Nordic Society Oikos
Elton Revisited: A Review of Evidence Linking Diversity and Invasibility
Author(s): Jonathan M. Levine and Carla M. D'Antonio
Source: Oikos, Vol. 87, No. 1 (Oct., 1999), pp. 15-26
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OIKOS87: 15-26. Copenhagen1999
M IN IREVIENW
Minireviews provides an opportunity to summarize existing knowledge of selected
ecologicalareas,with specialemphasison currenttopics whererapidand significant
advances are occurring. Reviews should be concise and not too wide-ranging. All key
referencesshould be cited. A summaryis required.
Elton revisited:a review of evidencelinking diversity and
invasibility
Jonathan M. Levine and Carla M. D'Antonio
Levine, J. M. and D'Antonio, C. M. 1999. Elton revisited:a review of evidence
linkingdiversityand invasibility.- Oikos 87: 15-26.
It is commonlybelievedthat diversecommunitiesbetter resist invasion by exotic
speciesthan do simplecommunities.We examinedthe history of this notion, and
evaluatedtheoreticaland empiricalwork linkingdiversityand invasions.We found
that much of the historicalwork that has contributedto the perceptionthat diverse
communitiesare less invasible, including Elton's observationsand MacArthur's
models, is based on controversialpremises.
species-packingand diversity-stability
Nevertheless,more recent theoreticalstudies consistentlysupportedthe predicted
negative relationshipbetween diversityand invasibility.The results of empirical
studies, however, were decidedlymixed. Constructedcommunitystudies directly
manipulatingdiversity found both positive and negative effects of diversity on
invasibilityin both fieldand microcosmsettings.Otherempiricalstudiestrackingthe
assemblyof ecologicalcommunitiesgenerallysuggestedthat communitiesdeclinein
invasibilityas speciesaccumulateover time, though the role of diversityitself was
often ambiguous.Studiesof the spatialcorrelationbetweendiversityand invasion
and studiesexperimentally
addinginvadersto naturalsystemsindicatedthat diverse
communitiestend to be moreinvasible.We arguethat theseresultsmost likelyreflect
environmentalfactorsspatiallycovaryingwith diversityin naturalcommunities(e.g.
resources,disturbance),and not the effects of diversity itself as uncoveredby
constructedcommunitystudies. Nevertheless,the consistent positive relationship
between exotic species abundanceand residentspecies diversityfound in spatial
patternstudiessuggeststhat invadersand residentspeciesaremoresimilarthan often
believed,and the implicationsof this for theoriesof invasionare discussed.
J. M. Levine and C. M. D'Antonio, Dept of Integrative Biology, Univ. of California,
Berkeley, CA 94720, USA (levinejm@socrates.berkeley.edu).
Concern over the impacts of biodiversity loss on the
functioning of ecosystems has stimulated renewed interest in the importance of species diversity to community
stability. Stability has several components; among these
is "resistance" - the ability of a community to resist
change in the face of a potentially perturbing force
(Connell and Sousa 1984, Pimm 1991). These forces are
often abiotic, such as storms, fires, and droughts,
Accepted19 April 1999
Copyright? OIKOS 1999
ISSN 0030-1299
Printedin Ireland- all rightsreserved
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though increasingly,the major perturbationsexperienced by naturalcommunitiesare biological in origin
(Drake et al. 1989). Extremelycommon is the humanmediated introductionof plant, animal, or pathogen
speciesinto communitieswherethey did not previously
exist. The ease with which these newcomersbecome
establishedmembersof communitiesdefinesthe "invasibility"of a system.Neither the generalcontrols over
communityinvasibilitynor the role of speciesdiversity
in influencingsusceptibilityto invasionare well understood. Yet, the widespreadoccurrenceof invasiveintroduced species, their documented impact on native
biological diversity (e.g. Mooney and Drake 1986,
Drake et al. 1989, Vitouseket al. 1997)and the developing interestin restorationof nativediversitymandate
a clear understandingof the community-levelprocesses
influencinginvasions. Here, we review empiricaland
theoreticalresearchlinkingdiversityand invasibilityin
an attempt to provide a critical frameworkfor approachingresearchin this area.
Historical considerations
It is widelybelievedthat high nativediversitydecreases
the invasibilityof communities(Lodge 1993), an idea
with perhapsthree origins.The first lies in the natural
history observationsand writingsof Elton (1958) and
the second and third emerge from classic ecological
theory exemplifiedby the work of MacArthur(1955,
1972) and colleagues.
In his book, The ecologyof invasionsby animalsand
plants, Elton (1958) argued that "the balance of relativelysimplecommunitiesof plantsand animalsis more
easily upset than that of richer ones; that is more
subject to destructiveoscillations in populations...
and more vulnerableto invasions".He supportedthis
argumentwith observationsthat "oceanicislands and
crop monoculturesare simple ecosystems that show
high vulnerabilityto invasions... and frequentoutbreaksof populationsubsequently".Elton'snotion that
diversesystems are less invasible(also see Allee et al.
1949) has been echoed many times by authorssuch as
Moyle (1986) examiningfish invasionsin North America and Moulton and Pimm (1983) examining bird
invasionsof Hawai'i.It is important,however,to clarify what Elton (1958) was proposing.
As evidencedby the above quotations, Elton was
interestedin communitystability, and focused on invaders with particularlylarge impacts. He did not
clearly distinguishbetween the ability of non-resident
speciesto establishin depauperatecommunitiesversus
the susceptibilityof organismsin those communitiesto
the effects of invaders.Only the former is strictly a
questionof invasibility.This confusionbetweeninvasibility and the vulnerabilityof communitiesto impact
permeatesmuch of the literaturelinking diversityand
invasion, and has fueled recent challengesto Elton's
observationthat speciespoor, oceanic islands are particularlyvulnerableto invasion.Simberloff(1986, 1995)
and D'Antonio and Dudley (1995)have concludedthat
while island species are often more susceptibleto the
impactsof invadersthan theircontinentalcounterparts,
thereare insufficientdata to evaluatethe inherentinvasibilityof intact island communities.
Classic ecological theory has also strongly contributedto the belief that more diversesystemsare less
invasible.Much of the researchconductedin the 1960's
and 1970'swas based on assumptionsthat niche space
in naturalcommunitiesis limitingand that communities are stronglystructuredby competition(May and
MacArthur1972). Several authors, but most notably
MacArthur(1970, 1972)exploredthe conditionsunder
which an assemblagearrayed along a resource axis
could be invaded by a new species. In general, this
work suggestedthat the more species occupyinga resourceaxis, the morefully resourcesweremonopolized,
and the more difficultit was to insertnew species(but
see Case 1991). These models, however, have been
challengedon severalgrounds,includingthe point that
competitorsalong a niche axis may indirectlyfacilitate
one another via competing with shared competitors.
When such indirectinteractionsare included,the same
types of models suggestthat for some combinationsof
species, diverse communitiesmight be more invasible
(Levine 1976, Lawlor 1979, Stone and Roberts 1991,
Levine 1999). In spite of the now widespreadacceptance that indirectinteractionsare common and more
generally,that many systemsare loosely structuredand
not at equilibrium(Wiens1977),conclusionsfrom classic nichetheorycontinueto stronglyinfluencethe study
of biologicalinvasions.
The third origin of the belief that more diverse
systems are less invasible lies in MacArthur's(1955)
classic work on the relationshipbetweendiversityand
stability.He suggestedthat systemswith fewerlinkages
were more subject to population fluctuationsif one
linkage was disruptedthan were systems with more
linkages,work whichspurredan enormousdebateover
the diversity-stabilityrelationship(May 1973, Pimm
1991). Though MacArthur(1955) did not evaluateinvasibility,this work has contributedto the perception
that diversesystemsare more stable and possibly less
invasibleas resistanceto invasionis a commonmeasure
of stability (Elton 1958). It is also importantto note
that MacArthur and May's models were based on
linkages among as well as within trophic levels. Yet
very few empiricalstudieshave examinedmulti-trophic
level interactionswhen invokingthe diversity-resistance
linkage.
In this manuscriptwe examine evidence for a link
betweendiversityand invasibilitywith the goal of clarifying some of the strengthsand weaknessesof current
approaches.Overall, we believe that the search for
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generality in this area will be improved by careful the direct effects of ecological factors that influence
definition of the important questions, attention to diversity is critical to properly interpreting these
mechanism,considerationof relevantspatialscales,and studies.
recognition that factors controlling native biological
diversityalso control invasions.
Review of the evidence
We locatedthe followingstudiesby conductinga BIOSIS searchof articlesdatingback to 1985,and examinThe most commonly cited and often implicit mecha- ing referencestherein.
nism by whichdiversityconfersresistanceto invasionis
that more diverseassemblagesmore fully utilize available resources,thus leaving little resource space for
Models
individuals of new species. This mechanismfollows
from the "species-packing"or "diffuse competition" All of the mathematicalmodels relatingdiversityand
modelsof MacArthur(1970)describedabove, and is an invasibilityindicate that increasingdiversitydecreases
extension of the "empty niche" concept in invasion invasibility(Robinson and Valentine 1979, Post and
biology (Herbold and Moyle 1986, Crawley 1987). Pimm 1983, Shigesadaet al. 1984, Drake 1988, 1990,
More diversecommunitiesare also more likely to have Case 1990, 1991, Law and Morton 1996).This general
a diverse guild of consumers,and this may limit the result was independentof whether the communities
number of prey species that can potentially invade were composed of species competingvia interference
(Pimm 1991,Naeem and Li 1998).By contrast,Palmer (Shigesada et al. 1984) or exploitation (Case 1990,
and Maurer(1997) point out that due to differences 1991), or if these specieswere membersof a single or
among plants in canopy height, rooting depth, rhizo- multiple trophic levels (Post and Pimm 1983, Drake
sphere microbialcommunities,etc., diverse communi- 1988, 1990).
ties contain more microheterogeneity than
Robinson and Valentine (1979) and Case (1990,
monocultures(Aarssen 1983), and might thereforebe 1991)examinedthe invasibilityof stablemodelcommumore invasible.
nitiesvaryingin diversity.The interactionsand dynamMore diverse communitiesare also more likely to ics of these systems were describedby Lotka-Voltera
contain species with particularlystrong impacts on equationswith interactionstrengthmost often drawn
invasibility.Whetheror not this mechanismis consid- from a uniformdistribution.All inter-and intraspecific
ered an effect of diversityper se has been considered pairwiseinteractionswerecompiledas the elementsof a
elsewhere(Huston 1997, Tilman 1997a).Regardless,if communitymatrix,with matricesof varyingsize reprea key speciesthat is more often found in more diverse sentingcommunitiesof varyingdiversity.Eachcommuassemblagesstronglydetersinvasion,diversecommuni- nity matrix was analyzed for local stability, and
ties will show enhanced resistance.Alternatively,key unstablecommunitieswerediscarded.The locallystable
species that are strong facilitatorscan cause diverse communitieswere then "invaded"by a new species,
systems to be more invasible. These facilitatorshave which expanded the matrix by one row and one
been termed "diversity promoters" by Palmer and column,the elementsof which were the interactionsof
Maurer (1997) and may be common in communities the invaderwith each of the residentspecies.Communiwhere facilitation is an important structuringforce ties were invasibleif the new species persistedin the
(Bertnessand Callaway1994,Callaway1995).In sum, expandedcommunityat equilibrium.
while it is commonly believed that diversity should
Whilethe modelsof Case (1990, 1991)and Robinson
enhanceresistanceto invasion,argumentscan be made and Valentine(1979) differedin how the elementsof
that diversitymay promoteinvasion.
the communitymatrixwere assigned,both found that
Understandinghow invasibilityvaries with diversity the proportionof invaded communitiesdeclinedwith
in natural systems is complicated by the fact that diversity. Case found that even invaders that were
variationin diversityis controlledby, and thus covaries equivalentcompetitorsto the residentspecieswere ofwith disturbance,resourceavailability,physical stress, ten unsuccessfulin more diversecommunities,a result
competitors,consumers,etc., the same factors known attributedto the increasedfrequencyof multiple doto influenceinvasibility(Rejmanek1989,Huston 1994, mainsof attractionin morediversesystems(Gilpinand
Robinsonet al. 1995,Wiseret al. 1998).These covary- Case 1976). These multiple domains of attractionor
ing factorsare not intrinsiceffects of diversity,though equilibriaare more familiarin the contextof the simple
most of the studieswe reviewdo not make this impor- Lotka-Volteratwo speciescompetitionmodel with untant distinction.Thus, recognizingthat correlationsbe- stable coexistencewhere the initially more abundant
tween diversityand invasibilityin naturalcommunities speciesdominates.Case suggestedthat the importance
reflectboth the effect of diversityon invasibility,and of these "priorityeffects"increaseswith speciesdiverWhy should diversity affect invasibility?
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sity,,and therebydecreasescommunityvulnerabilityto
competitorsenteringin low numbers,such as invaders.
The assembly models of Post and Pimm (1983),
Drake (1988, 1990), and Law and Morton (1996) are
also based on Lotka-Volteraequations, but they differed from those of Case (1990) and Robinson and
Valentine(1979) in how the communitieswere "assembled". These models began with a finite species pool
with all pairwiseinteractionsdrawn from a specified
range of values. Specieswere then randomlydrawnto
invadeinitiallydepauperatecommunities.Invasionwas
successfulif the invaderincreasedwhen rare,and maintained positive equilibrialabundanceas inferredfrom
the communitymatrixexpandedto includethat species
(for a mathematicalcritique,see Case 1991, Law and
Morton 1996). This process was iteratedhundredsof
times, with each successful invasion yielding a new
locally stable equilibrium.Law and Morton (1996)
providedan alternative"permanence"criteriafor successful invasion that allows for coexistenceor invader
successeven when speciesdo not tend to an equilibrium
point.
Regardlessof the invasioncriteria,all of these models indicatedthat the rate of successfulinvasions declinedwith time, a resultthat has beeninferredby some
to mean that diversityenhancesresistance.Case (1991),
however,notes that due to the finite speciespool, the
degreeto which this resultreflectsthe effects of diversity versusthe exhaustionof good invadersearlyin the
assembly process is unclear. Furthermore,Law and
Morton (1996) showed that certain combinationsof
speciesbetterresistinvasionthan othersof equaldiversity. These invasion resistant and presumablymore
connectedcommunitiesdevelop as the requisitemembers are introduced,and thus invasion resistancemay
developover time independentof communitydiversity.
Law and Morton(1996)also exploredhow the diversity of the speciespool influencescommunityinvasibility and found that communitiesassembledfrom richer
pools were more resistantto invasion.This resultwas
not an effect of local diversitysince all communities,
regardlessof the pool size, tendedtowardsfive species.
Rather, Law and Morton argued that communities
derived from richer pools have been tested by more
kinds of species and are thus less likely to be invaded
by a new species than are communitiesof the same
diversitybut assembledfrom a smallerpool.
Thereare severalfeaturesof all of these models that
we believequalifytheirgenerality.First, the predictions
may be most appropriatefor relativelysmall spatial
scales. Lotka-Volteramodels assumewell-mixedpopulations, such that all species interactwith a potential
invader.This does not invalidateLotka-Volterapredictions, but ratherrestrictstheir applicabilityto scalesat
whichall constituentspeciesdo interact- the neighborhood scale (Tilman 1994, Naeem et al. 1998). Yet, as
we will show, empiricalwork at this scale is rare.
In each of the models of diversityand invasion,the
interactionsof the invaderwere similarto those of the
residentspecies. In the assemblymodels, the invaders
weredrawnfrom the samespeciespool as the residents,
while Robinson and Valentine(1979) and Case (1991)
drew invaderand residentspeciesinteractionsfrom the
same distribution.Though Case (1991) showed that
increasingthe invader'sgrowthrate had little effect on
model results,what happenswhen invadersare better
competitorsor predatorsthan all of the native species?
Severalinvestigatorshave observedthat some successful invaders,particularlyones with large impacts,tend
to have qualitativelydifferenttraits than the resident
species(Vitousek1990,Chapinet al. 1994).We hypothesizethat wheninvadersare superiorcompetitorsor use
differentresourcesthan the nativespecies,the effectsof
diversityon invasibilityare likely to be weak.
Another important assumption of most of these
models is that a communityis invasibleif the invader
persistsat equilibrium.Crawley(1987) points out that
understandingwhat factors allow the equilibriumpersistence of invaders, does not in itself explain why
communitiesare invasiblein the first place (see also
Rejmanek1989, Law and Morton 1996).Furthermore,
invaders that fail to persist in communitiesat equilibriummay still stronglyimpactthese systems.One of
the outcomesof Case's(1990, 1991)modelsare whathe
terms"indirectfailures"- situationswherethe invader
populationinitiallygrows,but in the processinfluences
other speciessuch that its own populationgoes extinct.
Case (1991) notes that though the frequencyof these
indirectfailuresis relativelysmall, their frequencyincreases with diversity. Further exploring non-equilibriumoutcomesof invasionis an interestingarea for
futurework.
Lastly, in all of the models, prior to invasion, the
communitieshave reachedequilibrium,a state rarely
reachedby naturalsystems(Connelland Sousa 1984).
This mismatchbetweenthe models and field systemsis
furthercomplicatedby the fact that communitydiversity is often dynamic and the outcome of non-equilibriumprocesses.How diversityrelatesto invasibility
in successionalor unsaturatedsystemsis an interesting
questionripe for explorationin models.
Spatial pattern studies
Spatial pattern studies correlatethe abundanceof a
single or multiple invaders with the diversity of the
surroundingassemblage.These studiesare not mechanistic in that correlationsbetweendiversityand invasion reflectboth the independenteffects of diversityas
well as the effectsof processescovaryingwith diversity.
As we describebelow, it is these latter factors which
tend to drive broad scale field patterns.Nevertheless,
these studies addressthe question, "Are naturallydi-
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verse assemblagesmore or less invadedthan their species-poor counterparts?".Interestingly,most of the
studies we found suggest that more diverse assemblages are more invaded, contrary to Elton's (1958)
observations.
Note from the question above that spatial pattern
studies do not explicitlymeasureinvasibility,but instead use invader abundanceor diversityas a proxy
for susceptibilityto invasion.These measuresnot only
reflect invasibilityand features intrinsic to the community, but also externalfactors, such as variationin
propagule supply. In systems such as rivers, where
propagulesupply covarieswith residentspecies diversity (Nilsson et al. 1993),correlationsbetweeninvader
abundance and diversity may be driven entirely by
invaderinput. A second caveat about spatial pattern
studies is that they correlate invasion with current
diversity,which is not diversityat the time of invasion (but see Wiser et al. 1998). Given sufficienttime,
exotic species may reducethe diversityof invadedassemblages,so the resultsof some of these studiesmay
better reflect the impact of invaderson native diversity ratherthan vice versa.
Species lists from well defined areas, such as reserves, provide interestingdata sets to explore patterns of diversityand invasion. Fox and Fox (1986)
showed that the percentageof alien plant species is
negatively correlated with native plant diversity in
Australianheathlandand shrublandreserves.In contrast, Knops et al. (1995) showed that the percentage
of alien plant species was greater in more diverse
communitiesof coastal, central California.However,
Rejmanek (1989), Brown (1989), and others have
pointed out that the percentageof species that are
alien is a biased measureof invasibilitybecause even
if invasibilityis independentof diversity,diverse systems will contain a lower percentageof invaderssimply because of the high number of native species in
the denominator(similarproblemsemergein a study
by Bridgewaterand Backshall1981). For the study by
Knops et al., this means that the strengthof the positive correlationwas under-estimated.For the study by
Fox and Fox (1986), we recalculatedthe relationships.
Using the numberof invadersratherthan the percentage as the dependent variable, we found a positive
correlationbetweennative richnessand exotic richness
for shrublandsites (Fig. 1) and a non-significantrelationship for the heathlandsites (R2= 0.002, p = 0.80).
Similarly,Krugeret al. (1989) showed that for Mediterraneanplant systems in California,more diverse
native communities also contained more non-native
species.
Area can often be a confoundingvariablein these
correlational studies between diversity and invasion
because larger areas are likely to contain both more
exotics and more natives (Case and Bolger 1991),
leading to positive correlationsunrelatedto invasibil-
ity. For example,Timminsand Williams(1991) found
that area could explain the positive correlation between native plant and weed diversity among forest
and scrub reserves in New Zealand. By contrast,
MacDonaldet al. (1986, 1989) analyzedinvasion patterns among nature reserves in South Africa, and
found that while more diversereserveswere more invaded (R2= 0.44, p < 0.001), reservesize was not correlatedwith the numberof exotic species.The positive
correlation between native and exotic diversity was
attributedto the greaterenvironmentalheterogeneity
in diversereserves(also see Higginset al. 1999).
Many studies have used equal size areas to explore
patternsof diversityand invasion, and most indicated
positive correlationsbetweenthese factors. Examining
invasionpatternsin multipleplant communitiesof the
central United States, Stohlgren et al. (1998, 1999),
showed that more diverse communities contained
greater numbersof exotic species than their speciespoor counterparts,though within communities,at the
scale of 1 m2, resultswere mixed (see below). Focusing on ripariansystems,Planty-Tabacchiet al. (1996)
showed that sites with high native plant diversity
along the McKenzie River in Washington and the
Adour River in France containedmore exotic species
than sites with lower native diversity.They attributed
this result to riverinefactors covaryingwith diversity.
Pickard(1984) found that floristicallydiverse sites in
the Lord Howe Islands had more exotic species than
did species-poorsites, a resulthe attributedto the soil
nutrientstatus of diversesites.
In a rigorousanalysisof invasion patternsWiser et
al. (1998) found that the occurrenceof the exotic forb
50
g* 45 R2 = 0.77
40 -> P =0.002
S.40
.~ 35
*
I 30o 25 20 -
Z 15 10
0
....
20 40
60 80 100 120 140 160
Numberof NativeSpecies
of the relationship
betweendiversityand
Fig. 1. Reanalysis
invasionfor shrublandsites presentedby Fox and Fox (1986).
See text for biases in the originalpresentationof these data.
Data were obtained by digitizing Fig. 5 in Fox and Fox
(1986). We back-calculatedthe numberof exotic speciesper
site from the numberof native speciesand the percentageof
speciesthat were exotic.
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Hieraciumlepidulumin New Zealand was positively
correlatedwith species richnessacross 250 permanent
plots.Theirdataincludedthreetimepointsover23 years
and measuresof a wide varietyof other site conditions
that might influenceinvasion. Using multiple logistic
regression,they partitionedout the factors covarying
with speciesdiversity,and still found a positivecorrelation betweendiversityand invasion.In anotherinvestigationtrackingan invasionthroughtime,Holway(1998)
found that the spreadof 20 Argentineant populations
in Californiawas not correlatedwithnativeant richness.
Severalstudieshave found that invadedcommunities
are less diversethan their uninvadedcounterparts.In
each case, however,the invaderswere so abundantthat
the resultsmost likelyreflectedthe impactof the invader
on native diversity.Woods (1993) used the negative
correlationbetweenexotichoneysucklecoverand native
richnessin EasternUS foreststo arguethat honeysuckle
negativelyimpactednativediversity.Similarly,Morgan
(1998)founda weaknegativecorrelationbetweennative
richnessand exotic richness(R2= 0.16,p < 0.001)in an
Australiangrassland.By comparingplots with low and
highexoticcover,he arguedthatthiscorrelationreflected
the impact of the exotic species on native richness.
Similarly,Stohlgrenet al. (1999)reportedthat 1 m2plots
placed in more heavily invaded communitiesof the
CentralUS showednegativecorrelationsbetweennative
and exotic diversity,while those in less invadedareas
showed positive relationships.Pysek and Pysek (1995)
reportedthat habitatsin the CzechRepublicinvadedby
the tall forb Heracleum mantegazzianum had lower
diversityand richnessthan uninvadedplots. They reported that H. mantegazzianum occupied between 50%
and 100%cover in the study area and replacesnative
vegetation,providingthe simplestexplanationfor the
lower diversityof invadedareas.
Several investigatorshave explored biogeographic
scalepatternsof diversityand invasion.Caseand Bolger
(1991)founda weaknegativecorrelationbetweennative
and exotic reptile diversityon islands throughoutthe
world.Theynoted,though,that the degreeto whichthis
reflectsthe numberof native species per se versus the
evolutionaryisolation of species poor islands remains
difficultto untangle.Weakertrendsfor birdsand mammals are presentedby Brown (1989) and Case (1996).
Rejmanek(1996) found that for vascularplants, the
tropicsareless invadedthan the temperatezone, though
he concluded that this correlationwas unrelated to
diversity.In anotheranalysis,Rejmanek(1996)reported
a positivecorrelationbetweenthe numberof nativeand
exotic plants per log area on islandsbetween50?Sand
50?N. He arguedthat native diversityseemedto be an
indicator of favorable conditions. These results are
supportedby Lonsdale's(1997)studyof globalpatterns
plant invasions,whichshowedthat worldwide,communitiesricherin nativeplantspeciesarealsomoreinvaded.
Invader addition studies
Invaderaddition studies differ from the studies above
only in that invasibilityis measuredby adding a fixed
numberof propagulesto assemblagesvaryingnaturally
in diversity.Thus, the investigatorknows the diversity
of the assemblageat the time of invasion.This eliminates the possibility that the invader has somehow
influencedpatternsof native diversity.In addition,by
controllingthe numberof propagulesadded, invasibility reflectsfeaturesintrinsicto the community,and not
differentialpropagulesupply.Nevertheless,like spatial
pattern studies, diversity is not manipulated,so the
results are still driven by both diversity and factors
covarying with diversity. Nonetheless, invasibility is
actuallymeasured,though how this is done can influence the conclusions.
Invasion is a probabilisticprocess (Crawley 1987,
1989). Diversity does not deterministicallyrender a
communitycompletelyresistantor vulnerableto invasion, but rather,influencesthe probabilitythat a given
propagulewill be successful.One approachfor assessing invasibilityis to score communitiesas invaded or
not invadedafteraddinga given numberof propagules
(e.g. Robinsonand Dickerson1984,McGrady-Steedet
al. 1997, Tilman 1997b).However,with this approach,
the magnitudeof any effects on invasibilitydependon
the number of propagules added. Even if diversity
influences the probability of successful invasion, if
enough propagulesare added, all communitiesmay be
invasible.The sensitivityof invadersuccessto propagule input is well known from the purposefulintroduction of biocontrol agents (e.g. Crawley 1987, Hopper
and Roush 1993) and birds (Duncan 1997). Alternatively, by examining the proportion of successful
propagulesas a functionof diversity(e.g. Robinsonet
al. 1995),studiescan estimatethe per capitaprobability
of success.This probabilityis independentof the number of addedpropagulesas long as propaguledensityis
low enough to prevent interactions among the
colonists.
A secondproblemwith assessinginvasibilityis determining the point at which an invader is considered
"successful".We find the definitionof Crawley(1987)
useful:an invaderis successfulif it increaseswhen rare.
Using this definition,invaderadditionstudiesevaluating sexualor asexualpopulationgrowthmake the most
convincingcase for examininginvasibility.
Robinson et al. (1995) added seeds of California
poppy (Eschscholziacalifornica)to grasslandplots that
varied naturallyin diversityand found that more diverse plots were more invasible by this poppy than
species-poorplots. Specifically,they found that more
poppiesgerminated,flowered,and producedfruitin the
more diverseplots. This resultcan be partlyattributed
to the fact that Bromusdiandrus,a strongsuppressorof
poppies and other plants was more abundantin low
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diversity plots. In a similar study, Peart and Foin
(1985) examined the invasibilityof patches within a
coastal Californiagrasslandby addingthe seeds of five
grassesto plots varyingin composition.Though their
study did not focus on diversity,Peartand Foin found
that plots dominated (near 100%cover) by a single
productiveperennialgrassweremoredifficultto invade
than were mixed species plots of annual grasses and
forbs. More generally,low diversitypatchesmay often
be the least invasible when the low diversity results
from competitivedominanceby one or a few species.
Tilman (1997b) added seeds of 54 native species to
Minnesota grasslandplots varying naturallyin diversity. In contrast to Robinson et al. (1995) and Peart
and Foin (1985),he found that more diverseplots were
less invasible.The mechanism,however,remainedunclear. The effects of diversityon invasibilitywere not
mediated by effects on nitrogen, since as Tilman
pointed out, plots with the less nutrientswere more
invaded.
Assembly studies
Assemblystudiesassess patternsof diversityand invasion over time, asking,"Do communitiesbecomemore
difficultto invade as time progresseswith the accumulation of species?".Invasibilityis measuredas the number of new species establishing over a given time
interval.If diversecommunitiesbetter resist invasion,
the numberof new speciesin a communityshouldlevel
off with time. However,as with the assemblymodels,a
declining number of invasions over time may also
reflect the formation of more connectedcommunities
(Law and Morton 1996) or the exhaustion of good
invadersearly in the assemblyprocess,selectivelyleaving poorerinvadersto establishlater on (Case 1991).
Due to the difficultyof obtainingfrequentcensuses
of a developingcommunityand the long-termdata sets
required,most assemblystudies are conductedin microcosms. These have been reviewed elsewhere by
Drake et al. (1996), the generalresult being that communitiesdeclinein invasibilityover time. The degreeto
which this dependson diversityis less clear. Moulton
and Pimm (1983) took advantage of historical bird
counts to examinethe successof avian introductionsto
Hawai'i.Theyfound that on certainislands,the success
rate of introductionsdecreasedover time as the communities accumulatedmore introducedspecies. They
arguedthat this resultedfrom increasedcompetitionin
the more diversecommunities.Simberloffand Boecklen
(1991), however,showed that nearlyall of the successful invadersin Moulton and Pimm's study were successful when introduced throughout the Hawaiian
islands, regardlessof island diversityand unsuccessful
species tended to be unsuccessfuleverywhere,a result
which calls to question the diversity effect (but"see
Moulton 1993). In a similaranalysisof bird invasions
into New Zealand,Duncan(1997)was unableto isolate
an effect of diversity.
Constructed community studies
Studiesthat experimentallyconstructcommunities,directly manipulatingdiversity are the only ones that
experimentallyisolate the independenteffects of diversity on invasibility.In this light, they are the most
comparableto the modeling work. In addition, they
have the potentialto isolatethe mechanismsunderlying
the effects of diversity,though this has not yet been
done.
Knops et al. (1997) examinedthe numberof invasions into Minnesotagrasslandplots whereplant diversity had been experimentallymanipulated(see Tilman
et al. 1996).Theirresultsindicatedthat invasibilitywas
a negativebut asymptoticfunctionof diversity,providing some of the first empiricalevidencethat diversity
may deter invasion in a naturalsystem (Naeem et al.
1998).Palmerand Maurer(1997)examinedweed invasion into plots plantedwith one or five crop plants.As
in Tilman et al. (1996), the one-speciestreatmentincluded monoculturesof all species in the pool. They
found that more diverseplots were significantlymore
invaded,though the mechanismsremainedunclear.
Due to the relativeease of manipulatingcommunities
of microorganisms,these systems have proven useful
for examiningthe relationshipbetween diversityand
invasibility.Much like the models, these studiescreate
communitiesof varyingdiversityand then subjectthem
to invasion. In the studies we describe below, the
identityof the speciesin each replicatecommunitywas
not randomlyassigned,and priorto invasion,the communitieswere given time to equilibrate,duringwhich
species were lost. Thus it is difficultto determinethe
extent to which these studies reflectjust the independent effects of diversity.Nevertheless,since the initial
numberof speciesin each replicatewas determinedby
the investigator,diversityis still unlikelyto be highly
correlatedwith other environmentalfactors. In McGrady-Steedet al. (1997), roughly 17 microorganism
communitiescontaining up to 17 species, and three
trophic levels were invaded with a facultativeheterotroph.Of the five successfullyinvadedcommunities,all
contained fewer than six species. Thus, their work
generally supports the hypothesis that diversity enhancesresistanceto invasion,though they arguedthat
ratherthan a species-packingmechanism,the effect of
diversitywas attributableto particularkey speciesthat
were more abundantin the diversecommunities.
In a similartype of experiment,Robinsonand Dickerson (1984)used threedifferentinvadersto examineif
diversityenhancedecological resistance.The first in21
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exotic invaders, there is considerableopportunityto
explore the diversity/invasibilityrelationshipwith an
experimentalapproach.Some revegetationstudieshave
exploredthe effects of using variousnative seed mixes
on weed invasion(e.g. Tyseret al. 1998)but have not
specifically addressed the importance of species
diversity.
100
, 80
80.a 60
/
E 40^^^
o
o 20
Discussion
O
1
,
I
2
3
4
,
,
5
6
7
Species Richness of the Community
Fig. 2. Reanalysisof microcosmresultsfrom Robinson and
Dickerson(1984).We used simplelinearregressionto examine
the relationshipbetweencommunitydiversityand the percentage of communitiessuccessfullyinvaded three weeks after
introductionof (0) Staurastrum
(R2= 0.91,p < 0.05) and (@)
Dictyosphaerium. (R2 = 0.97, p < 0.05). In order for these re-
sults to be comparableto those of McGrady-Steedet al.
(1997),we selectedweek 3 data fromRobinsonand Dickerson
(1984)since week 2 data werenot availablefor both invaders
et al. presentedweek 2 data).Nevertheless,a
(McGrady-Steed
positive relationship between diversity and invasibility
emergedregardlessof when invasionwas assessed.Diversity
levels with four or fewer replicateswere excludeddue to the
inherentinaccuracyof percentagescalculatedfrom smallnumbers (all percentsin the figure were based on at least nine
replicates).
vader, though capable of growing in isolation, failed to
invade any community, regardless of diversity. For the
other two invaders, Robinson and Dickerson (1984)
concluded that persistencetime was independentof
diversity. This conclusion was based on a contingency
table analysis where the rows were progressively increasing levels of diversity, and the columns were progressively increasing invader persistence times. The
simple G-test used by the authors treated each cell as
independent, and was inappropriately weak considering
that both the rows and columns were ordered (Feinberg
1980). We reanalyzed their data using doubly ordered
contingency table analysis, and found that diversity
significantly influenced invader persistence time for
both species (linear by linear association tests, p <
0.05), but in contrast to their expectations, invaders
persisted longer in more diverse communities. We also
used simple linear regression to examine the relationship between community diversity and the percentage
of communities successfully invaded three weeks after
introduction (Fig. 2). These results also indicated a
significant positive relationship between diversity and
invasibility.
In spite of the possibilities provided by studies that
directly manipulate diversity, very little of such work is
currently published. We believe that particularly in light
of the large number of habitat restoration projects
currently taking place and management concerns over
Currentmodels evaluatingthe effects of diversityon
invasibilityunilaterallysupportthe commonbelief that
speciesdiversityenhancesresistanceto invasion.Those
empiricalstudiesmost similarto the models, the constructedcommunitystudies,only sometimessupported
this notion, suggestingthat diversitydoes not consistently enhanceresistancein naturalcommunities.The
most strikingfindingof this reviewwas that the majority of the spatial patternand invaderaddition studies
indicatedthat naturallydiverseassemblagestended to
be more invasiblethan their species-poorcounterparts,
contraryto Elton's (1958) observations.This findingis
particularlyimportantfrom a conservationstandpoint
since it suggeststhat our most diversehabitatsare the
most prone to invasion(Stohlgrenet al. 1999).
Why mightdiverseassemblagesbe the most invaded?
Nearly all of the spatialpatternstudiescited favorable
biotic or abiotic factors covaryingwith diversitythat
were presumed to underlie the positive correlations
between diversityand invasibility,includingmoisture,
nutrients,habitat heterogeneity,physical factors, and
competitors(e.g. Pickard1984,MacDonaldet al. 1989,
Robinson et al. 1995, Rejmanek1996, Stohlgrenet al.
1999).In general,unlessnativeand exotic speciesdiffer
markedly,the factorscontrollingnativediversityshould
similarly control invaders, and thus the number of
native speciessimplybecomesan indicatorof biotic or
abiotic conditions favorable to invasion (Rejmanek
1989;but see McIntyreand Lavorel 1994).
Because of the importanceof factors consistently
covaryingwith diversity,the observationthat naturally
diverse communities are more invasible cannot be
translatedto mean that diversity promotes invasion
(e.g. Stohlgren et al. 1999). While we believe that
positive effects of diversity on invasibility are very
much under-appreciated,
the small scale at which the
mechanismsunderlyingthe effects of diversityoperate
precludesthem from drivingcommunityor landscapelevel patterns.Each of the proposedmechanisms,such
as species-packingor the effectsof key species,operate
on the scale of species interactions,or the neighborhood (Naeem et al. 1998; but see Law and Morton
1996).Yet, the scale of nearlyall of the spatialpattern
and invader addition studies was significantlygreater
than the neighborhood,with most examining entire
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communitiesor landscapes.We believe that independent of whetherthe neighborhoodeffects of diversity
on invasion are positive or negative these effects are
likely to be swampedby factors covaryingwith diversity at broader spatial scales. This hypothesis is
analogous to the observationthat competitorswhich
are negativelyassociatedat small scales are often positively associated at broader scales due to similar
habitat requirements(Wiens 1986).
Positive correlationsbetween native and exotic diversity suggest that if local scale diversity enhances
resistanceto invasion, this effect is weak relative to
other factors influencinginvasions in these systems.
Quantitativelyevaluating the importanceof diversity
relative to disturbance, nutrients, consumers, and
other factors limiting invasions has rarely been accomplished, though is an important goal for future
work in this area. Such information is essential to
accuratelypredictingthe consequencesof species loss
for communityinvasibility.
Are native and exotic species all that different?
A common perceptionin the study of biologicalinvasions is that exotic species somehow differ from the
residents of the communitiesthey invade. However,
the results of spatial pattern and invader addition
studies suggest that exotic and native species respond
to the same factors. The notion that majordifferences
separateinvader and residentspecies is based largely
on classic theories of what makes a good invader
(Baker 1965) and the invaderimpact literature.While
it does seem true that invaders with large impacts
differ considerably from native species (Vitousek
1990, Chapin et al. 1994), the traits behind large impacts need not be the same as those allowing the
invader to enter in the first place. Moreover, while
the exact percentageis debated,most invadersdo not
have major impacts (Simberloff 1981, Herbold and
Moyle 1986, Moyle and Light 1996).
That invaders and resident species must be somewhat similar is also an implicit assumptionof arguments regarding species-packing: the resource
requirementsof the invader and the resident species
must overlap for the species-packingmechanism to
operate. If an invader requiresa portion of the resource space outside that of the residentspecies, then
residentspeciesdiversitymay be inconsequentialto its
invasion. Thus, if invaders with large impacts are
truly differentfrom the residentsof the communities
they invade, an interestingproblemarises:the factors
controllinginvasion may differ for species with large
and small impacts. We note that few diversity-invasibility investigationshave focused on high-impact
species.
The biotic resistance paradigm
Much of the researchand hypothesesconcerningthe
effects of diversity on invasion have been strongly
drivenby the focus on "bioticresistance",a focus that
is evidentin the seminalworkof Elton (1958).Basedon
the resultsof this review,we believethat resolvingthe
diversity-invasibilityrelationshipand more generally,
enhancingthe predictabilityof invasionsrequiresthat
we not only uncoverthe communitymembersthat repel
invaders,but also those that facilitateinvasion.A new
focus on speciesthat promoteinvasionsis beginningto
emerge.Richardsonet al. (1999) suggest that mutualisms between introducedplants and native organisms
(pollinators, dispersers,fungi, N-fixing bacteria) are
quite commonand are possiblyvery importantin promoting invasion.Palmerand Maurer(1997) and Wiser
et al. (1998) discuss "invasionpromoters",whose increased abundancein areas of greaterdiversitymake
these areasparticularlysusceptibleto invasion.Indeed,
a surprisingfraction of the empiricalstudies suggest
that in some systemsdiversitymight promoteinvasion
(Robinsonand Dickerson1984(reanalyzed),Robinson
et al. 1995,Palmerand Maurer1997,Wiseret al. 1998).
Evenmore generally,facilitations,both directand indirect (Bertness and Callaway 1994, Callaway 1995,
Levine 1999) are increasinglyrecognizedas important
structuringforcesin communities,and the implications
of this for the diversity-invasibility
relationshipshould
not be ignored.
Conclusions
Ecologistshave long been searchingfor a generaltheory of the factors controllinginvasions.Based on the
results of this review, and more specifically,the suggestion that exotic and resident species show similar
responsesto the environment,we believe that our understandingof the ecologicalcontrols over native species diversity may provide our best theory of the
controls over invasibility.It is no coincidencethat the
dominantfactors known to influencediversitysuch as
competition, disturbance, resource availability, and
propagule supply (see Huston 1994 for review) are
the same factorsknown to influenceinvasions.
Consideringthe controversialfoundationsand weak
empiricalsupport for a negative relationshipbetween
diversityand invasibility,we believethat thereis much
room for innovativemodelsand carefulempiricalstudies that go beyond currentapproaches.More specifically, we urge investigatorsto explorethe mechanisms
underlyingthe effects of diversityon invasibility.Empirical studies rigorously evaluating mechanismsare
conspicuouslyabsent from the literature,yet a mechanistic understandingof the diversity-invasibility
relationship is essential for accurately predicting the
23
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assemblages or circumstances where diversity matters
most. Furthermore, what mechanistic evidence we do
have provides little support for the often-cited species
packing mechanism and biotic resistance paradigm.
Moving beyond this paradigm is critical to better understanding the diversity-invasibility relationship and
more generally, enhancing the predictability of biological invasions.
- Commentsby Mary Power, Will SatAcknowledgements
terthwaiteand WayneSousagreatlyimprovedthe manuscript.
JML acknowledgessupport from a NSF graduateresearch
fellowship and dissertation improvementgrant, and the
Williamand Flora HewlettFoundation.CMD acknowledges
supportfrom the MillerInst. for Basic Researchin Science.
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