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6-2004

Exotic Weed Invasion Increases the Susceptibility of Native to Attack by a Biocontrol Herbivore

Tatyana A. Rand University of Nebraska - Lincoln, [email protected]

Svata M. Louda University of Nebraska - Lincoln, [email protected]

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Rand, Tatyana A. and Louda, Svata M., "Exotic Weed Invasion Increases the Susceptibility of Native Plants to Attack by a Biocontrol Herbivore" (2004). Faculty Publications in the Biological Sciences. 66. https://digitalcommons.unl.edu/bioscifacpub/66

This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in the Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Ecology, 85(6), 2004, pp. 1548±1554 ᭧ 2004 by the Ecological Society of America

EXOTIC WEED INVASION INCREASES THE SUSCEPTIBILITY OF NATIVE PLANTS TO ATTACK BY A BIOCONTROL HERBIVORE

TATYANA A. RAND1 AND SVATA M. LOUDA School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588-0118 USA

Abstract. Landscape change has great, yet infrequently measured, potential to in¯uence the susceptibility of natural systems to invasive species impacts. We quanti®ed attack by an invasive biological control weevil (Rhinocyllus conicus) on native thistles in relation to two types of landscape change: agricultural intensi®cation and invasion by an exotic thistle, Carduus nutans, the original target of biological control. Weevil egg load was measured on native thistles in three landscape types: (1) agriculture dominated, (2) grassland dom- inated with exotic thistles, and, (3) grassland dominated without exotic thistles. We found no difference in egg load on native thistles within grassland landscapes without exotic thistles vs. within agricultural landscapes, suggesting that agricultural intensi®cation per se does not in¯uence levels of weevil attack. However, attack on the native un- dulatum increased signi®cantly (three- to ®vefold) with increasing exotic thistle density. Within-patch exotic thistle density explained Ͼ50% of the variation in both the intensity and frequency of weevil attack. Since R. conicus feeding dramatically reduces seed pro- duction, exotic thistles likely exert a negative indirect effect on native thistles. This study provides some of the ®rst empirical evidence that invasion by an exotic can increase attack of native plants by shared insect herbivores. Key words: apparent competition; associational susceptibility; biological control; insect herbiv- ory; landscape change; plant invasion.

INTRODUCTION suggesting that plants may experience a relative refuge from their herbivores, including invasive insects, in Invasive species are a leading threat to the integrity fragmented landscapes. In our study system, the agri- of natural populations and communities (Wilcove et al. cultural (crop) matrix is not suitable habitat for the

Reports 1998, National Research Council 2002). While a land- biocontrol weevil, Rhinocyllus conicus, since it lacks scape-scale approach to evaluating community suscep- host plants. Thus, we predicted that weevil densities tibility to colonization and impact by invasive species would decrease with increasing amounts of agricultural is likely to provide key insights, few studies have done habitat within the larger landscape, resulting in reduced this quantitatively (but see Smallwood 1994, Suarez et attack on native thistles. al. 1998, Higgins et al. 1999, Hobbs 2001). In this Susceptibility of native species to invasive species study, we examined the in¯uence of landscape changes, impacts may also be in¯uenced by previous invasions. including agricultural intensi®cation and invasion by Areas that have been invaded by one species can be an exotic weed, on the susceptibility of native thistles more or less susceptible to invasion by another species, to attack by an invasive biocontrol weevil. depending on their interactive dynamics (Simberloff Landscape structure can affect the movement and and Von Holle 1999). In plant±herbivore systems, the population dynamics of species and, thus, may in¯u- presence of an invasive host plant likely facilitates ini- ence invasion dynamics (With 2002). For example, tial establishment of adapted exotic herbivores, which land-use practices in the habitat matrix surrounding may ultimately negatively impact the plant population. natural areas may promote large populations of exotic This is the desired outcome of classical biological con- or weedy species, which then serve as sources of col- trol (DeBach and Rosen 1990). However, in the absence onists into adjacent natural areas (Janzen 1983, Hobbs of signi®cant limitation by the insect, exotic plants may 2001). In contrast, natural areas surrounded by a highly maintain insect densities at high levels, thereby in- inhospitable matrix may experience reduced rates of creasing their impact on nontarget native species (Holt colonization by exotics, similar to isolated islands in and Hochberg 2001). The importance of exotic plants biogeography theory (MacArthur and Wilson 1967). in mediating the degree of nontarget attack of natives Previous studies have found reduced densities of her- by biological control insects has not been investigated bivores in more isolated or fragmented habitats (Kruess previously. We hypothesized that the presence of exotic and Tscharntke 1994, Steffan-Dewenter et al. 2001), thistles in a landscape would increase attack on co- occurring native thistles, compared with landscapes in Manuscript received 18 April 2003; revised 12 August 2003; which exotic thistles were absent or rare. accepted 18 November 2003. Corresponding Editor: D. L. Urban. To examine whether changes to the landscape alter 1 E-mail: tatyana [email protected] the susceptibility of native thistles to attack by R. con- 1548 June 2004 LANDSCAPE CHANGE AND INSECT INVASION 1549 icus, we quanti®ed nontarget use by R. conicus of two scapes ``without C. nutans,'' which had no, or very native thistle species, Cirsium undulatum and C. ¯od- low, densities (Ͻ10 thistles/ha) in any of the eight land manii, in grassland patches within three landscape parcels surrounding each patch. The replicate land- types: (1) agriculture (crop) dominated, (2) grassland scapes within each of the three landscape categories dominated with exotic thistles, and (3) grassland dom- were independent, i.e., nonoverlapping (Fig. 1A). inated without exotic thistles. We addressed two se- To keep patch characteristics as similar as possible, quential questions: (1) does the susceptibility of native we only selected grassland patches that had not been thistles to attack by the biocontrol insect differ between in agricultural use since at least 1971 (earliest land- landscape types, and, if so, (2) to what extent does cover data available) and had no evidence of being exotic thistle density, either within a patch or in the overgrazed (average vegetation height Ͼ20 cm). Patch- surrounding matrix, predict the level of attack? es were also matched using major soil and climatic variables extracted from a GIS database (Milner et al. MATERIALS AND METHODS 2002). Sites were selected such that soil variables Study system (based on data from USDA Soil Conservation Service [1994]) were held constant among all patches (root The study was done in the loess mixed grass prairie zone water holding capacity ϭ 302 mm; surface- of central Nebraska, USA. The common thistle species weighted soil organic matter ϭ 1.9%). Climate vari- in the region include one exotic, Carduus nutans L. ables did not signi®cantly differ between patches in (musk thistle), and two natives, Cirsium undulatum different landscape types (n ϭ 5 patches per landscape (Nutt.) Spreng. (wavyleaf thistle), and Cirsium ¯od- type; one-way ANOVA: growing degree days, F ϭ manii (Rydb.) Arthur (Flodman's thistle). 2,12 1.584, P ϭ 0.245; average precipitation, F ϭ 0.516, The weevil (Rhinocyllus conicus FroÈl.) was intro- 2,12 P ϭ 0.612). duced to the from Europe in 1969, and In the ®rst year (2001), we located and sampled to Nebraska in 1969±1972, against exotic Eurasian patches in grassland landscapes with or without exotic thistles, especially the Carduus nutans complex thistles (n ϭ 3 replicates per landscape type). Both (McCarty and Lamp 1982, ZwoÈlfer and Harris 1984, native thistle species were sampled within all six em- Gassmann and Louda 2001). In the spring, overwin- Reports bedded patches. In the second year (2002), we in- tered adults of R. conicus mate and lay eggs on the creased the sample size (n ϭ 5 replicates per landscape bracts of developing thistle ¯ower heads. After larvae type) and included patches within an agriculturally hatch, they burrow into the receptacle, feed for 25±40 dominated matrix (Ͼ50% crop cover). We were unable d, and then pupate in hardened cells within the base of to locate both thistle species in all patches. We found the ¯ower head (ZwoÈlfer and Harris 1984). In our re- C. undulatum in grassland patches within all except gion, R. conicus is univoltine. one agricultural landscape. C. ¯odmanii occurred in Selection of study areas patches within all ®ve agricultural landscapes, but only in three grassland landscapes with exotic thistles and South central Nebraska is comprised of a mosaic of in four without exotics. agricultural and natural (primarily grassland/range- land) habitats (Fig. 1A). Study areas were patches of Measurement of thistle densities prairie grassland (800 ϫ 800 m). Patches were em- bedded within a matrix composed of the eight sur- In 2002, we measured the density of bolting (¯ow- rounding 800 ϫ 800 m land parcels (Fig. 1B). Patch ering) individuals of both native and exotic thistle spe- plus matrix areas together make up what we de®ne as cies within each patch and the density of exotic thistles the landscape (total landscape area of 2.4 ϫ 2.4 km2). in the surrounding matrix. Within patch thistle densities Grassland patches were identi®ed using land-cover data were measured by walking ®ve 800 m long transects, from the National Land Cover Database (U.S. Geolog- ϳ200 m apart, starting at each patch edge (Fig. 1B). ical Survey 2000), derived from 1992 Landsat The- All ¯owering C. nutans individuals were counted in a matic Mapper satellite data. Potential grassland patches 30 m wide area (15 m to each side) along each transect. were selected in areas of high surrounding agricultural Because native thistles are much smaller and less ob- cover (Ͼ50% crop cover in the matrix) or low agri- vious, we counted all bolting individuals of all thistle cultural cover (Ͻ10% crop cover in the matrix). Within species in a 2 m wide band along each transect. areas of low matrix agricultural cover, grassland patch- Densities of C. nutans in the surrounding matrix es were selected in landscapes with or without the ex- were estimated quantitatively by doing point counts at otic thistle (Carduus nutans). We consulted with county the corner of each patch, as well as three points (200 weed agents and used the Nebraska scoring system to m apart) along each patch edge (total of 16 points; Fig. identify landscapes ``with C. nutans'' in which at least 1B). At each corner, the number of bolting exotic this- two of the eight, 800 ϫ 800 m, land parcels surrounding tles was counted in a 100 m radius arc (270Њ)inthe each patch were considered ``moderately to severely'' adjacent matrix, using binoculars. Similarly, at each infested by exotic thistles (Ͼ200 thistles/ha), and land- edge point we counted all bolting C. nutans within a Reports eiice(180 semicircle 1550 lnshdbe bevdpeiul.Tite were Thistles previously. (2001, observed July been where of edge had patch half a plants near ®rst initiated transects the along 2002) in intensively sampled ryaesrpeetcos td adcps(2.4 landscapes Study crops. represent areas gray trix. ifrn adcp ye:A agricultural; A, types: landscape different F netueo hslswti rsln ace was patches grassland within thistles of use Insect iga feprmna adcpscmoe facnrlpthadtesronigmti.Dse ie niaethe indicate counts lines point Dashed of location matrix. the surrounding represent points the matrix. black and surrounding while the densities, patch thistle in central within-patch densities quantify a estimate to to of used transects composed of landscapes location experimental of diagram IG .()Lyu fsuylnsae ncnrlNbak,UA ih ryaesrpeetntrlhbtt hl dark while habitat, natural represent areas gray Light USA. Nebraska, central in landscapes study of Layout (A) 1. . g est nntv thistles native on density Egg Њ f10mrdu nteajcn ma- adjacent the in radius m 100 of ) AYN .RN N VT .LOUDA M. SVATA AND RAND A. TATYANA ϩ ,ivddb xtcthistle; exotic by invaded E, ϫ . m r niae ybakotie qae.Dfeetltesrepresent letters Different squares. black-outlined by indicated are km) 2.4 iiulwsslce admy oa apesizes sample Total in- 10 randomly. an were clusters, selected in was occurred of thistles minimum dividual When a apart. at m encountered 10 were they as measured o w ie hr ewr nyal o®degtor eight ®nd to able of only were individuals we 12 where sites except 2002, two in available for was it each where for patch individuals per 20 species and 2001, in patch per dividuals isu ¯odmanii Cirsium Ϫ ,ntivddb xtctite B Schematic (B) thistle. exotic by invaded not E, .undulatum C. n 25 and . clg,Vl 5 o 6 No. 85, Vol. Ecology, .undulatum C. in- June 2004 LANDSCAPE CHANGE AND INSECT INVASION 1551

For each thistle, we measured R. conicus egg load on three ¯ower heads per plant: the primary terminal head, the ®rst subsidiary head on the ®rst branch, and the terminal head on the second branch. If one of the heads was unavailable for sampling (aborted or miss- ing), we selected the next available branch terminal head (®rst or third branch). For each ¯ower head, we also recorded diameter, ¯owering stage, and the number of R. conicus egg cases plus larval entrance holes as an estimate of the total number of eggs deposited per head. Statistical analyses The main response variable analyzed was the mean number of R. conicus eggs per head (egg load) for each plant species. These data could not be normalized, as many plants had no eggs. Thus, an analysis of variance (ANOVA) could not be used for the entire data set. As a result, we calculated a patch-level mean for R. conicus egg load for each native thistle species. Egg load data were power transformed (x0.4) prior to analysis to nor- malize distributions and meet assumptions of statistical models. We then used one-way ANOVA on patch means to test for differences in R. conicus egg load among landscape types. Planned contrasts were used to examine differences between two sets of landscapes Reports in 2002. First, to examine in¯uences of cultivated hab- FIG.2. Rhinocyllus conicus egg load (untransformed itat on weevil attack, we contrasted agricultural land- means Ϯ 1 SE) on the two native thistle species in grassland scapes vs. grassland landscapes without exotic thistles. patches within two landscape types in 2001, and three land- Second, to examine the effect of exotic weed invasion scape types in 2002. Results of planned contrasts comparing landscape pairs are presented above bars for 2002 (NS ϭ not on weevil attack, we contrasted grassland landscapes signi®cant; *P Ͻ 0.05). with vs. without exotic thistles. For 2002, we also cal- culated the frequency of R. conicus attack by scoring each plant at each site as having R. conicus eggs either present or absent. as having exotic thistles present, both within patches Since R. conicus oviposits early in the growing sea- and within the surrounding matrix (mean density Ϯ 1 son, egg load on the late-¯owering C. ¯odmanii was SE; patch ϭ 111.26 Ϯ 59.00 plants/ha, matrix ϭ 72.76 very low (mostly zeros). Thus, detailed analyses for Ϯ 22.7 plants/ha, n ϭ 5) vs. absent (patch ϭ 0.45 Ϯ 2002 were carried out only for C. undulatum. Densities 0.28 plants/ha, matrix ϭ 3.83 Ϯ 2.10 plants/ha, n ϭ of the exotic musk thistle, Carduus nutans, at the patch 5). Patch and matrix C. nutans densities in agricultural and matrix levels were highly correlated (r ϭ 0.76, P landscapes were similar to those in uninvaded grass- ϭ 0.001, n ϭ 14), and could not be included in a single land landscapes (patch density ϭ 2.38 Ϯ 1.04 plants/ model. Thus, we ran separate univariate regressions to ha, matrix density ϭ 4.54 Ϯ 4.15 plants/ha, n ϭ 4). examine the effects of thistle density (patch C. nutans We found that R. conicus eggs were present at all density, matrix C. nutans density, and patch C. undu- six sites in 2001 and 12 of 15 sites in 2002. Egg den- latum density) on mean R. conicus egg load on C. un- sities were generally higher in 2001 than 2002, and dulatum, and on the proportion of C. undulatum plants much higher on C. undulatum than on C. ¯odmanii (Fig. attacked. In these analyses, independent variables were 2). Egg load also differed among landscape types in also transformed to minimize problems associated with both years (Fig. 2). In 2001, mean R. conicus egg den- in¯uence and heteroscedasticity (Hamilton 1992). sity on the two native species was almost twice as great Thistle densities (both C. nutans and C. undulatum) in patches within landscapes with exotic thistles than were power transformed (x0.3) prior to analysis. within landscapes with extremely low densities of the exotic thistle. Given the variability observed, however, RESULTS these differences were not statistically signi®cant for

Although the exotic thistle, Carduus nutans, was pre- either species (one-way ANOVA: C. ¯odmanii, F1,4 ϭ sent at very low densities in landscapes that had been 0.722, P ϭ 0.443; C. undulatum, F1,4 ϭ 0.215, P ϭ classi®ed as ``exotic free,'' densities were more than 0.667). Low replication in 2001 (n ϭ 3 replicates per an order of magnitude higher in landscapes categorized landscape type) likely contributed to this result. Reports .conicus R. ( effect signi®cant no had density undulatum on C. load egg than in variation more site-to-site explaining the predictor, of best 50% the was density undulatum C. 1552 we adcp ye eecerysgicn for be- signi®cant loads clearly egg were in types differences landscape den- low thistles; tween con- very exotic with that of those landscapes in sities in than thistles higher exotic times tained four than more at fwei tako aiepat.Ti eutcon- result This plants. determi- native important on attack be weevil habitat of to nants increasing appear landscape-level not or the do plants discontinuity, host in native reduction of abundance as inten- such agricultural with si®cation, associated likely Thus, thistles. factors exotic landscapes other of densities grassland low similarly within had that dominated patches agriculturally and the landscapes within patches between thistles. exotic of in differences densities associated patch-level by largely explained be could without 2%,prleigteptenosre o g load. egg for observed for Similarly, pattern the paralleling (22%), raigdniisof densities creasing adcpswithout landscapes is h est of density The cies. R akdws®etmshge ngasadlandscapes grassland in by higher invaded times ®ve was tacked iiso xtctite oprdwt nesv agri- 2). intensive (Fig. with landscapes compared den- cultural thistles low exotic with of landscapes sities grassland within patches in ac n arxlvl Fg ) Within-patch 3). (Fig. levels matrix and patch adcps(5%). landscapes g odi eevd(i.3.However, average 3). the (Fig. on received effect it signi®cant load a egg have not did patch, lottiea ihi rsln adcpsinvaded landscapes grassland in by high as twice almost lne otat hwdta (1) that showed contrasts Planned patch in®atywt nraigpatch increasing with signi®cantly ihlwdniiso xtctite,ad()teewas there (2) in and difference thistles, no exotic those of to densities relative low thistles with exotic grassland by in invaded higher landscapes signi®cantly was thistles native on ( a ANOVA: way odon load on load dulatum dulatum ¯odmanii 2 vrl,tessetblt fntv thistles, native of susceptibility the Overall, were densities Egg stronger. was pattern the 2002, In g odo aietite i o ifrsigni®cantly differ not did thistles native on load Egg .nutans C. h ecnaeof percentage The h nuneo hsl este on densities thistle of in¯uence The ϭ .undulatum C. 0.49, .undulatum C. .undulatum C. and .nutans C. n20 Fg ) iial,tepooto of proportion the Similarly, 3). (Fig. 2002 in n agnlys for so marginally and ifrdaoglnsaetps hseffect This types. landscape among differed P nutans C. .¯odmanii C. 5% hni ihrgasadlandscapes grassland either in than (52%) .¯odmanii C. , lnsatce by attacked plants ϭ .¯odmanii C. F .conicus R. 0.005, 2,11 2% rarclua landscapes agricultural or (28%) .nutans C. est ( density .undulatum C. .undulatum C. D ϭ .nutans C. ISCUSSION nrae in®atywt in- with signi®cantly increased 2% hnete ngrassland in either than (25%) eedduo h hsl spe- thistle the upon depended n oatc yteeoi weevil exotic the by attack to , 3.434, ϭ h ecnaeo lnsat- plants of percentage the , g odo aiethistles native on load egg 4,btmatrix but 14), F P 2,9 esrda ohthe both at measured , ϭ agricultural or (4.5%) P AYN .RN N VT .LOUDA M. SVATA AND RAND A. TATYANA ϭ .conicus R. .undulatum C. esrdwti a within measured , 0.43). .conicus R. P lnsatce was attacked plants ϭ 4.664, .nutans C. ϭ .6;Fg 2). Fig. 0.069; .conicus R. .conicus R. .4,nrdid nor 0.14), P .nutans C. increased .nutans C. ϭ g load egg density .un- C. .un- C. 0.041; (one- egg egg C. otdi rvossuisweesgicn effects 2001). signi®cant al. et where (Steffan-Dewenter re- studies found that were previous than higher in is ported which habitat, contained still natural study that 25±40% this fact in the landscapes re¯ect Tscharntke agricultural may the results and in (Kruess disparity The increases 1994). patches between distance plant as host or 2001), landscape al. a et within (Steffan-Dewenter pro- decreases the habitat as natural insects of seed-feeding portion by damage reduction of a levels demonstrating in studies previous with trasts .2) rnfre aaaepotdfrbt hsl density thistle both for plotted ( are data Transformed 0.028). undulatum Cirsium iy( sity x matrix-level nutans 0.3 F IG and ) R .3. 2 est ( density ϭ .conicus R. 0.02, hnclu conicus Rhinocyllus .nutans C. F R 1,12 2 nrlto opthlvlcnpc® den- conspeci®c patch-level to relation in , ϭ ϭ g od( load egg 0.53, 0.23, est ( density P F 1,12 ϭ y g odo h aiethistle, native the on load egg R 0.4 .3) patch-level 0.639), 2 ϭ ). ϭ 13.56, clg,Vl 5 o 6 No. 85, Vol. Ecology, 0.34, F P 1,12 ϭ ϭ .0) and 0.003), 6.28, Carduus P ϭ June 2004 LANDSCAPE CHANGE AND INSECT INVASION 1553

Exotic thistle invasion strongly increased native thereby increasing the likelihood and magnitude of eco- plant susceptibility to herbivory. Both the intensity logical impacts on native species. Our results suggest (mean egg load) and frequency (proportion of plants that R. conicus is facilitated by the presence of the damaged with eggs) of attack by R. conicus were much exotic thistle, and past studies con®rm that it is often higher (two- to ®vefold) on native thistles within grass- limited in its ability to reduce weed population den- land landscapes that contained large populations of the sities (Gassmann and Louda 2001). Thus, persistent exotic thistles than in those with low densities. This exotic thistle populations appear to serve as a ``res- pattern was consistent both across species and years, ervoir'' of R. conicus, magnifying both the intensity suggesting its robustness. More detailed analysis re- and frequency of the weevil's attack on associated na- vealed that R. conicus egg load on C. undulatum in- tive thistles. creased signi®cantly with increases in both patch and The danger associated with nontarget feeding by bi- matrix densities of the exotic thistle. However, since ological control agents is widely recognized (Turner et patch and matrix densities were correlated, it was not al. 1987, Louda et al. 2003b). What is less obvious is possible to separate the relative importance of each. that the magnitude of the threat posed to nontarget Patch density explained more of the variation (53%) species can be determined largely by the dynamics of in R. conicus egg load on native thistles, however, and the control agent±target weed interaction (Holt and it was the only signi®cant predictor of the frequency Hochberg 2001), as appears to be the case here. In of attack. In contrast to the strong effects of exotics, situations where the control agent imposes only mod- patch-level densities of native conspeci®c thistles (C. erate to little control over its target prey species, the undulatum) had no signi®cant effect on either weevil exotic plant can remain suf®ciently abundant to support egg load or the frequency of attack. Thus, in this sys- large herbivore populations, resulting in ``spillover'' tem, R. conicus dynamics appear to be strongly linked onto nontarget native species with potentially serious to densities of the exotic rather than the native thistles. ecological consequences (Holt and Hochberg 2001). A Weevil feeding and larval development dramatically relatively small percentage (20%) of weed biological reduce seed production in early ¯owering native spe- control insect introductions show evidence of signi®- cies, including C. canescens and C. undulatum, since cant quantitative limitation of the targeted weed pop- R. conicus is active over the majority of their ¯owering ulation (Williamson and Fitter 1996). Thus, in many Reports period (Louda 1999). For example, seed production of cases, abundant weed populations and their associated C. undulatum is reduced by more than 80% in ¯ower exotic insects may remain in the environment. This heads with R. conicus feeding compared to those with- combination creates the potential for negative, syner- out (Louda 1999), and weevil egg load is signi®cantly gistic effects on native species, such as those docu- negatively correlated with seed production for ¯ower mented in this study. heads of a given size (r ϭϪ0.24, P Ͻ 0.0001; S. M. A number of other factors, including host-plant phe- Louda, unpublished data). In addition, nontarget feed- nology and herbivore feeding preferences, may addi- ing by R. conicus has led to severe declines in the tionally in¯uence the intensity of nontarget effects population densities of the native, Cirsium canescens (Louda et al. 2003b). We found that levels of attack of Nutt. (Louda et al. 2003a), and also likely impacts C. the late-¯owering native species C. ¯odmanii were undulatum in sand prairie (Louda 1999). Thus, in- much lower than on C. undulatum, which ¯owers syn- creased attack of C. undulatum within patches or land- chronously with the time when R. conicus is active. scapes invaded by exotic thistles will likely impact This result suggests that reduced temporal overlap be- populations of this native thistle. To our knowledge, tween plants and insects is likely to decrease the in- these results provide the ®rst empirical evidence that tensity of spillover effects. Herbivore feeding prefer- invasion by an exotic plant can increase the attack of, ences for a given plant species can in some cases reduce and thus potential impact on, a native plant by a shared use of less preferred host species in agricultural sys- exotic herbivore. We conclude that the exotic plant has tems (Atsatt and O'Dowd 1976). Thus, preference of the potential to exert a strong negative, indirect effect biocontrol herbivores for targeted host plants might on related native plant species. also be expected to reduce levels of attack on native The results parallel those of previous studies dem- species. However, we found substantial use of the na- onstrating that shared herbivores can generate negative tive C. undulatum in landscapes invaded by the exotic indirect interactions between native plant species despite a previously documented preference for, and (Parker and Root 1981, Rand 2003). The ®ndings also increased performance on, Carduus nutans over most are consistent with theoretical models, which predict Cirsium spp. (ZwoÈlfer and Harris 1984, Gassmann and that prey species that share a common predator can Louda 2001). Thus, clearly even less preferred host- have indirect negative effects on each other's popula- plant species are at risk from spillover effects. Al- tion dynamics, i.e., experience ``apparent competition'' though spillover is generally considered a minor prob- (Holt 1977). Finally, the data support the suggestion lem in weed biological control (Blossey et al. 2001), by Simberloff and Von Holle (1999) that nonindige- we suggest that the conditions under which it poses a nous species may facilitate one another's invasion, threat need to be evaluated much more extensively. Reports lse,B,R aarne .Twsuy .A ads R. Landis, A. D. Tewksbury, L. Casagrande, guilds. R. defense B., Plant Blossey, 1976. O'Dowd. J. D. and R., P. Atsatt, 1554 aueCnevnysDvdH mt osrainRe- Conservation the Smith of Program. DHS2004-01 H. Fellowship no. search David publication is Conservancy's This (#2001-35320-09882) Nature Louda. grant M. support USDA-NRI S. Additional a from to Rand. by Fellowship A. provided T. Research to was Conservation Conservancy Smith funded Nature H. was The research D. This a property. per- their by us on granted work generously to grateful who mission additionally individuals are numerous We the Dappen support. to Patti and and data Milner, GIS Maribeth provided assis- Mortensen, ®eld invaluable Dave Haishin provided tance. manuscript. Hawkins Shauna the and on Ozawa comments insightful for Russell even as serve may areas hosts. spe- natural secondary native that targeted of evidence within any release cies is the there if considering agents when control of caution ex- use great should substantial managers ercise that in suggests species result native can some ev- spillover the Finally, that herbivores. idence exotic of densities ulation pop- landscape- decreasing bene®t by could species to native densities co-occurring, patch plant related, exotic term, in long reductions the scale over data the that addition, In suggest dynamics. invasion effects of indirect studies under- into incorporating study of The importance plants. the native scores frequency on and attack intensity herbivore on the of feed increase also can that they herbivores natives, insect support plants otic eah . n .Rsn 90 aiiigbooia con- biological Maximizing 1990. Rosen. D. and P., DeBach, ot .D,adM .Hcbr.20.Idrc interactions, Indirect 2001. 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