9
990 Conservation Biology, Pages 990–998 Volume 17, No. 4, August 2003 Invasion of Exotic Plant Species in Tallgrass Prairie Fragments ANNE C. CULLY,*§ JACK F. CULLY JR.,† AND RONALD D. HIEBERT‡ *Division of Biology, Kansas State University, Manhattan, KS, 66506, U.S.A. †U.S. Geological Survey, Kansas Cooperative Fish and Wildlife Research Unit, Division of Biology, Kansas State University, Manhattan, KS 66506, U.S.A. ‡Midwest Region National Park Service, Omaha, NE 68102, U.S.A. Abstract: The tallgrass prairie is one of the most severely affected ecosystems in North America. As a result of extensive conversion to agriculture during the last century, as little as 1% of the original tallgrass prairie re- mains. The remaining fragments of tallgrass prairie communities have conservation significance, but ques- tions remain about their viability and importance to conservation. We investigated the effects of fragment size, native plant species diversity, and location on invasion by exotic plant species at 25 tallgrass prairie sites in central North America at various geographic scales. We used exotic species richness and relative cover as measures of invasion. Exotic species richness and cover were not related to area for all sites considered to- gether. There were no significant relationships between native species richness and exotic species richness at the cluster and regional scale or for all sites considered together. At the local scale, exotic species richness was positively related to native species richness at four sites and negatively related at one. The 10 most frequently occurring and abundant exotic plant species in the prairie fragments were cool-season, or C 3, species, in con- trast to the native plant community, which was dominated by warm-season, or C 4, species. This suggests that timing is important to the success of exotic species in the tallgrass prairie. Our study indicates that some small fragments of tallgrass prairie are relatively intact and should not be overlooked as long-term refuges for prai- rie species, sources of genetic variability, and material for restoration . Invasión de Especies Exóticas en Fragmentos de Pastizal Alto Resumen: El pastizal alto es uno de los ecosistemas más severamente afectados de Norte América. Sólo subsiste el 1% de la extensión original de pastizales, debido a su conversión extensiva a terrenos agrícolas durante el siglo pasado. Los remanentes de pastizal tienen significancia para la conservación, pero hay dudas sobre su viabilidad e importancia para la conservación. Se investigaron los efectos del tamaño del fragmento, de la diversidad de especies nativas y de la ubicación geográfica sobre la invasión por plantas exóticas en 25 sitios en el centro de Norte América a distintas escalas geográficas. Utilizamos la riqueza de especies exóticas y la cober- tura relativa como medidas de invasión. La riqueza de especies exóticas y la cobertura no se relacionaron con el área al considerar todos los sitios en conjunto. No hubo correlación significativa entre la riqueza de especies nativas y la de especies exóticas a escala de “cluster” o región ni al considerar todos los sitios en conjunto. A es- cala local, la riqueza de especies exóticas se correlacionó positivamente en cuatro sitios y negativamente en uno. Las 10 especies exóticas más frecuentes y abundantes en los fragmentos de pastizal fueron especies C 3 de temporada fresca, mientras que la comunidad de plantas nativas se integraba principalmente por especies C 4 de temporada cálida. Esto sugiere que la temporización juega un papel importante en el éxito de especies exóti- cas en el pastizal alto. Nuestro estudio indica que algunos fragmentos pequeños de pastizal alto están relativa- mente intactos y no deben dejar de tomarse en cuenta como refugios a largo plazo para especies de pastizal y como fuentes de variabilidad genética y de material para restauraciones. §Current address: Colorado Plateau Cooperative Ecosystem Studies Unit, P.O. Box 5765, Northern Arizona University, Flagstaff, AZ 86011–5765, U.S.A., email [email protected] Paper submitted March 12, 2002; revised manuscript accepted October 27, 2002.

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990

Conservation Biology, Pages 990–998Volume 17, No. 4, August 2003

Invasion of Exotic Plant Species in Tallgrass Prairie Fragments

ANNE C. CULLY,*§ JACK F. CULLY JR.,† AND RONALD D. HIEBERT‡

*Division of Biology, Kansas State University, Manhattan, KS, 66506, U.S.A.†U.S. Geological Survey, Kansas Cooperative Fish and Wildlife Research Unit, Division of Biology,Kansas State University, Manhattan, KS 66506, U.S.A.‡Midwest Region National Park Service, Omaha, NE 68102, U.S.A.

Abstract:

The tallgrass prairie is one of the most severely affected ecosystems in North America. As a result ofextensive conversion to agriculture during the last century, as little as 1% of the original tallgrass prairie re-mains. The remaining fragments of tallgrass prairie communities have conservation significance, but ques-tions remain about their viability and importance to conservation. We investigated the effects of fragmentsize, native plant species diversity, and location on invasion by exotic plant species at 25 tallgrass prairie sitesin central North America at various geographic scales. We used exotic species richness and relative cover asmeasures of invasion. Exotic species richness and cover were not related to area for all sites considered to-gether. There were no significant relationships between native species richness and exotic species richness atthe cluster and regional scale or for all sites considered together. At the local scale, exotic species richness waspositively related to native species richness at four sites and negatively related at one. The 10 most frequentlyoccurring and abundant exotic plant species in the prairie fragments were cool-season, or C

3,

species, in con-trast to the native plant community, which was dominated by warm-season, or C

4,

species. This suggests thattiming is important to the success of exotic species in the tallgrass prairie. Our study indicates that some smallfragments of tallgrass prairie are relatively intact and should not be overlooked as long-term refuges for prai-

rie species, sources of genetic variability, and material for restoration

.

Invasión de Especies Exóticas en Fragmentos de Pastizal Alto

Resumen:

El pastizal alto es uno de los ecosistemas más severamente afectados de Norte América. Sólo subsisteel 1% de la extensión original de pastizales, debido a su conversión extensiva a terrenos agrícolas durante elsiglo pasado. Los remanentes de pastizal tienen significancia para la conservación, pero hay dudas sobre suviabilidad e importancia para la conservación. Se investigaron los efectos del tamaño del fragmento, de ladiversidad de especies nativas y de la ubicación geográfica sobre la invasión por plantas exóticas en 25 sitios enel centro de Norte América a distintas escalas geográficas. Utilizamos la riqueza de especies exóticas y la cober-tura relativa como medidas de invasión. La riqueza de especies exóticas y la cobertura no se relacionaron conel área al considerar todos los sitios en conjunto. No hubo correlación significativa entre la riqueza de especiesnativas y la de especies exóticas a escala de “cluster” o región ni al considerar todos los sitios en conjunto. A es-cala local, la riqueza de especies exóticas se correlacionó positivamente en cuatro sitios y negativamente en

uno. Las 10 especies exóticas más frecuentes y abundantes en los fragmentos de pastizal fueron especies C

3

detemporada fresca, mientras que la comunidad de plantas nativas se integraba principalmente por especies C

4

de temporada cálida. Esto sugiere que la temporización juega un papel importante en el éxito de especies exóti-cas en el pastizal alto. Nuestro estudio indica que algunos fragmentos pequeños de pastizal alto están relativa-mente intactos y no deben dejar de tomarse en cuenta como refugios a largo plazo para especies de pastizal y

como fuentes de variabilidad genética y de material para restauraciones.

§

Current address: Colorado Plateau Cooperative Ecosystem Studies Unit, P.O. Box 5765, Northern Arizona University, Flagstaff, AZ 86011–5765, U.S.A., email [email protected] submitted March 12, 2002; revised manuscript accepted October 27, 2002.

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991

Introduction

Prior to European settlement in the region, the NorthAmerican tallgrass prairie extended from south-centralCanada to southern Texas (Fig. 1). Europeans arrived inthe prairie by the 1600s, but most of the conversion toagriculture took place in the last 100 years. Today, as lit-tle as 1% of the original tallgrass prairie remains. This isthe largest reduction in size for any major ecosystem inNorth America (Samson & Knopf 1994). The remainingtallgrass prairie occurs primarily at sites where rockyoutcrops and shallow soils make it impossible to plowand plant crops. The largest remaining continuous areaof tallgrass prairie extends from the Flint Hills of north-central Kansas to north-central Oklahoma. After settle-ment by Europeans, the Flint Hills region provided for-age for cattle, and livestock grazing continues to be thepredominant use of the land today. The tallgrass prairieis bordered on the east by deciduous woodlands. Onthis dynamic border, prairie patches occur within awoodland-grassland mosaic. Away from the woodlands,prairie patches have been isolated by human activitiesand are surrounded primarily by agricultural lands. Inthe tallgrass prairie area, annual precipitation averages60–80 cm. To the west, mid- and short-grass prairies bor-der the tallgrass prairie (Risser et al. 1981).

Fragments of tallgrass prairie have survived in scat-tered locations. Some are protected to conserve rem-nant plant and animal communities that were character-istic of the once-extensive ecosystem. Some are preserved

in areas that have been set aside for reasons other than con-servation (e.g., for their historical and cultural significance),such as Pipestone National Monument in southwesternMinnesota and Wilson’s Creek National Battlefield inMissouri. Most are unprotected. Considering the drasticreduction of the tallgrass prairie throughout NorthAmerica and the loss of natural ecosystem processes suchas fire and grazing, it is reasonable to question the con-servation value of the remaining fragments.

Fragmentation combined with the loss of area maycause species loss directly by eliminating habitats. Like-wise, species numbers or richness may decline in frag-ments as a result of isolation and lack of immigration ofpropagules from neighboring communities. Specific exam-ples of species decline in the tallgrass prairie over the last32–52 years are reported by Leach and Givnish (1996).The tallgrass prairie is relatively homogeneous in speciescomposition, with few endemics. Many prairie species oc-cur throughout the central part of the continent (GreatPlains Flora Association 1986). However, several tallgrass-prairie plant species are listed by the U.S. Fish and Wild-life Service as threatened (likely to become endangeredin the foreseeable future), including prairie bush clover(

Lespedeza leptostachya

), Meade’s milkweed (

Asclepiasmeadii

), and eastern and western fringed prairie orchid(

Platanthera leucophaea

and

P. praeclara

respectively).Running buffalo clover (

Trifolium stoloniferum

) is listedas endangered (U.S. Code of Federal Regulations 50, 17.11and 17.12, 31 October 1996). In addition, such a dra-matic loss of area may have led to the loss of ecotypes andassociated genetic diversity of more common species.

Fragmentation may also increase vulnerability to invasionby exotic species because small areas have a higher ratioof edge to area and thus more points of entry for exoticsas well as increased likelihood of disturbance (Hobbs &Huenneke 1992). Here, we define exotic species as thosefrom other continents arriving in North America afterthe time of Columbus, following the definition used bythe Great Plains Flora Association (1986). Exotic plantspecies may directly compete with native species andmay cause changes in ecosystem processes that haveprofound effects on native species (Mack 1989; Howe &Knopf 1991; Pimm 1991; Vitousek 1992; Christian & Wil-son 1999). The ecological consequences of most invasionsare undocumented, however, and their effects on ecosys-tem function are poorly understood (Pimm 1991; Parkeret al. 1999).

There is conflicting evidence from theoretical and em-pirical studies for the role of species diversity in the suc-cess or failure of invasions (Levine & D’Antonio 1999).Both negative (Rejmánek 1989; Pysek & Pysek 1995; Til-man 1997) and positive (Robinson et al. 1995; Smith &Knapp 1999) relationships between native species rich-ness and invasion by exotics have been found. Areasrich in species are thought by some to be resistant to in-vasion because resources are being fully used by species

Figure 1. Tallgrass, mid-grass, and short-grass prairies (Archibold 1995), and locations of four clusters of tallgrass prairie sites.

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Exotic Species Invasion of Tallgrass Prairie Cully et al.

Conservation BiologyVolume 17, No. 4, August 2003

already present and new species are unable to find unex-ploited resources ( MacArthur & Wilson 1967; Mac-Arthur 1972; Pimm 1991). Species-poor areas, on theother hand, may have unexploited resources that areavailable to new species.

Species richness can be viewed in terms of numbersof species per unit area or species density (Glass 1981;Eyster-Smith 1984; Holt et al. 1995; Kellman 1996; Harri-son 1999). Using a species-density approach in commu-nity studies of invasive species has the advantage of pro-viding information on the extent of invasion by exoticspecies. If exotics are frequent and abundant, they maybe considered successful invaders and the ones with thepotential to have a large ecological impact.

Variables that may influence invasion success includesimilarities in latitude, life history, climatic regime, andseasonality between the home of the exotic species andthe invaded area. Invasions may be limited to certaintimes of the year (Crawley 1989; Rejmánek 1989; Hobbs &Huenneke 1992; Levine & D’Antonio 1999; Stohlgren etal. 1999). Surrounding land use influences invasion; nat-ural areas surrounded by cultivated land, tame pasture( native grasslands converted to exotic species ), or ur-ban landscapes, are more prone to invasion ( Smith &Knapp 2001; Hobbs & Huenneke 1992) than natural ar-eas surrounded by native cover. Another influence on in-vasion by exotic species includes management of nativeplant communities.

We investigated fragmentation of the tallgrass prairieand how the location of the remaining fragments mayhave affected their invasion by exotic species. Specifi-cally, we asked the following questions: (1) Does exoticspecies richness increase as prairie fragments decreasein area? ( 2 ) Is exotic species richness in prairie frag-ments related to their native species richness? (3 ) Doprairie fragments surrounded by woodlands have lowerexotic species richness than those in agricultural set-tings? (4) What ecological characteristics are associatedwith the tallgrass prairie invaders? We asked these ques-tions at the local, cluster, and regional scales, and for allthe sites together.

Methods

Site Selection

The sites were grouped in four clusters; each cluster in-cluded a national monument and five other sites in thearea. We selected the first two clusters in the woodland-grassland mosaic region, where small patches of prairievegetation occur within a matrix of woodlands and for-ests. The first cluster was from sites in and around EffigyMounds National Monument, Iowa; sites ranged in sizefrom

0.1 to 16.0 ha. The shortest distance betweensites was 5 km and the longest was 40 km. The second

cluster was selected from sites near Wilson’s Creek Na-tional Monument, Missouri, where the sites ranged insize from 2.4 to 130 ha. The shortest distance betweensites was 30 km and the longest about 135 km. The thirdand fourth clusters were located in the Great Plains re-gion, where prairie fragments have been isolated by hu-man activities, primarily farming and urbanization. Thethird cluster was near Pipestone National Monument,Minnesota; sites ranged in size from 0.5 to 821 ha, withthe minimum distance between sites about 10 km andthe maximum about 50 km. The fourth cluster was cho-sen from sites around Homestead National Monument,Nebraska, where sites ranged in size from

0.5 ha to12,000 ha. The minimum distance between sites was 0.5km and the maximum distance about 270 km. Sites inthe Effigy Mounds and Wilson’s Creek clusters occurredon thin soils and rocky outcrops of limestone. All sitesbut two of the Homestead cluster fragments also hadsimilar soils and substrate. In the Pipestone area, shallowsoils rest on underlying formations of quartzite. Threeclusters had six sites and the fourth cluster had seven,including a restoration site. All sites were ungrazed, andmost were on a 3- or 4-year burning cycle.

Data Collection

In 1996 and 1997, we established six transects at each of25 sites. Transects were located in grassland with few orno trees, although some of the small sites were sur-rounded by trees and shrubs. Within each prairie, the or-igins of the six transects were randomly determined. Atthe larger-sized sites, all transects were located awayfrom the boundary, to avoid edge effects. We were notinterested in exotic species at the edge so much as theirincursion into the interior of patches of prairie. At thevery small sites, transects were unavoidably located nearthe edges. Some sites were heterogeneous in their phys-ical setting and included upland, slopes, and valley bot-toms. Other sites were entirely on uplands or slopes.Where topography allowed at a single site, we placedtwo transects on upland locations, two on slopes, andtwo in bottomlands. If a site did not have the range of to-pographic features, the six transects were then locatedbased on the topography (e.g., entirely on a slope). Forsites that were large enough, a grid was overlaid on amap of the site, grid squares numbered, and numbers se-lected randomly for the transect origins. We determinedtransect direction randomly. At four small sites, the loca-tion and direction of transects was constrained by thenecessity of fitting them all in without overlap. Mosttransects were 50 m long, except at one very small site.Five 10-m

2

circular sampling plots were located at 10-mintervals along each transect, for a total of 30 plots persite. At one small site, sampling plots were set out alongshorter transect lines at the same intervals of 10 m.More than five of the shorter transects were required to

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achieve a total of 30 sampling plots. No plot overlappedanother.

In 1997 and 1998, we recorded all vascular plant spe-cies and their abundance (measured as relative canopycover) at all the sites. We visited all the plots twice eachyear during the growing season, once in the early sum-mer and again in the late summer, to capture the twomajor peaks of growth and reproduction of the cool- andwarm-season species. We recorded the canopy coverageof each species using coverage classes similar to those ofDaubenmire (1959).

At all sites, we sampled equal numbers of plots toavoid bias due to unequal site size and sampling effort( Simpson 1964; Rosenzweig 1995). The primary focusof analysis was the number of native and exotic speciesper unit area, or species richness.

Analysis

Data from the early and late-period sampling for both1997 and 1998 were combined, and total numbers ofidentified species were calculated. The cover values foreach species and the total cover values for all species ateach site were calculated, and the percentage of the to-tal cover for each species was then determined. Wecompared native and exotic plant species at severalscales: local (within sites), clusters (sites within clusters),regional (clusters within regions), and for all sites com-bined. We compared species richness and cover valuesfollowing the methods of Ott (1993). We used PROCUnivariate and Levene’s test in PROC Glm (SAS Institute1996) to determine that the data were normally distrib-uted and that variances within clusters of sites wereequal. We used one-way analysis of variance to deter-mine whether clusters differed from one another in ex-otic species numbers and cover. When statistically sig-nificant differences occurred, we used the WallerDuncan

K-

ratio

t

test to determine which means weredifferent from the others. We also looked for relation-ships among area, species richness, and cover values of

native and exotic species by using Pearson correlationcoefficients, PROC Corr, and regression analysis (SPSS1997).

Results

Site Size and Exotic Species Numbers

We identified 573 plant taxa; 59 (10%) were exotic. (Alist of the exotic plant species can be obtained fromA.C.C.) The mean number of exotic species for all siteswas 9 (range of 2–18) (Table 1). For all sites consideredtogether, exotic species richness was not significantlyrelated to area (

p

0.85 ) ( Fig. 2 ). The two clusterswithin the woodland-grassland mosaic region were sig-nificantly different from each other in exotic speciesrichness (

p

0.05) (Table 1). The clusters in the GreatPlains region were also significantly different from eachother in richness of exotic species. Two clusters, onefrom the Great Plains region and one from the wood-land-grassland mosaic region, had significantly highernumbers of exotic species than the others (

p

0.05)( Table 1 ), suggesting that factors other than regionalvariables ( i.e., surrounding land uses, climate ) influ-enced invasion.

Exotic Species Cover

For all sites, about 16% (15.7

SD15.45) of total coverwas from exotic species (Table 1), with a minimum of0.15% and a maximum of 56%. As with species richness,there was no significant relationship between area andexotic species cover for sites considered overall (

p

0.81) (Fig. 3). However, exotic species cover decreasedsignificantly with increase in area (

p

0.02) within the

Table 1. Mean number of exotic plant species and mean percentage of exotic plant species cover (SD) ftom tallgrass prairie fragments.*

Region and clusterMean no. exotic

species (SD)Mean cover exotic

species (%)

Woodland-grasslandEffigy Mounds 6.1b (2.7) 3.9c (3.7)Wilson’s Creek 12.8a (4.9) 17.6b (18.5)

Great PlainsPipestone 12.1a (2.2) 32.8a (13.3)Homestead 6.7b (4.8) 9.5b (5.3)All sites 9.3 (4.8) 15.7 (15.5)

*

The letters a, b, and c demote significant differences between meanswithin columns (

p

0.05) (e.g., in column of mean number exoticspecies, 6.1b is significantly different from 12.8a, but not differentthan 6.7b) (ANOVA, SAS 6.1 1996).

Figure 2. Exotic plant species richness by area of tallgrass prairie fragments.

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Exotic Species Invasion of Tallgrass Prairie Cully et al.

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Wilson’s Creek cluster. The Pipestone cluster had thehighest exotic species cover at 33% (

p

0.05), and theEffigy Mounds cluster had the lowest exotic speciescover at 4% (

p

0.05) (Table 1).

Numbers of Native and Exotic Species

For all sites considered together, there was no signifi-cant relationship between the numbers of native and ex-otic plant species (

p

0.93) (Fig. 4). For the sites ofthe Effigy Mounds cluster, exotic species increased sig-nificantly (

p

0.04) with increased numbers of nativespecies (Fig. 4), but this result was strongly affected byan outlier.

At the local scale, we found a significant positive rela-tionship between native and exotic species richness at

four sites: two in the Wilson’s Creek cluster (

r

0.453,

p

0.012;

r

0.363,

p

0.049) and two in the EffigyMounds cluster (

r

0.498,

p

0.005;

r

0.527,

p

0.003). We found a significant negative relationship atone site in the Pipestone cluster (

r

0.521,

p

0.003).

Characteristics of Exotic Species

Twenty-seven percent of the exotic species were peren-nial; 13% (8 species) were perennial, rhizomatous grasses.In spite of their relatively low numbers, perennial, rhi-zomatous grasses made up 68% of the total exotic speciescover (Table 2). Two of the grasses, Kentucky bluegrass(

Poa pratensis)

and smooth brome (

Bromus inermis)

,together comprised 62% of the total exotic cover (Table2) and 10% of total cover for all plant species. Kentuckybluegrass was found in almost half of the 750 plots;smooth brome was the second-most frequently occur-ring species (Table 2). Annual species comprised a highpercentage (63%) of the total number of exotic speciesbut occurred less frequently and were less abundantthan perennial, rhizomatous grasses (Table 2). Biennialspecies made up the remaining cover for the top 10 spe-cies.

Smooth brome, tall fescue (

Festuca arundinacea

), Ken-tucky bluegrass, and Canada bluegrass (

Poa compressa

),4 of the 10 most frequently occurring and abundant ex-otic species in our study, were introduced into NorthAmerica as forage crops and for landscaping. These spe-cies have been extensively planted throughout the east-ern and midwestern regions of the United States formany years and have escaped into native plant commu-nities and become naturalized. They are considered ag-gressive weeds in settings where they are not purpose-fully planted ( Hitchcock 1971; Great Plains FloraAssociation 1986). Annual brome grasses were acciden-tally introduced to North America and are now agricul-tural and range pests (Knapp 1996; Whitson et al. 1999).Low hopclover (

Trifolium campestre

) is an herbaceousannual species that has become naturalized in parts ofthe Great Plains and is often seen in disturbed areas.One of two biennial species to make it into the list oftop 10 exotic species in our study, wild carrot (

Daucuscarota

), is found throughout the United States in oldpastures, meadows, and grasslands. Western salsify (

Tra-gopogon dubius

) has likewise become naturalized inNorth America (Great Plains Flora Association 1986;Whitson et al. 1999). These species are consideredweeds in the tallgrass prairie in the sense that they aregrowing in places where they are not wanted (Randall1997); their effects on the tallgrass prairie ecosystem arenot fully understood.

The 10 most frequently occurring and abundant ex-otic species (Table 2) were all characterized by the C

3

metabolic pathway (Downton 1975). The C

3

plant spe-cies are adapted to growth and reproduction during

Figure 3. Exotic plant species cover by area of tallgrass prairie fragments.

Figure 4. Exotic plant species richness by native plant species richness in tallgrass prairie fragments.

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cool, moist conditions and become dormant or at leastless productive during hot, dry conditions. These 10 spe-cies exhibit similar phenological traits, in that all are ca-pable of beginning their reproductive cycles early in thegrowing season ( Table 2 ). The annual brome grassesand the biennial species had the briefest period for com-pleting their phenology.

Discussion

Small natural areas are expected to have both fewer spe-cies overall and a higher proportion of exotic speciesthan larger areas (MacArthur & Wilson 1967; Hobbs &Huenneke 1992). Contrary to expectations, our studyshowed no significant relationship between area and ex-otic species richness or cover. This is in contrast to theresults of a study of serpentine grasslands of California,where small patches of grassland had higher numbers ofexotic plant species than larger, contiguous areas of hab-itat (Harrison 1999). The differences in the two outcomesmay be due to differing ecological factors that governthe potential for invasion in the two grassland systemsand to human factors. The serpentine grassland patchesare primarily a function of the presence of serpentineoutcrops; these outcrops are characterized by high ra-tios of magnesium to calcium in the soil, which mostplant species cannot tolerate. Tallgrass prairie fragmentsare primarily the result of breaking up of the sod on for-merly expansive and relatively contiguous grasslands.

In our study, we also found no significant relationshipbetween area and total species richness per samplingunit for all sites considered together. Similar patterns ofequivalent native species richness in both small andlarge areas have been reported in serpentine grasslands(Harrison 1999), other studies of tallgrass prairie (Glass1981; Eyster-Smith 1984; and Holt et al. 1995), and iso-lated gallery forests in the tropics (Kellman 1996).

Because the number of exotic species alone may notgive the full picture of the potential impact of invasion(Parker et al. 1999), we used cover as a rough estimateof the impact of exotic species at tallgrass prairie sites.Results for exotic species cover were similar to those forexotic species richness. For the all-site analysis, therewas no relationship between area and exotic speciescover. However, the exotic plant cover at sites in theWilson’s Creek cluster was significantly negatively re-lated to site size. Those sites with the highest number ofexotic species also had the highest percent cover ofexotics.

Exotic species richness in the tallgrass prairie did notappear related to regions in which the sites were located(woodland-grassland mosaic or Great Plains regions ),and the presence of a native woodland community sur-rounding the fragmented prairies did not necessarily di-minish the effects of invasion. The smallest sites of theWilson’s Creek cluster were imbedded in a woodland-grassland matrix, yet they have been invaded by manyexotic species. On the other hand, sites in the EffigyMounds cluster, also surrounded by woodlands, had fewexotic species. In addition to numbers of species, exoticplant cover was far less extensive in the Effigy Moundscluster than the Wilson’s Creek cluster. The Pipestonecluster in the Great Plains region included sites sur-rounded by croplands. These sites had high levels of ex-otic species richness and cover. The sites of the Home-stead cluster, also in the Great Plains region, weresurrounded by a mixture of land uses: grazing (includingon native prairie ), croplands, and urban areas. Thesesites had fewer exotic species and lower exotic covervalues than sites in their “sister” Pipestone cluster.

Communities with high species richness may be moreresistant to invaders than species-poor communities (El-ton 1958; MacArthur & Wilson 1967; Pimm 1991; Robin-son et al. 1995). In our study, there was no correlationbetween native species richness and exotic species

Table 2. Frequency of occurrence, percentage of cover, and ecological and phenological characteristics of the 10 most frequently occurring exotic plant taxa in tallgrass prairie fragments.

Plant taxaOccurrence of

exotics (%)Cover of

exotics (%) C

3

/C

4a

Lifeform

b

Phenology

c

Poa pratensis

49 39 C

3

G, P, Rh May–August

Bromus inermis

16 23 C

3

G, P, Rh May–July

Trifolium campestre

16 10 C

3

H, A May–September

Festuca arundinacea

7 2 C

3

G, P, Rh May–October

Tragopogon dubius

5 1 C

3

? H, B May–July

Bromus tectorum

5

1 C

3

G, A May–June

Bromus japonicus

4 4 C

3

G, A May–July

Poa compressa

4 4 C3 G, P, Rh June–AugustDaucus carota 4 1 C3? H, B April–JuneBromus sp. 3 7 C3 G, A May–?aTaken from Downton (1975) and Sage et al. (1999); ?, species not listed; C3 or C4 determined by phylogenetic relationships and phenology.bB, biennial; G, grass; H, herbaceous; P, perennial; Rh, rhizomatous.cTaken from Great Plains Flora Association (1986).

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numbers when all sites were analyzed together. Wefound significant positive correlations between nativeand exotic species richness at the local scale at 4 of the25 sites, and a significant negative correlation at 1 site.Smith and Knapp (1999) reported a significant positiverelationship between native and exotic plant speciesnumbers at the local scale at the Konza Prairie BiologicalStation. Stohlgren et al. ( 1999 ) found that, as in ourstudy, the relationship between the number of nativeand exotic species varies depending on the scale of sam-pling: exotic species diversity is negatively related to na-tive diversity at the subplot scale (samples within largerplots) but positively related at the site scale. Because welooked at invasion after the fact, we cannot be surewhether or not species diversity played a role in thepast. We found little evidence, however, that native spe-cies diversity influences or determines exotic speciessuccess in tallgrass prairie.

The ecological and growth-form characteristics of theexotic species in our study suggest that the tallgrass prai-rie is vulnerable to invasive plants that have certain char-acteristics. All of the 10 most frequent and abundantplant taxa were cool-season, or C3, species. This fits thepattern reported by Smith and Knapp ( 1999 ) for theKonza Prairie Research Natural Area in Kansas, where90% of the exotic flora is C3 species. The dominance ofcool-season exotic invaders is in distinct contrast to thedominance of native C4 grasses in the prairie vegetation.It isn’t clear why C3 invaders are successful, but it maybe related to the fact that many of the invasive speciesare capable of beginning their reproductive cycle earlyin the year and can flower, produce fruit, and disperseseed before the peak of growth occurs in the warm-sea-son species. Those species that can use available spaceand light before the warm-season species’ canopy reachesits full extent may be able to maintain themselves in theplant community. Later in the growing season, warm-sea-son species reach their full abundance, obscuring andovershadowing the cool-season species, many of whichhave completed their reproduction and photosynthesis.Perhaps during the spring and early summer more openconditions provide the best opportunity for new speciesto enter the plant community. Fire and grazing patterns ofthe past probably also played a role in invasions by exoticspecies such as Kentucky bluegrass, which are now wide-spread and abundant.

The effect of exotic species on ecosystem processeswas not the focus of this study, but their pervasive pres-ence and abundance suggests that invasions may havehad a significant but undocumented effect on species di-versity (and perhaps ecosystem processes) in the rem-nants of tallgrass prairie. Exotic perennial, rhizhomatousgrass invaders may compete for nutrients and moisturewith species of similar life form or phenology (Wedin &Tilman 1990; Nernberg & Dale 1997; van der Kamp etal. 1999). Early-season native species that may be dis-

placed by exotics include leguminous forbs (i.e., speciesin the genera Psoralea and Dalea) and perennial grasses(i.e., Koeleria cristata and Dichanthelium spp.). Forbsare the source of much of the native species diversity inthe tallgrass prairie, and the effects of invasion on thiscomponent of the community could be severe. Domi-nant native species in our study included big bluestem( Andropogon gerardii ), Indian grass ( Sorghastrumnutans), and switchgrass (Panicum virgatum), whichare also perennial rhizomatous grasses. Annual bromegrasses have altered ecosystems in the western UnitedStates by changing the fire regime (Mack 1989; Knapp1996) and have altered nutrient cycling and soil biota inwestern semiarid communities (Belnap & Phillips 2001;Evans et al. 2001). The presence of exotic annual spe-cies in the tallgrass prairie may displace native annualspecies such as six-weeks fescue (Festuca octoflora )and daisy fleabane (Erigeron strigosus), as well as seed-lings of native perennials.

Area, region, and native species richness provided lit-tle explanation for invasion of tallgrass prairie fragmentsby exotic species. Consequently, we must look at otherfactors for more complete understanding of invasion inprairie fragments (Howe 1993; Kowarik 1999). Our re-sults suggest that cool-season species have a high proba-bility of success in the tallgrass prairie. This informationmay be useful in predicting which new exotic speciesare likely to become invaders; limited resources canthen be applied most effectively to future invasions.Other factors involved in successful invasions of thetallgrass plant communities may include many we didnot measure or analyze. Soil characteristics, moistureavailability, and other ecological factors may be relevant,but management and use of land surrounding the sitesare probably also key to explaining invasions. Additionalstudies, addressing adjacent land use, species composi-tion of surrounding areas, management regimes, andecological characteristics will be important in assessingthe potential for future invasions of tallgrass prairie.

In the past, it was assumed that fragmentation of andexotic invasion into prairie fragments had caused loss ofnative species. Our results show that some small patchesof tallgrass prairie are relatively intact and can support anear-full complement of native species. Although thesetallgrass prairie units are not a substitute for large pro-tected areas, small fragments of prairie should receive at-tention from conservationists and land managers as long-term refuges for prairie species and sources of geneticvariability and material for restorations.

Acknowledgments

The U.S. Geological Survey provided funding for thisstudy through the Natural Resources Preservation Pro-gram. The Division of Biology at Kansas State University

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Cully et al. Exotic Species Invasion of Tallgrass Prairie 997

also provided support. The Iowa Department of NaturalResources, Konza Prairie Biological Station, the Minne-sota Department of Conservation, the Minnesota Depart-ment of Natural Resources, the Minnesota Historical So-ciety, the Missouri Department of Conservation, theMissouri Department of Natural Resources, the NationalPark Service, The Nature Conservancy, and the Wiscon-sin Department of Natural Resources gave us permissionto work on prairies under their management. R. Rovang,L. Thomas, G. Willson, and M. Skinner helped locateprairies for the study. R. Hamilton helped locate studyareas and provided logistical support. I. Barnard, G.Towne, and A. Paulin helped with plant identification.Our excellent field technicians included A. Ricehill, A.Paulin, M. Wong, C. Perchellet, and T. Swanson. T. M.Barkley, A. Knapp, and J. Blair reviewed the manuscriptat an early stage. Comments by S. Timming and S. Wil-son greatly improved the paper.

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