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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
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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.
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