The Community-Level Consequences of Seed Dispersal Patterns
Author(s): Jonathan M. Levine and David J. Murrell
Source: Annual Review of Ecology, Evolution, and Systematics, Vol. 34 (2003), pp. 549-574
Published by: Annual Reviews
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Annu. Rev. Ecol. Evol. Syst. 2003. 34:549-74
doi: 10.1146/132400
Copyright@ 2003 by AnnualReviews. All rightsreserved
First publishedonline as a Review in Advance on July 30, 2003
OF
THE COMMUNITY-LEVEL
CONSEQUENCES
PATTERNS
SEEDDISPERSAL
M.Levine'andDavidJ.Murrell2
Jonathan
andMarine
Evolution,
Biology,
University
of California,
ofEcology,
1Department
SantaBarbara,
93106;email:[email protected]
California
atSilwood
2Center
Park,Ascot,
forPopulation
Biology,
Imperial
College
Berkshire
email:[email protected]
SL57PYUnited
Kingdom;
distribution,
KeyWords abundance,
aggregation,
diversity
U Abstract Becauseit laysthetemplate
fromwhichcommunities
develop,thepatternof dispersed
seedis commonly
believedtoinfluence
structure.
Totest
community
thevalidityofthisnotion,weevaluated
theoretical
andempirical
worklinkingdispersal
kernelsto therelativeabundance,
andcoexistence
of species.
distribution,
dispersion,
Wefoundconsiderable
theoretical
evidencethatseeddispersal
affectsspeciescoexistenceby slowingdownexclusionthrough
localdispersal
anda competition-dispersal
wasscant.Instead,mostempirical
extrade-off,
yet empirical
support
investigations
aminedhowdispersalaffectsspeciesdistribution
anddispersion,
with
little
subjects
theory.Thisworkalsoreliedheavilyondispersal
proxiesandcorrelational
analysesof
methodsunableto excludealternative
community
patterns,
hypotheses.
Owingto the
overalldichotomy
betweentheoryandempirical
results,we arguethattheimportance
of dispersal
cannotbetakenforgranted.
Weconcludeby advocating
that
experiments
the
seed
and
models
that
documanipulate
dispersal
pattern,
incorporate
empirically
menteddispersal
kernels.
INTRODUCTION
the importanceof dispersalfor the
Althoughecologistshave long appreciated
and
of
spread persistence populations(Harper1977,Howe& Smallwood1982,
Skellam1951),thelastdecadehaswitnesseda surgeof interestin howthisphase
of the life cycle influencescommunitystructure
(Bullocket al. 2002, Cainet al.
2000,Clobertet al. 2001,Nathan2003,Nathan& Muller-Landau
2000,Wang&
Smith2002).Theoreticalmodelshavebeenan important
motivatingforce,with
numerousstudiesemphasizingthe importance
of spatialstructure
in influencing
speciesinteractions.
Particularly
tantalizingareresultssuggestingthatlocalseed
colonizationtrade-offsfavorthecoexistenceof competidispersalorcompetition
tors (Murrellet al. 2001, Pacala 1997, Rees et al. 1996, Tilman 1994). Results
such as these are mirroredin the tropical forest literature,where theories emphasizing the importanceof limited dispersalhave gained prominence(Hubbell
1543-592X/03/1215-0549$14.00
549
550
LEVINEE MURRELL
2001). Meanwhile, empiricalecology is increasinglyimplicatingdispersalas an
andobcontroloverspeciesdiversity.Numerousrecentexperimental
important
servationalresults suggest that local communities are seed limited, with diversity limited largely by the regional species pool (Cornell 1993, Srivastava1999,
et al.2000).Interesthasalsobeenheightened
Turnbull
proby dispersal-mediated
cesses in conservationbiology, includinghabitatfragmentation(Hanski& Gilpin
1997), species abilityto migratewith climatechange (Clark1998), andthe spread
et al. 1989).
invasions
of biological
(Drake
Althoughthe influenceof dispersalon communitystructureis only beginningto
causalrelationship.
seemtoexpectanimportant
berigorously
examined,
ecologists
This is likely because dispersalis believed to set the templatefrom which com-
to influencepopulationspread
munitypatternsdevelop,andis well documented
andpersistence(Hanski& Gilpin1997,Harper1977,Skellam1951).However,
spreadandpersistenceareverydifferentresponsevariablesfrommostmeasures
of communitystructure,includingpatternsof abundance,distribution,and coex-
the templatelaidby dispersal,oftenreferredto as the
istence.Moreimportantly,
seedrain,is influencedby otherpotentiallymoreimportant
factors,includingthe
distribution,density,andfecundityof parentplants(Clarket al. 1998, Platt 1975),
as well as landscapefeaturesthattrapseeds (Schneider& Sharitz1988) (Figure1).
Moreover,as notedby severalauthors(Nathan& Muller-Landau2000, Schupp&
Fuentes 1995, Wang& Smith 2002), a numberof importantlife historyprocesses
to adultplants.Speciesinteractions
occurbetweendispersalandtheprogression
andenvironmentalfactorsstronglyinfluencethese transitionsandcan significantly
changethe templatelaid by dispersal(Figure1). Thus,unless populationsare substantiallyseed limited, the importanceof the dispersalkernel for the abundance,
distribution,and diversityof species should not be assumeda priori.
In thispaper,we criticallyreviewtheoreticalandempiricalworkrelatingpatternsof dispersalto spatialpatternsin communitiesin an attemptto providea
critical frameworkfor researchin this area. More specifically, we ask how importantthe specific seed dispersalkernelor seed shadowis for explainingrelative
abundance,distributions,andcoexistencein naturalcommunities.By dispersalkernel, we mean the probabilitydensity function describingthe probabilityof seed
transportto various distances from the parentplant. Although both theoretical
andempiricalapproachesaddressthe importanceof seed dispersalfor community
structure,a large gap exists in the coverage and motivationbehind the different
methods. As we demonstrate,the modeling work is focused largely on coexistence, motivatedby interest in how incorporatingspatial processes changes the
predictionsof earliernonspatialmodels. Meanwhile, the empiricalwork focuses
largely on dispersal'seffect on species distributions,motivatedby naturalhistory
observationsrelated to dispersalkernels, the movement of animal vectors, seed
trappingpatterns,or the clumping of parentplants. Thus, of primaryinterestin
our review is how empiricalresultsmatchthe predictionsof theory.
To encourage a greaterexchange of ideas and questions between empirical
and theoreticalapproaches,we organize our review aroundthe influence of dispersal kernels on four key features of community structure:patternsof relative
DISPERSAL
EFFECTS
ONCOMMUNITIES 551
Distribution
of SeedSources
Densityof SeedSources
Dispersal Kernel
SeedProduction
features
that
Landscape
trapseeds
Pattern of
Seed Rain
Environmental
Factors
Species
Interactions
Abundance,
Distribution,
andDiversity
of Species
Figure 1 Pathwayby whichthe shapeof speciesdispersalkernelscan influencethe
abundance,distribution,and diversityof species. Shownin bold is the link between
dispersalkernalsandcommunitypatternsthatwe examinein thisreview.Weemphasize
the multitudeof factorsotherthandispersalkernelsinfluencingthe seed rain,andthe
multitudeof factorsotherthanseed raininfluencingthe abundance,distribution,and
diversityof species.
abundance,distribution,dispersion,and coexistence. For each of these features,
we firstcharttheoreticalpredictionson the importanceof dispersalandthenreview
evidence for these predictionsin the empiricalliterature.We located our papers
by electronicallysearchingthe Science CitationIndex and examiningreferences
therein.Because of the large body of theoreticalwork on coexistence, we divide
this literatureinto two sections, one describingthe effects of local dispersal,the
otherfocused on competition-dispersaltrade-offs.For similarreasons, we review
the work examiningdispersaleffects on dispersionseparatelyfrom work on other
types of distributionpatterns.We do not reviewdispersaleffects on persistenceand
spread(Hanski& Gilpin 1997, Howe & Smallwood 1982, Shigesada& Kawasaki
2002, Skellam 1951), the evolution of dispersal (Clobertet al. 2001), or the effects of colonization on communitypatternsachieved throughdormancyor high
fecundity.Still, it shouldbe notedthatboth dormancyandfecunditycombinewith
dispersalto influencecolonization(Harper1977).
RELATIVE
ABUNDANCE
Theoretical
Background
Over the past decade, it has become increasinglycommon to regardlocal populations as embeddedwithin a largermetapopulationstructure.In classic (Levins
&Gilpin1997)metapopulation
1969)andcontemporary
(Hanski
models,species
abundance at the metapopulationscale is a function of the colonization and
552
LEVINEm MURRELL
or patches.Thus,speciesabilityto disextinctionof individualsubpopulations
of relativeabundance-whichspeciesare
determinant
persemaybe animportant
commonandwhicharerare.
alsoemerges
thatdispersalis positivelyrelatedto abundance
Theexpectation
in severalothertypes of models(Turnbullet al. 2000). In spatialmass effect
habimodels(Shmida& Ellner1984), speciesoccupymarginallyunfavorable
tatsbecauseof seed inputfromother,morefavorable,locations.Greaterinput
in thesesystems.Similarly,
causedby increaseddispersalcanenhanceabundance
if communitydynamicscan be conceivedas a competitivelottery(Chesson&
Warner1981),speciescan dominatesystemsby havinghighcolonizationrates,
achievablethrougheffectivedispersalor high fecundity.Greaterabundanceof
hypothesis
better-dispersing
speciesis also predictedunderthe Janzen-Connell
(Connell1971,Howe1989,Janzen1970,Schupp&Fuentes1995),wheredispersalawayfromtheparentplantconfersgreatlyreduceddensity-dependent
mortality
(Ellner2001,Lawet al. 2003,Pacala& Silander1985).Althoughsimilarpredictionsemergefromthesemodelscollectively,it is themetapopulation
predictions
how
abundance
at
tests
of
in motivating
thathavebeenmostinfluential
empirical
scalerelatesto dispersalability(Eriksson1997,Eriksson&
the metapopulation
Jakobsson1998).
Thesetests, however,may not have consideredthatlong-rangedispersalis
in models.Forexample,if the landscapeis variable
sometimesdisadvantageous
in (abiotic)quality,dependingon the spatialscaleof favorableandunfavorable
thanlong-rangedisdispersalmayleadto higherabundance
patches,short-range
&
Travis
et
al.
1998,
Dytham1999).In thesecases
persal(Bolker2003,Dockery
thanoutweighsthe increased
more
in
a
of
the importance remaining goodpatch
from
often
dispersal.
short-range
resulting
competition
intraspecific
EmpiricalEvidencefor a RelationshipBetween
Dispersaland Abundance
levelwould
Inadditionto theoretical
empiricalworkatthepopulation
predictions,
seemto suggestthatspeciesabilityto disperseis an important
predictorof relaatleastin somesystems.A numberof seedadditionexperiments
tiveabundance,
(see Turnbullet al. 2000 for review) suggest that for early successional systems
seedlimitationis common,andthusgreaterdispersalshouldconfer
in particular,
Nonetheless,in ourreviewof empiricalevidence,we found
greaterabundance.
was controlledby dislittle supportfor the expectationthatrelativeabundance
persalpatterns.Forexample,Rabinowitz& Rapp(1981)foundno relationship
betweenabundanceand dispersalunderfield conditionsin a Missouriprairie.
Similarly,Eriksson& Jakobsson(1998)foundthatdispersalmodewasunrelated
to abundanceandgeographicrangesize for over 80 grasslandplantspeciesin
Sweden. Also in Sweden, the ability of 17 species to disperse on the fur of animals was unrelatedto theiroccupancyratesin seminaturalgrasslands(Kiviniemi
& Eriksson 1999). In the herbaceousflora of centralEngland, seed dispersalas
DISPERSAL
EFFECTS
ONCOMMUNITIES 553
estimated through terminal velocity was very weakly related to species abundance as assessed by their UK range (Thompsonet al. 1999). Thompson et al.
(1999) andEriksson& Jakobsson(1998) reviewedthe literaturerelatingdispersal
mode to geographic range size more generally and found similarly ambiguous
results.
Support for the notion that dispersal dictates commonness and rarity might
seem to come from annual plant communities. It is often found that common
species are small seeded, whereaslarge-seededspecies are consistentlyrare(Guo
et al. 2000, Levine & Rees 2002, Maranon& Grubb1993, Rees 1995, Rees et al.
1996). However,althoughsmall-seeded species may be bettercolonizers, this is
more likely the resultof a relationshipbetween seed size andfecundityratherthan
seed size and dispersal. Small-seeded species consistently produce more seeds
(Jakobsson& Eriksson2000, Leishman2001, Rees 1995, Shipley & Dion 1992,
Turnbullet al. 1999), yet seed size is very poorly related to dispersal (Carey &
Watkinson1993, Westobyet al. 1996).
How can we explain the absence of a relationshipbetween abundanceand
seed dispersalwhen experimentsoften show seed-limitedpopulations?One likely
possibility is that the evidence for seed limitationis more a productof low seed
productionor a low density of adult plants than of poor dispersal. In addition,
numerousotherprocesses, such as competition,dormancy,and habitatvariation,
may simplybe moreimportantthandispersalin controllingrelativeabundancepatternsin communities(Figure1). Because dispersalcan clearlyinfluencethe rateof
species arrival,it may be more importantin controllingtemporalpatternsof abundance afterdisturbance.In a simulationstudy,Hovestadtet al. (2000) showedthat
long-rangedisperserswere more abundantin the colonizationphase immediately
after disturbance,but dependingon model details, short-rangedisperserssubsequentlyobtaineda higherrelativeabundance.Indeed,on lake islands in Sweden,
species lacking traitsfor water,wind, or animaldispersalare rareor absentearly
in succession (Rydin & Borgegard1991), but become abundantyears later.Despite these temporalpatterns,we conclude that little empiricalevidence supports
the expectationthatinterspecificdifferencesin dispersalcontrolcommonnessand
rarityat metapopulationscales.
SPATIALDISTRIBUTION
TheoreticalBackground
The distance and direction a plant disperses its seeds should play an important
role in the distributionof that species. However, as illustratedin Figure 1 (left),
the influence of the dispersal kernel will depend strongly on the importanceof
other factors influencing the seed rain. For example, Levine (2003) modeled a
streamsideplant assemblage where species occur in discrete habitatpatches linearly arrayedalong the channel. Species dispersed 60% of their seeds to other
patches and 95% of those seeds to patches downstream.In such a system, one
554
LEVINEm MURRELL
thanupstream.
However,Levine
naturally
expectsgreaterdepositiondownstream
of parentplantsthroughout
the
thatwith a uniformdistribution
demonstrated
comes
from
the
one
a
reasonable
most
seed
and
kernel,
input
dispersal
system
of the firstfew
or two patchesupstreamof the targetpatch.Thus,downstream
in
the
seed
increases
Still,
only marginally. thisrelatively
system,
input
patches
increases
variationin seeddepositioncoulddrivedownstream
smalldownstream
are
in population
size anddiversity,butonlyif thecomponent
populations highly
Thisresult
seedlimited,asresultingfromverylowfecundityorrecentdisturbance.
between
1.
the
two pointsintroduced
demonstrates
by Figure First, relationship
the seed-dispersal
kernelandthe seedraincanbe complicated,
deservingsignifiandempiricists.
fromboththeoreticians
Second,forpatterns
cantlymoreattention
the componentpopulationsmust
of seed rainto influencespeciesdistributions,
or environmental
andnot speciesinteractions
be constrained
by seedavailability
factors.
The Importanceof Seed-TrappingAgents
In contrastto theory,numerousempiricalstudieshaverelatedseeddepositionto
yet in mostof the work,spatialvariationin depositionis
speciesdistributions,
not easily relatedto the dispersalkernels.Instead,it is drivenlargelyby landstill
Differencesin seedmorphology
scapeelementsthattrapseedsorpropagules.
withthe
influencedepositionpatternsbutdo so largelythroughtheirinteraction
trappingagents.Forexample,Schneider& Sharitz(1988)trackedthe dispersal
UnitedStates.Seedswereiniof treeseedsin a swampforestin the southeastern
levels
as
water
but
then
rose,theywereredistributed
by
tiallygravitydispersed,
structures
to locationsagainstemergent
includingtwigs,trees,logs,
hydrochory
branches,knees,and stumps.Some of these substrates,such as treesand tree
knees,providedelevatedstablemicrosites,andtreeseedlingsweredisproportioninfluenced
seedmorphology
deposition
atelyfoundintheselocations.Importantly,
andseedlingpatternsacrossspecies.Thesmall,angularcypressseedsweremore
frequentlytrappedby kneesthanthe largerellipsoidtupelofruits.Consequently,
45%of the cypressseedlingsoccurredon kneesin comparisonto only 27%of
tupeloseedlings.
reSeveralstudiesconductedin northernSwedishrivershaveexperimentally
theirdepositionwithspecies
mimicsandcorrelated
orpropagule
leasedpropagules
and diversity.Althoughnot a seed-dispersal
distributions
study,Johansson&
Nilsson(1993)taggeduniformlysizedrametsof the vegetativelydispersingRatheirdepositionwiththe presenceof established
nunculuslinguaandcorrelated
found
that
ramet
high in curves
depositionwas disproportionately
plants.They
standstended
established
where
locations
also
the
the
andatobstaclesalong river,
a
similar
to be found(see Anderssonet al. 2000 for
focusingon diverapproach
sity). Patternssuch as these may relateto propagulecharacteristics.Nilsson et al.
(1991) found that long-floatingspecies tended to be more abundantin areasthat
trappedfloating seed mimics, whereas the distributionof short-floatingspecies
EFFECTS
ONCOMMUNITIES 555
DISPERSAL
was unrelatedto trappingpatterns.Danvind& Nilsson(1997) foundno correlationbetweenfloatingtime anddistribution
patternsalongan alpineSwedish
river.
hasalsobeencorrelated
withspeciesdistriSeeddepositiondrivenby trapping
studies.Rabinowitz(1978)hypothesized
thatthe different
butionsin nonriverine
sized seedsof the threemangrovedominantsin Panamaweretrappedat differentpointsalongthetidalelevationgradient,matchingtheelevationaldistribution
of mangrove
of adulttrees.Supportwas providedby the experimental
transport
outside
their
tidal
which
showed
across
theelevation
zone,
survivorship
propagules
recent
work
Sousa
&
B.
inreview)
Nonetheless,
Mitchell,manuscript
(W.
gradient.
in
the
kernels
the
same
forests
has
found
no eviestimating dispersal
mangrove
In a similarsystem,Rand(2000)foundthat
dencefortidalsortingof propagules.
of severalsaltmarshspeciesto particular
therestricted
distribution
tidalelevations
andphysiological
stressesthanseeddeposition
wasmorea functionof competition
forms
patterns.In contrast,in theNegevdesertof Israel,Anasticahierochuntica
reticulatedistribution
thatrelateto seeddepositionin thecracksthatform
patterns
withthewettinganddryingof thesoil (Friedman
& Stein1980).Peart& Clifford
thesegregation
of grassspeciesacrossdifferentsoil typesto the
(1987)attributed
interactionof the soil textureandcrackingwith the differentawn typesof the
variousspecies.
In thesestudies,patternsof seeddepositionresultfromstructures
or topograthat
or
sorts
Seed
then
influences
not
traps
phy
propagules. morphology
onlyhow
seedsmove,butmaybemoreimportantly,
whereseeds stop,a less appreciated
andmoredifficultto predictcomponentof thedispersalkernel.Therealizeddistributionof seedsmaythereforebe verydifferentthanthe potentialdistribution
surroundbythedispersalkernelalone.Inaddition,thelocalcommunity
predicted
inga dispersingindividual
maystronglyinfluencethedispersalkernelby trapping
seedsandinfluencing
thesizeof thedisperserthroughcompetition.
Consequently,
furtherworkclarifyingtherelationship
betweendispersalkernelsandpatternsof
for clarifyingits influenceon
deposition(Figure1, left) is particularly
important
distributions
et al. 2000).
(Alcantara
Distributions Driven by Dispersal Kernels
kernelsto distribution
Relativelyfew studiesrelatedseed-dispersal
patterns.In
one of the only studiesrelatingdispersalto the seed rain,Dallinget al. (2002)
demonstrated
thatspatialpatternsof seedrainformanyneotropical
pioneertrees
were drivenlargelyby limiteddispersal.The resultingseed rainpatternswere
an important
in forestgaps. Similarly,Platt&
predictorof seedlingabundance
Weiss(1977)examinedfield-derived
dispersalkernelsandcompetitivetraitsof
on
mounds
in anIowaprairie.Thespeciessegregate
fugitiveplantsliving badger
acrossa habitatgradientin mounddensitysuchthatthe morepoorlydispersing
species dominate the portion of habitat with closely spaced mounds, whereas
better-dispersingspecies dominatethe areawith distantlyspacedmounds.Parallel
556
LEVINEm MURRELL
differences
inphysiological
tolerance
in soilmoisture
andinterspecific
gradients
maintain
thespeciessegregation.
thatasymmetric
Several
riverine
studies
downstream
beginwiththeassumption
in
seed
in
these
drives
variation
systems(butsee
deposition
dispersal longitudinal
increases
in diversity
todispersal.
Levine2003).Theythenattribute
downstream
oftheVindelriverinSwedencontained
Nilssonetal.(1994)foundthattributaries
tothe
onlya subsetofthosespeciesfoundinthemainstem,aresulttheyattributed
seeds.
et
al.
downstream
and
accumulation
of
Honnay (2001)analyzed
transport
networks
ofsmall
inplantcommunities
ofdiversity
alongdendritic
spatial
patterns
see
Friedman
&
came
similar
conclusions
Stein
foreststreams
and
to
(also
1980).
of community
Thesestudies,
aresimplycorrelational
however,
analyses
patterns.
orlimitation
aremade,andthusas
of seeddispersal,
Nomeasurements
deposition,
environotherprocesses,
Nilssonetal.(1994)acknowledge,
changing
particularly
thediversity
couldalsoexplain
conditions
mental
gradient,
alongthedownstream
wastakenbyLevine(2001),whodocuA moremanipulative
approach
pattern.
in diversity
andindividual
increases
menteddownstream
plantabundance
along
mimics
released
theEelriverinCalifomrnia.
successfully
Experimentally propagule
were
andthestreambed
tosuitable
microsites
downstream,
assemblages
dispersed
whenseedsupplywasexperimentally
seedlimited.Mostimportantly,
equalized
colonization
of themost
therewasno greater
acrossthedownstream
gradient,
even
withthose5 kmupstream.
habitats
as compared
downstream
Nonetheless,
to
drive
downis
sufficient
whether
downstream
withallthisevidence,
dispersal
inthisandotherwork.
untested
remains
increases
in seeddeposition
stream
ourreviewdocumented
in
of
the
relative
rarity hydrochorynature,
Considering
influenced
where
water
number
of
studies
a disproportionate
species
dispersal
movement
to
the
obvious
directional
attributed
Inpart,thiscanbe
distributions.
thatlineriversand
theplantcommunities
Inaddition,
of waterin manysystems.
suchascompetition
arereadilydisturbed,
lakeshores
processes
likelypreventing
theirfullimpacts.
fromexerting
Last,thefloodingthatoccursin thesehabitats
seedlimitation
canexportmostof theseed,favoring
(Levine2001).Despitethe
few
insystems
withhydrochory,
fordistributions
ofdispersal
importance
apparent
orexamined
testedforseedlimitation
studiesintheseorotherhabitats
empirical
to adultplants.
andtheprogression
betweenseedarrival
theprocesses
occurring
to resultfrom
are
of whether
thedistribution
Thus,regardless
argued
patterns
as
a
whole
is highly
evidence
the
or
kernels,
empirical
agents dispersal
trapping
for
the
alternative
unable
to
exclude
often
correlational,
putative
explanations
distribution
patterns.
dispersal-driven
DISPERSION
The aggregationof species in communitiescan influence the rate of competitive
(Stoll& Prati2001),patternsof resourceavailability(Pastoret al.
displacement
and
1999),
patternsincludingspecies-areacurvesandspeciesmacroecological
distributions
abundance
(Chaveet al. 2002).Becauselocaldispersalis anobvious
EFFECTS
ONCOMMUNITIES 557
DISPERSAL
sourceof clumping,numerousstudiesattributeadultaggregationto restricted
seed transport.
However,as is truewith distribution
patternsmoregenerally,a
numberof conditionshaveto be met beforedispersalcontrolsdispersionpatterns(Schupp& Fuentes1995).Not only mustthe componentpopulationsbe
so sparselyarrayedthatlocal dispersaldrivesclumpingof dispersedseeds,but
cannotbe so severeasto eliminatetheaggregation
of
mortality
density-dependent
seedlings.
Models Where LocalDispersalGeneratesAggregation
Bleheret al. (2002)usedsimulationmodelsto showthatlocaldispersaland,to a
lesserdegree,low adultdensitystronglyinfluencedthe clumpingof foresttrees.
Bleheret al. accomplishedthis by constraining
fecunditysuchthatall species
one
but
the
relevance
of suchgrowthratesto natueffectivelyproduce offspring,
ralsystemsis unclear.Presumably,
withdifferentfecundityacrossspecies,some
wouldgrowandtheirpatcheswouldcoalesce,whereasotherswould
populations
declineandtheirclumpscontract.LikeBleheret al., Chaveet al. (2002)examined clumpingpatternsin neutralmodels(wherebirthratesjust balancedeath
rates),andshowedgreaterclumpingwithincreasedlocaldispersal.Chaveet al.
alsoexploredtheinfluenceof localdispersalin modelswherestablecoexistence
is achievedthrougha competition-fecundity
trade-offanddensitydependence.
Theyshowedthatwhentheseotherprocessesgeneratecoexistence,localdispersal can stronglyinfluenceclumping,whichcausesthe species-areacurveto rise
moregraduallythanwhenspeciesaremorediffuselyspreadthroughthehabitat.
Dispersal-generated
clumpingcanalsoinfluenceecosystemprocesses.In a simulationmodelof borealforestwherespeciesdifferin decomposability,
Pastoret al.
thataltersthe
(1999) showedhow local dispersalgeneratesspeciesaggregation
spatialpatternof nitrogenavailability.
Furthersupportfortheinfluenceof localdispersalon clumpingis explicitlyor
its impacton coexistence(reviewed
implicitlyprovidedby studiesdemonstrating
it
is
to
remember
that
below).Still,
important
dispersalis justone of severalspatialprocessesthatshapethepatternof individuals
acrossthelandscape(Figure1)
&
Fuentes
For
because
interactions
betweenindividuals
1995). example,
(Schupp
alsotendtobelocalizedin space,offspringexperience
intensekincompetition
with
localdispersal.Theoryshowsthatlocalinteractions
cancausetherealizedpattern
of adultsto be random,overdispersed
(spatiallysegregatedor evenlyspaced)or
clumped(Ellner2001, Lawet al. 2003, Molofskyet al 2002, Pacala& Silander
to achieveaggregation
in homogeneous
1985).Generally,
spacewithlocaldispermustoccuron a spatialscalesimilarto thatof thedispersalkernel
sal,interactions
(Ellner2001,Lawet al. 2003, Pacala& Silander1985).If dispersaloccursover
muchlargerscalesthanneighborhood
interactions
thenanevenspacingof conspecificindividuals
is expected(Lawet al. 2003).Alternatively,
processesotherthan
dispersal(Figure 1), such as spatialheterogeneityin the externalenvironment,or
reducedpollinationof isolatedindividuals,may also generateaggregation.In sum,
theory suggests that dependingon the spatial scale of density dependence,local
558
LEVINEN MURRELL
dispersalcandrivea widerangeof dispersionpatterns,patternsthatcanalsobe
explainedby variationin environment.
EmpiricalEvidence
localseeddispersalandanaggregated
A largebodyof empiricalworkdocuments
of adults,and suggestsa causallink betweenthe two (e.g., Bleher
distribution
& Bohning-Gaese 2001, Fragaso 1997, Westelaken & Maun 1985). However,
as arguedby Schupp& Fuentes(1995)andputforthby theoreticalworkmore
betweenseedarrivaland
generally,becauseof theprimacyof processesoccurring
to demonstrate
is
insufficient
evidence
correlative
to
adult
this
plants,
maturity
local
documented
Overton
Indeed,
(1996)
dispersalof
patterns.
dispersal-driven
in the numberof
mistletoe,butthis hadno effecton the spatialautocorrelation
studieshavefoundthattheaggregated
numerous
mistletoepertree.Moregenerally,
as
of seedsandseedlingsfollowinglocaldispersaltendsto disappear
distribution
theseedlingsmature(Barotet al. 1999,Houle1995,Rey&Alcantara
2000,Schupp
and
ourreviewon severalmorequantitative
&Fuentes1995).Wethusconcentrate
for
of
the
to assessing importance dispersal aggregation
approaches
comparative
patterns.
to dispersalfor explaininga clumpedspecies
Becausethe majoralternative
distributioninvolves patchyenvironmentalvariables,one approachfor testing the
toaskwhetherspeciesare
of localdispersalis tousemultipleregression
importance
moreclumpedthancan be explainedby spatialvariationin the environmentalone.
of fourpalmspeciesin an AndeanrainSvenning(2001)foundthataggregation
forestcouldnotbe explainedby variationin foreststructure,
topographic-edaphic
conditions,altitude,or aspect.This,coupledwithgreaterdensitiesof seedlings
near adult plants, caused the investigatorto implicate dispersalas a control over
the clumped distributionof these species. With a similar approach,Svenning &
Skov (2002) found that in a managed forest in Denmark,20 of 60 understorey
plant species exhibited aggregationunexplainableby environmentalparameters
to dispersal.Moreover,animal-andwind-dispersed
andthusattributable
species
showedless clumpingthanspecieswithless-efficientdispersalmodes.Incontrast
variablesin influencingtree
of environmental
to theseresults,thepredominance
clumping patternswas suggested for the palm Borassa aethiopumin an African
savanna(Barotet al. 1999)andforspeciesoccupyingSouthPacificisland(Webb
& Fa'aumu1999)andMalaysian(Plotkinet al. 2002)forest.
havebeenusedto attribute
Similarapproaches
throughspace
speciesturnover
to dispersal.Tuomistoet al. (2003) found thatdecreasingfloristicsimilaritywith
distance in Amazonian rainforestscould not be entirely explained by changing
environmentswith distance,pointingto the potentialimportanceof local dispersal.
Moreover,the importanceof geographicdistancealone (a proxyfor local dispersal)
versus environmentalfactors was comparativelyless importantin pteridophytes
than in the more poorly dispersedMelastome shrubs,furthersupportingthe role
of dispersal.Similarly,Condit et al. (2002) used predictionsof Hubbell's (2001)
DISPERSAL
EFFECTS
ONCOMMUNITIES 559
of speciesturnover
neutralmodeltoarguethatlocaldispersalcouldexplainpatterns
overthe scaleof 0.2 to 50 km.
in tropicalrainforests
influencespatterns
An alternative
approachfor assessinghow seed transport
of aggregationassumesthatdispersalmodeis a predictorof dispersalkernels
(Willson1993),andcomparesclumpingacrossspeciesdifferingindispersalmode.
Workingin a CostaRicandryforest,Hubbell(1979)foundthattherateat which
densitydeclinedwithdistancefromadultswas steepestfor speciesdispersedby
mammals,followedby wind,andthenby birdsandbats.Conditet al. (2000)
foundthatwind-orexplosivelydispersedspecieswereless clumpedthananimalforest,butthisdifferencewas nonsignificant.
dispersedspeciesin a Panamanian
withtheirpoorlydispersedseeds
Nonetheless,in a Malaysianforest,dipterocarps,
weremoreaggregatedthannondipterocarps
(Conditet al. 2000).Also studying
howseed-dispersal
mode
rainforesttrees,Plotkinetal.(2002)described
Malaysian
of largeandsmallindividualswithina cluster.
influencesthe spatialdistribution
Inearlierwork,Plotkinet al. (2000)showedclusteringof individuals
independent
of
driven
of topography,
dispersal
suggestive
aggregation.
Resultsfor speciesotherthantropicaltreesaremoreequivocal.Niederet al.
(2000) foundthatwhetherepiphyteswere dispersedvia wind or animalswas
unrelated
to theirdegreeof clumping.Incontrastto theHubbell(1979)results,but
at a muchsmallerscale(2 m x 0.5 m plots),Myster& Picket(1992)foundthat
treesinvadinganoldfieldweremoreclumpedthanthosedispersed
bird-dispersed
Theperchingbehaviorof birdspresumably
wind
or
mammals.
by
generatesclumps
of seedatthissmallerspatialscale.A numberof otherstudieshavedemonstrated
of seeds(Howe1989).
thatanimaldispersalcausesverylocalaggregation
Limitationsof CurrentApproaches
One very importantlimitationof the work relatingaggregationto dispersalis that
nearly all of the evidence is correlationalor indirect.These results are thus best
aspatterns
thatgeneratehypotheses,ratherthandefinitivesupportforthe
regarded
of
areimplicitwhendispersal
importance dispersal.A numberof keyassumptions
is assessedastheresidualclumpingunexplained
environmental
variables(asin
by
&
Skov
Tuomisto
et
al.
Most
2002,
2003).
Svenning2001,Svenning
significantly,
we mustassumethatall potentiallyimportantenvironmental
variables,past or
variablesmust
present,areaccountedforin thestatisticalmodel.Anyunmeasured
at leastbe correlated
withthosethatarequantified.
Thisis probablyanunreasonableassumption
becausean historicalprocesssuchas a forestgapfourdecades
agocouldeasilyinfluenceclumpingpatternstoday,yet unlessit left a signaturein
variables,suchan effectwouldbe incorrectly
currentlymeasuredenvironmental
todispersal.
attributed
Inaddition,thesestudiesassumethatpositivedensitydepenorsharedsoilmutualists,
is notimportant.
dence,asmightarisethoughpollination
Otherconcernsexistforstudiesusingdispersalmodeasa proxyforthedispersal
kernel or mean dispersal distance. Dispersal mode is often shared across members of a family, such as wind dispersalin the Asteraceae,and is thus likely to be
560
N MURRELL
LEVINE
correlated
withotherfactorsthatcouldinfluenceclumping,suchas seedproductionorcompetitive
ability.Indeed,Horvitz&LeCorff(1993)foundthatwithinthe
herbsof the Marantaceae,
ant-versusbird-dispersed
tropicalunderstorey
plants
didnotdifferin theirdegreeof clumping.Thepotentialpowerof alternative
experimentalapproaches
forassessingtheinfluenceof dispersalpatterns
on aggregation
is emphasized
et
al.
of
limestone
Turnbull
When
annual
(1999).
by
species
grasslandweredispersedrandomly
thecommunity
thatdeveloped
by theinvestigators,
stillshowedstrongaggregation,
variablesexertimindicatingthatenvironmental
controls
over
in
the
portant
dispersionpatterns
system.
is a scale-dependent
A moregeneralproblemin thisworkis thataggregation
at
measure,andthusspeciesclumpedat one scalemaybe randomlydistributed
to the degreeof
another.Thus,if the questionis whetherdispersalis important
thenthe measurement
of aggregation
needsto be madeoverscales
aggregation,
at scaleslargerthandispersimilarto the spatialscaleof dispersal.Aggregations
of larger-scale
sal mayindicatethe importance
processessuchas environmental
Forexample,Peres& Baider's(1997)hypothesisthatclumpingin
heterogeneity.
thatthespatial
Brazilnut
treesis dispersaldrivenmayseemreasonable
considering
scaleof the seed-dispersal
kernelgeneratedby agoutismatchesthe scaleof tree
thatdispersalmodedoesnotinfluence
clumping.By contrast,it is notsurprising
x
of
10
km
at
the
scale
10
gridcellsdividingtheUnitedKingdom
plantclumping
et
al.
1994).
(Quinn
COEXISTENCETHROUGHLOCALDISPERSAL,
AND SEGREGATION
AGGREGATION,
ClassicLotka-Volterra
competitionmodelsassumethatdispersalandspeciesinMuchof therecentinterestin theinfluenceof
teractionsarespatiallyunrestricted.
work
hasbeenmotivated
on
structure
by theoretical
dispersal
community
species
slows
rates
of
local
often
Results
that
this
dispersal
suggest
relaxing assumption.
Murrell
&
Law
Law
et
al.
&
Pacala
2003,
1999,
(Bolker
competitive
displacement
2003).This,alongwithcoexistenceachievedthrougha competition-colonization
trade-offhasgenerated
a surgeof interestin spatialprocessesinplantcommunities
Murrell
& Law 2003). However,as we explainbelow,the
et
al.
2001,
(Murrell
local
literature
dispersalto coexistenceis plaguedby ambiguityoverthe
relating
temporalscalesoverwhichlocaldispersalinfluencescoexistence.
Models ShowingLocalDispersalEffectson Coexistence
Anincreasingly
amongecologistshasbeenthatlocaldispersal
popularperception
indipromotescoexistenceby causingthe spatialsegregationof heterospecific
viduals across a landscape (e.g., Green 1989, Murrellet al. 2001, Pacala 1997,
Pacala & Levin 1997,Weiner & Conte 1981). In homogeneous environments
(as assumed in most community theory), mathematicalmodels for two-species
DISPERSAL
EFFECTS
ONCOMMUNITIES 561
moreto theaggregation
of concompetitionshowthatlocaldispersalcontributes
proximitythanit does to aggregationof hetspecificsthroughparent-offspring
&Law2003).Thissegregation
of speciesreducestherelative
erospecifics(Murrell
of
inter-versus
interactions
(Pacala
1997);moregenerally,
frequency
intraspecific
weakerinter-versus
favors
coexistence
(Chesson2000).
intraspecific
competition
Localinteractionsare also key in thesemodels(Bolker& Pacala1997, 1999;
Dieckmann
et al.2000;Lawet al. 2001,2003;Murrell&Law2003).If speciesinteractwithotherindividuals
in a systemovera sufficiently
largespatialscale,local
will
have
little
effect
on
the
of
versusconspecific
dispersal
frequency heterospecific
interactions.
of suchspatialsegregation
forlong-termcoexistence
However,theimportance
hasrecentlybeenchallengedon severalcounts.First,it is apparent
thatinequality
in dispersalkernelsbetweenotherwisesimilarspecieswill leadtotheexclusionof
themoreaggregated
allelsebeingequal)(Bolker&
species(theshortestdisperser,
Pacala1999,Durrett& Levin1998,Murrell& Law2003,Pacala1986).Second,
even if dispersalis symmetric,segregationon its own is not enoughto prevent
exclusionwhereit is predicted
in thenonspatial
case(Chesson&Neuhauser
2002,
Durrett& Levin1998,Ghandiet al. 1998,Neuhauser& Pacala1999,Takenaka
et al. 1997).In these models,the dynamicsmay be thoughtof as havingtwo
phases:the initialphasewheremonospecificclustersbuildup owing to local
Itis thesecond
dispersal,andthesecondphasewheretheseclustersstarttointeract.
that
is
most
for
the
outcome
phase
important determining long-term(equilibrium)
of competition,andin particular
it is the interactions
at the clusterboundaries
thatareof greatestimportance
2002,Ghandiet al. 1998).
(Chesson& Neuhauser
interactions
are
and
Here,heterospecific
relativelyfrequent thestronger
competitor
wins.Thus,clustersof the strongerspecieswill slowlybutsurelyoverwhelmthe
clustersof theweakerspecies.It is notablethatthe speedwithwhichthisoccurs
is dependenton the geometryof the clusterboundary;the largerthe curvature
of the clusterinterfacethe fasterthe rateof exclusion(Ghandiet al. 1998).The
curvature
of theclustersis greatlydependenton thedispersalkernel,providinga
mechanisticlinkbetweenthedispersaldistanceandtherateof exclusion.
Thus,ratherthana stabilizingforceforcoexistence,localizeddispersalmaybe
thoughtof as an equalizingprocessbecauseit slowsdownthe dynamicswithout
(Chesson2000,Ghandiet al. 1998).Nonethechangingtheexpectedequilibrium
less, by slowingexclusionto suchlongtimescales,otherprocessessuchas immigration(Hubbell2001)andselection(Aarssen1984,Park&Lloyd1955,Pimentel
Inneutralmodelsexploredby Hubbell(2001)
1968)mayactto maintaindiversity.
andChaveet al. (2002),local dispersalslows the rateat whichspeciesdriftto
extinction.Becausethesemodelsalso incorporate
externalimmigration
or speincreasesspeciesrichnessby changingthe
ciation,this slowingof displacement
balancebetweenextinctionandspeciation(or colonization).In doingso, local
distribution
dispersalalso changesthe species-abundance
(Chaveet al. 2002).
Similarresults are achievedwhen species coexist throughdensity dependenceor
fecundity-competitiontrade-offs.
562
LEVINE0 MURRELL
In a comparativelyrareexampleof theoryexaminingthe effects of local dispersal in spatiallyheterogeneousenvironments,Snyder& Chesson (2003) found that
local dispersalincreasedthe degreeof coexistence as comparedwith thatachieved
under global dispersal. This result requiresniche differentiationamong species
and dispersaloccurringover smaller spatial scales than the environmentalautocorrelation.However,in the model, environmentalheterogeneityis fixed, and as
the authorscaution,longer-rangedispersalmay be more importantin temporally
heterogeneousenvironments.
A possibly moresurprisingresultof segregationis that,at least in discrete-space
models where interactionsoccur in very small neighborhoods(nearestneighbor
on a grid), local dispersalcan hindercoexistence (Bolker et al. 2003, Neuhauser
& Pacala 1999). This occurs when species are competitivelyunequalbut intrais greaterthan interspecificcompetition, allowing coexistence in the nonspatial
analog. Nonetheless, this effect only serves to reduce the amountof coexistence
where it is marginalin the firstplace.
Much of the above theoryis based on the well knownLotka-Volterracompetition equations,which areextendedto includelocal interactionsandlocal dispersal.
Clark& Ji (1995) used a more mechanistic,patch-basedmodel to show thatlocal
dispersalbetweenneighboringpatchesanda disturbanceregimethatresetpatches
periodically could aid coexistence as long as there was spatial variationin seed
deposition (caused by both seed limitation and local dispersal),and a nonlinear
relationshipbetween fecundity and patch density. As in a spatial-storageeffect
(Chesson 2000), high seed productionin relativelyuncrowdedpatchesmore than
outweighs the poor seed productionin crowdedpatches, allowing stable coexistence. Incorporatinga more mechanisticapproach,such as that used by Clark&
Ji, while still including local interactionsand local dispersal,would be of much
value in extendingthe theoryon dispersaland coexistence.
Field Evidence that Local Dispersal Influences Coexistence
Motivatedby the results of recent theory, a large number of empirical studies
now speculatethat local interactionsfavor coexistence (e.g., Hubbellet al. 1999,
Tuomistoet al. 2003). However,largely owing to the only recent developmentof
the models, the rigorousempiricaltests requiredto justify such claims have yet to
be completed.Rees et al. (1996) used models fit to monitoringdata of sand dune
annualsin Britainto show that species sufferedintense intraspecificcompetition
butlittle interspecificcompetitionin the field. They attributedthis resultto the high
degree of intraspecificaggregationfound in the system. The degree to which this
clumping resultedfrom local dispersalversus species specializationon different
habitattypes was unclear.Stoll & Prati(2001) examinedcompetitiveinteractions
among species experimentallyplanted in clumped versus randomdistributions.
Consistent with aggregationenhancing the impacts of intra-versusinterspecific
interactions,competitively inferior species performedbetter, and competitively
superiorspecies performedworse in the aggregatedtreatment.These results are
similarto thosein a longer-termstudyby Schmidt(Rejmanek2002, Schmidt1981),
DISPERSAL
EFFECTS
ONCOMMUNITIES 563
whichshowedthatovera periodof threeyears,intraspecific
allowed
aggregation
the exotic Solidago canadensis to coexist with the native Urtica dioicia, whereas
withouttheaggregation,
S. canadensiswasquicklyexcluded.Bothstudiesfollow
froma historyof appliedresearchexamininghow spatialpatterninginfluences
theimpactsof weedson crops(Garrett
& Dixon1998).Weemphasize,however,
thatlocal dispersalneed not alwaysbe important.Webb& Peart(2001) used
modelsparameterized
withfielddatato suggestthatlocaldispersalwasrelatively
for
tree
coexistence
in a Borneantropicalforest.
unimportant
Weconcludefrompublishedworkthatlocaldispersaldoesnotfavorthelongtermcoexistenceof speciesbut insteadsimplyslows the rateof displacement.
thecoexistenceof speciesin a naturalcommunityto
Thus,if we wantto attribute
thelocalnatureof dispersal,we needto firstclarifythetimescalesoverwhichwe
areattempting
to explaincoexistenceandthendemonstrate
thatlocaldispersalis
sufficientto explaincoexistenceoverthosetimescales.Thisis verydifferentthan
the almosttrivialresultthatlocal dispersalslowsdowndisplacedemonstrating
ment.Incorporating
timescaleswill almostundoubtedly
requiretheuseof models
withfielddata,as advocatedin ourconclusions.
parameterized
COEXISTENCE
THROUGHCOMPETITION-DISPERSAL
TRADE-OFFS
andsuperiorcolonizercan
Ecologistshavelongknownthata superiorcompetitor
coexistin homogeneous
modelsystems(Hastings1980,Holmes& Wilson1998,
Horn&MacArthur
1972,Hutchinson
1951,Levins& Culver1971,Tilman1994).
thatthis mechanismof coexistenceextends
However,the recentdemonstration
to anynumberof species(Tilman1994)has generateda surgeof interestin this
area.Coexistenceoccursbecausethe superiorcompetitorlacksthe colonization
abilityto fill all availablehabitats,leavingspacefor morepoorlycompetingbut
better-colonizing
species.Althoughcolonizationis a functionof bothfecundity
anddispersalability,mosttheoryhasassumeda competition-fecundity
trade-off
(Hastings1980,Tilman1994);only morerecentlyhas dispersaldistancebeen
consideredexplicitly(Bolker& Pacala1999,Dytham1994,Holmes& Wilson
interestis coexistencethrough
1998,Murrell& Law2003).Althoughourprimary
resultsincortrade-offs,we alsoreviewrelevanttheoretical
competition-dispersal
trade-offs.
poratingcompetition-fecundity
Assumptions UnderlyingTheoreticalResults
Theresultthatnumerousspeciescancoexistthrougha competition-colonization
trade-off(Tilman1994)dependson severalquestionable
First,there
assumptions.
mustbe a stricthierarchyof competitioninverselyrelatedto colonization.Second,the colonizationof a strongercompetitormustalwayseliminateanyestablished weaker competitorfrom its location, and do so prior to its reproduction
(Tilman 1994, Yu & Wilson 2001). This rapid displacementassumptionseems
particularlyunrealisticfor manyplants(Levine & Rees 2002, Yu & Wilson 2001)
564
LEVINE0 MURRELL
because seedlings are unlikely to outcompeteestablished individuals.Relaxing
this assumptionrecovers so-called lottery models, where competitionfor empty
sites occurs at the juvenile stage (Yu & Wilson 2001). In such lotterymodels, the
competition-colonizationtrade-offis insufficientto producecoexistence,although
coexistencecanbe achievedwith environmentalheterogeneity,fecundity-dispersal
trade-offs,or stochasticvariationin seed arrival(Chesson& Warner1981, Comins
& Noble 1985, Kisdi & Geritz2003, Kohyama1993, Yu & Wilson 2001).
Althoughthe above assumptionspertainto competition-colonizationtrade-offs
generally,thenatureof competitionis also key to coexistenceproducedspecifically
by a competition-dispersaltrade-off.Species with longer-rangedispersalcan coexist with superiorcompetitors(Bolker & Pacala 1999, Law & Dieckmann2000,
Murrell& Law 2003), but this requiresa relativelylarge asymmetryin competition (Murrell& Law 2003). Withoutstronglyasymmetriccompetition,the species
possessing an optimal combinationof competition and colonization dominates
the system. A similarcompetitivehierarchyis requiredin competition-fecundity
trade-offmodels (Adler & Mosquera2000, Geritzet al. 1999). If this assumption
is met, Holmes & Wilson (1998) show thatspecies with greaterdispersalcan also
coexist with those that are simultaneouslybetter competitorsand more fecund.
Nonetheless,this resultwas only found for a small set of parametercombinations.
The ability of the competition-colonizationtrade-offto generatecoexistence
is also sensitive to the density and fecundity of the superiorcompetitor.If the
superiorcompetitorhas fecundity high enough that it leaves only a small fraction of unoccupiedpatches, the inferiorcompetitoris unlikely to persist (Bolker
et al. 2003). High density can also be achievedthroughhigh dispersal,which reduces parent-offspringcompetition,favoringa more even distributionof individuals across space (Bolker & Pacala 1997, Ellner2001, Law et al. 2003). However,
this morediffuse distributionof individualsmay still leave temporarygaps thatthe
weakercompetitorcan exploit as long as it more rapidlycompletes its life cycle.
weakercompetitorscan coexist with a long-rangeIn fact, short-range-dispersing
dispersing dominantby having a higher turnoverrate (Bolker & Pacala 1999).
In sum, the main conclusion from the theory is that while competitiondispersal
trade-offsfavorcoexistence, this requiresseveralassumptionsthatmay not apply
to real systems.
EmpiricalSupport
Likethe theoreticalwork,mostof the empiricalstudiesexaminingcompetitionforcoexistenceexaminefecunditycolonizationtrade-offsandtheirimplications
competitiontrade-offs(Levine& Rees 2002). Evidencefor a dispersal-competition
trade-offis sparseand comes largelyfrom systemswith regulardisturbance.
Breweret al. (1998) foundonly weak evidencefor a competition-dispersaltrade-off
amongclonal grassescoexistingin a regularlydisturbedsaltmarshhabitat.Instead
they attributedcoexistence to interspecificdifferencesin physiological tolerance
of gap conditions.Yeaton& Bond (1991) showed that ant dispersalgives a competitively inferior South African fynbos shrub an advantagein colonizing the
DISPERSAL
EFFECTS
ONCOMMUNITIES 565
open areas after disturbance.However,Markovchain models suggested that this
dispersal advantagewas not sufficientto explain long-termcoexistence with the
competitivedominantshrubin the system. In some of the best supportfor coexistence achievedthrougha competitiondispersaltrade-off,Platt(1975) showed that
the species occupying matureIowa prairie(the competitivedominants)tended to
dispersemorepoorlythan"fugitive"species living primarilyon badgermounddisturbances.However,dispersalcapacity and propaguleproductionwere positively
correlated;thus, the source of the colonizationadvantageis unclear.
The best support for coexistence achieved through a competition-dispersal
trade-offcomes from models parameterizedwith field data, althougheven here
evidence is not definitive.Workingin temperateforest with two codominanttree
species, Nanami et al. (1999) documentedclumpingin the gravity-dispersedand
dioecious-competitivedominant,which they hypothesizefavoredthe persistence
of the bird-dispersedcompetitiveinferior.Althoughthis is simply a patternanalysis, they followed the work with mathematicalmodels testing the suitabilityof a
competition-dispersaltrade-offas a coexistencemechanismin the system(Nanami
et al. 2000). Resultsindicatedthatbecause male trees of the competitivedominant
do not dropseeds below the parentcanopy,this createsgaps thatare differentially
colonized by the better-dispersingcompetitiveinferior.Still, this result depends
stronglyon the dioecy, restrictingits generalityto other systems.
In Pacala et al.'s (1993) analysis of their SORTIEforest simulation model,
which they parameterizedwith field-derivedmeasuresof vital rates, coexistence
in EasternU.S. forest trees is achieved in part througha documentedtrade-off
between dispersaland the ability to cast and surviveshade.Althoughothertradeoffs are also importantto coexistence in their simulation,Ribbens et al. (1994)
show a tremendousimpact of changing mean dispersal distance on coexistence
and dominance.Still, althougha numberof studiesimplicitly or explicitly invoke
competition-colonizationtrade-offs,relativelylittle definitiveempiricalevidence
exists to supportcoexistence achievedthroughthis mechanism.
CONCLUSIONS
Ourreview of the literatureuncovereda dichotomyof supportfor the importance
of seed dispersalfor communitypatterns.Although we found an ever expanding
body of theory suggesting that seed dispersalaffects species coexistence through
local dispersaland a competition-dispersaltrade-off,empiricalsupportwas scant.
Instead,most empiricalinvestigationsexaminedhow dispersaland seed-trapping
agents affect species distributionand dispersion,subjectswith little theory.In addition, this work relied heavily on dispersalproxies and correlationalanalyses of
communitypatterns,methods unable to exclude alternativehypotheses. Interestingly, this relativelytepid supportfor dispersal'sinfluenceon communitypatterns
is in contrastto work at the populationlevel, where dispersalis well appreciated
to stronglyinfluence fitness, colonization, spread,and persistence(Harper1977,
Howe & Smallwood 1982, Skellam 1951).
566
LEVINEm MURRELL
Thus, the main conclusion of our review is that it may be prematureto expect
influence
structure.
Ofcourse,
thatpatterns
of seeddispersal
community
strongly
species withoutany dispersalcould not spreadbeyond a foundingindividual,but
it remainsunclearwhetherthespecificpatternof dispersedseedis a strongdeterminantof relativeabundance,
distribution,
dispersion,andcoexistencein natural
systems.Althoughthis lack of claritystemsfromthe weak empiricalsupportin the
thisweaksupportcouldbe interpreted
in severalways.Itmaybethatthe
literature,
butcurrent
is important,
approaches
methodological
shapeof thedispersal
kemrnel
in thefield.
to definitively
demonstrate
itsimpactsonpattemrns
aretoocorrelational
believe.
Resoluthan
we
be
less
commonly
dispersalmay
important
Altemrnatively,
to
the
more
tionof thesealternatives
rigorousapproaches understanding
requires
of dispersal.
importance
Evidence
theEmpirical
Improving
in the field is difBecause estimating and manipulatingseed-dispersalkemrnels
for community structurecan
ficult, testing the importanceof dispersal kemrnels
be challenging. In principle,the ideal empiricalstudy would (a) documentseed
shadows and dispersionpatterns,(b) correlatethese with patternsof community
structure,and then (c) demonstratethat experimentallymanipulatingthe seed
shadow changes populationor community structure(Schupp & Fuentes 1995).
Althoughexamplesof each of these steps can be found in the literature,we found
no single study that performedall of them. Instead,most of the empiricalwork
relating dispersal to community propertiestended to be correlational,often involving proxies for dispersalkernels, such as dispersalmode. These studies thus
reliedheavily on severalpotentiallyprecariousassumptions,includingthe fact that
dispersalmode is a reasonablepredictorof dispersalkernelsand that aggregation
unrelatedto currentenvironmentalvariablesis attributableto dispersal.These assumptionsmay be valid in much of the work (Willson 1993), but withoutfurther
supportsome conclusions may be incorrect.This is illustratedby the often-cited
example where dispersalinfluences patternsof mangrovetree zonation through
the tidal sorting of propagules (Rabinowitz 1978). Although Rabinowitz's hypothesis has intuitiveappeal,recent work actuallyquantifyingthe seed-dispersal
kernelsof mangrovetrees in the same forests suggests the tidal sortingof propagules is unlikely to generatethe zonation (W. Sousa & B. Mitchell, unpublished
data).
How can we more definitively demonstratethat dispersal influences relative
abundance,distribution,dispersion, and coexistence? To this end, we strongly
encourageexperimentsthat directly manipulatethe seed-dispersalkernel, as advocatedin more specific cases by Bolker & Pacala(1999), Pacala& Rees (1998),
and Schupp & Fuentes (1995). Such experimentsare not substitutesfor quantifying dispersalkernels and communitypatterns,but they are complementaryand
uniquelypoised to definitivelytest the mechanismssuggestedby the patterns.The
basic methodology involves manipulatingthe seed-dispersalkernel in replicate
DISPERSAL
EFFECTS
ONCOMMUNITIES 567
distriplotsandcomparingtheresultingcommunitypattern(relativeabundance,
control.Thekernelis manipulated
bution,coexistence)to thatin anunmanipulated
by firstcollectingall seedproducedin a plotandthendependingon theresearch
question,dispersingit randomlyor locally.Community
patternsin an additional
treatment,whereseed is dispersedfollowingthe estimatednaturalkernels,can
be comparedwith the unmanipulated
controlto test for any artifactsassociated
with seed handling.Thisbasicapproachhas beensuccessfullyusedto examine
thepopulation-level
consequencesof thedispersalkernelin a tropicalforesttree
&
(Augspurger Kitajima1992).
If dispersalcontrolscommonnessandrarity,thenforcingall species'dispersal to follow the across-speciesmeanor mediankernelshouldcausethe more
commonspeciesto declineandthe rarerspeciesto increaserelativeto controls.
If dispersalkernelscontrolaggregationor otherdistribution
patterns,thendispersingall seed globallyshouldeliminate,or at leastbeginto homogenize,the
distribution
or aggregation
patterns(e.g., Levine2001, Turnbullet al. 1999).If
speciescoexistthroughlocaldispersal,thendispersingseedsgloballyshouldenhancecompetitivedisplacement
(Bolker& Pacala1999).Lastly,if speciescoexist througha competition-dispersal
trade-off,thenequalizingthe dispersalkernel acrossspeciesshouldresultin the displacement
of species(Pacala& Rees
1998).
Theexperiments
will be mosttractablewithcommunities
of annualor shortlivedperennialplantswheredispersaloccursoverrelativelysmallspatialscales.
trendsin thepredicteddirectionwithearly
Still,evenwithlonger-lived
organisms,
life stages(Augspurger
& Kitajima1992) can be used to bolstercorrelational
evidence.In addition,seed additionexperimentslocatedat differentlocations
relativetoexistingdistributions
couldfollowtherationale
of theexperiments
above
butbe conductedoverlargerspatialscales.For example,in studiesattributing
adultclumpingto localdispersal,experiments
shouldshowseedlimitationaway
fromtheclump.In otherwords,if seedsdidtravelfurther,adultscouldestablish.
conductedin realecologicalhabitatswhereother
Last,we encourageexperiments
factors
are
freeto exerttheirimpacts.Ourreviewdoesnot
potentiallyimportant
anddiversity,
distribution,
questionwhetherdispersalhasanyeffectonabundance,
butratherquestionstheimportance
of suchaneffectin comparison
to otherfactors
(Figure1).
FutureDirections for Theory
doesnotlead
trade-offs,aggregation
Theoryhasshownthatwithoutinterspecific
to stablecoexistence(Bolker& Pacala1999,Durrett& Levin 1998,Murrell&
Law2003,Neuhauser
&Pacala1999,Takenaka
et al. 1997).Yetthemodelsusedto
this
result
are
based
on
the
Lotka-Volterra
produce
largely
competition
equations,
andmostincorporate
lineardensitydependence.
morecomplexproIncorporating
cesses such as nonlinearcompetitionmay change some of these predictionsor at
the very least lead to new strategies for coexistence (Bolker & Pacala 1999).
568
LEVINEN MURRELL
However,few modelshavetakenthis approach(see Pacala1986for a rareexception).Incorporating
processessuchas nonlineareffectsof densitymaybe at
theexpenseof analyticaltractability,
butthetechniquesavailableto spatialtheory
aresophisticated
to
make
it
possible(Dieckmannet al. 2000, Tilman&
enough
Kareiva1997).
Theoryhasalsofocusedlargelyon thequestionof coexistence.Yetothercomfromtheoretical
munitydynamicsrequirecloserattention
ecologists.Forexample,
theworkof Chaveet al.(2002)showedthatthescaleof dispersalis themostimportantinfluenceon manymeasuresof communitystructure.
Still,it is notknownif
theseresultsarerobustto inequalityin dispersalabilityacrossspecies.Althoughit
is oftenassumedthatlonger-range
arethemoreabundant,
thisprediction
dispersers
favoringshort-range
mightchangewhenthelandscapeis spatiallyheterogeneous,
dispersal(Bolker2003,Travis& Dytham1999).
Last,empiricalworkshouldmotivateinteresting
modelingquestions.Mostnotably,we founda surprisingnumberof empiricalstudiesthatdocumentedthe
of trapping
patternsof seedarrival.Interestingly,
importance
agentsin controlling
whereasclumpingthatresultsfromlocaldispersalshouldenhanceintraspecific
agclumpingthatresultsfromgeneraltrapping
gregationandthusslowdisplacement,
contact.Alternatively,
trappingmay segreagentscouldincreaseheterospecific
influences
if
seed
trappingpatterns,as in Schneider&
morphology
gatespecies
Sharitz(1988). How trappingagents,theirspeciesspecificity,andtheirspatial
andcoexistenceareissuesripefor
influenceabundance,
distribution,
arrangement
theoretical
exploration.
Closing the Gap BetweenTheory and EmpiricalWork
literature
a cleardichotomybetweentheempiricalandtheoretical
Wedocumented
this
is
to
kernels
gap essential
communitypatterns.Closing
relatingdispersal
of dispersal.To this end,we stronglyadvocatethe
to clarifyingthe importance
documented
withempirically
modelsparameterized
of mathematical
development
kernels
and
other
realistic
(as in Wu &
parameters
demographic
seed-dispersal
can uniquelyaddresswhetherthe predictionsof
Levin 1994).Suchapproaches
modelsreasonablydescribethe dynamicsof real ecological
the mathematical
to askthe key longwill also forceinvestigators
communities.
Suchapproaches
orwhatcreates
thedispersal-driven
termquestionssuchaswhatmaintains
patterns,
for exploring
informative
seed limitation.Modelsshouldalso proveparticularly
on
theinfluenceof seed-dispersal
kernels,parentplantdensity,andseedproduction
betweendispersalkernels
seeddepositionacrossthelandscape.Therelationship
but critical,linkagebetweendispersaland
and seed rainis an underexplored,
communitypatterns.
of seeddispersalforcommunitydynamicshaslong
Thepotentialimportance
been acknowledged,and recenttheoreticalresults supportthis expectation.However, the results of our review suggest that the importanceof dispersal cannot
be taken for granted;empirical supportfor the theoreticalpredictionsis largely
DISPERSAL
EFFECTS
ONCOMMUNITIES 569
lacking. A firmerunderstandingof the role of dispersalin communitystructureis
achievableif we begin with more rigorousfield approachesdirectlymanipulating
seed-dispersalkernels.These resultsmust thenby coupled with the predictionsof
models incorporatingempiricallyderiveddispersalkernels.
The Annual Reviewof Ecology,Evolution,and Systematicsis online at
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