumption,sufficientevidence to: 1) reject the importanceof past competitionas a selection pressure and 2) indicate that species coexistence must be explainedby mechanismsthat have little or nothingto do with competition having any significantevolutionary consequences(e.g. Watson 1980, Rogers 1983, Silvertown 1983). Giller (1984: 133) provides a clear statement of this view "Someanalyseshave found that species overlapor separationdoes not differmarkedlyfrom Plant ecologists have noticeablyabstainedfrom this debate. Horn (1979: 50) stated, "...botanists are amused at the zoologist's debate over whether populationregulationis density-dependentor density-independent. Crowdingis too common and too dramatica phenomenonin plantcommunitiesfor its importanceto be doubted." Yet, plant ecologists have repeatedly drawnattentionto the generalshortageof evidencefor differentiationthat confers opportunitiesto avoid (or reduce the extent of) interactionamong species within plant communitiescomparedwith that for animalcommunities(Harper1968, Willson1973, Grubb1977, Antonovics1978, Pickett 1980, Silvertownand Law 1987). This presents an interesting paradox: competition is regardedas relativelyimportantin plantsbut the traditional evidence requiredto avoid rejectingthe importance of past competitionas a selection pressure(i.e. differentiationpermittingsome measureof interaction avoidance)is relativelyscarce. This paradox is examined in the present paper. If there is little evidence to suggest that naturalselection from competitionamong plants commonlyhas evolutionaryconsequencesinvolvingdifferentiationthat permits reduction in the extent of interaction, then the common observation of species coexistence suggests that 1) selection from competitionis, in fact, relatively uncommon (e.g. den Boer 1986, Wiens 1987), or 2) selection commonly leads to types of differentiation permittinginteraction reduction which have not yet been widely documented or documented at all (e.g. Grubb1977, 1986,Cody 1986),or 3) thereis an alternative evolutionaryconsequenceof competitionthat permits species coexistence that need not involve differentiation permittinginteractionreduction. This paper explores the third hypothesis. The problem requires first an examinationof the factorsthat affect individual fitness in contexts of competition.I then focus on the unique role of competitive ability in affecting species coexistence and the roles of environment,chance and genetic variationin affecting the relative competitive abilities of neighbours.Following this, I present evidence of selectionfor improvedcompetitiveabilityfrom a multi-generationcompetition experiment involving Senecio vulgaris and Phleum pratense. Finally, I explore the potential evolutionaryconsequencesof such selection operatingwithin a communityof several species. This leads to a view of species coexistence based on predictionsconcerningthe potentialfates of competing individualswithin local neighbourhoods;"the 'plant'seye' view is what is relevantto explainthe distribution, adaptationand the processof changewithinspeciesand withincommunities"(Harper1977:706). Individualfitnessand competitiveabilityin plants that in ... randomized analogues.... One must conclude Differencesin fitnessamongindividualswhen resources that competition has not been a force in organizing are contestedwill be affectedprimarilyby three things: these assemblages". 1) differences in the intensity of competition experi25* OIKOS 56:3 (1989) 387 enced, i.e. differencesin the extent to whichan individual or its offspringare denied resources(e.g. measured as suppressionin size or growthrate) as a consequence of interactionwithneighbors;2) differencesin the limiting intensityof competition,i.e. differencesin the upper limit of intensity of resource denial necessary to causemortalitybeforereproductionandhence preclude the coexistenceof anydescendantswiththe descendants of neighbors;3) differencesin the ability to maximize fecundityusing resourcesdenied to neighbors.Each of these componentsis examinedin detail below: 1) The intensity of competition imposed by different neighbouringspecies upon a 'target' individual may commonly be equivalent within plant communities (Goldberg and Werner 1983). The reasons for this equivalencehowever may differ for each target/neighbor pair because the competitionintensityexperienced by a target (i.e. the "competitiveresponse"of the target), or imposedby a neighbor (i.e. the "competitive effect" of a neighbor) (Goldberg and Werner 1983, Goldbergand Fleetwood 1987)will be affectedby four principalfactorswhichmay interactto variousdegrees: a) The intensity of competition experienced (or imposed) will decrease with a decrease in the extent to which combined demands (of the individual and its neighbors)on resources (e.g. as affected by density) exceed the local supply (e.g. as affected by resource cyclingor input rates). b) The intensity of competition experienced (or imposed) will decrease with a decrease in the extent to which the individualmakes demandson the same resource units as its neighbors(which will decrease the opportunityfor interactionwith neighbors). c) The intensity of competition experienced (or imposed) may be mitigatedby concomitantbeneficialinteractionwith these same neighbors(Hunterand Aarssen 1988). d) The intensityof competitionexperiencedby an individualwill decreasewith an increasein its relativeability to deny contestedresourcesto its neighborsor to its neighbors' offspring and thereby procure these resources for itself or for its offspring.This will depend upon the relativeabilityto deplete resourcesrapidlyor to a low level (exploitationcompetition)or on the relative ability to interfere with access to resources (interferencecompetition).Similarly,the intensityof competition imposed by a neighbor will increasewith an increase in this relative ability. The relative ability to deny contestedresourcesto neighborsis regardedhere as one of three maincomponentsof competitiveability (see also 2) and 3) below). Potential interactionamong the above factorsin affectingthe intensityof competitionexperienced(or imposed) can be illustratedwith a hypotheticalexample: SupposethatplantA andplantB makedemandson the same resourcesand have similarabilitiesto deny these resources to each other. Here, plant B will be sup388 pressedby A to a certainlevel. If A and B do not make demandson exactlythe same resourceshowever, plant B may still be suppressedto the same level if the ability of A to deny any remainingcontestedresourcesto B is greaterthan the abilityof B to deny these resourcesto A. 2) The limiting intensity of competition can also be re- gardedas a componentof competitiveability.An analogy here is with a boxing competition. The boxer's competitiveabilitydepends upon the relativeintensity of his punchesbut also on his relativeabilityto tolerate punchesenoughto avoida knockout.Twoboxerstherefore, may deliverthe same intensityof punchesbut the one left standingin the end will be the winner. Similarly, the competitive ability of a plant may depend upon its relative abilityto deny contested resourcesto neighborsas well as its relative tolerancethresholdof resourcedepletionor interferenceby neighbors(Aarssen 1983, 1984, Goldberg and Fleetwood 1987). The latter may involve, for example, the use of resources stored in seed endospermor from luxuryconsumption during times when resource supply exceeded the demands, or it may involve temporaryvegetative dormancyduringcompetition-mediatedresourceimpoverishment (e.g. shade tolerance), or resistanceto allelopathic chemicals. Such traits may be extremely importantfor seedlingsat very high densitieswhere the 'winners'may have, not a higher resource depletion rate, but rather,a greaterabilityto withstand(i.e. without mortality) the extreme resource impoverishment associatedwith high seedlingdensities.The fitnessgain for such plants is conferred by enduringcompetition long enough to exploit the new space resultingfrom thinningof less tolerantneighbors. Two plants therefore, may have the same limiting intensityof competitionand one may excludethe other becausethey have sufficientlydifferentabilitiesto deny contested resourcesto each other. Alternativelyhowever, the plants may have the same abilities to deny contestedresourcesto each other but one may exclude the other becausethey have sufficientlydifferentlimiting intensitiesof competition. 3) Allocation to fecundity of resources denied to neigh- bors can also be regardedas a componentof competitive ability. An ability to produce more offspringper unit of resourcesdenied to neighborsmay offset the potentialfitnesscost of interactionwith a neighborthat has a higherresourcedepletionrate. GenotypesA and B for example,are identicalin everyrespectexcept that A producesmanysmallseeds andgenotypeB, usingthe sameavailableresources,can produceonly halfas many seeds but each is twice the seed size of A. When they interact,genotypeB, becauseits seed is doublethe size, has a fasterseedlinggrowthrate and hence denies twice as manyresourcesto A as A denies to B. All else being equalhowever,A andB alwayshave the samefecundity OIKOS 56:3 (1989) Fig. 1. Three general hypotheses for avoiding competitive exclusion (coexistence) derived from corollaries of three general conditions necessary for competitive exclusion to proceed. See text for details. General hypotheses for avoiding competitive exclusion I _ I Demandson resources Demandson resourcesdo sufficiently exceed the supply not sufficiently exceed the supply (e.g. due to disturbance or predation) A. Limiting resource supply/demand ratio Species do not make demands on sufficiently different resource units I Species make demands on sufficiently different resource units B. Limiting extent to which demands are made on the same resource units Speciesdiffersiufficiently in competitive abiility Competitive ex clusion I Species do not differ sufficiently in competitive ability C. Limitingdissimilarity of competitive abilities because A requires only half as many resources to produce the same number of seeds. Despite, therefore, B's greater ability to deplete resources under competition, neither genotype is superior in its ability to exclude the other. If, however, genotype A could deny just as many resources to B as B denies to A because of, for example, an earlier germination time for A, then the higher fecundity of A would result in the competitive exclusion of B. Because all three of the above components may be necessary to fully account for differences in fitness when resources are contested, they may all be necessary to define the intensity of natural selection resulting from competition. 'Intensity of competition' in this context therefore, is an experience of an individual and should not be confused with 'intensity of selection resulting from competition'. The latter reflects the differential in this experience and is also affected by the differential among individuals in the tolerance threshold of this experience and the differential in ability to maximize fecundity using resources denied to neighbors. The effect of relative competitive ability on relative fitness may be most often represented by differences in abilities to deny contested resources to neighbors or their offspring. Any differences however, in the tolerance threshold of resource depletion or interference by neighbors or in the allocation to fecundity of resources OIKOS 56:3 (1989) denied to neighbors would be expected to have an increasing effect on relative fitness as abilities to deny resources to neighbors become more similar. The relationship among these three components of competitive ability however, has never been explicitly investigated. It is not difficult to imagine how, when two of these components are held constant, the third can fully account for differences in competitive ability. It is less certain how they interact to define differences in competitive ability when they all vary. The role of competitive ability in species coexistence From the 'plant's-eye' view, all mechanisms of species coexistence have one critical consequence in common: i.e. there are always at least some individuals of each coexisting species that do not reach their limiting intensity of competition (see above) and can, therefore, continue to leave descendants. The critical question here is: What conditions are necessary to achieve this? One approach to identifying these conditions derives from the assumption that exactly three distinct conditions are required before plant A can competitively exclude plant B: 1) demands on resources must "sufficiently" exceed the supply, 2) A and B must make demands on a "sufficiently" similar set of resource units, and 3) A must have a "sufficiently" greater competitive ability for these resource units (Fig. 1). Accordingly, avoidance of competitive exclusion at the whole population level may depend upon a "limiting resource supply/demand ratio", a "limiting extent to which demands are made on the same resource units" and a "limiting dissimilarity of competitive abilities" within local neighborhoods (Fig. 1). The latter of these general hypotheses distinguishes the role of competitive ability in species coexistence. If demands on resources exceed the supply and if individuals of different species do not make demands on 'sufficiently' different resource units, coexistence may still be possible if the competitive abilities (as defined above) of individuals of coexisting species are not sufficiently different to result in the competitive exclusion of an entire population of any of these species (Aarssen 1983, 1984, 1985, Agren and Fagerstrom 1984, Ghilarov 1984, Hubbell and Foster 1986, Goldberg 1987) (Fig. 1). For example, the number of species which can coexist may increase in the presence of intermediate levels of disturbance, predation or parasitism (Harper 1969, Connell 1978, Grime 1979, Risch and Carroll 1986). This may result because the species that have the best competitive abilities (i.e. the 'dominants') in the absence of these factors are disproportionately suppressed when these factors are in effect. Under these circumstances, demands on resources may commonly exceed the supply, but the individuals of different species are more equally equipped to deny contested resources to each other and consequently, more species can coexist. Coexistence by similar competitive abilities may not 389 be indefinitelystable, i.e. if a species is rare, it may not deterministicallyincrease in relative abundance and may thus experiencea 'random-walk'(or 'drift')to extinctionfrom the community(Chessonand Case 1986). Indefinitestabilityrequires,theoretically,thatindividuals of a species be at an advantagewhen relativelyrare, such as when: 1) individualsof differentspecies make demands on sufficientlydifferent resource units (i.e. ecological combiningability- Harper 1977), or 2) interspecificcompetitiveabilityand intraspecificcompetitive ability are negatively correlated leading to frequency-dependentgenetic feedback (Pimentel et al. 1965), or 3) recruitmentor survivalis less successful near intraspecific neighbors than near interspecific neighborsbecause of species-specificpredationor increasing pathogen infection rate with increasinglocal dominance(Janzen1970, Fox 1977). Alternatively,stable coexistence may result if species differ in their responses to heterogeneityin the environment(e.g. climate, soil conditions,abundanceof predatorsor parasites) and if there is sufficient temporal or spatial heterogeneityin these environmentalfactorsto alter(or obliterate) the rank order of species competitiveabilities beforeexclusionof any speciesresults(e.g. Hutchinson 1961, Stewardand Levin 1973, Fowler 1982, Tilman 1984, 1986, Chesson 1986, Ellner 1987). The lattermechanisminvolvesa species/environment interaction,i.e. each species has a certain set of local and/or temporary environmental conditions under which it has a superiorcompetitiveability over other coexistingspecies. An analogousmechanismis examined below involvingan interactioneffect at a smaller, 'individualistic'scale, i.e. between the genotype defining the competitive ability of a plant and the correspondinggenotypic identity of its neighbors,irrespective of species identity. This requires first an examination of the roles of environment, chance and genotypein affectingthe relativecompetitiveabilitiesof neighbors. Determinantsof relativecompetitiveabilitiesof neighbors Neighboringindividualswhich are geneticallyidentical may differin theircompetitiveabilitybecauseof differences occurringby chance, in their experiencesof their local physicalenvironments.For example, if the physical environmentvariessignificantlyon the scale of the individual,then one of two neighboringindividualsmay experience better physical conditions for germination and establishment or for reproductive development (Shmidaand Ellner 1984).Such'goodfortune'maygive an individualthe edge in denyingresourcesto neighbors throughearlieror more rapidresourcedepletion. There are also sources of randomnessin the experience of plantswhichneed not dependon environmental heterogeneity(Agren and Fagerstrom1984).For example, when several seeds (belongingto several species) 390 establishas adjacentneighbors,their relative competitive abilities may depend upon: 1) which individuals happenedto encounterdispersalagents (e.g. wind currents)firstand hence happenedto arriveat the site and germinatefirst;2) maternalfactorsaffectingseed size, qualityor ripeningand dispersaltime and hence germination time or seedling growth rate, e.g. due to the position the seed happen to have had on the parent plant (Cavers and Harper 1966) or due to the local environmentalconditionsthat happento have been experiencedby the parentplant on whichthe seeds were produced (Parrishand Bazzaz 1985); 3) the angle at which the seed happens to land on the soil surface (Sheldon 1974);or 4) the activityof burrowinganimals affectinglocal emergencetime from the seed bank in a given site. Passive, random seed dispersal combined with the sessile post-germinationphase characteristicof terrestrial plants, may allow each species an equal chance of being affectedby the above randomfactors. Hence, if thereis no geneticvariationin competitiveabilityeither within or between species, the superior competitor among a randomlychosen group of neighborsmay be just as likely to belongto one speciesas to another.The net effect would be that no whole populationcould be competitivelyexcluded deterministicallyby any others (Fagerstrom1988). Differencesin the competitiveabilitiesof neighboring plantsmay alternativelyhave a significantgenetic component. Genotypicvariationin responseto competition has been reportedfor severalplant species (Turkington and Harper 1979, Joy and Laitinen 1980, Martinand Harding1981,McNeilly1981, 1984,Matheret al. 1982, Wolek1984,AarssenandTurkington1985a,b, Evanset al. 1985, Siddiqi et al. 1985, Clay and Levin 1986). When demandson resourcesexceed the supply and if competitiveabilityis geneticallyvariable,naturalselection may favorthose genotypeswith the greatestability to deny contested resources to neighbors and/or the highest tolerance threshold of resource depletion or interferenceby neighborsand/orthe greatestabilityto maximize fecundity using resources denied to neighbors. The best direct evidence to date for selection in response to competitionhas come from multigeneration experimentsusing Drosophila.Three differenttypes of consequencesof this selection have been reported: 1) improvementin overallcompetitiveabilityof one of the componentspecies (e.g. Moore 1952,Mueller1988);2) oscillationsin the relativefrequenciesof genotypeswith good intraspecificversusgood interspecificcompetitive abilities (e.g. Pimentel et al. 1965); and 3) increased differentiationin resourceuse (Seaton and Antonovics 1967). In a similar multi-generationapproachwithin growth-chambers,I found evidenceof selection for improved competitiveability throughearliergermination time in the autogamous,short generationannualSenecio vulgarisL. in responseto intraspecificcompetition OIKOS 56:3 (1989) CUMULATIVE PERCENT GERMINATION and interspecific competition with a standard commercial source of Phleum pratense L. This experiment is described below. 100 80 60 Selection for competitive ability in Senecio vulgaris Methods 40 Seeds of Senecio vulgaris were obtained from 21 different geographical localities including populations from the United States (California, Washington, Oregon, Florida), Canada (Guelph, London, Ottawa, Port Perry, Toronto) and England (Dorset, Liverpool, Malpas, Oxford, Shropshire, Staffordshire, Warwick). Biotypes resistant and tolerant to several herbicides were included. Seeds from all sources were mixed to promote as much initial genetic variation as possible. Senecio seeds were planted in boxes 60x60x20 cm deep filled with sterilized sandy loam soil. Based on percentage 20 GENERATION 1 .- P 0 . t , - I . .W . - , i* * . . . * ? * -l Is 100 80 germination, 60 seeds were planted: 1) in monoculture to obtain 1000 seedlings per square meter, 2) in monoculture to obtain 2000 seedlings per square meter, and 3) in equi-proportioned mixture with Phleum pratense to obtain a component density of 1000 seedlings per square meter. Plants were grown in a growth chamber under controlled conditions of 22?C for 16 h of light and 15?Cfor 8 hours of dark. The boxes were watered uniformly with 2 1 of tap water every other day and were repositioned randomly within the growth chamber once per week. 40 20 0 100 For each treatment, 80 LOW DENSITY 60 HIGH DENSITY 40 LOW DENSITY WITH PHLEUM 20 GENERATION 3 - 0 0 5 10 I I 15 0 - 20 DAY Fig. 2. Cumulativepercentgerminationin Seneciovulgarisfor a) a mixture of seeds from 21 different geographic localities (generation 1), b) seeds derived from generation 1 plants grown under three different competition treatments (see text for details) (generation 2), and c) seeds derived from generation 2 plants grown under the three different competition treatments (generation 3). OIKOS 56:3 (1989) mature Senecio seeds were col- lected and stored in the dark at 5?C. After six weeks of storage, seeds were tested for percent germination on the same sandy loam soil and under the same growth chamber conditions as indicated above. Based on values for percent germination, seeds of this second generation were sown under the same treatments from which they were collected, using the same source of Phleum (for the mixture). Third generation Senecio seeds were similarly collected from each treatment and sown under the same corresponding treatment. The storage time (dormancy period) was kept constant (6 wk) between gener ations. For each generation, after 51 d, 50 randomly chosen individuals of Senecio were harvested from each treatment and 50 randomly chosen individuals of Phleum were harvested from the mixture treatment. Individuals were oven-dried and above-ground biomass was recorded for each (Roots could not be separated among individuals). Hence, three generations of selection under three competition treatments were accomplished for Senecio. Selection in Phleum however was not followed since the same stock source of Phleum was used in each generation (rather than seed produced by the previous generation). 391 Tab. 1. Detailsof cumulativepercentgerminationon days2, 3, 4 and5 for generation3 Seneciovulgarisseeds frompopulations under three different competition treatments. Values are means (N = 10 samples) of the number of seeds germinated out of 100. Valuesfor the threepopulationson a givendaywhichdo not havethe samesuperscriptletteraresignificantly(P < 0.05) different basedon Tukey'sHSD. Day 3 4 5 7.0a 38.6a 36.8a 78.4a 14.9b 68.1b 66.4a 73.0a 84.0b 2 Low densitymonoculture High densitymonoculture Low densitywith Phleumpratense Results and interpretation Strong selection in Senecio for earlier germination time was evident in all three treatments (Fig. 2). Selection however, was most intense in mixture with Phleum and was least intense in the low density monoculture. By day 3 of the germination experiment for generation 3, almost twice as many seeds had germinated from the population grown in mixture with Phleum (68.1%) compared with seeds from the low density monoculture population (38.6%) (Tab. 1). The Phleum seeds used in mixture with Senecio from each generation did not differ in germination rate. Earlier germination time in later generations was associated with significantly (P < 0.05) larger individual Senecio above-ground biomass at harvest in later generations for the mixture treatment with Phleum but not for either of the two monoculture treatments (Fig. 3). All the plants in monocultures were the product of selection in the previous generation, i.e. derived from plants with the earliest germination times (and perhaps MEAN DRY WEIGHT (g) 0.4 (N =50) LOW DENSITY LOW DENSITY WITH PHLEUM / i HGH DENSITY 0.3 0.2 83.9ab 89.6b other traits) and hence, the best competitive abilities. Hence, although the average individual in different generations may have had different characteristics that affect its competitive ability (e.g. germination time), the performance of the average individual did not differ across generations because the neighbors of the average individual also possessed competitive ability traits that were also favoured by selection in the previous generation. The same interpretation does not apply however, to the behaviour of Senecio in the mixture treatment. Phleum individuals were not the product of selection in previous generations and there was opportunity therefore, for selection in Senecio to increase its average competitive ability (by earlier germination time) relative to Phleum neighbors. This apparently accounts for an increase in individual above-ground biomass at harvest in later generations of Senecio in mixture but a corresponding decrease in biomass for Phieum (Fig. 4). By generation 3, Senecio individuals significantly (P < 0.05) out-yielded Phleum individuals in mixture. Total mixture yield did not change significantly across the MEAN DRY WEIGHT (g) 0.47 (N=50) SENECIO PHLEUM n 0.3 0.2 0.1 0.1 0 GENERATION 0 GENERATION1 GENERATION2 GENERATION3 Fig. 3. Mean above-ground dry weight (N = 50, with standard error bars) for Senecio vulgaris populations derived initially from a common composite seed source and grown under three different competition treatments for each of three successive generations. 392 1 GENERATION 2 GENERATION3 Fig. 4. Meanabove-grounddryweight(N = 50, withstandard error bars) for: 1) Senecio vulgaris populations derived initially from a common composite seed source and grown with Phleurm pratense for three successive generations, and 2) Phleum pratense grown with Senecio vulgaris in each of the three generations and derived from the same commercial seed source in each generation. OIKOS 56:3 (1989) Fig. 5. Proposed relationship among attributes of competitive ability in plants. 'Primary traits' are those which have the most proximate role in determining the relative competitive abilities of neighbors. Some of these are determined by several 'secondary traits' and some of these may in turn be affected by several additional 'tertiary traits'. All of the tertiary traits affect each of the secondary traits indicated by arrows. Groups of secondary traits affect the primary traits indicated. TERTIARY TRAITS SECONDARYTRAITS PRIMARY TRAITS depletion greater rate of water greater root greater extension lateral of roots density 4- arrival early dispersal earlier faster uptake into root hairs greater of root density hairs larger 4- depletion light 4- taller plant larger leaf greater extension height greater density number/ of flowers 4- to ability dispersal 4- interference greater with recruitment of neighbors litter greater deposition interference Greater with pollination more effective pollen allelopathy of 4 to chemicals to more resistant or predators pathogens of low better able to encourage or predators pathogens affecting neighbors greater physical resistance disturbance to rate depletion greater resource of another neighbors of more release toxic allelopathic in the chemicals consumption of greater production more toxic allelopathic chemi cals more tolerant temperatures number/density greater of seeds/fruits more attractive/ seeds/fruits rewarding luxury more resistant allelopathic more attractive/ flowers rewarding greater attract agents of more effective association with mycorrhizae more effective leaf orientation to ability pollinators size 4-- area lateral of shoots seed rate higher photosynthesis greater greater attract time germination 4- depletion greater rate of a mineral nutrient N, P, K) (e.g. greater rate of from time tolerance higher of depletion threshold resource of another longevity greater through clonal (e.g. growth) soil tolerance higher of water threshold by neighbors depletion tolerance higher of mineral threshold by neighbors depletion tolerance higher threshold of light by neighbors depletion more resistant to allelopathic chemicals to to ability greater maximize fecundity resources using to neighbors denied OIKOS 56:3 (1989) 393 A. Assumptions SPECIES1 SPECIES3 Fig. 6. An intransitivenetworkof relativecompetitiveabilities of hypotheticalgenotypesbelongingto three differentspecies which make demands on the same resource units. Arrows indicatepairwisecomparisonsof competitiveabilitieswith the inferiorcompetitorat the head of the arrow. Lines without arrow heads connect genotypes which do not differ significantlyin competitiveability.See text. three generations, indicating that the extent to which the two components made demands on the same resource units remained unchanged across generations. If those genotypes with the best competitive abilities all belong to one species, then the resulting increase in average competitive ability of this species may lead to the exclusion of other species. If these genotypes belong to several different species however, then ongoing reciprocal selection may maintain a close similarity of average competitive abilities among species. Such a selectional consequence of competition may play an important role in preventing competitive exclusion at the species level within vegetation. This forms the basis of the competitive combining ability hypothesis for species coexistence (Aarssen 1983, 1985). Below, I develop this hypothesis further than in previous reports by a detailed examination of its assumptions and predictions. Selection for competitive combining ability: assumptions and predictions If relative competitive abilities of genotypes form a linear hierarchy, then natural selection leading to competitive balance among species would be a "progressive escalation" characteristic of an "arms race" (Dawkins and Krebs 1979). Competitive exclusion may be delayed but would not be avoided if there was a single 'topranking' genotype belonging to one species that could exclude all others. Below, I examine several assumptions which suggest that such an all-superior genotype may be relatively rare in plants. 394 1) Several genetically variable attributes of a plant interact to affect competitive ability for even a single resource. Plants may commonly adjust their consumption of different resources so that growth is usually limited by more than one resource at any given time (Bloom et al. 1985). Nevertheless, even if relative fitness were determined primarily by relative abilities to deny to neighbors a single resource which is the most limiting at a given time and place, there would be several possible attributes and attribute combinations which might affect (directly or indirectly) the ability to compete for that single resource. Competitive ability in terrestrial plants depends directly upon the 'primary' traits in Fig. 5 but numerous different combinations of the 'secondary' and/or 'tertiary' traits indicated may result in the same 'phenotype' for a given primary trait. For example, if the supply of a particular nutrient cannot meet the combined demands of neighbors, then the relative ability of a plant to deny that nutrient to neighbors or their offspring may be partially determined by the physiology of absorption, uptake and storage (e.g. Caldwell et al. 1985) but may also be an indirect consequence of any combination of several genetically variable attributes such as the following: time of arrival (through dispersal) at a site (e.g. Platt and Weis 1985), germination time (e.g. Weaver 1984, Peters 1984), seed weight (e.g. Peters 1985, Wulff 1986), ability to fully exploit seed reserves (Negbi 1986), growth rate of seedling roots at low temperatures (e.g. Harris and Wilson 1970), time of initiation of spring growth (in perennials) (e.g. Cable 1969), effective association with mycorrhizae (e.g. Fitter 1977, Allen and Allen 1984), rate of root elongation (e.g. McCown and Williams 1968), effective branching pattern, crown architecture or leaf density for shading neighbors (e.g. Kuppers 1985, Roush and Radosevich 1985), tolerance of parasites (e.g. Burdon et al. 1984, Price et al. 1986), tolerance of defoliation (e.g. Windle and Franz 1979), tolerance of drought (e.g. Thomas 1984), greater potential longevity (e.g. Connell and Slatyer 1977) which may involve clonal spread, or the ability to deny a second nutrient to neighbors or to tolerate a lower concentration of a second nutrient (e.g. Tilman 1977, 1986). Greater potential longevity may not affect an individual's relative ability to deny resources to a neighbor but it may confer a greater ability to deny resources to that neighbor's offspring. The fitness advantage here would be augmented if the tolerance of competition from the longer-lived plant was greater for its own offspring (e.g. through greater shade tolerance or resistance to litter accumulation or allelopathic chemicals) than for the offspring of shorter-lived neighbors. 2) Genetic constraints will generally prevent any single genotype from possessing all of the attributes required to outcompete all other genotypes of either its own species OIKOS 56:3 (1989) or any other coexisting species within the community. Pleiotropism, epistasis, modifier genes or gene linkage will generally preclude certain attribute combinations and cause some attributes to be negatively correlated (Antonovics 1976, Bradshaw 1984). This assumption has never been explicitly tested, firstly because of the logistic difficulties of examining all combinations of all genotypes of all species within a community, but also because of the detailed genetic work required. sider three boxing traits for which there exists a certain level of variability in each boxer resulting from variable experiences. In terms of strength for punching intensity, three boxers are ranked A > C > B, with underlining indicating that, owing to variable experiences, the difference between two boxers is not generally great enough to significantly affect the outcome of competition between them. For their abilities to tolerate punches, the three boxers are ranked B > A > C, and in terms of speed, C > B > A. Hence, boxer A gener3) Genotypes belonging to several species within a com- ally outcompetes boxer B because of greater punching munity may form a complex intransitive rank order of intensity, B generally outcompetes C because of a relative competitive abilities defined by the different attri- higher tolerance threshold for punches received, but C bute complexes that they possess (e.g. Fig. 6). Species generally outcompetes A because of greater speed. coexistence resulting from intransitive competitive netSimilarly, consider three plant genotypes, A, B and C works at the species level has been developed theoret- and three traits affecting competitive ability: nutrient ically (Gilpin 1975, May and Leonard 1975) and has depletion rate, threshold tolerance level of phosphate been reported among species of encrusting marine in- depletion and ability to attract pollinators. A plant's vertebrates (Jackson and Buss 1975, Buss and Jackson nutrient depletion rate will be greater with a greater 1979, Russ 1980, Rubin 1982). Below, I consider three root density which may result from a longer period of mechanisms for an intransitive competitive relationship growth, resulting in turn from an earlier germination at the genotype level in plants, irrespective of species time (see Fig. 5). Suppose that for earliness of germination time, A > C > B with insignificant differences reidentity: a) Interference-mediated intransitivity. In cases where sulting from phenotypic plasticity indicated by undercompetitive ability involves interference effects such as lining. Hence, while germination time has a significant neighbor-specific allelopathy or encouragement of host- genetic component, each genotype has a certain level of specific pathogens that affect competitors (e.g. Rice and phenotypic variability resulting from the range of different microenvironmental conditions that it may encounWestoby 1982), intransitivity may result if genotype A interferes with B but not with C, B interferes with C but ter within the habitat. Genotypes A and B are genetnot with A, and C interferes with A but not with B. ically different enough to confer a statistically signifb) Resource-division-mediated intransitivity. Consider icant difference in mean germination time over the three genotypes A, B, and C and three critical resources range of microenvironmental conditions under which x, y and z. Genotypes A and B make demands on the they may interact as neighbors. Genotypes A and C same units of resource x but, for each of resources y and however are less genetically different in germination z, they make demands on different units (e.g. from time and the different microenvironmental conditions different soil depths, at different times of the year, or in experienced by neighboring individuals of genotypes A different forms) and hence, do not compete for these and C frequently overrides this genetic difference. Conresources. Similarly, genotypes B and C make demands sequently, neighboring individuals of genotypes A and on the same units of resource y but do not compete for C (or of genotypes C and B) do not differ significantly in resource x or resource z. Finally, genotypes A and C mean germination times. Similarly, for mean tolerance make demands on the same units of resource z but do of phosphate depletion, B > A > C (i.e. genotype B not compete for the other two resources. In a transitive has a significantly higher tolerance threshold of phosrelationship, A > B in competitive ability for resource phate depletion than C) and for mean ability to attract x, B > C in competitive ability for resource y, and A > pollinators, C > B > A (i.e. genotype C has signifC in competitive ability for resource z. This would result icantly more attractive flowers that A). in the exclusion of C by A and B in competition for These traits may all affect the reproductive output of resources z and y respectively, and eventually, the ex- each genotype growing in isolation, but this may be a clusion of B by A in competition for resource x. If poor predictor of its relative performance when interhowever, competitive abilities were intransitive such acting with another genotype. Based on the above attrithat A > B for resource x, B > C for resource y, and C bute rankings we can predict that, when demands on > A for resource z, then a net balance results and it is resources exceed the supply, A would deny more nutrinot possible to predict that any genotype will compet- ents to B than B would deny to A because of a signifitively exclude any other. Thus, intransitivity promotes icantly earlier germination time which confers a greater coexistence here without changing the extent to which root density for A. A and B do not differ significantly in the three genotypes make demands on the same re- the phenotypes of any other traits and so, if just A and source units. B interact, A could potentially exclude B, albeit slowly. c) Plasticity-mediated intransitivity. Again, an analogy We also predict that genotype B could potentially excan be made here with competition among boxers. Con- clude C but in this case, germination time is not a factor; OIKOS 56:3 (1989) 395 superiorcompetitiveability here is linked to a higher tolerance thresholdof phosphatedepletion. Similarly, genotypeC could excludeA for yet a differentreasongreaterabilityto attractpollinators. Several of the traits in Fig. 5 may be importantin definingdifferencesin competitiveabilityand opportunities for intransitivitywill increase as more traits are involvedand as moregenotypesare involved.Stillother traitswill be importantonly for within-speciescompetition, e.g. a larger pollen tube or a faster pollen tube growthrate (Mulcahyet al. 1983, Willsonand Burley 1983). Intransitivitytherefore, may be an inevitable consequenceof the fact thatcompetitiveabilityis not an intrinsictrait of an individualbecause it depends as much on the traits of neighborsas on an individual's own traits. Germinationtime for example, may be an importantfactor affecting relative competitive ability against a neighbor whose germinationtime is significantlyearlier or later but not againsta neighborwith the same germinationtime. The potential complexity when just twelve genotypesare involvedlooks distressingly unmanagable(Fig. 6) but it is preciselythis complexity that may have far-reachingimplicationsfor explainingcoexistence at the species level within vegetation. B. Predictions Assumptions1 and 2 predictthat severalcombinations of geneticallyvariableattributesmay confer the same overall competitiveability and that the attributecomplexes that define relativecompetitiveabilitymaydiffer for each pairof genotypeswithina communityirrespective of species identity. Hence, while genotypic variabilityfor taxonomictraits will always (by definition) be greater between species than within species, the range of genotypic variabilityfor competitive ability (defined by complexesof many traits (Fig. 2), most of whichare not taxonomicallyimportant)maybe no greater between species than withinspecies. Consequently, there may exist withina community,a groupof several genotypesbelongingto severalspecies withinwhich:1) no two genotypes differ significantlyin their competitive abilityagainsteach other, and 2) each genotypeis either superioror equivalentin competitiveability to any genotype outside the group. Those genotypesoutside this group are inferiorin competitiveabilityto at least one other genotype within the communityand have a probabilityof exclusionproportionalto the number of genotypesagainstwhichit is an inferiorcompetitor. Those individualswhich produce the most offspring therefore, will involve several genotypes, and because these genotypes belong to several species, no single populationis capableof competitivelyexcluding any other. The offspringof these superiorgenotypes however, will include genotypes with inferiorcompetitive abilities resulting from genetic recombination withineach species. Hence, there are alwayssome indi396 vidualsbeing excludedby competitionas naturalselection continuallyfavorsthose genotypeswithineach species whichare inferiorin competitiveabilityto the least numberof other genotypesof all species. Speciescoexistence here is not so muchconditionalupon this ongoing selection as it is merely a consequenceof it. If assumption3 is accepted, coexistence is also predicted but for a differentreason. Intransitivecompetitive abilities at the genotype level predictsthat there will alwaysbe some genotypewhich is a superiorcompetitor to the most commongenotype within the community or within a local neighborhood.Accordingto this intransitivityassumption,the most persistentgenotypes will be those which are superiorin competitive abilityto some genotypesbut are of necessity, inferior to some others.Consequently,theirrelativefrequencies will be in a constant state of flux driven by natural selection associatedwith genotype-intransitive competitive abilities.Becauseindividualsare sessileandcannot choose their neighbors, a given genotype may have neighboringgenotypeswithmostlysuperiorcompetitive abilities in one site within the habitat, but neighbors with mostly inferiorcompetitiveabilitieswithin another, otherwiseidenticalsite. Hence, there will alwaysbe some genotypesthat are temporarilyand locally disadvantaged and perhaps even excluded by competition fromneighborhoodscontaininggenotypeswithsuperior competitive abilities. These genotypes however, may later re-immigrateor re-emergefrom the seed bank in this site and subsequentlyincrease in frequencyafter their superiorcompetitorsare, in turn suppressedby genotypes which are superiorto them in competitive ability. In many neighborhoods,intransitiveinteractions among three or more genotypes simultaneously may have the effect of suppressing all neighbors equally. In this contextof naturalselectiontherefore,changes in genotypefrequenciesare ongoing but may rarelybe detectable at the whole populationlevel because the 'rules of the game' are continuallychangingin both space and time within the community.This is not a consequence here of genotype- (or species-) specific responseto spatialor temporalvariationin predation, parasitism,disturbanceor the backgroundphysicalenvironment. Rather, it is a consequence of genotypespecificresponseto local variationin the genotypesof neighbors,i.e. variabilityin the way that differentsessile genotypes respond to the presence of each other when resourcesare contested. The precise directionof change in genotype frequencymay vary over a spatial scale much smallerthan that of the whole population being studied.Hence, while temporaryand/orlocal exclusion of genotypeswill occur by competition,exclusion of entire species may be avoided. If there is genotype/environmentinteraction in affecting phenotype, heterogeneityin the physicalenvironmentmay alterthe rank order within an intransitivenetwork, but is not necessaryto achieve the propertyof intransitivity. OIKOS 56:3 (1989) The relative abundances of different species may fluctuate randomly under this model. Several factors however, will serve to resist 'random-walks' to permanent extinction (from the community) of entire populations of species. These include: 1) ongoing selection driven by the intransitivity at the genotype level proposed here; 2) the small effective neighborhood size and unpredictable neighborhood composition for any given individual (Aarssen 1983, Hubbell and Foster 1986); and 3) the potential for re-immigration (mass effects - Shmida and Ellner 1984) and re-emergence of genotypes from the dormant seed bank. The random elimination of all the genotypes of a given species may therefore, be extremely slow and the time scale involved may be comparable to the time scale for speciation (Hubbell and Foster 1986, Chesson and Case 1986). Given enough time, even an equilibrium coexistence involving for example, character divergence will cease due to speciation and elimination of species for reasons that do not involve competitive exclusion. It has not yet been established empirically whether, in real (as opposed to theoretical) communities, the usual time scale for equilibrium coexistence (i.e. before inevitable extinctions occur) is significantly different from the usual time scale for coexistence by similar competitive abilities. The 'net' number of coexisting species over long time scales may be maintained at similar levels in each case. Discussion According to traditional theory, the coexistence of species in a diverse community must be explainable in terms of differentiation permitting some level of interaction avoidance. "We say that all those grasses in a pasture live side by side because speciation through character displacement has found ways in which they can grow in the same field with minimal competition ... We can understand that these local inhabitants can live together provided that they do it without competing. Now we must show how there can be so many ways of not competing" (Colinvaux 1978: 178). More recent literature conveys the same view: "It is generally accepted that in order to coexist more than transiently, species must differ - they must show niche separation. If species are too similar all but one will be eliminated in competition" (Newman 1982: 61); "The competitive exclusion principle is so completely accepted that if a study reveals two species appearing to occupy the same niche, it is suspected that the study is incomplete and that further investigations will uncover differences in habitat, behaviour, or food" (Moore 1985: 508). Finally, Murray (1986: 153) called the competitive exclusion principle a "law", stated as: "two species using a homogeneously distributed, limiting resource cannot coexist for more than a short period of time". The above view has led to predictions, proposed first by Darwin (1859), that competition should be most intense between the most closely related forms and OIKOS 56:3 (1989) should therefore lead to the exclusion of one by another so that they coexist less often than expected by chance (e.g. Willson 1973: 80). A very different view however, has received attention recently. "In most plant communities, individuals of any one species will come into contact with plants of many different species. Hence, it is unrealistic to except strong selection for reduction of overlap in resource utilization between any particular pair of species because of variable and possibly opposing selection pressures, depending upon the array of neighbours" (Goldberg and Werner 1983: 1102; see also Connell 1980). Selection for divergence may also conflict with convergent adaptation. It is expected that species living in a particular habitat type will have certain attributes in common. The grasses of a grassland, for example, all share a growth habit which is adapted to grazing. Spring ephemerals share a similar life cycle permitting their growth and reproduction before the woodland canopy casts its deep shade. Antonovics (1978: 246) remarked, "Even the conflict between convergent adaptation to a common environment and divergent adaptation to other members of the community, has never been explicitly investigated." A decade later the problem remains: "Is coexistence associated with convergence or divergence? The matter is still a major problem in ecology" (Bradshaw 1987: 18). Loehle (1987) has drawn attention to the need in ecology for theory maturation before strong inference can be effective. The principle aim of this paper is to bring competitive combining ability theory to greater maturity. The competitive combining ability hypothesis derives from a 'plant's-eye' view of coexistence, i.e. it interprets coexistence at the species level as a consequence of selection resulting from interactions at the individual level within local neighborhoods. Selection for competitive combining ability is an evolutionary mechanism of coexistence, i.e. it involves evolutionary changes as a consequence of selection from competition and depends upon within-species genotypic variation (in this case, for competitive ability). The evolutionary consequence of selection for competitive combining ability however does not involve differentiation permitting reduction in the extent of interaction as in selection for ecological combining ability (Harper 1977), nor does it involve alternating frequencies of genotypes which are good interspecific competitors versus good intraspecific competitors as in Pimentel et al.'s (1965) genetic feedback mechanism. Several questions are of central importance in evaluating the plausibility of the competitive combining ability hypothesis and are hence an important focus for future research: 1) To what extent are differences in competitive abilities of neighbors a consequence of differences in genotype versus different environmental or chance experiences? Without genetic variation for competitive ability, coexistence cannot result from selection for competitive combining ability. 397 2) Can more than one combinationof plant traits(e.g. Fig. 5) result in the same relative competitive ability between neighbors? 3) What is the relative importanceof the ability to deplete resourcesversus the tolerancethresholdof resource depletion versus the allocation to fecundityof resourcesdenied to neighborsin defining the relative competitiveabilitiesof neighbors?How do these three componentsinteract? 4) To what extent do pairwiserelativecompetitiveabilities of differentgenotypes(regardlessof species) form a linear hierarchyversus a more complex intransitive network(Fig. 6)? Intransitivityat the genotype level has never been explicitlyinvestigated.Even intransitivityat the species level in plants has rarely been adequately tested. A competition matrix is needed in which each pairwise speciescomparisonof relativesuppressiveeffectsis presented (Aarssen1988).Rankingof the columnmeansor row means from such a matrixgives a rankingof average competitive abilities (e.g. Mitchley and Grubb 1986). Such a rankinghowever, can never be anything but transitive. An adequate test for intransitivityrequires a more detailed analysisof relative competitive abilities in each pairwise interaction as reflected for examplein a constellationdiagram(e.g. Fig. 6). Some studies have suggested a transitiverelationshipat the specieslevel (e.g. see Aarssen1988)but arbitrarilychosen densitiesin manystudiesoften makeit impossibleto distinguishdifferencesin relative competitiveabilities from differences in the extent to which demands are made on the same resourceunits or differencesin the resource supply/demandratio in different mixtures (Aarssen 1985, Taylor and Aarssen, in press). Many studieshave includedonly post-juvenileinteractionsor have encouraged simultaneous seedling emergence. Furthermore,while averagecompetitiveabilitiesat the species level may be transitive,this does not preclude the possibility that competitive abilities among genotypes are intransitiveand that this intransitivitymay span acrosstaxonomicboundaries.Since it is individuals that compete within the field, investigationsof intransitivityat the individualgenotype level are more relevant to an interpretationof the potential consequences of interactionsin the field, than are investigations at the species level. Since so manygeneticallyvariableattributesmay affect competitive ability under naturalconditions (e.g. Fig. 5), investigationsinto the above questionswill be complicatedby the need to: 1) accountfor the entirelife cycle, not just interactionsat post-juvenilephases; 2) ensurethat attributessuchas toleranceto pathogens,or affinity for mycorrhizalinfection have opportunityto affect competitiveability;3) performthe experiments under a variety of environmentalconditionsto determine whether intransitivityexists under some conditions but not others:and 4) replicategenotypesin order to make statisticalcomparisons. 398 If the top-rankinggenotype(s) belong(s) to only one species, then selectionfor competitivecombiningability cannot fully explain species coexistence. If genotypes form a transitivehierarchy,but the top-rankinggenotypes belong to several species, selection for competitive combiningabilitymay delay competitiveexclusion but there would be a higher probabilityof randomwalks to extinction than if competitive abilities were intransitive.Selectionfor competitivecombiningability under these instances may nevertheless represent an important evolutionary consequence of competition that operates in conjunction with other mechanisms (e.g. environmentalheterogeneity,ecological combining ability,or 'lottery'mechanisms)to preventcompetitive exclusion. For instance, species that otherwise could not coexist because they did not make demands on sufficientlydifferentresource units, may coexist if they have sufficientlysimilar competitive abilities for these contested resource units maintainedby continuous selection. Genotypes with inferior competitive abilities resultingfrom genetic recombinationmay be continuouslyousted as directionalselection favors genotypes with the best possible competitive abilities withineach species. Suchepisodesof selectionfor competitivecombiningabilitytherefore,mayset the level of "limitingsimilarity"of resourceuse and coexistencein many cases would then be incompletelyaccountedfor by ecologicalcombiningabilityalone. Selection for competitive combining ability is only one of severalpossible mechanismswhichmay operate in concertto preventcompetitiveexclusionat the population level within plant communities.Unlike other hypothesesfor species coexistence however, the competitive combiningability hypothesisalso predictsthe evolutionary consequences that might be expected withincommunitieswherecrowdingis too commonand too dramatica phenomenonfor its importanceto be doubtedand whereindividualshave apparentlyfew opportunitiesto avoid the effects of this crowdingfrom other species. - Helpfulcommentson earlierdraftsof this Acknowledgements paper were providedby B. J. Aarssen, D. Goldberg,J. B. Grace, D. Harmsen,M. J. Hutchings,P. A. Keddy, R. D. Montgomerie,and D. R. Taylor.Seed sourcesof Seneciovulgariswere graciouslysuppliedby P. B. Cavers,N. Helseth, J. S. Holt, P. Hull, G. S. Oxford,P. D. Putwain,S. R. Radosevich, H. J. Segall and S. I. Warwick.Researchreportedhere was supportedby the NaturalSciences and EngineeringResearchCouncilof Canada. References Aarssen, L. W. 1983. Ecologicalcombiningability and competitivecombiningabilityin plants:Towarda generalevolutionarytheoryof coexistencein systemsof competition.Am. Nat. 122:707-731. - 1984. On the distinctionbetween niche and competitive ability: Implicationsfor coexistence theory. - Acta Biotheor. 33: 67-83. OIKOS 56:3 (1989) - 1985. Interpretation of the evolutionary consequences of competition in plants: an experimental approach. - Oikos 45: 99-109. - 1988. 'Pecking order' of four plant species from pastures of different ages. - Oikos 51: 3-12. - and Turkington, R. 1985a. Biotic specialization between neighbouring genotypes in Lolium perenne and Trifolium repens from a permanent pasture. - J. Ecol. 73: 605-614. - and Turkington, R. 1985b. Competitive relations among species from pastures of different ages. - Can. J. Bot. 63: 2319-2325. Agren, G. I. and Fagerstrom, T. 1984. Limiting dissimilarity in plants: randomness prevents exclusion of species with similar competitive abilities. - Oikos 43: 369-375. Allen, E. B. and Allen, A. F. 1984. Competition between plants of different successional stages: mycorrhizae as regulators. - Can. J. Bot. 62: 2625-2629. Antonovics, J. 1976. The nature of limits to natural selection. Ann. Missouri Bot. Gard. 63: 224-247. - 1978. The population genetics of mixtures. - In: Wilson, J. R. (ed.), Plant relations in pastures. CSIRO, East Melbourne, Australia, pp. 233-252. Bloom, A. J., Chapin III, F. S. and Mooney, H. A. 1985. Resource limitation in plants- an economic analogy. Ann. Rev. Ecol. Syst. 16: 363-392. den Boer, P. J. 1986. The present status of the competitive exclusion principle. - Trends Ecol. Evol. 1: 25-28. Bradshaw, A. D. 1984. The importance of evolutionary ideas in ecology and vice versa. - In: Shorrocks, B. (ed.), Evolutionary ecology. Blackwell, Oxford, pp. 1-25. - 1987. Comparison - its scope and limitations. - New Phytol. 106 (Suppl.): 3-21. Burdon, J. J., Groves, R. H., Kaye, P. E. and Speer, S. S. 1984. Competition in mixtures of susceptible and resistant genotypes of Chondrilla juncea differentially infected with rust. - Oecologia (Berl.) 64: 199-203. Buss, L. W. 1980. Competitive intransitivity and size frequency distributions of interacting populations. - Proc. Natl Acad. Sci. USA 77: 5355-5359. - and Jackson, J. B. C. 1979. Competitive networks: Nontransitive competitive relationships in cryptic coral reef environments. - Am. Nat. 113: 223-234. Cable, D. R. 1969. Competition in the semidesert grass-shrub type as influenced by root systems, growth habits, and soil moisture extraction. - Ecology 50: 27-39. Caldwell, M. M., Eissenstat, D. M., Richards, J. H. and Allen, M. F. 1985. Competition for phosphorus: differential uptake from dual-isotapelabelled soil interspaces between shrub and grass. - Science 229: 384-386. Cavers, P. B. and Harper, J. L. 1966. Germination polymorphism in Rumex crispus and Rumex obtusifolius. - J. Ecol. 54: 367-382. Chesson, P. L. 1986. Environmental variation and the coexistence of species. - In: Diamond, J. and Case, T. J. (eds), Community ecology. Harper & Row, New York, pp. 240256. - and Case, T. J. 1986. Overview: nonequilibrium community theories: chance, variability, history, and coexistence. - In: Diamond, J. and Case, T. J. (eds), Community ecology. Harper & Row, New York, pp. 229-239. Clay, K. and Levin, D. A. 1986. Environment-dependent intraspecific competition in Phlox drummondii. - Ecology 67: 37-45. Cody, M. L. 1986. Structural niches in plant communities. - In: Diamond, J. and Case, T. J. (eds), Community ecology. Harper & Row, New York, pp. 381-405. Colinvaux, P. A. 1978. Why big fierce animals are rare: An ecologist's perspective. - Princeton Univ. Press, Princeton, NJ. Connell, J. H. 1978. Diversity in tropical rainforests and coral reefs. - Science 199: 1302-1310. OIKOS 56:3 (1989) - 1980. Diversity and the coevolution of competitors, or the ghost of competition past. - Oikos 35: 131-138. - and Slatyer, R. 0. 1977. Mechanismsof successionin naturalcommunitiesand their role in communitystability and organization.- Am. Nat. 111: 1119-1144. Connor,E. F. andSimberloff,D. 1986.Competition,scientific method and null models in ecology. - Am. Sci. 74: 155-162. Darwin,C. 1859.On the originof species.Facsimileof the first edition. - Harvard Univ. Press, Cambridge, MA. Dawkins, R. and Krebs, J. R. 1979. Arms races between and within species. - Proc. R. Soc. Lond. (B) 205: 489-511. Ellner, S. 1987. Alternative plant life history strategies and coexistence in randomly varying environments. - Vegetatio 69: 199-208. Evans, D. R., Hill, J., Williams, T. A. and Rhodes, I. 1985. Effects of coexistence on the performance of white cloverperennial ryegrass mixtures. - Oecologia (Berl.) 66: 536539. Fagerstrom, T. 1988. Lotteries in communities of sessile organisms. - Trends Ecol. Evol. 3: 303-306. Fitter, A. H. 1977. Influence of mycorrhizal infection on competition for phosphorus and potassium by two grasses. New Phytol. 79: 119-125. Fowler, N. 1982. Competitionand coexistence in a North Carolina grassland. III. Mixtures of component species. - J. Ecol. 70: 77-92. Fox, J. F. 1977. Alternation and coexistence of tree species. - Am. Nat. 111:69-89. Ghilarov,A. M. 1984. The paradoxof the planktonreconsidered;or, why do species coexist?- Oikos 43: 46-52. Giller,P. S. 1984.Communitystructureandthe niche.- Chapman and Hall, London. Gilpin,M. E. 1975.Limitcyclesin competitioncommunities.Am. Nat. 109:51-60. Goldberg,D. E. 1987. Neighborhoodcompetitionin an old field plantcommunity.- Ecology 68: 1211-1223. - and Werner, P. A. 1983. Equivalenceof competitorsin plant communities:A null hypothesisand a field experimentalapproach.- Am. J. Bot. 70: 1098-1104. - andFleetwood,L. 1987.Competitiveeffectandresponsein four annual plants. - J. Ecol. 75: 1131-1141. Grime, J. P. 1979. Plant strategies and vegetation processes. Wiley, New York. Grubb, P. J. 1977. The maintenance of species-richness in plant communities: The importance of the regeneration niche. Biol. Rev. 52: 107-145. - 1986. Problems posed by sparse and patchily distributed species in species-rich plant communities. - In: Diamond, J. and Case, T. J. (eds), Community ecology. Harper & Row, New York. pp. 207-225. Haila, Y. 1982. Hypothetico - deductivism and the competition controversy in ecology. - Ann. Zool. Fennici 19: 255263. Harper, J. L. 1968. The regulation of numbers and mass in plant populations. - In: Lewontin, R. C. (ed.), Population biology and evolution. Syracuse, NY, pp. 139-158. - 1969. The role of predation in vegetational diversity. - In: Diversity and stability in ecological systems. Brookhaven Symp. Biol. 22: 48-62. - 1977. Population biology of plants. Academic Press, London. Harris, G. A. and Wilson, A. M. 1970. Competition for moisture among seedlings of annual and perennial grasses as influenced by root elongation at low temperature. - Ecology 51: 530-534. Harvey, P. and Silvertown, J. 1983. Can theoretical ecology keep a competitive edge? - New Scientist 99: 760-763. Horn, H. S. 1979. Adaptation from the perspective of optimality. - In: Solbrig, 0. T., Jain, S., Johnson, G. B. and Raven, P. H. (eds), Topics in plant population biology. Columbia Univ. Press, New York, pp. 48-61. Hubbell, S. P. and Foster, R. B. 1986. Biology, chance, and 399 in terrestrialvegetation.- In: Newman, E. I. (ed.), The historyandthe structureof tropicalrainforesttree communities.- In: Diamond,J. andCase, T. J. (eds), Community plantcommunityas a workingmechanism.Blackwell,Oxecology. Harper& Row, New York, pp. 314-329. ford, pp. 61-76. Hunter,A. F and Aarssen,L. W. 1988.Plantshelpingplants. Parrish,J. A. D. and Bazzaz, F. A. 1985.Nutrientcontentof - Bioscience 38: 34-40. Abutilontheophrastiseeds and the competitiveability of the resultingplants.- Oecologia(Berl.) 65: 247-251. Hutchinson,G. E. 1961.The paradoxof the plankton.- Am. Nat. 95: 137-145. Peters,N. C. B. 1984.Timeof onset of competitionandeffects of various fractionsof an Avena fatua L. populationon Jackson, J. B. C. and Buss, L. W. 1975. Allelopathy and spatialcompetitionamongcoralreef invertebrates.- Proc. springbarley.- Weed Research24: 305-315 - 1985. Competitiveeffects of Avenafatua L. plantsderived Natl Acad. Sci. USA 72: 5160-5163. from seeds of different weights. - Weed Research 25: Janzen,D. H. 1970.Herbivoresandthe numberof tree species in tropicalforests.- Am. Nat. 104:501-528. 67-77. Joy, P. and Laitinen,A. 1980. Breedingfor coadaptationbe- Pickett,S. T. A. 1980.Non-equilibrium coexistenceof plants. - Bull. TorreyBot. Club 107:238-248. tween red cloverand timothy. Hankkija'sseed Publ.No. 13. HankkijaPlantBreedingInstitute,Finland. Pimentel,D., Feinburg,E. H., Wood, P. W. and Hayes, J. T. 1965. Selection,spatialdistributionand the coexistenceof Kuppers,M. 1985. Carbonrelationsandcompetitionbetween woody species in a central European hedgerow. IV. competingfly species.- Am. Nat. 99: 97-109. Growthformandpartitioning.- Oecologia(Berl.) 66: 343- Platt, W. J. and Weis, I. M. 1985. An experimentalstudy of 352. competitionamong fugitive prairieplants. - Ecology 66: Lewin, R. 1983. Santa Rosalia was a goat. - Science 221: 708-720. 636-639. Price, B., Rice, B., Atsatt, P. R., Fritz, R., Thompson,J. N. Loehle, C. 1987. Hypothesistestingin ecology:psychological and Mobley, K. 1986. Parasitemediationin ecologicalinteractions.- Ann. Rev. Ecol. Syst. 17: 487-505. aspectsand the importanceof theorymaturation.- Quart. Rev. Biol. 62: 397-409. Rice, B. and Westoby,M. 1982. Heteroeciousrustsas agents of interferencecompetition.- Evol. Theory6: 43-52. Lundberg,S. and Stenseth,N. C. 1985. Coevolutionof competingspecies:Ecologicalcharacterdisplacement.- Theor. Risch, S. J. and Carroll,C. R. 1986.Effectsof seed predation Popul. Biol. 27: 105-119. by a tropicalant on competitionamongweeds. - Ecology Martin,M. M. and Harding,J. 1981. Evidencefor the evolu67: 1319-1327. tion of competitionbetweentwo speciesof annualplants.Rogers, R. S. 1983. Small-areacoexistence of vernal forest Evolution356: 975-987. herbs:Does functionalsimilarityof plantsmatter?- Am. Mather,K., Hill, J. and Caligari,P. D. S. 1982. Analysisof Nat. 121: 835-850. competitiveabilityamonggenotypesof perennialryegrass. Roush, M. L. and Radosevich,R. S. 1985.Relationsbetween - Heredity 48: 421-432. growth and competitivenessof four annual weeds. - J. May, R. M. and Leonard,W. J. 1975. Nonlinearaspectsof Appl. Ecol. 22: 895-905. competitionbetweenthreespecies. SIAMJ. Appl. Math. Rubin,J. A. 1986.The degreeof intransitivity andits measure29: 243-253. mentin an assemblageof encrustingcheilostomebryozoa.J. Exp. Mar. Biol. Ecol. 60: 119-128. Mayr,E. 1970. Populations,speciesand evolution.An abridgement of animalspecies evolution.- HarvardUniversity Russ, G. R. 1980. Overgrowthin a marineepifaunalcommuPress. Cambridge. nity: competitivehierarchiesand competitivenetworks.McCown,R. L. and Williams,W. A. 1968. Competitionfor Oecologia(Berl.) 53: 12-19. nutrientsand light between the annualgrasslandspecies Salisbury,E. J. 1936. Natural selection and competition.Bromus mollis and Erodium botrys. Ecology 49: 981-990. Proc. Roy. Soc. Lond. (B) 121:47-49. McNeilly,T. 1981. Ecotypicdifferentiationin Poa annua:In- Salt, G. W. (ed.) 1984. Ecology and evolutionarybiology:A round table on research.- Univ. of ChicagoPress, Chiterpopulationdifferencesin response to competitionand cutting.- New Phytol. 88: 539-547. cago. - 1984. Ecotypic differentiationin Poa annua:within pop- Schoener,T. W. 1982.The controversyover interspecificcomulationvariationin responseto competitionand cutting.petition.- Am. Sci. 70: 586-595. - 1983. Field experimentson interspecificcompetition. New Phytol. 96: 307-316. Am. Nat. 122:240-285. Mitchley,J. and Grubb,P. J. 1986. Controlof relativeabundanceof perennialsin chalkgrasslandin southernEngland. Seaton,A. J. P. andAntonovics,J. 1967.PopulationinterrelaI. Constancyof rank order and results of pot- and fieldtionships.I. Evolutionin mixturesof Drosophilamutants.experimentson the role of interference.- J. Ecol. 74: Heredity(Lond.) 22: 19-33. 1139-1166. Sheldon,J. C. 1974. The behaviourof seeds in soil. III. The Moore, J. A. 1952.CompetitionbetweenDrosophilamelanoinfluenceof seed morphologyand the behaviourof seedgaster and Drosophila simulans. II. The improvement of lings on the establishmentof plants from surface lying competitiveability throughselection. Proc. Natl Acad. seeds. - J. Ecol. 62: 47-66. Sci. USA 38: 381-407. Shmida,A. andEllner,S. P. 1984.Coexistenceof plantspecies - 1985. Science as a way of knowing - human ecology. - Am. with similarniches.- Vegetatio58: 29-55. Zool. 25: 483-637. Siddiqi,M. Y., Glass, A. D. M., Hsiao, A. I. and Minjas,A. Mueller,L. D. 1988. Evolutionof competitiveabilityin DroN. 1985. Wild oat/barleyinteractions:Varietaldifferences naturalselection.- Proc.Natl sophilaby density-dependent in competitivenessin relationto K+supply.- Ann. Bot. 56: Acad. Sci. USA 85: 4383-4386. 1-7. Mulcahy,D. L., Curtis,P. S. and Snow, A. A. 1983. Pollen Silvertown,J. W. 1983.The distributionof plantsin limestone competitionin a naturalpopulation.- In: Jones, C. E. and pavement:tests of speciesinteractionand nicheseparation Little, J. R. (eds), Handbookof experimentalpollination. againstnull hypotheses.- J. Ecol. 71: 819-828. - and Law, R. 1987. Do plants need niches? Some recent Van NostrandReinhold,pp. 330-337. Murray,B. G. Jr. 1986.The structureof theory,andthe role of developmentsin plant communityecology. - TrendsEcol. competitionin communitydynamics.- Oikos 46: 145-158. Evol. 2: 24-26. Negbi, M. 1986.The scutellumof Avena:a structureto maxi- Simberloff,D. 1982.The statusof competitiontheoryin ecolmize exploitationof endospermreserves.- Bot. J. Linn. ogy. - Ann. Zool. Fennici19: 241-253. Soc. 93: 247-258. Steward, F. M. and Levin, B. R. 1973. Partitioningof reNewman,E. I. 1982.Niche separationandspeciescoexistence sources and the outcome of interspecificcompetition:a 400 OIKOS56:3 (1989) model and some generalconsiderations.- Am. Nat. 107: 171-198. Strong,D. R., Simberloff,D., Abele, L. G. andThistle,A. B. (eds). 1984.Ecologicalcommunities:conceptualissuesand the evidence. PrincetonUniv. Press, Princeton. Taylor,D. R. and Aarssen, L. W. (in press). On the densitydependence of replacement series competition experi- Watson,M. A. 1980.Patternsof habitatoccupationin mosses - Relevance to considerationsof the niche. - Bull. Torr. Bot. Club 107:346-372. Weaver,S. E. 1984. Differentialgrowthand competitiveability of Amaranthus retroflexus, A. powellii and A. hybridus. - Can. J. PlantSci. 64: 715-724. Wiens,J. A. 1987.Competitionor peacefulcoexistence?- In: ments. - J. Ecol. Eldredge,N. (ed.), The naturalhistoryreaderin evolution. Thomas,H. 1984. Effects of droughton growthand competColumbiaUniv. Press, New York, pp. 71-78. itive ability of perennialryegrassand white clover. - J. Willson,M. F. 1973.Evolutionaryecologyof plants,a review. PartIV. Niches and competition.- Biologist55: 74-82. Appl. Ecol. 21: 591-602. Tilman, D. 1977. Resource competitionbetween planktonic - andBurley,N. 1983.Matechoicein plants:Tactics,mechanisms and consequences.- PrincetonUniv. Press, Princealgae: An experimentaland theoreticalapproach.- Ecology 58: 338-348. ton, NJ. - 1984.Plantdominancealongan experimentalnutrientgra- Windle, P. N. and Franz, E. H. 1979. The effects of insect dient. Ecology 65: 1445-1453. parasitismon plant competition:greenbugsand barley. - 1986. Resources, competitionand the dynamicsof plant Ecology60: 521-529. communities. In: Crawley,M. J. (ed.), Plant ecology. Wolek, J. 1984. Intraspecificvariationand the competitive Blackwell,Oxford,pp. 51-65. abilities of Spirodela polyrrhiza (L.) Schleiden. - Ekol. pol. Turkington,R. and Harper,J. L. 1979. The growth,distribu32: 637-649. tion and neighbor relationshipsof Trifoliumrepens in a Wulff, R. D. 1986. Seed size variationin Desmodium panicpermanentpasture.IV. Fine-scalebiotic differentiation.ulatum.III. Effects on reproductiveyield and competitive J. Ecol. 67: 245-254. ability.- J. Ecol. 74: 115-121. 26 OIKOS 56:3 (1989) 401