Society for Conservation Biology

Disturbance, Diversity, and Invasion: Implications for Conservation Author(s): Richard J. Hobbs and Laura F. Huenneke Source: Conservation Biology, Vol. 6, No. 3 (Sep., 1992), pp. 324-337 Published by: Blackwell Publishing for Society for Conservation Biology Stable URL: http://www.jstor.org/stable/2386033 . Accessed: 26/01/2011 13:02
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Review

Disturbance, and Invasion: Diversity, Implications forConservation

RICHARDJ. HOBBS
CSIRO Division of Wildlife & Ecology LMB 4, PO Midland WesternAustralia 6056, Australia

LAURAF. HUENNEKE
Department of Biology New Mexico StateUniversity Box 30001/Dept 3AF Las Cruces,New Mexico 88003, U.S.A.

Abstract: Disturbance is an important componentof many ecosystems, and variations in disturbanceregimecan affect ecosystemand communitystructureand functioning.The "intermediate disturbancehypothesis" suggeststhat species diversity should be highest at moderatelevelsofdisturbance. However,disturbanceis also known to increase the invasibility of communities.Disturbance therefore poses an importantproblemfor conservationmanagement Here,we review the effects of disturbancessuch as fire,grazing soil disturbance, and nutrient addition on plant speciesdiversity and invasion, withparticular emphasis on grassland vegetation.Individual componentsof thedisturbanceregimecan

have markedeffects on species diversity, but it is oftenmodificationsof the existingregimethathave the largestinfluence. Similarly,disturbancecan enhance invasion of natural communities, butfrequently it is theinteraction between disturbancesthathas thelargesteffectThe natural different disturbanceregimeis now unlikelytopersistwithinconservation areas, since fragmentationand human intervention have usually modifiedphysical and biotic conditions. Active managementdecisions must now be made on what disturbance regimeis required, and thisrequiresdecisions on what species are to be encouraged or discouraged.

Introduction
Preservationof natural communitieshas historically consisted of measures protectingthem fromphysical disturbance. Timberharvestsand livestockgrazingare usuallyexcluded frompreserves,and firesuppression has been practiced-within the U.S. systemof national parks, forexample.Ecologistsand conservationists have come to recognize,however,thatmanyforms ofdisturbance are important components of naturalsystems. Manyplantcommunities and species are dependenton
Addressall correspondence to RichardJ Hobbs. Paper submitted June 19, 1991; revisedmanuscriptacceptedFebruary 14, 1992.

disturbance, especially for regeneration (Pickett & White1985). Preserves shouldbe largeenoughto allow the naturaldisturbanceregimeto operate and to support a mosaic of patches in different stages of disturbance, successional recovery, and community maturation (Pickett & Thompson 1978). In addition,both theory(the intermediate disturbancehypothesis, Connell 1978) and growing empiricalevidence suggestthat moderatefrequenciesor intensities of disturbance fostermaximum species richness. To preservebioticdiversityand functioning natural ecosystems, then,conservation effortsmust include explicit consideration of disturbance processes. Disturbance acts in plant communitiesin another way, however,by promotinginvasionsby non-native

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and weedy plant species (Ewel 1986; Hobbs 1989, 1991; Rejmanek1989). Invasivespecies have recently gained notorietyas major conservationand manage(see MacDonald et ecosystems mentconcernsin natural al. 1989; Soule 1990; Westman 1990). The control of non-native plantshas become one ofthemostexpensive and urgenttasks of managersin several U.S. national parks,in island preserves such as the Galapagos, and elsewhere.Invasiveplantscan reduce or displacenative species,both plantand animal,and mayeven altereco(Vitousek 1986; Schofield1989). They system function as significant conhave become recognized,therefore, servation concerns. to conservaDisturbancethuspresentsa conundrum the continuedexistenceofparticular tionmanagement: species or communitiesoftenrequires disturbanceof regimesmustbe insome type-and hence disturbance may plans-but disturbance tegrated withmanagement of naturalcomlead to the degradation simultaneously invasions. Here we examinethis munities by promoting imporproblemby discussingthe typesof disturbance and thosethat plantspecies diversity tantin maintaining cases where We identify particular encourageinvasions. conflictsare most likely to arise. Our examples are we drawnprimarily although from grassland vegetation, and discuss other ecosystemtypessuch as shrublands woodlands. We close by suggesting guidelinesforevaluating the proper role of disturbancein the managementof a naturalarea or preserve.

Theoretical Background
of Therehas been considerabledebate on thedefinition and on what does and does not constitute disturbance, a disturbanceto any given community or ecosystem (see Rykiel 1985; van Andel & van den Berg 1987). Definitions of disturbancevary,fromGrime's (1979) as a process removing or damaging view of disturbance of biomass, to White and Pickett's(1985) definition ecodiscreteeventin timethatdisrupts "anyrelatively and changes or populationstructure system, community or thephysicalenvironavailability, resources, substrate furet al. (1989) expand the definition ment."Petraitis ther to include any "process that altersthe birthand presentin the patch" by dideath rates of individuals resourcelevels, individuals or by affecting rectly killing in ways thataltersurnaturalenemies,or competitors vival and fecundity.Temporal and spatial scale are in our recognitionof the "discreteclearlyimportant ness" ofa disturbance event,as nearlyanyecological or fallunder the last,most biogeochemicalprocess might Pickettet al. (1989) definea disinclusivedefinition. excaused by factors turbanceas a change in structure ofinterest; ternalto the hierarchical level ofthe system disturbance fromother thisis necessaryto distinguish

In our discussionbelow,we will changesin the system. include both direct disturbances(those affecting the survivorship of individuals directly)and indirect disturbance (those affecting resource levels or other conditionsthattheninfluence individuals in the patch). Disturbances to plant communities thus include such events as fires,storms,and floods; but other changes such as alteredgrazing regimes or nutrient inputs would also be classed as disturbance iftheyaffected resource levels and demographic processes. Within a givenpatch,the responseof anycommunity to a disturbance (or to the disturbance regime,characterisedby the naturaldistribution of disturbance sizes, frequencies, intensities, and timing)is determinedby the attributes of component species. Disturbancefrequencyis also important; thetimeinterval betweensuccessivedisturbances can have significant effects on community response.This is because species composition changeswithtimesince disturbance, and manyspecies requiresome timeafter disturbance to reach reproductivematurity. Ifa second disturbance occursbeforethey reach thatstage,therewill not be anypropagulesavailable to recolonizethepatch.The responseofa commuis thenpredictedon the basis of the nityto disturbance lifehistory responsesof those species available forrecruitment or invasion(Noble & Slatyer1980; Moore & Noble 1990). Therehas been increasing recognition amongecological researchersof the importanceof natural disturbance in the function of terrestrial ecosystems.Pickett and White(1985) provideda comprehensive reviewof in the dynamics therole ofdisturbance ofmanyecosystem types.They distinguished several components of natural disturbance intenregimes, including frequency, sity,and size of disturbance(White & Pickett 1985), each acting in a distinctive way on communitiesand populations.Petraitiset al. (1989) presented a more detailed analysisof these components,and recognized thathypothesesabout the relationship of disturbance and community responsecan be sortedintotwo groups: thosepostulating selectivemortality or actionfora specific targetgroup,and those dealing with random or Petraitis et al. (1989) suggested catastrophic mortality. thatselectivemortality could maintain species diversity or richnessat some equilibriumlevel, while random would preventthe establishment of commumortality nity equilibrium(for example, preventingthe dominance of one superiorcompetitor and the exclusion of otherspecies). Theypointed out thatboth equilibrium and nonequilibriummodels of communitiespredict greatestspecies richnessat intermediate levels of disturbance. Variousversionsof this"intermediate disturthuspredicta similar bance hypothesis" result-highest occur at intermespecies numberswhen disturbances diate frequenciesor with intermediate intensities (Fig. 1)-despite different underlying theoriesofcommunity

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C,)

a2)

a1)
U)

Low

High Disturbance frequency/intensity

Figure 1. The intermediate disturbancehypothesis, which indicates thatspecies diversity withina given patch should be highestat intermediate frequencies or intensities of disturbance(afterConnell 1978). function(see Fox 1979; Huston 1979; Sousa 1984). These arguments based on the factthatonlya are often few species (ruderals) can persist in the face of frequent,severe disturbance; onlya fewspecies (the longest-lived, best competitors, and those able to regenerate withoutdisturbance)can persistover the long termin theabsence ofdisturbance; but manyspecies (including some representatives of each of these,plus intermediates) can findsome place to survivein a region comprising patches in variousstagesof recovery, arisingat some intermediate frequency. How is "intermediate" defined? It is perhapseasiestto relatethe frequency of discreteeventsto the longevity of major species in the system. halfthe Approximately lifespanof the dominantspecies has been used as one estimation of intermediate disturbance frequency (Hobbs et al. 1984). Definitions of intermediate intensitymayhave fewerexternalreferents, however;intensitycan be evaluatedin termsofpercentageof individuals killed, or the degree of structuralor resource alteration caused. The above discussion concentrateson within-patch but disturbanceis also imdiversity (alpha diversity), between portantfor creatingor maintaining diversity patches or at the landscape level (beta diversity). By creating patches of different ages and successional structural and habitatdiverstages,disturbanceaffects While we consityas well as overall species diversity. in this review,the centrateon within-patch diversity in creating role ofdisturbance landscapemosaicsshould also be noted (see Turner1987). While disturbance is important diverformaintaining bothwithincommunities and at a landscapelevel,it sity has become increasingly recognized that disturbance effects. mayalso have undesirable Particularly important is the recognition thatdisturbance may act to increase

the likelihoodof invasionof a community. For invasion to occur theremustbe availablepropagulesof an invasive species capable of dispersinginto a given plant and therethenhas to be a suitablemicrocommunity, siteforgermination and establishment to occur. That is, therehas to be a suitableinvasion"window"(Johnstone 1986). Disturbanceusually acts primarily by affecting the availability of suitable microsites,althoughsome forms of disturbance the availability mayaffect of invasive propagules. For instance, non-nativeherbivores maybringseed into an area eitheron theircoats or in feces. Here we will discuss primarily the effect of disturbanceon micrositeavailability. The spatialand temporaldistribution of disturbance in a regionor an ecosystem givesriseto the disturbance mosaic of an area. Pickett and Thompson (1978) pointed out thatthe recurrenceof disturbances necessitatesthe preservation of a "minimum dynamicarea," or an area large enough to containwithinit multiple patches in various stages of disturbanceor recovery such thatinternal recolonizationcan contribute to the maintenance of the overallecosystem. The dynamics of patch disturbance and of biotic exchanges among whichdetermine patches, thepattern ofrecovery, are of major concern in defining the minimum criticalsize of ecosystems (see Lewin 1984), thesize requiredto maintaincharacteristic and system species composition function.Withincreasing ofnatural fragmentation areas,it is likelythatthese minimum areas are now to be found only withinthe largestconservationunits,and disturbance regimesand biotic exchanges between patches are liable to be significantly alteredin smallerremnant areas (Hobbs 1987; Saunderset al. 1991). In particular, invasionsare likelyto become more important. How shall managers respond to or compensate for the changednatureof disturbance? We approachthisquestion by surveying the major types of disturbanceand reviewingtheireffects on plant species diversity and invasions.We mostlyconsider grasslands, but we also include illustrativeexamples from other vegetation types.

EmpiricalEvidence
1. Fire The central role offire in maintaining theopen natureof the vegetation has been acknowledgedformanygrassin mesic regions.Further, lands, particularly research has documentedthatfirecan stimulate or maintain high In tall-grassprairies of North primaryproductivity. America,fireenhances productivity by removingthe thicklitter the microclimate and nulayerand altering trientcontent of surfacesoil (see Knapp & Seastedt 1986). Fire also influencesspecies diversity and the characteristic structureof these prairie communities. Classical work on fireecology of prairies (Kucera &

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Koelling 1964; Abramset al. 1986) foundthatannual burning favored tallwarm-season grassesand resulted in low abundanceof typicalprairieforbsafter 5-10 years. Biennial burning resulted in the highest communitydiversity with mixed grassesand forbs. Areaswith longfire-free periodsresembledunburned areas in their heavylitteraccumulationand decline in grasses. Firesmayfavorthe dominant "matrix" prairiegrasses and thuscan actuallydecrease diversity (Collins 1987). Apparently most prairie fires stimulate individual grassesand do not kill them;few openingsare created forthe establishment of new individuals or species. As we have noted previously, however,species diversity comprisestwo maincomponents: species density or alpha diversity withina patch,and patch diversity or the numberof typesof different patches or microhabitats. Glenn-Lewin and ver Hoef (1988) reportedthatgrasslandsvaryin the degree to which these two contribute to overalldiversity. In threegrasslands, patch diversity rather thanspecies density was themajorcontributor to overall communitydiversity. Fire (and other disturbances) may create a heterogeneouspatch structure, even ifwithin patchesit servesto decrease species density. Lifehistory, of course, determinesthe vulnerability and response of plants to fire.In annual grasslandsin California, firehad only temporary effects on botanical composition(forbsincreasedand grassdominancedecreased fora brieftime). Here the restructuring of the communityeach autumn with germinationquickly swamps any temporary effect on the seed bank or on conditions(Heady 1972). germination offiresin ecosystems Suppression dominatedby fireadaptedspecies can cause severe disruption of communityand ecosystem processes,which mayhave implicationsfortheconservation ofnative, fire-tolerant species. For example,Cowlinget al. (1986) foundthatfiresuppressionhas been responsiblefor the conversionof a South African open, grassyveld to a vegetationnow dominatedby undesirablenon-native shrubs.They suggestedfrequent prescribedfiresas the best mechanism forrestoring the originalopen natureof the vegetation and formaintaining populationsofthe region'sendemic geophytes.Strang(1973) similarly suggestedthatfire was an expensive but necessarypart of reversing the conversionof moistgrassland in south-central Africa to brush.Firecan also be used morepreciselyto favor the of one species over another.For example, performance in an attempt to restoreprairieon the site of an abandoned agricultural site,fire was used successfully to create openingsin a turf of non-native Poa species and to enhance the colonizationand expansionof trueprairie species (Curtis & Partch1948). As earlyworkin tall-grass prairieconfirmed, theoverall fireregimeratherthanany singlefireis the critical

in determining factor community response.Firesof differingintensity or occurringin different seasons are likelyto affect species diversity in a variety of ways by altering thepotential ofindividual species to regenerate. Hobbs et al. (1984) provide an example of how fire can alterthe diversity intervals of species thatare able to regeneratein heathland,and hence affectoverall An intermediate community diversity. fire frequency resultedin the highestspecies diversity. Fire has been discussed as a factorthatcan increase the likelihood of invasions (Christensen & Burrows 1986). Fire acts to remove much of the plant canopy and usuallyhas a short-term fertilizing effect on the soil; hence both light and nutrientavailability can be increased temporarily. Zedler and Scheid (1988) discuss the invasionof coastal chaparral by Carpobrotusedulis fire.There is clear evidence, however, that following not all firesresultin increasedinvasionand thatvariations in fireregime can affect the extent of invasion. Hobbs and Atkins (1990) have illustrated how invasion of Banksia woodlands differs between firesburned in versusautumn. In some cases,fire spring per se does not affect the degree of invasion,or will do so only when combinedwithsome othertypeof disturbance, such as mechanicaldisturbance ofthesoil or nutrient input.For instance, Hesterand Hobbs (1992) studiedburnedand unburnedshrubland patches withinan area of remant vegetation in the Western Australianwheatbelt and foundthatinvasion by non-native annualswas restricted to theremant edges,even following In adjacent burning. woodland,the abundanceofnon-native species actually declinedfollowing thefire. Followinganother firein the same area, this time in heathiandvegetation, invasion increasedonlywhere the fireimpingedon a roadverge thathad been subject to priordisturbance duringroad grading.This interactionis important when management of roadside vegetation corridorsis considered (see Loney & Hobbs, 1991; Panetta& Hopkins 1991). Because species vary in theirresponse to fires, fire may favorone set of species over another;these relationshipscan explain the balance between native and non-native species in some fire-impactedsystems. Wherenativespecies are sensitiveto fire(because fuel loads were such thatfiresin the nativeecosystemwere of low frequency and intensity), firecan enhance the invasionofnon-native fire-tolerant species. When these fire-tolerant species contribute to increased fuel loads and inflammability, the disturbance regime can be shifted toward more frequentand intensefires;these fires further enhance the dominanceof non-native over nativespecies.Justsuch a cycle has enhanced invasion of woody species in South African Mediterranean systems,and of annual grassesinto other Mediterraneanclimateregions(MacDonald et al. 1989). Similarly, invasion of fire-tolerant grassesin dryHawaiian lowlands

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on nativespecies (Hughes et al. has had severe effects 1991). 2. Grazing features animalsare conspicuousand important Grazing it has long been knownthatsome of manygrasslands; while othersare not,and plantsare tolerantof grazing and that grazing alters the appearance, productivity, Milchunaset al. (1988) have of grasslands. composition of grazingby large herbivoreson reviewed the effects and relatetheseto the interdiffering typesofgrassland Theysuggestthatgrazhypothesis. mediatedisturbance onlywhere the evolutiona disturbance ing constitutes ary history of grazing is short. This has also been (1980) and Peet et discussed by Naveh and Whittaker a however,thatin anysituation al. (1983). We suggest, change in grazingregimewill constitutea significant animals(or difofgrazing Thus,imposition disturbance. subjectto notpreviously herbivores)on a system ferent that type or level of grazingwill constitutea distura system from bance. So, too,will theremovalofgrazing will be Species diversity with a long grazinghistory. affected by the directionof change in grazingregime relativeto the historicalregime(Ranwell 1960; White 1961; van der Maarel 1971; Milchunaset al. 1990; Dolman & Sutherland1991). Numerous authorshave reunder intermediate ported maximumspecies diversity (Zeevalking& Fresco 1977; Milchunas levels of grazing et al. 1988; Puertoet al. 1990). of how grazingafThe most detailed understanding the chalkgrassstructure comes from fectscommunity sites Europe;theseinfertile and northern landsofBritain support a diverse mixtureof grasses and forbs,with kindsand scales species adaptedto openingsofdifferent admittedly although (Grubb 1976). These communities, or grazing), (clearing,fires, of human activity artifacts have long been prominentfeaturesof the landscape; today they are of major conservationvalue both for rare species. Repeatand forparticular theirdiversity is an importhatgrazing edlyit has been demonstrated diverof chalkgrassland in the maintenance tantfactor leads to dominanceofa few thecessationofgrazing sity; grasses, and even to incursions by shrubs or other woody species (Wells 1969). Entirecomponentsof the flora may be lost; for example, During and Willems (1986) blamed the loss of mostlichensand the impoverishment of the bryophteflorain Dutch chalk grasslands on the absence of grazing. Grazing maintainshigh species diversityin other is an important as well. Grazing management grasslands, and diversity and successfultechnique for preserving and pasturesin Envalue of old grasslands conservation gland (Hopkins & Wainwright1989). Sykora et al. in the (1990) found that grasslandon embankments

Netherlands was convertedto woody scrub in the absence of grazing;under light grazing,a species-poor grasslandresultedfromcompetitionfroma few competitivegrasses.Under more intensivegrazing,those grassesdid not dominate, and a more diversegrassland was maintained. Mediterranean-climate grasslands may respondsimilarly to grazing management; in a California grassland on serpentine substrate, cessationoflivestock grazingenhanced the dominance of non-native annual grassesand led to a rapid decline in abundance of the diversenativeannualforb flora (Huenneke et al.,unpublished data). One straightforward effect of grazingis the eliminationoftreesand shrubs invading mesic grasslands. Without grazing, many North Americanprairie sites have been convertedto woodland. Similarly, there are also documented cases of grazingpreventing or reversing the succession ofAfrican savannato woodland. For example, Smartet al. (1985) found that in Uganda the exclusion of elephantswas even more important than firesuppression in encouraging acacia invasion, leading the originalgrassto the loss of manyspecies including In these regions,a long evolutionary land dominants. history ofgrazing has led to the dominanceofgrassland plantsadaptedto and tolerant ofgrazing pressure.Caldwell's work(forexample,Caldwell et al. 1981) has documented the many physiological traits that affecta losses. plant'stoleranceof grazing In contrast, regionswithno recenthistory of grazing are oftendominatedby plantsthatlack these tolerance Extremeexamples are presentedby ocemechanisms. anic islands with no native mammalian herbivores, oflivestock or othergrazershas where theintroduction in its effect on nativevegetausuallybeen catastrophic tion-for example, the effectof feral goats on island in floras (Coblentz 1978) and of introducedherbivores the Galapagos on native vegetation (Hamann 1975, 1979). A less obvious but stillmajor impact has been made on regionswithfew nativegrazers(at least since West post-Pleistocene time),such as the intermountain (Mack & Thompson 1982). In semi-aridgrasslandsin the AmericanSouthwest, has declined and, in manycases, the species diversity of the vegetationhas been alteredfrom physiognomy desert scrub. perennialgrasslandto shrub-dominated and ecology is The chiefquestionofrangemanagement rate: what the determination of the proper utilization and maintain will maximizeproductivity level ofgrazing itis not thegrassland's generalcharacter? Unfortunately, knownwhat utilizationlevel maximizesplant species or whether the same level or productivity, diversity maximizes both.Westobyet al. (1989) outlinedthe difthatwould resultfrom in grazing ferences management successional conconsidering grazingin an equilibrial, text versus a nonequilibrialseries of alternatestates;

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with the second mentalmodel requiresmuch working more activemanagement to "seize opportunities and to evade hazards." Givengrazing's impacton community ithas structure, been used as a management tool in conservation applications.One example is a grassland restoration project, where an abandoned, species-poorpasturein Holland was beinggrazedby cattle;seed inputsfrom cattlefeces (togetherwith openings created by grazing) contributed significantly to increasingspecies diversity (Bulow-Olsen 1980). In anothercase, sheep were used to restoreabandonedfields(Gibson et al. 1987), againby importing seeds and creating openingsforrecruitment. Severalgrassesin the Middle East,wild cereal ancestors of conservation interest,are negativelyaffectedby heavygrazingbut also vulnerableto competition from tallperennialgrasses.Therefore the two sets of species alternate on lightly grazedor protectedsites(Noy-Meir 1990). UplandBritish grassland species of conservation value varyin theirresponse.Some benefit from removal ofgrazing, while othersare negatively influenced by the resultingincrease in grass (Rawes & Welch 1972). Wells (1969) commented that grazing(or mowing) duringthe season when the dominantgrass species is growingmost rapidlyis usuallythe most effective way to maintain in chalk grassland. diversity He statedthat the cessationof grazing is the majorconservation problem in those grasslands,eliminating many forbs and causingincreasesoflitter and woody species. He added, however,thatgrazing shouldbe timedto avoid the sensitivephases in the life cycle of species vulnerableto grazing. This raises an important point:Effects of grazingare That is, two species in the same comspecies-specific. munity may varyin theirresponse to grazingor to a specific grazing regime.For example,in an English highelevationgrasslandon limestone, aftersheep were excluded from one site,severalrareshrubs benefited from but one species declined (Elkington1981). protection, The optimaldesignofgrazing management maythusbe difficult. Vinther(1983) found that a mesic meadow was maintained as open meadow if it was heavily grazed-because tree seedlingswere killed by browsing-or if it was not grazed at all-because seedlings couldn'testablishin the dense herb layer.Intermediate grazinglevels allowed woody regeneration and loss of the meadow's open character. Unfortunately, these same intermediate levels of grazingare those maximizingtherichnessofherbaceousspecies in theshortterm. An alternate means of preventingwoody plant encroachment would then be necessaryto allow continued management formaximumspecies diversity. Grazing'simpact presentsan interesting contrastto mowing,which is oftensuggestedas an alternative to grazing management. Mowingcan reduce the growth of competitively dominantgrasses, allowing the persis-

tence of less competitive species,but it does not create openingsforrecruitment of seedlingsas grazingdoes. et al. (1990) emphasizedthe different Sykora resultsof the two,with grazingcreatingmore microsites forestablishment and greater heterogeneity, while providing seed dispersalin animalfeces,hooves,and coats.As van den Bos and Bakker(1990) pointedout,grazersdo not use an entirearea evenlybut alwaysprefer some spots to others,so they create greaterheterogeneity than does mowing.There is also a difference in the formin which nutrients are returned or retainedin the system (Rizand et al. 1989). Grazingis thusan amalgamof different effects. ifmowingis to be used by manClearly, agersin preference to grazing, moresophisticated methods involving in mowingtimeand pattern variations and degree of mulchremovalshould be investigated. Grazinganimalsmayfrequently be implicatedin the invasionof naturalcommunities. Grazers may import non-native plantpropagulesinto nativevegetation, but theymayalso act to providemicrosites forinvasion.In particular, where grazing altersthevegetation structure or is accompaniedby soil disturbance (trampling, digging,and so forth), conditionsare modifiedin such a way thatinvadingspecies can become established.For instance, Cross (1981) showed thatgrazing by the nonnative sika deer facilitated the invasion of oak woodbaceous understory and providingmore safe sites for establishment. The arrival of largenumbersof livestock following European settlement has been implicatedin thedeclinein nativeperennial grassesand their replacementwithnon-native annualgrassesin severalgrassland areas in North America and Australia(Moore 1970; Mack 1981, 1989). Braithwaite et al. (1989) suggested thatwater buffalo aid in the establishment activities of Mimosa pigra in northern Australia. Pickard(1984) implicatedgrazing disturbance as one of the majorfactors influencing invasionon Lord Howe Island in the South
Pacific. lands by Rhododendronponticum by removing the her-

3. Soil Disturbances In grasslands, as in most plant community types,soil disturbancecreates openings for establishment, frequently of weedy or ruderal species. It is unclear whethertemporary increasesin nutrients and otherresourcesare directly forthisenhancement responsible of establishment or whetherreduced competitionfrom neighboring plantcanopies and rootsis moreimportant, and it is usually difficult to separate the two effects. Where such disturbance has long been a componentof theecosystem, thereis likely a substantial ofthe fraction flora that is specialized or adapted to establishment there.Thus in the Mediterranean where human region, and otheractivity agricultural has long createdsuch soil disturbance, there is a large and successfulgroup of

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that weedy species. These are the colonistsand invaders sites elsewhere have become so pervasivein disturbed has a much activity in the world, where agricultural shorter history and where few native species are adapted to such a habitat(Naveh 1967; Hobbs & Hopkins,1990). Plowing is said to diminishspecies richness,espe(Fuller 1987). ciallythatofdicots,in lowlandgrasslands species mayrequireplowingto perEven so, particular distursist(Preston & Whitehouse1986). Smaller-scale opportuin providing bances maybe equallyimportant forexample,in nitiesboth ecological and evolutionary; prairies,mounds created by badger excavatall-grass and diversefloraof"fugitive" tionssupporta distinctive prairie plants that live only on those mounds (Platt subgroupofspecies contributes 1975). Thisdistinctive parof those prairies, to the overall diversity stantially or ones inwhichthebackground to overgrazed ticularly by species-poor.Otherdisturbances is relatively matrix and gophersalso have significant prairiedogs,buffaloes, (Coppock et al. 1983; Collins on prairiediversity effects & Inouye 1988; Whicker& Det& Barber1985; Huntly et al. 1990). Mounds of bare soil ling 1988; Martensen ofpocket gophersact in Califorformed by the activity forseedling to providesubstrates nianannualgrasslands of lower densityand in an environment establishment status(Hobbs & and soil nutrient alteredmicroclimate and Lauenroth Mooney 1985; Koide et al. 1987). Coffin (1988) used a modelingapproach and foundthatthe effectof soil disturbances(ant mounds and mammal a funcwas chiefly community burrows)on a shortgrass of disturand secondarily frequency tionof disturbance bance size. While soil disturbances, especiallyby animals,often effects on the dynamicsof nativeplant have important thereare also numerousexamplesofsuch communities, invasionby non-native spesoil disturbances facilitating cies. Disturbanceby gopherswas foundby Hobbs and factorin the Mooney (1985, 1991) to be an important by Bromus mollis and grassland invasionof serpentine other non-native annual grasses following years of Bromus mollis became estababove-averagerainfall. lished in greaterabundance on gophermoundsthanin arabsentfrom and was virtually undisturbed grassland, eas where gopherswere excluded. Bromus mollis was able to disperseseeds onto gophermoundsmore effectivelythan some of the native species because of its and it then survivedbetteron the tallerinflorescence, thanin the undisturbed grassmore open microhabitat land. were in which artificial soil disturbances Experiments withthe effects varying createdhave had mixed results, Hobbs and Atkins plant communities. among different (1988) found that some communities were more readilyinvaded than others,and that soil disturbance did not necessarilyincrease the ease with which non-

Disor survive. nativespecies could become established in the communities that turbancehad the largesteffect were alreadymore susceptibleto invasion. Disturfacilitate invasion? Whydoes soil disturbance bance mayact primarily by providing a roughersurface on which seeds can lodge; in otherwords, the disturof safe sites (Hobbs & bance increases the availability Atkins1988). Hobbs and Mooney (1985) found that species grewmuch plantsofbothnativeand non-native than it undislargeron gopher mound microhabitats but Koide et al. (1987) found that turbed grassland, nutrient availability was actually lower in gopher soil. Hence removalof moundsoils thanin undisturbed competitors maybe the majorfactorin thiscase. 4. Nutrient Inputs whichis often less obvious, Another typeofdisturbance, in an is a change in the inputand cyclingof nutrients ninutrients, particularly ecosystem. Inputofadditional in low-fertility sites can be as trogenand phosphorus, as eutrophication in freshwater ecosystems. devastating has contributed to a markeddecline in speFertilization cies richness in Britishand Dutch grasslands(Willis 1963; Bakker1987; Fuller 1987). Grassesare oftenthe enspecies to respondand to dominateunder nutrient of broadleavedplants.Durrichment, to the detriment ing and Willems(1986) suggestedthatcontinuedinput and nitrogen were partially ofpollutants responsiblefor the floristicimpoverishment of nonvascular flora in Dutch chalk grassland.Input of atmosphericnitrogen to blame forthe increasingdominance was apparently and other ofone grassspecies and theloss ofmanyforbs grasses,regardlessof management(mowing, grazing, (Bobbink & Willems1987). burning)in chalkgrassland the problemof increaseddepositionof nutriCertainly ents fromthe atmosphereis likelyto be chronic and widespread. Gough and Marrs(1990) suggestedthathigh phosphorus levels in the soil of abandoned pastures preof species-rich grassland cluded the reestablishment there. Natural or successional losses of phosphorus were too slow froma management perspective;incurincreased sion of scrub or woody species apparently levels of extractablephosphorus.They suggestedthat managersuse cropping(cutting and removingaboveground biomass each season) or heavy leaching to lower soil-extractable phosphoruslevels more quickly. to reduce soil Marrs(1985) reporteda similareffort in a site where managerswere attempting to fertility reestablishan acid heathland.In another twenty-twoyear experimentwith cutting,Rizand et al. (1989) foundthatretaining clippingson the site keptphosphorus availability high,with a possible negativeinfluence on species composition, comparedwithremovalofclipGreen (1972) pointed out early pings or with grazing.

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on thatchalkgrassland, and heathwere dune grassland, all seral,low-fertility withhighconservation ecosystems value. He suggestedmore studyof nutrient budgetson thosesystems and pointedout thatgrazing, and burning, mowingall decreased the likelihoodof nutrient accumulations. In North American old fields, nutrientenrichedfields supportedlower species richnessand retaineda weedy annual,largelynon-native flora(Carson & Barrett1988) ratherthan the perennialgrasses typicalof fieldsof equivalentage. In ecosystems with predominantlynutrient-poor soils,additionofnutrients can constitute a majordisturbance, which has been shown in manyexamples to facilitateinvasionby non-native species. Huennekeet al. (1990) have shown that a serpentinegrasslanddominated by annualforbscan be transformed in two years into one dominatedby non-native grassesby the addition of nutrients, and phosphorus. particularly nitrogen Hobbs et al. (1988) produced similar results and showed thatsurvivalof non-native grasseswas significantlyenhancedon fertilized plots,while thatof native forbs was reduced.In boththesecases, invasion was not relateddirectly to soil disturbance and,in fact, Hobbs et al. (1988) found that subsequent gopher disturbance actuallyreduced the dominance of non-native grasses and allowed the re-establishment of nativeforbs. Nutrient invainputhas also been shown to facilitate sion ofAustralian Heddle and Specht plantcommunities. (1975) reported increased abundances of non-native herbaceous species in areas of heathlandthathad received fertilizer. Other studieshave indicateda strong between the degree of invasion by nonrelationship native species and soil nutrient of levels, particularly phosphorus (Cale & Hobbs 1991; Hester & Hobbs 1992). Experimentswhere nutrients were added to in plotswithina numberof different plantcommunities WesternAustraliashowed thatincreased nutrients resulted in increased growth of non-nativespecies in but not others(Hobbs & Atsome plant communities kins 1988). Of particular was the finding thata interest addition combinationof soil disturbanceand nutrient had the greatesteffect in enhancingthe establishment and growthof non-native species. 5. Trampling Like the other disturbances we have discussed, trampling can create openings in vegetationthat provide opportunitiesfor new individuals to become established,and it can slow the growthof dominant species to allow thepersistence ofless vigorousspesufficiently cies. Again,intermediate levels of trampling seem most at maintaining effective because of highspecies richness the suppression of competitive dominants (Liddle 1975). The season or timing of trampling has a significanteffect on thechance,rate,and species composition

ofrecovery (Harrison1981). There are species-specific responses to trampling: in one studymost but not all species were negativelyaffected (Crawford & Liddle 1977): invertebrates seem farmoresensitive thanplants (Duffey1975). We have encounteredlittleinformation on the effects of trampling on invasions, althoughtrampling effects are frequently considered togetherwith those of grazing. 6. Fragmentation The fragmentation and insularization of ecosystemsis nota disturbance within an individual system but a landscape-leveldisturbance in the rearrangement resulting ofthe landscapematrix. By influencing and edge effects the likelihood of movementof nutrients, propagules, and faunafromadjacent patches,fragmentation affects disturbanceregimesin individualpatches of remnant vegetation(Hobbs 1987; Saunders et al. 1991). How does fragmentation affect the species compositionand richnessof grasslands? and Gotelli (1984) Simberloff surveyedpatches of prairieand foundthat "archipelagoes" ofsmallgrassland patchessupported morespecies than did single large patches of equivalent total area. Thus small patch size does not constraintotal species richness. Quinnand Robinson(1987) and Robinsonand Quinn (1988) used an experimental approach to this question, subdividing annual grassland into fenced patchesseparatedby heavilygrazedzones; species richness was substantially higherin the more subdivided treatments. Singlespecies frequently came to dominate single plots, so a region with a greater number of patches supportedboth more dominantspecies (alternate dominants in different plots) and more edge species (growing along the greaterperimeter). Murphy (1989) has pointed out that Robinson and Quinn's (1988) studywas carriedout at an inappropriate scale and in a grasslandthatis dominatedby non-native annuals.However,thepointthatfragmentation will lead to an increasein edge species is important. Froma conservation managementperspective,one would want to know just which species are being favoredby edge efA highertotalspecies richnesscould be primarily fects. due to an increasednumberofruderalor weedy species of low conservationvalue (as found,for example for invertebrates by Webb & Hopkins [1984]), or to a highernumberof legitimate community members. 7. Interaction ofDisturbances Of course,mostecosystems experiencemultipledisturbances and are shaped by multiplefactors.In many cases the resultsare not merelyadditive,and disturbances can act synergistically. For example,grazingreduced fuel loads, reduced firefrequency, and allowed the invasion of woody species into many regions of semi-arid grassland (such as the historical expansionof

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vegetationinto westernU.S. grasslands; pinyon-juniper study,Collins Wright et al. 1979). In an experimental increased species (1987) found that fire significantly prairiebut not on ungrazed diversity in grazedtallgrass and fire ofgrazing in some respectstheeffects grassland; were additive.Collins and Gibson (1990) have further soil disturand small-scale how grazing, fire, illustrated of these grasslands the matrixstructure bance all affect to increasecommuand hence can interact differently, Leighet al. (1987) foundthatrabbitpopnity diversity. ulationsincreasedon burnedareas ofsubalpinevegetation, while Noy-Meir (1988) found that elevated on grasspopulationsof voles had the greatesteffects Sykora et al. was minimized. landswhere othergrazing increased in Dutch grasslands thatfire (1990) suggested nutrients and thusincreasedthe likelihoodof "ruderalization"-increasingdominanceby a fewgrassesleading Hodgkin (1984) found that to a decline in diversity. woody encroachment increased soil fertilityand changed the nature of Britishdune grassland.It was decline in rabsuggestedthatthe myxomatosis-caused bit populationshad resultedin the increasedestablishscrub and thatthe resulting mentofwoody vegetation, to the point that weedy had increased soil nutrients plantspecies were favored. Myrica faya onto Invasion by the nitrogen-fixing younglava flowsin Hawaii has been shown to alterthe nature of ecosystem developmentfollowingvolcanic eruptions (Vitousek et al. 1987; Vitousek & Walker 1989). In thisand othercases, such as thatofMimosa et al. 1989), the invading (Braithwaite pigra in Australia a majordisturbance to the constitute plantsthemselves theyare invading. systems

The relationship between soil disturbanceand invasion is also complex,and mechanicaldisturbance in the absence ofnutrient additionmaynot necessarily lead to enhancedinvasion(see Hobbs 1989). Frequently, howand nutrient ever,physicaldisturbance enrichment coincide,as when rabbitsscrape the soil and defecateat the same time,or when disturbance enhances nitrogen Animportant mineralization. problemforsystems witha statusis the gradualnutrient naturally low nutrient enrichment thatcan occur via atmosphericinput,windblown fertilizer, or inputfromlivestockfeces (Landsberg et al. 1990; Cale & Hobbs 1991). An increased baselinenutrient status will have important implications forthe whole ecosystem, but in the shorttermit may exacerbate the likelihoodof invasionsby weedy pest species.

Conclusions
No systemcan remain immune from certain disturbances (such as nutrient the atmosphere);in inputfrom thefuture, fewareaswill even be protectedfrom direct humanactivity. Some disturbance typescan be modified by on-site management (fireand grazing regimes)while disturotherscannot (floods,storms).Human-induced bances such as road construction can also be minimized. "Natural disturbance regimes"maybe desirablebut are in the alteredsettings often ofcontempoimpracticable raryreserves.We need to acknowledgethe actual disin a reserve,and turbanceregimeoperatingcurrently the currentpropagule rain,which determinesthe immanportanceof coping withlikelyinvasions.Further, agers need to take an active role in designingthe disturbance it to the landscape,the biotic regime, tailoring and theirspecificconservation community, goals. Denslow (1980) hypothesized thatany naturalcomin species adaptedto establishmunity would be richest mentin the type of patch most commonlycreated by disturbance.For example, where large scale disturbances are the norm,most species will establishthere and species richness will decline through timeand sucin an ecosystemwhere small-scale cession. In contrast, are normal, disturbances most species will establishin small scale gaps or in undisturbed sites,and diversity will increasewith time after a large disturbance. Total of nativespecies at the landscape level will be diversity greatestwhen disturbanceoccurs at its historicalfrequencyand in thehistorical pattern (Fig. 2). Changesin the size of the frequency, as well as the type,of disturbance will mean thatmostnativespecies will no longer be well adaptedforrecruitment or establishment. In addition, even when disturbance regimeshave not been significantly of weedy or altered,the availability invasivespecies may alter systemresponse to disturbance. Management mustconsidernot only alterations

Bad:Conflicts Turned GoodDisturbances

is a necessarycomAre therecases where disturbance but also and community dynamics, ponentofecosystem Fromtheforegoing, ofinvasion? enhancesthelikelihood can itwould seem thatvirtually anytypeofdisturbance Invasion invasionundercertaincircumstances. facilitate a subsetofthepossiblerecolonization is,after all,simply et al. As an example, Griffin response to disturbance. (1989) have shown how periodic floodingcan lead to theinvasionofaridzone riversystems by Tamarix aphbut rather certain ylla It is not the typeof disturbance thatshift the system aspects of its action in a particular of invasionsat the expense resulttowardenhancement et al. 1988). For example,it is of natives(see McIntyre not fireper se but the combinationof firewith other or the adoption of a fireregimeinapprodisturbance, priate to the life historiesof nativeplants,thatfavors fire-tolerant non-native species at the expense of naA primary mustbe thesuiteof tives. consideration, then, and lifehistories foundin the nativeplants, adaptations value. those of conservation particularly

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Disturbance, andInvasion 333 Diversity,

Natural Disturbance Regime maintains native species diversity

(historical type, frequency, intensity of disturbance)

decrease
ina /

chafrge
i'r \

increase
ina

intensity

frequency/

of disturbance Elimination of natives; Enhancement of invasions

(direct damage to natives: creation of new microsites)

se ty,

frequency/

intensity

Decreased diversity of natives

(dominance of competitively superior species)

Elimination of natives; Enhancement of invasions

(direct damage to natives; creation of new microsites)

ing managersto make deliberatechoices of which taxa to favor. * Managers mayhave to choose between specificconservationtargets, such as preventing the spread of invasivespecies,and the more generalgoal ofmaintaining overallspecies diversity. * Nearlyall systems are likelyto be nonequilibrial in the future;we must be activists in determining which species to encourage and which to discourage. We cannot just managepassively, or formaximal diversity, but mustbe selectiveand tailormanagementto specificgoals.

Acknowledgments
We thank JuliArmstrong, RichardGroves,and two referees for constructive commentson the draftmanuscript. Literature Cited
Abrams, M. D., A. K Knapp,and L. C. Hulbert.1986. A ten-year record of abovegroundbiomass in a Kansas taligrass prairie: effects of fireand topographic position.American Journalof Botany73:1509-1515. Bakker, J.P. 1987. Restoration ofspecies-rich grassland after a period offertiliser application. Pages 185-200 inJ.van Andel, J.P. Bakker, and R. W. Snaydon, editors.Disturbancein grasslands: causes, effects and processes.Junk, Dordrecht. Bobbink, R.,andJ.H. Willems.1987. Increasing dominanceof Brachypodiumpinnatum in chalk grasslands:a threatto a species-rich ecosystem. Biological Conservation 40:301-314. Braithwaite, R. W., W. M. Lonsdale, and J.A. Estbergs.1989. Alienvegetation and nativebiota in tropicalAustralia: the impact ofMimosa pigra Biological Conservation 48:189-210. Bulow-Olsen, A. 1980. Changesin the species compositionin an area dominatedby Deschampsia flexuosa as a result of cattlegrazing. Biological Conservation 18:257-270. Caldwell,M. M.,J.H. Richards, D. A.Johnson, R. S. Nowak,and R. S. Dzurec. 1981. Copingwithherbivory: photosynthetic capacity and resource allocation in two semiaridAgropyron bunchgrasses. Oecologia 50:14-24. Cale, P., and R.J.Hobbs. 1991. Conditionof roadside vegetationin relation to nutrient status. Pages 353-362 in D. A. Saundersand R.J.Hobbs,editors. Natureconservation 2: therole of corridors. Surrey-Beatty, ChippingNorton, Australia. Carson,W. P., and G. W. Barrett. 1988. Succession in old-field plantcommunities: effects of contrasting typesof nutrient enrichment. Ecology 69:984-994. Chase,A. 1987. Playing god inYellowstone.The destruction of America's first nationalpark.Harcourt BraceJovanovich, New York.

Figure2. Any change in thehistoricaldisturbance regimeof an ecosystem may alter species composition by reducingthe importanceof native species,by creatingopportunities for invasive species,or both. ofthe original disturbance in but also alteration regime, the pool of potential responding species (in other words,the availability of colonistsor pests). The responseofinvaders to disturbance is an extreme case of an underlying, unavoidableconflict-anydisturbance and any managementregime will be good for some species and bad forothers.The decision may be easy (althoughthe techniquesformanagement maynot be) when the choice is between nativesand non-native pest species. The dilemmais thornier when non-natives have some appeal of theirown (forinstancein termsof grazingvalue), and it is still more difflcult when the choice is betweenone set ofnativespecies and another. In the end, the wisest choice maybe to use a diversity of management to encourage different strategies, species in different partsof the reserveor in different reserveswithina region.There is no singleoptimalstrategy;managersmustmake decisionsbased on the likely costs and benefits in termsof maintenance of diversity versusinvasionby non-natives. We draw the following conclusionsfromthisreview of scientific researchon disturbanceand species comin grasslands. positionand diversity Disturbance plays an integralrole in structuring plantcommunities, but some typesor combinations ofdisturbance can increasethepotentialofinvasion by non-native species. * Background levels ofdisturbance, resourceavailability,and the pool of potentialspecies in any ecosystem all differ now fromprimevalcondition.This is true even in the largest parks and reserves (see Chase 1987). It is not enoughto saythattheoriginal disturbance regimeis the desired state. * Species varyin their responseto disturbance, requir*

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P. E., and N. D. Burrows.1986. Fire: an old tool Christensen, J.Burdon, witha new use. Pages 57-66 in R. H. Grovesand J. perspecan Australian Ecologyofbiologicalinvasions: editors. Australia. Academyof Science, Canberra, tive.Australian offeralgoats(Capra hircus) Coblentz,B. E. 1978. The effects 13:279-286. Biological Conservation on islandecosystems. of disturCoffin, D. P., and W. K Lauenroth.1988.The effect plant community. bance size and frequencyon a shortgrass Ecology69:1609-1617. in tallgrass praiofdisturbances Collins,S. L. 1987. Interaction Ecology 68:1243-1250. rie: a fieldexperiment. on of disturbance Collins,S. L., and S. C. Barber.1985. Effects in mixed-grass prairie.Vegetatio64:87-94. diversity offireon commuCollins,S. L.,and D. J.Gibson. 1990. Effects Pages 81-98 prairie. and mixed-grass in tallgrass nity structure in S. L. Collins and L. L. Wallace, editors.Fire in NorthAmeriof OklahomaPress,Norman, prairies.University can tallgrass Oklahoma. and coral in tropicalrainforests J.H. 1978. Diversity Connell, reefs.Science 199:1302-1310. Coppock, D. L.,J.K Detling,J.E. Ellis, and M. I. Dyer. 1983. mixed-grass in a NorthAmerican interactions Plant-herbivore prairiedogs on intraseasonal of black-tailed prairie1. Effects and species dynamics plantbiomassand nutrient aboveground Oecologia (Berlin) 56:1-9. diversity. R. M.,S. M. Pierce,and E.J.Moll. 1986. Conservation Cowling, an endangered and utilizationof South Coast Renosterveld, South Africanvegetationtype. Biological Conservation37: 363-377. oftrampling A. K, and M.J.Liddle. 1977. The effect Crawford, 12:135-142. on naturalgrassland. Biological Conservation ofRhododendron pontiCross,J.R. 1981. The establishment of Ecolcum in the Killarny oakwoods,S. W. Ireland.Journal ogy 69:807-824. of fireon the comCurtis, J.T., and M. L. Partch.1948. Effect petitionbetween blue grassand certainprairieplants.American MidlandNaturalist 39:437-443. of plantspecies diversity during Denslow,J.S. 1980. Patterns disturbance Oecologia 46: regimes. successionunderdifferent 18-21. 1991. Historicalclues to conDolman,P., and W. Sutherland. servation. New Scientist1749:22-25. on the fauna E. 1975. The effects of humantrampling Duffey, litter. of grassland 7:255-274. Biological Conservation of During,H.J.,and J.H. Willems.1986. The impoverishment in oftheDutch chalkgrasslands thebryophyte and lichenflora the thirty 36:143years 1953-1983. BiologicalConservation 158. T. T. 1981. Effects of excluding grazinganimals Elkington, fromgrasslandon sugarlimestonein Teesdale, England.Bio20:25-35. logical Conservation

Ewel,J. 1986. Invasibility: lessons fromSouth Florida.Pages 214-230 in H. A. Mooney and J. A. Drake,editors.Ecology of biological invasionsof NorthAmericaand Hawaii. SpringerVerlag, New York. F. 1979. Intermediate-disturbance Fox, J. hypothesis. Science 204:1344-1345. Fuller,R. M. 1987. The changingextentand conservation inin Englandand Wales: a reviewof terestoflowlandgrasslands grassland surveys1930-84. Biological Conservation 40:281300. and V. K Brown.1987. The use of Gibson,C. W. D., T. A. Watt, sheep grazingto recreate species-richgrasslandfromabandoned arable land. Biological Conservation 42:165-183. M. ver Hoef. 1988. Scale, pattern D. C., and J. Glenn-Lewin, in grasslands. and species diversity analysis, Pages 115-129 in M.J. H.J.During, A. Werger, andJ. H. Willems,editors.Diverin plantcommunities. SPB AcademicPublishsityand pattern ing,The Hague,The Netherlands. Gough, M. W., and R. H. Marrs. 1990. A comparison of soil between semi-natural and agricultural fertility plant communities: forthecreationofspecies-rich implications grassland or abandoned agricultural land. Biological Conservation51:8396. and Green,B. H. 1972. The relevanceof seral eutrophication plantcompetition to themanagement ofsuccessionalcommunities.BiologicalConservation 4:378-384. G. F.,D. M. Stafford S. R. Morton, G. E. Allan,and Griffin, Smith, K A. Masters.1989. Statusand implications of the invasionof tamarisk Northern Ter(Tamarix aphylla) on theFinkeRiver, Australia. Journalof Environmental ritory, Management29: 297-315. and vegetationprocesses. Grime, J.P. 1979. Plant strategies Wiley,New York. Grubb,P.J. 1976. A theoretical backgroundto the conservationof ecologicallydistinct groupsof annualsand biennialsin thechalkgrassland ecosystem. BiologicalConservation 10:5376. Hamann,0. 1975. Vegetational changes in the Galapagos Islands duringthe period 1966-73. Biological Conservation 7: 37-59. 0. 1979. Regeneration ofvegetation on SantaFe and Hamann, PintaIslands,Galapagos,after the eradication of goats.Biological Conservation 15:215. C. 1981. Recoveryof lowland grasslandand heathHarrison, land in southern Englandfromdisturbance by seasonal trampling.Biological Conservation 19:119-130. Heady, H. F. 1972. Burningand the grasslandsin California. AnnualTall TimbersFire Ecology Proceedingsof the Twelfth Conference. Heddle, E. M., and R. L. Specht. 1975. Dark Island Heath VIII. The effects of fertil(Ninety-Mile Plain,SouthAustralia). izerson composition and growth. Australian Journal ofBotany 23:151-164.

Conservation Biology Volume 6, No. 3, September1992

& Huenneke Hobbs Hester,A.J.,and R.J. Hobbs. 1992. Influenceof fireand soil vegeannualsat remnant nutrients on nativeand non-native Journalof wheatbelt. tationedges in the WesternAustralian Science. 3:101-108. Vegetation of natural Hobbs,R.J. 1987. Disturbanceregimesin remnants vegetation.Pages 233-240 in D.A. Saunders,G. W. Arnold, editors.Natureconservaand A.J.M. Hopkins, A.A. Burbidge, Surrey Beatty, of nativevegetation. tion:the role of remnants Australia. ChippingNorton, relaof disturbance Hobbs, R.J. 1989. The natureand effects Pages 389-405 in J.A. Drake,H. A. Mooney, tiveto invasions. F. di Castri,R. H. Groves,F.J. Kruger,M. Rejmanek,and M. A globalperspective. editors. Biologicalinvasions. Williamson, England. Wiley,Chichester, to weed invasion as a precursor Hobbs,R.J.1991. Disturbance 6:99-104. PlantProtectionQuarterly in nativevegetation. and ofdisturbance 1988. The effect Hobbs,R.J.,and L. Atkins. nutrient addition on native and introducedannuals in the WesternAustralian wheatbelt.Australian Journalof Ecology 13:171-9. dynamicsof a Hobbs, R.J.,and L. Atkins.1990. Fire-related Australian Western Australia. Banksia woodland in south-west Journal of Botany38:97-110. to fragHobbs, R.J.,and A.J.M. Hopkins.1990. Fromfrontier Proceedings ments: vegetation. Europeanimpacton Australia's of the Ecological Societyof Australia 16:93-114. and popuHobbs, R.J.,and H. A. Mooney. 1985. Community annualsin relationto grassland of serpentine lationdynamics Oecologia (Berlin) 67:342-351. gopherdisturbances. variof rainfall Hobbs, R.J.,and H. A. Mooney. 1991. Effects annualgrassland on serpentine and gopherdisturbance ability in N. California. Ecology 72:59-68. dynamics V.J.Hobbs,and H. A. Mooney.1988. S. L. Gulmon, Hobbs,R.J., Effects addition and subsequent gopher disturof fertilizer annualgrassland bance on a serpentine community. Oecologia (Berlin) 75:29 1-295. 1984. Studies Hobbs, R.J.,A. U. Mallik,and C. H. Gimingham. III. Vitalattributes on firein Scottishheathlandcommunities. of Ecology 72:963-976. of the species. Journal and itseffects on soil S. E. 1984. Scrubencroachment Hodgkin, Wales. Biological on NewboroughWarren, Anglesey, fertility Conservation 29:99-119. 1989. Changes in botanical Hopkins,A., and J. Wainwright. of enclosed grassmanagement compositionand agricultural land in uplandareas ofEnglandand Wales, 1970-86, and some conservationimplications.Biological Conservation47:219235. R. Koide, H. A. Mooney,and Huenneke,L. F., S. P. Hamburg, P. M. Vitousek.1990. Effects ofsoil resourceson plantinvasion and community structure in Californian serpentine grassland. Ecology 71:478 -491.

andInvasion 335 Disturbance, Diversity, R. F.,P. M. Vitousek, Hughes, andJ.T. Tunison.1991. Effects of invasionby fire-enhancing C4 grasseson nativeshrubsin Hawaii Volcanoes NationalPark.Ecology 72:743-746. Huntly, N., and R. Inouye. 1988. Pocket gophers in ecosystems:patterns and mechanisms. BioScience 38:786-793. Huston,M. 1979. A general hypothesisof species diversity. American Naturalist 113:81-101. I. M. 1986. Plant invasionwindows: a time-based Johnstone, classification ofinvasion potential. BiologicalReviews61:369394. Knapp,A. K, and T. R. Seastedt.1986. Detritusaccumulation limits productivity oftallgrass prairie. BioScience 36:662-668. Koide, R., L. F. Huenneke,and H. A. Mooney. 1987. Gopher moundsoil reduces growthand affects ion uptakeof two annual grassland species. Oecologia (Berlin) 72:284-290. Kucera,C. L., and M. Koelling.1964. The influence of fireon compositionof central Missouri prairie.AmericanMidland Naturalist 72:142-147. Landsberg, J., J.Morse,and P. Khanna.1990. Tree dieback and insect dynamicsin remnants of nativewoodlands on farms. Proceedings oftheEcologicalSocietyofAustralia 16:149-165. Leigh,J.H., D. J. Wimbush,D. H. Wood, M. D. Holgate,A.V. and R. I. Forrester. Slee, M. G. Stanger, 1987. Effects of rabbit I. Herbaceous grazingand fireon a subalpine environment. and shrubby Australian Journal of Botany35:433vegetation. 464. Lewin,R. 1984. Parks:how big is big enough?Science 225: 611-612. Liddle,M.J. 1975. A selectivereviewof the ecological effects on natural ofhumantrampling ecosystems. BiologicalConservation7:17-36. Loney,B., and R.J.Hobbs. 1991. Establishment, maintenance and rehabilitation of vegetationcorridors. Pages 299-311 in D. A. Saundersand R.J.Hobbs, editors.Natureconservation 2: the role of corridors. AustraSurrey-Beatty, ChippingNorton, lia. MacDonald,I. A. W., L. L. Loope, M. B. Usher,and 0. Hamann. 1989. Wildlifeconservationand the invasion of nature reservesby introduced species: a globalperspective. Pages 215R. H. Groves,F.J. 255 inJ.A. Drake,H. A. Mooney,F. di Castri, M. Rejm'anek, and M. Williamson, editors.Biological Kruger, a global perspective. invasions: Wiley,Chichester, England. L. intowestMack,R. N. 1981. InvasionofBromus tectorum ern NorthAmerica:an ecological chronicle.Agro-Ecosystems 7:145-165. Mack, R. N. 1989. Temperategrasslandsvulnerableto plant and consequences.Pages 155-179 in invasions: characteristics R. H. Groves, F.J.Kruger, J.A. Drake,H. A. Mooney,F. di Castri, M. Rejmanek, and M. Williamson, editors.Biologicalinvasions: a global perspective: Wiley,Chichester, England.

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336

andInvasion Disturbance, Diversity,

Hobbs & Huenneke 54 inW. Holzner, M.J.A. Werger, and I. Ikusima, editors. Man's impacton vegetation. The Hague, The Netherlands. Junk, Petraitis, P. S., R. E. Latham, and R.A. Niesenbaum.1989. The maintenance ofspecies diversity by disturbance. Quarterly Review of Biology64:393-418. Pickard, J. 1984. Exotic plantson Lord Howe Island:distribution in space and time.Journal of Biogeography 11:181-208. Pickett, S. T. A.,andJ.N. Thompson.1978. Patchdynamics and the designofnaturereserves.BiologicalConservation 13:2737. Pickett, S. T. A., and P. S. White,editors.1985. The ecology of natural and patch dynamics. disturbance Academic Press,Orlando,Florida. Pickett, S. T. A.,J.Kolasa,J. J.Armesto, and S. L. Collins. 1989. The ecological concept of disturbanceand its expression at varioushierarchical levels. Oikos 54:129-136. Platt,W.J. 1975. The colonisationand formation of equilibriumplant species associationson badger disturbancesin a tall-grass prairie.Ecological Monographs 45:285-305. C. D., and H. L. K Whitehouse.1986. The habitatof Preston, in Cambridgeshire, Lythrum hyssopifolium its onlysurviving Englishlocality.Biological Conservation 35:41-62. Puerto,A., M. Rico, M. D. Matias,and J.A. Garcia. 1990. Variin Mediterranean ation in structure and diversity grasslands relatedto trophicstatusand grazing Journal intensity. ofVegetationScience 1:445-452. Quinn,J.F., and G. R. Robinson.1987. The effects of experimentalsubdivision on flowering in a California plantdiversity annualgrassland. Journal of Ecology 75:837-855. Ranwell, D. S. 1960. Newborough Warren, Anglesey. III. Changes in vegetationon partsof the dune systemafterthe loss of rabbitsby myxomatosis. Journalof Ecology 48:385397. Rawes,M., and D. Welch. 1972. Trialsto recreatefloristically rich vegetationby plant introduction in the NorthernPennines,England.Biological Conservation 4:135-140. M. 1989. Invasibility of plant communities. Rejm'anek, Pages R. H. Groves, 369-388 inJ.A. Drake,H. A. Mooney,F. di Castri, M. Rejm'anek, and M. Williamson, F.J.Kruger, editors.Biological invasions:a global perspective.Wiley, Chichester,England. M. W. Gough,and T. C. E. Wells. 1989. Rizand, A.,R. H. Marrs, effects Long-term of variousconservation treatmanagement mentson selectedsoil properties ofchalkgrassland. Biological Conservation 49:105-112. Robinson,G. R., and J.F. Quinn. 1988. Extinction, turnover in an experimentally and species diversity Califorfragmented nia annualgrassland. Oecologia (Berlin) 76:71-82. Rykiel, of ecological disturE.J. 1985. Towards a definition bance. Australian Journal of Ecology 10:361-365.

Mack, R. N., and J.N. Thompson. 1982. Evolutionin steppe 119: with few large,hooved mammals.AmericanNaturalist 757-773. for Marrs,R. H. 1985. Techniques for reducingsoil fertility to research purposes:a reviewin relation natureconservation 34: England. BiologicalConservation at Roper'sHeath,Suffolk, 307-332. 1990. Imand T. G. Whitham. Martensen, G. D., J.H. Cushman, in on plantspecies diversity pact ofpocketgopherdisturbance a shortgrass Oecologia (Berlin) 83:132prairiecommunity. 138. McIntyre, S., P. Y. Ladiges,and G. Adams. 1988. Plantspeciesof richnessand invasionby exotics in relationto disturbance wetland communities on the RiverinePlain,NSW. Australian Journal of Ecology 13:361-373. P. L. Chapman,and M. K Milchunas,D. G., W. K Lauenroth, attributes along a perturbation Kazempour.1990. Community in a shortgrass ofVegetation Science steppe.Journal gradient 1:375-384. D. G., 0. E. Sala, and W. K Lauenroth. 1988. A genMilchunas, ofgrazing by largeherbivores on eralizedmodel ofthe effects structure. AmericanNaturalist 132:87grassland community 106. model of Moore,A. D., and I. R. Noble. 1990. An individualistic standdynamics. Journal of Environmental Managevegetation ment31:61-81. Australian National grasslands. Moore, R. M. 1970. Australian Australia. University Press,Canberra, and confusion: wrongspeD. D. 1989. Conservation Murphy, Biology cies, wrong scale, wrong conclusions. Conservation 3:82-84. Naveh, Z. 1967. Mediterraneanecosystems and vegetation and Israel.Ecology 48:445-459. typesin California and floristic 1980. Structural Naveh,Z., and R. H. Whittaker. and woodlands in northern Israel and of shrublands diversity areas.Vegetatio41:171-190. otherMediterranean 1980. The use of vitalattributes Noble, I. R.,and R. 0. Slatyer. to predictsuccessionalchangesin plantcommunities subject to recurrent disturbances. Vegetatio43:5-21. I. 1988. Dominantgrassesreplacedby ruderalforbs Noy-Meir, Jourin a vole year in undergrazed Mediterranean grasslands. nal of Biogeography 15:579-587. I. 1990. The effect of grazingon the abundance of Noy-Meir, wild wheat,barleyand oat in Israel. Biological Conservation 51:299-310. F. D., and A.J.M. Hopkins.1991. Weeds in corridors: Panetta, invasionand management. Pages 341-351 in D.A. Saunders and R.J. Hobbs, editors.Nature conservation2: the role of Australia. corridors. ChippingNorton, Surrey-Beatty, and J.WalkerWolf.1983. PrePeet, R. K, D. C. Glenn-Lewin, Pages 41dictionof man's impacton plantspecies diversity.

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Hobbs& Huenneke

Disturbance, Diversity, and Invasion

337

D. A., R.J.Hobbs, and C. R. Margules.1991. BiologSaunders, Conservation ical consequences of ecosystemfragmentation. Biology5:18-32. plantsand animals of introduced E. K 1989. Effects Schofield, on islandvegetation:examples fromthe Galapagos ArchipelBiology3:227-238. ago. Conservation on ofinsularization D., and N. Gotelli.1984. Effects Simberloff, ecotone. BiologicalConspecies richnessin the prairie-forest servation 29:27-46. Smart, N. 0. E., J.C. Hatton,and D. H. N. Spence. 1985. The on vegetation exclusionoflargeherbivores oflong-term effect in MurchisonFalls NationalPark,Uganda. Biological Conservation33:229-245. Soule, M. E. 1990. The onslaughtof alien species, and other challenges in the coming decades. ConservationBiology 4: 233-239. in natural commuSousa,W. P. 1984. The role of disturbance 15:353-391. AnnualReviewofEcologyand Systematics nities. and veld management R. M. 1973. Bush encroachment Strang, Biological in south-central Africa: the need fora reappraisal. Conservation 5:96-104. and J.Rademakers. 1990. VegK V., G. van der Krogt, Sykora, in the southwestern part of etationchange on embankments of different management the Netherlands underthe influence practices(in particularsheep grazing).Biological Conservation 52:49-81. and disTurner,M. G. editor. 1987. Landscape heterogenity turbance.Springer, New York. van Andel,J.,and J.P. van den Bergh. 1987. Disturbanceof J.P. Outline of theme.Pages 3-13 in J.van Andel, grasslands. and R. W. Snaydon, editors.Disturbancein grasslands: Bakker, Dordrecht. and processes.Junk, causes, effects van den Bos, J.,and J.P. Bakker.1990. The developmentof in at low stocking density by cattlegrazing patterns vegetation 51:263-272. the Netherlands. Biological Conservation in relationto van der Maarel,E. 1971. Plantspecies diversity and A. S. Watt, editors. Pages 45-63 in E. Duffey management. of animaland plant communities management The scientific EnOxford, BlackwellScientific Publications, forconservation. gland. E. 1983. Invasion of Alnus glutinosa in a former Vinther, Biintensities. grazing grazedmeadow in relationto different 25:75-89. ological Conservation

propand ecosystem Vitousek, P. M. 1986. Biologicalinvasions Pages 163-176 in H. A. erties:can species make a difference? Mooney and J.A. Drake, editors.Ecology of biological invaNew York. sions of NorthAmericaand Hawaii. Springer, P. M., and L. R. Walker.1989. Biological invasionby Vitousek, fixation, nitrogen Myricafaya in Hawaii: plant demography, Ecological Monographs59:247-265. ecosystemeffects. Vitousek,P. M., L. R. Walker, L. D. Whiteaker,D. MuellerDombois, and P. A. Matson. 1987. Biological invasion by development in Hawaii.Science Myricafaya altersecosystem 238:802-804. diversity on Webb,N. R.,and P.J.Hopkins.1984. Invertebrate Journal ofAppliedEcology21: Calluna heathland. fragmented 921-933. manageWells,T. C. E. 1969. Botanicalaspectsofconservation 2:36-44. Biological Conservation mentof chalkgrasslands. W. E. 1990. Parkmanagement of exotic plant speWestman, cies: problemsand issues. Conservation Biology4:251-259. and I. Noy-Meir. 1989. RangemanageWestoby, M.,B. Walker, menton thebasis ofa model which does not seek to establish Journal of AridEnvironments 17:235-240. equilibrium. Whicker,A. D., and J.K Detling. 1988. Ecological conseBioScience 38:778-784. quences of prairiedog disturbances. on the vegetationof White,D. J.B. 1961. Some observations the disappearanceof rabfollowing BlakeneyPoint,Norfolk, of Ecology49:113-118. bits in 1954. Journal and P. S., and S. T. A. Pickett.1985. Naturaldisturbance White, an introduction. Pages 3-13 in S. T. A. Pickett patchdynamics: and P. S. White,editors.The ecology of naturaldisturbance and patch dynamics. Academic Press,Orlando,Florida. on the vegeA.J. 1963. BrauntonBurrows:the effects Willis, to dune soils.Jourtationof the additionof mineralnutrients nal of Ecology 51:353-374. and C. M. Britton. H. A., L. F. Neuenschwander, 1979. Wright, and pinyon-juniper The role and use offirein sagebrush-grass USDA Forest Service General Technical plant communities. ReportINT-58. Zedler,P. H., and G. A. Scheid. 1988. Invasionof Carpobrotus site firein a coastal chaparral edulis and Salix lasiolepis after in SantaBarbaraCounty, California. 35:196-201. Madronio H.J.,and L. F. M. Fresco. 1977. Rabbitgrazingand Zeevalking, in a dune area. Vegetatio35:193-196. species diversity

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