An Invasive Plant Promotes Unstable Host–Parasitoid

Ecology, 85(10), 2004, pp. 2772±2782 ᭧ 2004 by the Ecological Society of America

AN INVASIVE PLANT PROMOTES UNSTABLE HOST±PARASITOID PATCH DYNAMICS

JAMES T. C RONIN1 AND KYLE J. HAYNES Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803-1715 USA

Abstract. In theory, the rate of interpatch dispersal signi®cantly in¯uences the population dynamics of predators and their prey, yet there are relatively few ®eld experiments that provide a strong link between these two processes. In tallgrass prairies of North America, the planthopper, Prokelisia crocea, and its specialist parasitoid, Anagrus columbi, exist among discrete host-plant patches (prairie cordgrass, Spartina pectinata). In many areas, the matrix, or habitat between patches, has become dominated by the invasive exotic grass, smooth brome (Bromus inermis). We performed a landscape-level ®eld study in which replicate cordgrass networks (identical in number, size, quality, and distribution of cordgrass patches) were embedded in a matrix composed of either mud¯at (a native matrix habitat) or smooth brome. Mark±recapture experiments with the planthopper and parasitoid revealed that the rate of movement among cordgrass patches for both species was 3±11 times higher in smooth brome than in mud¯at. Within three generations, planthopper and parasitoid densities per patch were on average ϳ50% lower and spatially 50±87% more variable for patches embedded in a brome as compared to a mud¯at matrix. A brome-dominated landscape also promoted extinction rates per patch that were 4±5 times higher than the rates per patch in native mud¯at habitat. The effect was more acute for the parasitoid. We suggest that the differences in population dynamics between networks of patches in brome and those in mud¯at were driven by underlying differences in interpatch dispersal (i.e., patch connectivity). To our knowledge, this is the ®rst experimental study to reveal that matrix composition, in particular, the presence of an invasive plant species, affects the spatial and temporal dynamics of an herbivore and its natural enemy. Key words: Anagrus columbi; Bromus inermis; connectivity; emigration; extinction; host±parasitoid interactions; immigration; matrix; Prokelisia crocea; tallgrass prairie.

INTRODUCTION Taylor 1997, Ims and Yaccoz 1997, Hanski 1999, The most signi®cant threats to population persistence Thomas and Kunin 1999). If there is too little connec- and biodiversity are the loss and fragmentation of hab- tivity among patches, patches should exhibit indepen- itats, and the invasion and spread of exotic species dent ¯uctuations in densities and have a low probability (Wilcox and Murphy 1985, Drake et al. 1989, Saunders of being rescued from extinction or re-colonized fol- et al. 1991, Debinski and Holt 2000). For herbivores lowing an extinction event. Alternatively, if connec- of native plant species, exotic plants may occupy much tivity among patches is too high, patches are likely to of the habitat between their host-plant patches (i.e., the have lower mean densities (if high emigration losses matrix). A growing body of evidence suggests that the cannot be compensated for by immigration or density- composition of the matrix can signi®cantly affect independent reproduction), increased spatial synchrony terpatch movement rates of herbivores (Roland et al. in densities, and a relatively high risk of extinction for 2000, Ricketts 2001, Goodwin and Fahrig 2002, the whole ensemble of patches. Invasive plant species Haynes and Cronin 2003) and their natural enemies may greatly affect connectivity by displacing native (Cronin 2003a), and that these changes in movement vegetation and either altering patch geography (size or rates can theoretically affect population dynamics and isolation) and/or affecting matrix resistance to animal persistence (e.g., Reeve 1988, Comins et al. 1992, Van- movement. Despite the signi®cance of dispersal to the dermeer and Carvajal 2001). A plausible, but undoc- local and regional dynamics of populations, relatively umented, way in which exotic plant species might af- few ®eld studies have provided a strong link between fect native faunas is via their effects on connectivity the two, particularly with regard to predators and their among native habitat patches. prey (but see, e.g., Huffaker 1958, Kareiva 1987, Connectivity is considered critical to the regional Dempster et al. 1995; recently reviewed in Bowne and persistence of populations residing in subdivided hab- Bowers 2004). Furthermore, no experimental studies itat patches (Holyoak and Lawler 1996, Harrison and to date have documented the effects of invasive, non- native plant species on predator±prey dispersal and Manuscript received 11 February 2004; revised 5 April 2004; accepted 14 April 2004. Corresponding Editor: N. Cappuccino. population dynamics within spatially subdivided land- 1 E-mail: [email protected] scapes. 2772 October 2004 HOST±PARASITOID PATCH DYNAMICS 2773

In the North American Great Plains, patchily dis- lished by invading disturbed prairie and through re- tributed prairie cordgrass (Spartina pectinata Link; Po- peated introductions for soil erosion control and animal aceae) hosts an obligate specialist planthopper (Pro- graze (D'Antonio and Vitousek 1992, Larson et al. kelisia crocea Van Duzee; Hemiptera: Delphacidae) 2001, Haynes and Cronin 2003). and its stenophagous egg parasitoid (Anagrus columbi The planthopper, Prokelisia crocea, is the dominant Perkins; Hymenoptera: Mymaridae) (Cronin 2003a, b, herbivore of prairie cordgrass (Holder and Wilson c). These insects exhibit mainland-island metapopu- 1992, Cronin 2003b). In North Dakota, ®rst instar lation dynamics among host-plant patches within a nymphs emerge from their overwintering sites (senes- prairie landscape. Local population extinctions fol- cent leaves from the previous year) in late May, reach lowed by the colonization of cordgrass patches are a peak adult densities in mid June, and then lay eggs common occurrence among the many small patches beneath the adaxial surface of cordgrass leaves. Adults (Ͻ50 m2) but have never been reported for the few from this second generation reach a peak in early Au- large patches (Ͼ3 ha) in a prairie landscape (Cronin gust. One of the most important natural enemies of the 2003a, b, 2004). The matrix habitat within which the planthopper is the egg parasitoid Anagrus columbi cordgrass patches are embedded has a signi®cant im- (Cronin 2003a, c; see Plate 1). Parasitism rates per pact on planthopper and parasitoid interpatch move- cordgrass patch range from 0 to 100%, with an average ment rates, at least at distances of Ͻ5 m (Cronin 2003a, of 21% (Cronin 2003c). In our study area, the para- Haynes and Cronin 2003). Planthoppers and parasitoids sitoid's only host is P. crocea. A. columbi also has two dispersing through a matrix composed of the invasive, generations per year, with adult densities coinciding non-native grass smooth brome (Bromus inermis) with the occurrence of planthopper eggs. (D'Antonio and Vitousek 1992, Larson et al. 2001) colonized cordgrass patches at a rate that was 5±6 times Experimental design higher than the rate for individuals traversing a native The experiment was conducted in a 32-ha ®eld dom- matrix habitat (mud¯at) (Cronin 2003a, Haynes and inated by smooth brome and lacking any native cord- Cronin 2003). In this study, we created replicate cordgrass (Grand Forks County, North Dakota, USA). In grass networks (identical in number, size, quality, and June 2002, replicate cordgrass networks were estab- distribution of cordgrass patches) embedded in a matrix lished in either unmanipulated brome habitat or in ex- composed of either mud¯at (experimentally created) or perimentally created mud¯ats (assigned at random). smooth brome. P. crocea and A. columbi populations Mud¯ats were created by spraying areas of brome with were established within each network and their move- Glyphomax Plus herbicide (Dow AgroSciences LLC, ment among cordgrass patches in each matrix type Indianapolis, Indiana, USA), and then plowing under quanti®ed with mark±recapture experiments. In addi- the dead vegetation. The experimental mud¯ats were tion, we examined how the two matrix types in¯uenced re-treated with herbicides (excluding cordgrass patch- local patch dynamics (density, spatial variability in es) and plowed twice per summer, always at times when density among patches, and extinction rates) of the planthoppers and parasitoids were in sedentary stages planthopper and parasitoid over three generations. We (i.e., eggs or early instar larvae). This procedure was show that by signi®cantly increasing patch connectiv- very effective at maintaining a relatively vegetation- ity, the brome as compared to the mud¯at matrix pro- free matrix habitat (any existing vegetation was con- moted very unstable host and parasitoid patch dynamics. siderably shorter in stature than that found in the brome matrix). Three replicate networks were established in METHODS each matrix type. Replicates were separated by at least 150 m, a distance very rarely traversed by P. crocea Study system or A. columbi (Cronin 2003b, c, Haynes and Cronin Prairie cordgrass is a native species of North Amer- 2003). ican grasslands and in northeast North Dakota exists Each network consisted of 15 cordgrass patches (0.7 as numerous discrete patches ranging in size from 0.1 ϫ 0.9 m) divided into ®ve clusters of three patches m to 4 ha (Hitchcock 1963, Cronin 2003b). The max- (Fig. 1). Patches within a cluster were spaced 5 m apart, imum isolation of a cordgrass patch from its nearest and the midpoint of the central cluster was 30 m from neighbor is only ϳ46 m (Cronin 2003b). The matrix the midpoint of each of the four surrounding clusters. within which these patches are embedded can be clas- At a distance of just a few meters between a source si®ed into three main types: (1) periodically ¯ooded and target patch, the rates of dispersal for P. crocea mud¯ats sometimes dominated by saltwort (Salicornia and A. columbi are Ͻ10% (Cronin 2003b, c, Haynes rubra Nels.); (2) mixtures of predominantly native and Cronin 2003). Moreover, previous small-scale grasses (primarily foxtail barley Hordeum jubatum L., studies (Cronin 2003b, c, Haynes 2004) suggested that western wheatgrass Agropyron smithii Rydb., and little the dispersal rate for both species should decay ap- bluestem Andropogon scoparius Michx.); and (3) proximately exponentially with distance from a source monospeci®c stands of smooth brome (Cronin 2003a, patch. Therefore, the scale of this study was potentially Haynes and Cronin 2003). Brome has become estab- large enough, and interpatch dispersal low enough (see 2774 JAMES T. CRONIN AND KYLE J. HAYNES Ecology, Vol. 85, No. 10

PLATE 1. (Top left) Female Prokelisia crocea and (top right) female Anagrus columbi. (Bottom) Experimental study site consisting of replicate cordgrass networks embedded in either a brome or experimental mud¯at matrix. For scale, mud¯at replicates have a diameter of 100 m. Photo credit: J. T. Cronin.

Hastings 1993, Bowne and Bowers 2004), for asyn- planthoppers and parasitoids were still in their over- chronous local patch dynamics to occur. In this paper, wintering sites, either within the dead vegetation or we focused more generally on the local patch dynamics beneath the soil surface (Cronin 2003b, c). Because of the system, and defered consideration of the regional source plants were purposely obtained from an area (e.g., metapopulation) dynamics to a later paper (J. T. with very low planthopper densities the previous year Cronin, unpublished data). (Ͻ1 per 50 stems, based on sweep net samples), we The cordgrass for this experiment was excavated in expected that the densities of both species initially clumps from a nearby prairie in May 2002 and planted would be low in our experimental networks. Also, be- ¯ush to the ground. A 25-cm aluminum barrier was cause the excavated clumps of cordgrass were distrib- inserted into the ground along the perimeter of each uted randomly among experimental networks, it was patch to limit the outward spread of cordgrass and the very unlikely that any initial bias in insect distributions encroachment of brome. Cordgrass patches of this size occurred between matrix types. Through regular fer- are equal to, or larger than, 22% of the patches found tilization (Osmocote Outdoor and Indoor Slow Release in nearby prairie landscapes (Cronin 2003b) and pos- Plant Food; Scotts, Maryville, Ohio, USA), and wa- sess an average (mean Ϯ 1 SE) of 355 Ϯ 7 cordgrass tering of patches, variation in patch nutritional quality stems. At the time cordgrass patches were created, was minimized between matrix treatments. October 2004 HOST±PARASITOID PATCH DYNAMICS 2775

To determine if the microclimate within patches was dependent on matrix type, we placed a single Hobo Pro data logger (Onset Computer Corporation, Pocasset, Massachusetts, USA) into the center of one cordgrass patch per replicate network (n ϭ 6). The data logger was positioned 25 cm above ground, approximately one half of the mean height of the cordgrass, and recorded temperature and humidity at hourly intervals from 1 to 21 August 2002 (coinciding with peak activity of adult planthoppers in the second generation). From each patch, the daily mean, minimum, and maximum temperature and humidity were determined. We then averaged these values among the three replicates per matrix type for a total of 21 daily temperature and humidity readings (mean, minimum, and maximum). Sep- arate paired t tests were used to determine if patches FIG. 1. Diagram of an experimental cordgrass network. in brome and mud¯at differed with respect to each Each network consisted of 15 cordgrass patches (small boxes; weather-related variable. An additional set of Hobo 0.66 m2 in area), divided into ®ve clusters of three. Patches data loggers were simultaneously deployed within the within a cluster were 5 m apart. The distance from the mid- matrix itself, one in each of the replicate brome and point of the central cluster to the midpoint of the other four clusters was 30 m. Each network was embedded in either a mud¯at networks. Data loggers were placed near the brome matrix (n ϭ 3) or an experimentally created mud¯at center of each network, but at least 5 m from the cord- matrix (ploughed brome; n ϭ 3). Shaded patches represent grass patches. We used a similar procedure to evaluate those in which marked planthoppers were released. Parasit- whether temperature and humidity levels differed in oids were marked in three of the shaded patches (center, northeast, and southwest clusters). each of the two matrix habitats.

Host and parasitoid dispersal patches per replicate network (see Fig. 1) were dusted One month after the transplantation of cordgrass, we with a different color of ¯uorescent powder (using a performed a release of planthoppers into the cordgrass hand-cranked dust blower). The powder was reapplied networks. Five hundred recently eclosed adult plant- as needed to ensure a thin dry coating on the plants hoppers, at a ratio of ϳ12 females to one male (cor- for most of the duration of the study. As parasitoids responding to ambient proportions), were released into emerged from host eggs and walked about the leaves, ®ve patches per network (Fig. 1). This corresponds to they became self-marked (see also Corbett and Rosen- ϳ1.4 planthoppers per stem; an intermediate density heim 1996). Dispersing parasitoids were then captured for naturally occurring patches (Cronin 2003b, Cronin on yellow sticky traps (8 ϫ 13 cm Dayglo Saturn yel- et al. 2004). Planthoppers were marked with ¯uorescent low index cards coated with Tanglefoot; Tanglefoot powder (Dayglo Corporation, Cleveland, Ohio, USA), Company, Grand Rapids, Michigan, USA) attached to using a different color in each patch. The mark is de- the tops of 0.5-m tall polyvinyl chloride (PVC) poles tectable for ϳ2 wk and has no apparent effect on plant- (Cronin 2003a, c). The traps were positioned around hopper survival or dispersal (Cronin 2003b). For 7 d each dusted patch at distances of 0.5 m (n ϭ 2 traps), following the release, all cordgrass patches were in- 1.0m(n ϭ 4), 2.5 m (n ϭ 6), and 5.0 m (n ϭ 8). At spected daily for the presence of marked individuals. each distance, traps were spaced evenly apart. There- While searching for planthoppers in the brome land- fore, it was possible for an emigrant parasitoid to be scapes, observers reduced trampling of vegetation by captured on sticky traps 5 m from its patch of origin, stepping in their footprints and avoiding the creation or at traps positioned around one of the other two dust- of direct pathways between patches. The cumulative ed patches, a distance of 20±50 m away. The traps were number of marked planthoppers detected per patch at deployed for the duration of the parasitoid emergence 5 m, 20±40 m, and 50±60 m from the release patch period (3 wk), after which time the traps were examined was recorded as a proportion of the total numbers of with a dissecting microscope (25ϫ) for A. columbi planthoppers marked (500). Because marked planthop- marked with one of the three colors (usually no more pers were observed in patches other than their patch than a few particles of dust were present, and colors of origin, the proportion of marked individuals that were easily distinguishable). Based on laboratory trials, were sighted represents a true measure of immigration virtually 100% of the parasitoids emerging and dis- success or connectivity between patches at a given dispersing away from ¯uorescent-marked leaves carried tance. the marker (J. T. Cronin, unpublished data). Trap cap- Parasitoid dispersal through brome and mud¯at was tures were divided into distance categories that cor- determined from established populations in the third responded to those for the planthopper. The cumulative generation (2003-II). In August 2003, three cordgrass number captured per trap at each distance was ex- 2776 JAMES T. CRONIN AND KYLE J. HAYNES Ecology, Vol. 85, No. 10 pressed as a proportion of the total numbers of para- independent of host extinctions. Similarly, if hosts sitoids marked (emerging) from within a patch (deter- were absent from the patch, we considered those mined from the patch census at 2003-II; see Methods: patches unavailable for the colonization of parasit- Local patch dynamics). For the parasitoid, trap captures oids. Differences in density (ln-transformed), CV, and are positively correlated with the rate of immigration extinction rate between matrix types were assessed to cordgrass patches at the same distance (Cronin with separate repeated-measures ANOVAs. Genera- 2003c; J. T. Cronin, unpublished data), and thus the tion (n ϭ 3) was the repeated measure and the re- proportion captured on traps is a good surrogate mea- sponses of the planthopper and parasitoid to the matrix sure of patch connectivity. were evaluated separately. For both the planthopper and parasitoid, differences in the proportion of marked insects that were sighted RESULTS or captured (square-root transformed) between matrix Planthopper and parasitoid connectivities among types were evaluated with Pro®le ANOVA (Tabachnick cordgrass patches within experimental networks were and Fidell 2000). Here, pro®le ANOVA is a multivar- signi®cantly higher in a non-native brome than a native iate test (comparable to a repeated-measures ANOVA) mud¯at matrix. On average, the proportions of marked that allows for the trap distances associated with each individuals that were sighted or captured at each dis- dusted patch to be non-independent (traps share a com- tance were 3.4 and 10.9 times higher in brome than in mon source patch and are potentially correlated in A. mud¯at for the planthopper and parasitoid, respectively columbi captures). Matrix type was the main effect and (planthopper, F1,4 ϭ 30.2, P ϭ 0.005; parasitoid, F1,4 trap distance was the non-independent factor (see also ϭ 20.4, P ϭ 0.011; Fig. 2). For each species, there was Cronin 2003a, c). no signi®cant matrix±distance interaction (P Ͼ 0.05), suggesting that the decline in recaptures with distance Local patch dynamics was similar between matrix types. For three generations following the creation of the In addition to affecting connectivity, matrix com- replicate cordgrass networks (three per matrix), we de- position also had a substantial impact on the dynamic termined the incidence and density of each species per properties of planthopper and parasitoid subpopula- cordgrass patch. Each census was initiated after the tions (existing within individual cordgrass patches) planthopper eggs had hatched and parasitoid adults within the cordgrass patch networks. Beginning one emerged, mid July or late August. At these times, plant- generation after the release of insects into the experi- hopper-infested leaves possessed a complete record of mental plots, and for two subsequent generations, patch P. crocea eggs laid and parasitism, but no live insects. densities of the two species were, on average, 50% For each patch, a 10 ϫ 25 cm sampling frame was lower in a brome than a mud¯at matrix (planthopper, randomly placed at six locations (three at the edge and F1,4 ϭ 43.8, P ϭ 0.002; parasitoid, F1,4 ϭ 27.8, P ϭ three in the interior of the patch), and from within each 0.006; Fig. 3A). For both species, variability in den- frame we counted the number of cordgrass stems and sities per patch within the cordgrass network (based on leaves bearing planthopper oviposition scars. A max- the coef®cient of variation [CV]) were initially indis- imum of 10 oviposition-damaged leaves were collected tinguishable between matrix types (2002-II; based on from the patch edge and interior. If no infested leaves separate within-generation t tests, P Ͼ 0.50; Fig. 3B). were found, the remainder of the patch was thoroughly However, by the second and third generations, the CVs searched to ascertain patch occupancy. Leaves were in densities per patch were signi®cantly higher in the dissected to determine the number of unparasitized and brome than in the mud¯at matrix (planthopper, F1,4 ϭ parasitized hosts per leaf (easily determined from the 15.4, P ϭ 0.017; parasitoid, F1,4 ϭ 25.4, P ϭ 0.007; shape of the exit hole in the egg chorions). These leaves Fig. 3B). Parasitoid densities in brome-embedded contained only traces of the occurrence of the two spe- patches were substantially more variable than for any cies (i.e., cast chorions and emergence holes), so their other matrix±species combination, and as a result, the collection did not affect densities per patch (Cronin mean CV for the parasitoid was signi®cantly higher than 2003a, b, c). From these leaves, we determined the den- the mean CV for the planthopper (repeated-measures sity per stem of planthoppers (eggs) and parasitoids ANOVA with matrix and species as main effects; F1,9 (emerged adults). ϭ 25.3, P Ͻ 0.001). Owing most likely to lower and For each species and replicate cordgrass network, more variable densities, patch populations of the plant- we also computed the extinction rate (proportion of hopper and parasitoid were ®ve times and four times patches occupied in generation t that were subse- more prone to extinction, respectively, when embedded quently vacant in generation t ϩ 1), colonization rate in a brome than a mud¯at matrix (planthopper, F1,4 ϭ

(proportion of vacant patches at t that were colonized 8.69, P ϭ 0.042; parasitoid, F1,4 ϭ 48.6, P ϭ 0.002; at t ϩ 1), and the coef®cient of variation in density Fig. 3C). Finally, in mud¯at-embedded patches, plant- among patches (CV). In the calculation of parasitoid hoppers and parasitoids had similar rates of extinction extinction rate, we excluded patches in which the host (F1,4 ϭ 0.8, P ϭ 0.42), but in brome-embedded patches, went extinct; therefore, parasitoid extinctions were the rate of extinction for the parasitoid averaged three October 2004 HOST±PARASITOID PATCH DYNAMICS 2777

conditions. Daily maximum and minimum temperatures and relative humidity were indistinguishable between patches embedded in brome and mud¯at (P Ͼ 0.05 for all tests; Table 1). However, there were small but signi®cant differences in climatic conditions between the two matrix habitats. Experimental mud¯ats were, on average, 0.5ЊC warmer and had nighttime lows that were 1.4ЊC higher, than brome habitats (Table 1). Mud¯ats were also on average 2.2% less humid, and had daily lows that were 3.4% lower than the brome habitats (Table 1).

FIG. 2. Proportion (log scale) of marked planthoppers and parasitoids that were sighted or captured dispersing from their patch of origin. On average, (A) planthoppers and (B) parasitoids had signi®cantly higher rates of dispersal in a brome matrix than a mud¯at matrix (F1,4 ϭ 30.2, P ϭ 0.005 and F1,4 ϭ 20.4, P ϭ 0.011, respectively). Means Ϯ 1 SE per patch (planthoppers) or sticky trap (parasitoids) are reported. Be- yond a distance of 5 m, no marked parasitoids were captured in the mud¯at.

times higher than the rate for its host (25% vs. 8%; F1,4 ϭ 25.2, P ϭ 0.007; Fig. 3C). Through three generations, there were insuf®cient data to evaluate whether planthopper and parasitoid colonization rates were matrix dependent. Most patches had viable planthopper and parasitoid populations in 2002-II, and only for the cordgrass networks in brome were there suf®cient numbers of patch vacancies in 2003-I to quantify colonization rates in the following generation. Based on these limited data, planthopper and parasitoid colonization of patches in brome occurred at a rate of 66.7% Ϯ FIG. 3. (A) Density per patch (log scale), (B) coef®cient 16.7% and 72.2% Ϯ 14.7% (means Ϯ 1 SE) per gen- of variation in density among patches (CV), and (C) the pro- eration, respectively; a statistically indistinguishable portion of patches that went extinct per generation for the planthopper (open symbols) and parasitoid (solid symbols) difference (t ϭ 0.25, df ϭ 4, P ϭ 0.81). in either a mud¯at matrix (squares) or brome matrix (circles). Finally, cordgrass patches within each matrix type Means Ϯ 1 SE are based on three replicate cordgrass networks did not appear to be exposed to different environmental per matrix treatment and three consecutive generations. 2778 JAMES T. CRONIN AND KYLE J. HAYNES Ecology, Vol. 85, No. 10

TABLE 1. Temperature and humidity levels within cordgrass patches embedded in a brome or mud¯at matrix, or within the matrix itself.

Daily temperature (ЊC) Daily humidity (%) Habitat type Mean Minimum Maximum Mean Minimum Maximum Within patch Brome 19.1 Ϯ 0.7 10.9 Ϯ 0.7 27.3 Ϯ 0.9 78.5 Ϯ 1.7 52.7 Ϯ 2.8 98.0 Ϯ 0.5 Mud¯at 19.0 Ϯ 0.7 11.0 Ϯ 0.7 27.0 Ϯ 0.9 79.4 Ϯ 1.8 52.2 Ϯ 2.7 98.8 Ϯ 0.9 t statistic (P) 1.7 (0.11) 0.4 (0.68) 0.8 (0.40) 1.8 (0.09) 0.5 (0.59) 1.7 (0.10) Within matrix Brome 19.1 Ϯ 0.7 11.2 Ϯ 0.7 27.1 Ϯ 0.9 79.5 Ϯ 1.6 53.3 Ϯ 2.7 98.7 Ϯ 0.3 Mud¯at 19.6 Ϯ 0.7 12.6 Ϯ 0.7 27.0 Ϯ 1.0 77.3 Ϯ 2.0 49.9 Ϯ 3.1 98.0 Ϯ 0.6 t statistic (P) 6.2 (Ͻ0.01) 11.4 (Ͻ0.01) 0.5 (0.62) 4.7 (Ͻ0.01) 3.6 (Ͻ0.01) 1.8 (0.08)

Notes: Daily mean, minimum, and maximum values of temperature and humidity, reported as means Ϯ 1 SE among days, were determined for 21 d from three replicate Hobo data loggers per habitat type. Every day, an average for each of the six weather variables was obtained from the three replicates per habitat type. A paired t test was used to determine if the daily mean in brome (patches or matrix) differed signi®cantly from the daily mean in mud¯at (patches or matrix). A separate t test was performed for each of the six weather statistics, and P values are reported in parentheses.

DISCUSSION study, the greater proportion of captures at 1±5 m in At a spatial scale comparable to the maximum iso- the mud¯at relative to the brome matrix was therefore lation distance between cordgrass patches (ϳ46 m; not likely due to a density effect on dispersal. Finally, Cronin 2003b), connectivity among patches for the it seems unlikely that the density of hosts and para- planthopper and parasitoid appears to be 3±11 times sitoids in a source patch would in¯uence the range of higher in the non-native grass, smooth brome, than in dispersal of A. columbi: In the mud¯at, no parasitoids the native matrix, mud¯at. These results correspond were captured beyond a distance of 5 m, but in brome, very closely to ®ndings from our earlier small-scale parasitoids were captured at distances of Ͼ20 m. experiments with this system (Cronin 2003a, Haynes To date, most matrix studies have involved naturally and Cronin 2003, Haynes 2004). Although in this study occurring habitat patches in which the quality of the we did not consider the impact of the native grass ma- patch (e.g., plant height, density, ¯owering rates, tissue trix (predominantly consisting of foxtail barley H. ju- nitrogen) may have been confounded with matrix com- batum, western wheatgrass A. smithii, and little blue- position (Haynes and Cronin 2004). For example, nat- stem A. scoparius) on planthopper and parasitoid ural cordgrass patches in mud¯at are more nitrogen rich movement, our previous studies indicate that connec- than patches in a grass matrix (Haynes and Cronin tivity among patches in a native matrix is intermediate 2003). Because patch quality is known to in¯uence between that of the brome and mud¯at matrix (Haynes emigration (e.g., Cook and Denno 1994, Kuussaari et and Cronin 2003, J. T. Cronin, unpublished data). Our al. 1996, Fownes and Roland 2002) and immigration studies add to the growing body of evidence that matrix (Matter and Roland 2002), differences in patch con- composition signi®cantly affects interpatch movement nectivity among matrix types in many of these studies rates (reviewed in Haynes and Cronin 2004). may have been driven by host patch quality, not matrix For A. columbi, the mark±recapture experiment was composition. In this experiment, and the one by Haynes performed at a time when both host and parasitoid den- and Cronin (2003), we controlled or attempted to min- sities were, on average, higher in mud¯at- than in imize the differences among patches in each matrix; brome-embedded patches (Fig. 3A). Therefore, it is therefore, the matrix per se is the likely factor causing conceivable that the eleven-fold difference in recap- the differences in cordgrass patch connectivity. tures-with-distance between the two matrix types was Higher rates of dispersal through a brome, as com- due to the parasitoid's response to host and/or conspe- pared to a mud¯at matrix can be attributed to the re- ci®c densities in the source patch. However, several sponse of these insects to the matrix±cordgrass edge lines of evidence suggest that density was not a miti- and to their behavior in the matrix. For both species, gating factor in causing the difference in dispersal be- the cordgrass±mud¯at edge poses a strong barrier to tween the mud¯at and brome. First, the ratio of hosts emigration, whereas the cordgrass±brome edge is quite to parasitoids was equally high for patches embedded porous (Cronin 2003a, Haynes and Cronin 2003). Once in the two matrix types: 15.7 Ϯ 0.6 for patches in brome in the matrix, the planthoppers and parasitoids also and 16.6 Ϯ 1.9 for patches in mud¯at (Fig. 2). Second, exhibit very different patterns of movement depending the proportion of A. columbi adults in a source patch on the composition of the matrix; highly directional that colonized a target patch three meters away was pathways in mud¯at and circuitous pathways in brome independent of both host and parasitoid density in the (Cronin 2003a, Haynes and Cronin 2003, Haynes source patch (matrix composition held constant; anal- 2004). The latter movement pattern may increase ysis based on data from Cronin 2003a). In the present patch-®nding abilities and increase immigration rates October 2004 HOST±PARASITOID PATCH DYNAMICS 2779 by these insects when the distribution of patches is spatially 50±87% more variable for patches embedded aggregated (Baum and Grant 2001, Haynes and Cronin in a brome as compared to a mud¯at matrix. A brome- 2003; but see Zollner and Lima 1999); as is the case dominated landscape also promoted subpopulation ex- for cordgrass patches in our system (J. T. Cronin, un- tinction rates that were 4±5 times higher than the rates published data). In fact, both planthoppers and para- in native mud¯at habitat. sitoids have signi®cantly higher probabilities of im- We suggest that the differences in population dy- migrating into patches embedded in brome than in namics between networks of patches in brome and mud¯at (for patches isolated from a source patch by 3 those in mud¯at were driven by underlying differences m; Cronin 2003a, Haynes and Cronin 2003). In both in patch connectivity, not by matrix-speci®c differenc- matrix types, the likelihood of ®nding a new cordgrass es in the quality and/or microclimate of cordgrass patch appears to be very small, even when suitable patches. All patches were derived from the same soil patches are just a few meters away (Cronin 2003a, source and regularly fertilized and watered. Interspe- Haynes and Cronin 2003). Whether the low immigra- ci®c competition with matrix plants was further re- tion rate at the spatial scale of this study is due to high duced by the presence of an aluminum barrier inserted mortality during dispersal, an inef®cient search strat- into the ground around the perimeter of the patch. Tis- egy, or some other mechanism, is presently unknown. sue nitrogen levels, a strong indicator of plant quality The effect of matrix composition on subpopulation to many planthopper species (Cook and Denno 1994), or metapopulation dynamics has been explored theo- were indistinguishable between patches embedded in retically in only a few studies (Gustafson and Gardner brome and mud¯at during the course of this study (J. 1996, Moilanen and Hanski 1998, Cantrell and Cosner T. Cronin, unpublished data). Finally, daily mean, min- 1999, Vandermeer and Carvajal 2001). For example, imum, and maximum temperatures and relative hu- Vandermeer and Carvajal (2001) demonstrated that a midities were similar between cordgrass patches em- high-quality matrix (one that favors a high rate of col- bedded in each matrix type (P Ͼ 0.05 for all tests). onization of empty patches) generally buffers a meta- There were temperature and humidity differences in population against global extinction, but may promote the matrix itself: Mud¯ats averaged 0.5ЊC warmer and chaotic subpopulation dynamics with a higher proba- 2.2% less humid than brome habitats. However, it bility of subpopulation extinction. Under some circum- seems unlikely that these subtle differences between stances, extinction-prone subpopulations can become matrix types could have caused such profound differ- persistent when matrix quality is high. Overall, Van- ences in planthopper and parasitoid population dynam- dermeer and Carvajal's (2001) study suggests that ma- ics in the two landscapes. trix composition can have very complex and signi®cant In a landscape with high connectivity among patches, effects on the dynamics of fragmented populations. dogma suggests that an abundance of immigrants will Empirical evaluations of the population-dynamic ef- not only reduce the variability in density among patch- fects of the matrix are few (but see, e.g., Kareiva 1987, es, but also rescue those patches from extinction Roland and Taylor 1997, Moilanen and Hanski 1998), (Brown and Kodric-Brown 1977, Hanski 1999). The and until this study, limited to the correlation between discrepancy between our results and this theory can matrix composition and patch incidence or density. For best be understood by considering the birth±immigra- example, Moilanen and Hanski (1998) concluded that tion±death±emigration (BIDE) processes operating patch occupancy of the Glanville fritillary was mostly within a patch (Pulliam 1988, Watkinson and Suther- unrelated to the composition of the matrix. On the other land 1995, Holyoak and Lawler 1996, Donahue et al. hand, Cronin (2003a, 2004) and Haynes and Cronin 2003). In the absence of immigration and emigration (2003) found that patch incidences and densities, and (e.g., a caged patch), patch populations of the plant- rates of extinction of P. crocea and A. columbi were hopper and parasitoid are self-sustaining or have pos- signi®cantly matrix dependent (see also Walker et al. itive growth (B Ն D; J. T. Cronin, unpublished data). 2003). These survey data are consistent with the ex- Mud¯at-embedded patches also tend to be self-sus- perimental data presented herein. taining, but are also net exporters of individuals (i.e., To our knowledge, this is the ®rst experimental study source populations in which E Ͼ I; Cronin 2003a, to reveal that matrix composition, in particular, the Haynes and Cronin 2003). Even though I is greater for presence of an invasive plant species, affects the spatial brome- than mud¯at-embedded patches, brome-em- and temporal dynamics of an herbivore (and its natural bedded patches have such high emigration losses that enemy). Manipulation of the matrix composition of E often exceeds B ϩ I Ϫ D, and the patches go extinct. identical networks of cordgrass patches (in terms of Extinctions resulting from the overriding effects of quality, size, number, and dispersion of patches), sig- high emigration are most often associated with small ni®cantly affected not only the connectivity among patches (Kareiva 1987, Andreassen and Ims 2001). As cordgrass patches, but also the spatial and temporal populations in brome-embedded patches decline to- population dynamics of P. crocea and A. columbi. ward lower densities, stochasticity in demographic Within three generations, planthopper and parasitoid (BIDE) processes may increase variability in popula- densities per patch were on average ϳ50% lower and tion densities and further contribute to the risk of patch 2780 JAMES T. CRONIN AND KYLE J. HAYNES Ecology, Vol. 85, No. 10 extinction (Lande 1998). This study exempli®es the has expanded its range within these sites (J. T. Cronin, need for detailed experiments on the movements of unpublished data). Not only has brome displaced whole organisms among habitat patches if we wish to under- cordgrass patches and other native vegetation, but also stand the source-sink or regional dynamics of organ- it has invaded low elevation areas of mud¯at (see also isms (Watkinson and Sutherland 1995, Holyoak and Blankespoor and May 1996). Given the continued Lawler 1996, Andreassen and Ims 2001, Cronin spread of brome, we would anticipate increases in 2003a, b, c, Donahue et al. 2003, Bowne and Bowers planthopper and parasitoid emigration and immigration 2004). rates at the site or regional level. The consequences of Finally, this experimental study suggests that a this appear to be instability at the patch level. We are change in landscape structure, e.g., brought about by currently exploring the consequences of brome inva- the invasion and spread of exotic plant species, may sion and spread at the regional level using simulation have a greater impact on higher rather than lower tro- models (J. D. Reeve, J. T. Cronin, and K. J. Haynes, phic levels. In a mud¯at-dominated landscape, plant- unpublished data). hoppers and parasitoids had comparable rates of sub- The broad implications of this study are four fold. population extinction, but in a brome-dominated land- First, our study reveals a novel and potentially impor- scape, parasitoid extinction rates were three times high- tant mechanism underlying the negative effects that er than for the planthopper. This result is congruent invasive exotic plant species can have on native faunas with the expectation that predators are more prone to (Drake et al. 1989, D'Antonio and Vitousek 1992). By extinction than their prey (Pimm and Lawton 1977, changing the composition of the matrix habitat within Diamond 1984, Pimm 1991, Kruess and Tscharntke a landscape, exotic plants may alter animal movement 1994, Holt 1996, 2002, Davies et al. 2000). In a seven- and therefore the connectivity among existing native generation survey of cordgrass patches, Cronin (2004) habitat patches. Our study adds to the growing body found that A. columbi's extinction rate averaged over of empirical evidence that changes in dispersal patterns all landscapes matrix types was 1.7 times higher than ultimately can affect the population dynamics of pred- the rate for its host. Extinction rate in A. columbi was ators and their prey (see also, e.g., Kareiva 1987, Hol- dependent on factors that spanned three trophic levels yoak and Lawler 1996, van Nouhuys and Hanski 2002). (plant, planthopper, and parasitoid abundance per Until additional studies are performed, we will not patch), whereas planthopper extinction rate was de- know how common such a mechanism is in disrupting pendent only on landscape structure (patch size and the population dynamics of native species. Second, the matrix composition). The dependency on multiple tro- invasion of exotic plant species, and the subsequent phic levels may explain the overall higher extinction change in landscape structure, may be more detrimental rate for the parasitoid than its host (see also Schoener to trophic levels higher up in the food web. Third, a 1989, Holt 1996, 2002, Komonen et al. 2000). There change in matrix composition can signi®cantly affect are also several possible explanations for why the patch connectivity: a common goal in conservation pro- brome matrix had a greater impact on A. columbi than P. crocea extinction rates. First, in brome-embedded grams (Rosenberg et al. 1997, Tewksbury et al. 2002, patches, A. columbi densities were an order of mag- Haddad et al. 2003). It may be possible to employ a nitude lower than the densities of its host, making them matrix that facilitates dispersal (i.e., brome), either particularly vulnerable to extinction (Cronin 2004). alone, or in combination with stepping stones or cor- Second, whereas 98% of the mud¯at-embedded patches ridors to enhance movement among isolated habitat were occupied by planthoppers during the latter two fragments (Rosenberg et al. 1997, Wiens 1997, Baum generations of this study, only 83% of the brome-em- et al. 2004). Finally, as a cautionary note, in striving bedded patches were occupied by this species. A. col- to attain high connectivity among fragmented popu- umbi, therefore, experienced a more fragmented land- lations, local reproduction and immigration may be- scape than its host in brome. Several studies have come overridden by emigration leading to unstable lo- shown that predators and parasitoids are more sensitive cal patch dynamics. For habitat fragments that are to habitat fragmentation than their prey (e.g., Kruess small, as is often the case for populations in need of and Tscharntke 1994, 2000, Komonen et al. 2000, Thies conservation, fragments already may be hard to ®nd et al. 2003; but see Holyoak and Lawler 1996). and easy to lose for the organisms that live among them Since the settlement of Europeans in North America, (e.g., Kareiva 1987, Turchin 1986, Kindvall 1999, An- prairie habitat has declined in area by over 99% (Sam- dreassen and Ims 2001). Promoting higher rates of dis- son and Knopf 1996). Many of the remaining prairie persal among those fragments could tip the balance in fragments in the Great Plains have been invaded by favor of local extinction (B ϩ I Ͻ D ϩ E) if emigration smooth brome (Wilson and Belcher 1989, D'Antonio rates are more strongly impacted than immigration and Vitousek 1992, Larson et al. 2001). At our study rates. In altering the landscape to promote high con- sites in North Dakota, the matrix is composed of ap- nectivity among fragments, conservation biologists proximately 30% mud¯at, 40% native non-host grass- should consider how those changes affect emigration es, and 30% brome. Within the past ®ve years, brome and immigration (see also Bowne and Bowers 2004). October 2004 HOST±PARASITOID PATCH DYNAMICS 2781

ACKNOWLEDGMENTS Dempster, J. P., D. A. Atkinson, and M. C. French. 1995. The spatial population dynamics of insects exploiting a T. Arbour, E. Bless, J. Carlson, A. Caro, D. Cronin, F. patchy food resource. II. Movements between patches. Oec- Dillimuth, K. Legleu, C. Nelson, C. Rhodes, N. Shah, and ologia 10:354±362. A. Widdell assisted with various aspects of this project. J. Diamond, J. M. 1984. `Normal' extinctions of isolated pop- LaDuke granted me permission to work on property owned ulations. Pages 191±246 in M. H. Nitecki, editor. Extinc- by the University of North Dakota. K. Baum, N. Cappuccino, tions. Chicago University Press, Chicago, Illinois, USA. J. Reeve, and two anonymous reviewers provided helpful Donahue, M. J., M. Holyoak, and C. Feng. 2003. Patterns of comments on previous drafts of this manuscript. This work dispersal and dynamics among habitat patches varying in was supported by the Louisiana State University and the Na- quality. American Naturalist 162:302±317. tional Science Foundation grants DEB-0296141 and DEB- Drake, J. A., F. DiCastri, R. H. Groves, F. J. Kruger, H. A. 0211359 and an REU Supplement. Mooney, M. Rejmanek, and M. H. Williamson. 1989. Bi- ological invasions: a global perspective. Wiley, New York, LITERATURE CITED New York, USA. Andreassen, H. P., and R. A. Ims. 2001. Dispersal in patchy Fownes, S., and J. Roland. 2002. Effects of meadow suit- vole populations: role of patch con®guration, density de- ability on female behaviour in the alpine butter¯y Parnas- pendence, and demography. Ecology 82:2911±2926. sius smintheus. Ecological Entomology 27:457±466. Baum, K. A., and W. E. Grant. 2001. Hummingbird foraging Goodwin, B. J., and L. Fahrig. 2002. Effect of landscape behavior in different patch types: simulation of alternate structure on the movement behaviour of a specialized gold- strategies. Ecological Modelling 137:201±209. enrod beetle, Trirhabda borealis. Canadian Journal of Zo- Baum, K. A., K. J. Haynes, F. P. Dillemuth, and J. T. Cronin. ology 80:24±35. 2004. The matrix enhances the effectiveness of corridors Gustafson, E. J., and R. H. Gardner. 1996. The effect of and stepping stones. Ecology 85:2671±2676. landscape heterogeneity on the probability of patch colo- Blankespoor, G. W., and J. K. May. 1996. Alien smooth nization. Ecology 77:94±107. brome (Bromus inermis Leyss) in a tallgrass prairie rem- Haddad, N. M., D. R. Bowne, A. Cunningham, B. J. Dan- nant: seed bank, seedling establishment, and growth dy- ielson, D. J. Levey, S. Sargent, and T. Spira. 2003. Corridor namics. Natural Areas Journal 16:289±294. use by diverse taxa. Ecology 84:609±615. Bowne, D. R, and M. A. Bowers. 2004. Interpatch move- Hanski, I. 1999. Metapopulation ecology. Oxford University ments in spatially structured populations: a literature re- Press, New York, New York, USA. view. Landscape Ecology 19:1±20. Harrison, S., and A. D. Taylor. 1997. Empirical evidence for Brown, J. H., and A. Kodric-Brown. 1977. Turnover rates in metapopulation dynamics. Pages 27±42 in I. Hanski and insular biogeography: effects of immigration on extinction. M. E. Gilpin, editors. Metapopulation biology: ecology, Ecology 58:445±449. genetics, and evolution. Academic Press, San Diego, Cal- Cantrell, R. S., and C. Cosner. 1999. Diffusion models for ifornia, USA. population dynamics incorporating individual behavior at Hastings, A. 1993. Complex interactions between dispersal boundaries: applications to refuge design. Theoretical Pop- and dynamics: lessons from coupled logistic equations. ulation Biology 55:189±207. Ecology 72:896±903. Comins, H. N., M. P. Hassell, and R. M. May. 1992. The Haynes, K. J. 2004. Herbivore movement and spatial pop- spatial dynamics of host±parasitoid systems. Journal of An- ulation dynamics in a heterogeneous landscape. Disserta- imal Ecology 61:735±748. tion. Louisiana State University, Baton Rouge, Louisiana, Cook, A. G., and R. F. Denno. 1994. Planthopper/plant in- USA. teractions: feeding behavior, plant nutrition, plant defense, Haynes, K. J., and J. T. Cronin. 2003. Matrix composition and host±plant specialization. Pages 114±139 in R. F. Den- affects the spatial ecology of a prairie planthopper. Ecology no, and T. J. Perfect, editors. Planthoppers: their ecology 84:2856±2866. and management. Chapman and Hall, New York, New Haynes, K. J., and J. T. Cronin. 2004. Confounding of patch York, USA. quality and matrix effects in herbivore movement studies. Corbett, A., and J. A. Rosenheim. 1996. Quantifying move- Landscape Ecology 19:119±124. ment of a minute parasitoid, Anagrus epos (Hymenoptera: Hitchcock, A. S. 1963. Manual of the grasses of the United Mymaridae), using ¯uorescent dust marking and recapture. States. Dover Publications, New York, New York, USA. Biological Control 6:35±44. Holder, M. W., and S. W. Wilson. 1992. Life history and Cronin, J. T. 2003a. Matrix heterogeneity and planthopper± descriptions of the immature stages of the planthopper Pro- parasitoid interactions in space. Ecology 84:1506±1516. kelisia crocea (Van Duzee) (Homoptera: Delphacidae). Cronin, J. T. 2003b. Movement and spatial population struc- Journal of the New York Entomological Society 100:491± ture of a prairie planthopper. Ecology 84:1179±1188. 497. Cronin, J. T. 2003c. Patch structure, oviposition behavior, Holt, R. D. 1996. Food webs in space: an island biogeo- and the distribution of parasitism risk. Ecological Mono- graphic perspective. Pages 313±323 in G. A. Polis and K. graphs 73:283±300. O. Winemiller, editors. Food webs: integration of patterns Cronin, J. T. 2004. Host±parasitoid extinction and coloni- and dynamics. Chapman and Hall, New York, New York, zation in a fragmented prairie landscape. Oecologia 139: USA. 503±514. Holt, R. D. 2002. Food webs in space: on the interplay of D'Antonio, C. M., and P. M. Vitousek. 1992. Biological in- dynamic instability and spatial processes. Ecological Re- vasions by exotic grasses, the grass/®re cycle, and global search 17:261±273. change. Annual Review of Ecology and Systematics 23: Holyoak, M., and S. P. Lawler. 1996. Persistence of an ex- 63±87. tinction-prone predator±prey interaction through metapop- Davies, K. E., C. R. Margules, and J. E. Lawrence. 2000. ulation dynamics. Ecology 77:1867±1879. Which traits of species predict population declines in ex- Huffaker, C. B. 1958. Experimental studies on predation: perimental forest fragments? Ecology 81:1450±1461. dispersion factors and predator±prey oscillations. Hilgardia Debinski, D. M., and R. D. Holt. 2000. A survey and over- 27:343±383. view of habitat fragmentation experiments. Conservation Ims, R. A., and N. G. Yaccoz. 1997. Studying transfer pro- Biology 14:342±355. cesses in metapopulations: emigration, migration, and col- 2782 JAMES T. CRONIN AND KYLE J. HAYNES Ecology, Vol. 85, No. 10

onization. Pages 247±265 in I. Hanski and M. E. Gilpin, Rosenberg, D. K., B. R. Noon, and E. C. Meslow. 1997. editors. Metapopulation biology: ecology, genetics, and Biological corridors, form, function, and ef®cacy. Bio- evolution. Academic Press, San Diego, California, USA. Science 47:677±687. Kareiva, P. 1987. Habitat fragmentation and the stability of Samson, F., and F. Knopf. 1996. Prairie conservation: pre- predator±prey interactions. Nature 326:388±390. serving North America's most endangered ecosystem. Is- Kindvall, O. 1999. Dispersal in a metapopulation of the bush land Press, Washington, D.C., USA. cricket, Metrioptera bicolor (Orthoptera Tettigoniidae). Saunders, D. A., R. J. Hobbs, and C. R. Margules. 1991. Journal of Animal Ecology 68:172±185. Biological consequences of ecosystem fragmentation. Con- Komonen, A., R. PenttilaÈ, M. Lindgren, and I. Hanski. 2000. servation Biology 5:18±32. Forest fragmentation truncates a food chain based on an Schoener, T. W. 1989. Food webs from the small to the large. old-growth forest bracket fungus. Oikos 90:119±126. Ecology 70:1559±1589. Kruess, A., and T. Tscharntke. 1994. Habitat fragmentation, Tabachnick, B. G., and L. S. Fidell. 2000. Using multivariate species loss, and biological control. Science 264:1581± statistics. Allyn and Bacon, Boston, Massachusetts, USA. 1584. Tewksbury, J. J., D. J. Levey, N. M. Haddad, S. Sargent, J. Kruess, A., and T. Tscharntke. 2000. Species richness and L. Orrock, A. Weldon, B. J. Danielson, J. Brinkerhoff, E. parasitism in a fragmented landscape: experiments and ®eld I. Damschen, and P. Townsend. 2002. Corridors affect studies with insects on Vicia sepium. Oecologia 122:129± plants, animals, and their interactions in fragmented land- 137. scapes. Proceedings of the National Academy of Sciences Kuussaari, M., M. Nieminen, and I. Hanski. 1996. An ex- of the United States of America 99:12923±12926. perimental study of migration in the Glanville fritillary Thies, C., I. Steffan-Dewenter, and T. Tscharntke. 2003. Ef- butter¯y Melitaea cinxia. Journal of Animal Ecology 65: fects of landscape context on herbivore and parasitism at 791±801. different spatial scales. Oikos 18:18±25. Lande, R. 1998. Anthropogenic, ecological and genetic fac- Thomas, C. D., and W. E. Kunin. 1999. The spatial structure tors in extinction and conservation. Researches on Popu- of populations. Journal of Animal Ecology 68:647±657. lation Ecology 40:259±269. Turchin, P. B. 1986. Modelling the effect of host patch size Larson, D. L., P. J. Anderson, and W. Newton. 2001. Alien on Mexican bean beetle emigration. Ecology 67:124±132. plant invasion in mixed-grass prairie: effects of vegetation Vandermeer, J., and R. Carvajal. 2001. Metapopulation dy- type and anthropogenic disturbance. Ecological Applica- namics and the quality of the matrix. American Naturalist tions 11:128±141. 158:211±220. Matter, S. F., and J. Roland. 2002. An experimental exami- van Nouhuys, S., and I. Hanski. 2002. Colonization rates and nation of the effects of habitat quality on the dispersal and distances of a host butter¯y and two speci®c parasitoids in local abundance of the butter¯y Parnassius smintheus. Eco- a fragmented landscape. Journal of Animal Ecology 71: logical Entomology 27:308±316. 639±650. Moilanen, A., and I. Hanski. 1998. Metapopulation dynam- Walker, R. S., A. J. Novaro, and L. C. Branch. 2003. Effects ics: effects of habitat quality and landscape structure. Ecol- of patch attributes, barriers, and distance between patches ogy 79:2503±2515. on the distribution of a rock-dwelling rodent (Lagidium Pimm, S. L. 1991. The balance of nature? Chicago University viscacia). Landscape Ecology 18:187±194. Press, Chicago, Illinois, USA. Watkinson, A. R., and W. J. Sutherland. 1995. Sources, sinks Pimm, S. L., and J. H. Lawton. 1977. Number of trophic and pseudo-sinks. Journal of Animal Ecology 64:126±130. levels in ecological communities. Nature 268:329±331. Wiens, J. A. 1997. Metapopulation dynamics and landscape Pulliam, H. R. 1988. Sources, sinks, and population regu- ecology. Pages 43±62 in I. Hanski and M. E. Gilpin, editors. lation. American Naturalist 132:652±661. Metapopulation biology: ecology, genetics, and evolution. Reeve, J. D. 1988. Environmental variability, migration, and Academic Press, San Diego, California, USA. persistence in host±parasitoid systems. American Naturalist Wilcox, B. A., and D. D. Murphy. 1985. Conservation strat- 132:810±836. egy: the effects of fragmentation on extinction. American Ricketts, T. H. 2001. The matrix matters: effective isolation Naturalist 125:879±887. in fragmented landscapes. American Naturalist 158:87±99. Wilson, S. D., and J. W. Belcher. 1989. Plant and bird com- Roland, J., N. Keyghobadi, and S. Fownes. 2000. Alpine munities of native prairie and introduced Eurasian vege- Parnassius butter¯y dispersal: effects of landscape and tation in Manitoba, Canada. Conservation Biology 3:39± population size. Ecology 81:1642±1653. 44. Roland, J., and P. D. Taylor. 1997. Insect parasitoid species Zollner, P. A., and S. L. Lima. 1999. Search strategies for respond to forest structure at different spatial scales. Nature landscape-level interpatch movements. Ecology 80:1019± 386:710±713. 1030.