Oikos 118: 1477Á1486, 2009 doi: 10.1111/j.1600-0706.2009.17720.x, # 2009 The Authors. Journal compilation # 2009 Oikos Subject Editor: Daniel Gruner. Accepted 6 April 2009
Insect herbivory in an experimental agroecosystem: the relative importance of habitat area, fragmentation, and the matrix
Kyle J. Haynes and Thomas O. Crist
K. J. Haynes ([email protected]), Dept of Biology, Univ. of Louisiana, PO Box 42451, Lafayette, LA 70504, USA. Á T. O. Crist, Dept of Zoology, Miami Univ., Oxford, OH 45056, USA.
Habitat area, fragmentation, and the surrounding matrix influence levels of herbivory in various ecosystems, but the relative importance of these effects has rarely been assessed. We compared levels of herbivory and densities of dominant arthropod herbivores (the hemipteran insects Agallia constricta, Empoasca fabae, Therioaphis trifolii, Lygus lineolaris and Halticus bractatus) among experimental plots that varied in the area and fragmentation of clover habitat and the composition of the matrix (bare ground or grass) surrounding clover habitat. To assess levels of herbivory, we compared clover biomass within herbivore exclosures to the biomass accessible to herbivores. The area and fragmentation of clover habitat, as well as matrix composition, significantly influenced the collective densities of herbivores, although each species exhibited unique responses to habitat structure. Herbivory was strongest in plots with large (64 m2) as compared to small (16 m2) amounts of clover habitat. The difference in clover biomass between the inside and outside of exclosures increased significantly with increasing density of Empoasca fabae but was unrelated to the densities of the other herbivores, suggesting that Empoasca fabae was an exceptionally important herbivore in this system. This study supports the view that herbivore densities and herbivory generally increase with increasing area of plant monocultures, but emphasizes that levels of herbivory may be driven primarily by one or a few key herbivore species.
There is a large body of literature on the effects of the area Dickman 1998). Fragmentation of a focal habitat type may and fragmentation of a focal habitat type and composition have positive effects on a habitat generalist by increasing the of the surrounding matrix on the distributions and extent to which complementary resources in the matrix abundances of species (Moilanen and Hanski 1998, occur within the organism’s dispersal range (Law and Debinski and Holt 2000, Tscharntke et al. 2002, Cronin Dickman 1998, Fahrig 2003). Finally, whereas habitat 2003). The effects of these factors on levels of herbivory specialists may respond more strongly to the area and have received a smaller, but still considerable, amount of fragmentation of a focal habitat type, habitat generalists attention (Thies et al. 2003, O¨ sterga˚rd and Ehrle´n 2005, may be more sensitive to the composition of the matrix Valladares et al. 2006). However, few studies have evaluated (Brotons et al. 2003, Steffan-Dewenter 2003). For example, the relative importance of habitat area, fragmentation, and Haynes et al. (2007) found that (adult) densities of the matrix composition to levels of herbivory (but see Dieko¨tter polyphagous grasshopper Melanoplus femurrubrum in a et al. 2007). focal habitat type (clover) were more strongly influenced If one or a few herbivore species are responsible for most by the availability of complementary resources in the matrix of the herbivory in a given community, the feeding than by the area and fragmentation of the focal habitat. specialization of these key species may determine the Assessing the relative importance of different attributes manner and strength with which habitat area, fragmenta- of habitat structure and composition to herbivory presents tion and matrix composition affect levels of herbivory. particular challenges. The habitat attributes of interest often Positive, negative, and neutral density responses to habitat covary in natural landscapes, hindering a researcher’s ability area are frequently observed (Connor et al. 2000, Matter to isolate their independent effects. For example, Fahrig’s 2000, Zaviezo et al. 2006), but species with strong (2003) review revealed that most studies examining the preferences for a focal habitat type are more likely to effects of habitat area and fragmentation on population or display positive densityÁarea relationships in the preferred community dynamics confounded the effects of these two habitat type than are habitat-generalist species (Hamba¨ck factors. Furthermore, plant size or quality may covary with et al. 2007). The fragmentation of a focal habitat type is landscape features (e.g. matrix composition; Haynes and generally thought to adversely affect populations but, in Cronin 2004), making it difficult to isolate the effects of fact, positive effects of habitat fragmentation may be more herbivory from the effects of other factors on measures of likely for species that use multiple habitat types (Law and plant growth (e.g. biomass, leaf area). One approach to
1477 evaluating the relative importance of different habitat Experimental plots attributes to herbivory is to combine observational data on herbivore densities and plant growth with experimental We conducted the experiment in the summer of 2006 in a manipulations of both the habitat attributes and herbivore 2-ha field at Miami Univ. Ecology Research Center near densities. Oxford, OH. Two years earlier (in 2004), we created In this study, we examine the relative importance of replicated 14 14 m plots, each containing four patches habitat area, habitat fragmentation, and matrix composition (or subplots) of red clover. The clover subplots varied in fragmentation (continuous or isolated by 2 m), habitat area in determining levels of herbivory. We created a model 2 agroecosystem consisting of replicated plots containing (4 or 16 m ), and matrix type (grass or bare ground) subplots of the forage-crop plant red clover Trifolium according to a fully factorial design (Fig. 1). Each combination of fragmentation, area, and matrix was pratense. We manipulated the area and fragmentation of originally replicated in four separate plots, and arranged clover habitat and composition of the matrix (grass or bare- in a completely randomized design. However, we excluded ground) according to a factorial design. Unlike many two plots from the experiment due to clover mortality in previous experimental studies (Fahrig 2003), our design the spring of 2006, leaving two treatment combinations manipulated habitat area independently of habitat frag- (large clover area/bare-ground matrix/fragmented and small mentation. In the experimental plots, we recorded the clover area/grass matrix/continuous) with three replicate densities of the five numerically dominant herbivores: plots. We established the clover subplots and grass matrix Agallia constricta, Empoasca fabae, Therioaphis trifolii, Lygus by sowing the plots with seeds of red clover Trifolium lineolaris and Halticus bractatus. To quantify levels of pratense and orchard grass Dactylis glomerata. We main- herbivory, we placed small herbivore exclosures in the tained bare-ground matrix within experimental plots and in experimental plots. We also examined the impacts of each the 8-m strips between plots by applying herbicide at herbivore species on clover biomass based on regressions of monthly intervals. We kept the grass matrix free of forbs by paired exclosure-control differences in clover biomass and applying 2,4-D herbicide annually in early summer (June). herbivore abundance. Since clover represents the preferred We mowed the grass monthly to minimize variation in the habitat for all of the dominant herbivore species (Methods), height of vegetation among plots because the structural we expected that densities and herbivory would increase complexity of matrix habitats may influence rates of with the area of clover habitat. We also expected that movement into and out of focal patches (Kareiva 1985, habitat-generalist species would have higher densities in Lawrence and Bach 1989). Finally, we regularly weeded all clover habitat bordered by the grass matrix because it may clover habitat. provide complementary resources. Furthermore, we ex- pected fragmentation to positively affect habitat generalists. Herbivory experiment Effects of habitat fragmentation on specialist herbivores may be positive or negative, because although dispersal To quantify the effects of herbivores on clover biomass, we mortality and densities of habitat-generalist predators may placed small exclosures in one randomly selected subplot increase with fragmentation, parasitoids often are less per plot. Within each selected subplot, we placed the effective in fragmented landscapes (Kruess and Tscharntke exclosure at a stratified random location. An exclosure 1994, Tscharntke and Brandl 2004). consisted of fine-mesh (0.25 mm) polyester ‘no-see-um’ netting sewn to fit over a small (0.25w 0.4l 0.5h m) frame constructed of PVC tubing. We pushed the legs of Methods the frame 5 cm into the soil. We prevented insects from entering the exclosures by anchoring the base of the netting Study system firmly against the ground using iron rods. To kill any insects that may have been inside the exclosures, we sprayed The focal plant in this study was the herbaceous, perennial 0.15 l of an aqueous solution containing organic pyrethrin red clover Trifolium pratense. Red clover is an important forage crop worldwide, both in intensely managed cultiva- tion and extensively managed pastures (Guretzky et al. 2005), and is commonly grown in clover/grass polycultures (Heath et al. 1973). The dominant herbivores of clover at our study site were all Hemiptera. They consisted of the leafhoppers Agallia constricta and Empoasca fabae (Cicadel- lidae), the aphid Therioaphis trifolii (Aphididae), the plant bug Lygus lineolaris (Mirididae), and the fleahopper Halticus bractatus (Mirididae). Therioaphis trifolii is only known to feed on legumes (e.g. alfalfa, clovers; Milne 1998, Nair et al. 2003). The remaining herbivore species are known to feed on a wide variety of herbaceous plants (Osborn 1928, Henry 1983, Young 1986, USDA 2002), but were found in much higher densities on clover than grass in our system Figure 1. Aerial view of the field containing 36 14 14 m (Haynes unpubl.). experimental plots. Photo credits: Beth Dickman.
1478 pesticide through the netting onto the clover inside. Because Following significant results from a MANOVA, we eval- the pesticide was diluted in water (1:500 dilution), we uated the effects of habitat area, fragmentation, and matrix sprayed an equivalent amount of water onto an equivalent composition on the individual herbivore species using area of clover within the same subplot, which was used as a univariate ANOVA (Quinn and Keough 2002). We control. We assigned each control area to a stratified analyzed the July and August data separately because the random location. Experiments testing for potential effects effects of herbivores on clover biomass could potentially shift of the exclosures or pesticide on clover are described in the over time. To protect against inflated type I error due to following section. conducting two non-independent tests (on July and August The exclosures were in place for a 6-week period in 2006 densities), we set the significance level for MANOVA and while insects were at peak abundance (mid July to late multiple regression analyses to a 0.025 (0.05/2). To August). After six weeks, we compared clover biomass minimize heterogeneity of variance and to normalize inside the exclosures to clover biomass at control locations. residuals, the densities of each insect species were square- We clipped the clover biomass at these two locations using a root transformed prior to the analyses. As with the clover rectangular quadrat (0.2 0.35 m) to standardize the area biomass data, we removed linear spatial trends in the sampled. The plant material was dried at 608C for 48 h and densities of three herbivore species (Halticus bractatus in then weighed. July and August, Empoasca fabae in July, and Therioaphis We evaluated effects of herbivore exclusion on clover trifolii in July) prior to fitting the MANOVA and ANOVA biomass using a profile ANOVA (Tabachnick and Fidell models. 2000). This procedure, which is comparable to repeated Insect dispersal or spatially correlated environmental measures ANOVA, allows for the two clover biomass conditions (e.g. soil quality) could potentially have lead to measurements (exclosure and control) taken from each non-independence of the insect density or clover biomass plot to be non-independent. Clover biomass measures taken measurements taken from neighboring plots. We tested for from the same plot could potentially be more similar than spatial autocorrelation of the residuals from the ANOVA measures taken in different plots due to differences in and regression models (Ver Hoef and Cressie 1993) using abiotic conditions (e.g. soil quality). We also used the the nonparametric spatial correlation function (Bjørnstad profile ANOVA to test whether the effect of herbivore and Falck 2001), which revealed that none of the residuals exclusion on clover biomass was dependent on clover exhibited significant spatial autocorrelation at any lag dis- habitat area, habitat fragmentation or matrix composition. tance between plots. In addition, we tested whether clover biomass at control locations was influenced by the plot treatments using a three-way ANOVA. The clover biomass data were square- Exclosure and pesticide effects on clover root transformed prior to these analyses to homogenize variances and improve normality of residuals. We also Based on a previous field study (Cronin 2007) using insect removed a linear spatial trend in the control-location cages similar to ours, we did not expect the exclosures to biomass data that we found by performing a regression affect clover biomass. Nonetheless, we conducted a separate against the x and y spatial positions of the plots (Crist et al. but concurrent experiment to examine exclosure effects on 2006). We did not use detrended data in the profile plant biomass. We built ‘leaky’ exclosures, which allowed ANOVA, however, because this would preclude direct insects to access the clover inside. These ‘leaky’ exclosures comparison of differences in biomass inside and outside were identical to the exclosures used in the herbivory of exclosures within each plot. experiment except that there were two large rectangular We measured the densities of the herbivore species in the holes in the netting on opposite sides of the exclosure. The clover habitat of each experimental plot in mid July and late holes were 10 cm wide and extended from the soil to a August. For each plot, we collected insects from the subplot height of 20 cm. We placed ten ‘leaky exclosures’ in a small containing the herbivore exclosure using a D-vac insect secondary field ( 0.2 ha) of red clover 1 km from the vacuum. Within each of these subplots, we placed the experimental plots. Exclosures and paired control locations 0.08 m2 sampling head of the D-vac over the clover at four were arrayed along a linear transect. Exclosure-control pairs stratified random locations. The suction samples were were spaced 2 m apart. We placed each exclosure 1 m to transferred to plastic bags and placed in a freezer until all the left or right of the transect (at random) and located the insects were dead. We then counted the insects using a paired control on the opposite side (also 1 m from the stereoscopic dissecting microscope. To evaluate the relation- transect). After six weeks, we sampled clover biomass at ships between the densities of individual herbivore species each location using methods described previously. We and the level of herbivore damage to clover, we performed tested whether clover biomass differed between the exclo- multiple regression analysis using the densities of each sures and controls using a paired t-test. Prior to this herbivore species as predictor variables and the difference in analysis, the clover biomass data were ln-transformed. clover biomass between the exclosure and control location We also experimentally tested whether clover sprayed (exclosure biomass Á control biomass) as the response with the aqueous pesticide solution differed from clover variable. In addition, we examined the collective effects of sprayed with water, as a check on the direct effects of the herbivores on clover biomass by performing a linear pyrethrins on clover growth. We established 20 herbivore regression with total herbivore density as the predictor exclosures in the secondary clover field. We sprayed half of variable. We also evaluated the effects of the area and the exclosures with the pesticide solution and other half fragmentation of clover habitat and matrix composition on with an equivalent amount of water. The treatments were the densities of the five herbivore species using MANOVA. assigned to the exclosures at random and clover biomass was
1479 measured after six weeks. We assessed whether clover 20 Bare, continuous biomass differed between exclosures sprayed with pesticide Bare, fragmented Grass, continuous solution or water with ANOVA. Clover biomass was ln- ]) 1 -2 Grass, fragmented transformed prior to this analysis. 16
1, 2 12 Results 1, 2 2 Herbivory experiment 8
We found a significant interactive effect of clover habitat area and matrix composition on clover biomass at control 4 locations (Table 1). In plots with 64 m2 of clover habitat, Sq. root (clover biomass [g m biomass was relatively constant across the combinations of 0 fragmentation and matrix composition (Fig. 2). On the Large Small other hand, clover biomass in plots with 16 m2 of habitat Habitat area was substantially higher in plots with bare-ground matrix Figure 2. Effects of habitat area, habitat fragmentation, and than in plots with grass matrix. matrix composition on clover biomass in control locations Clover biomass was significantly higher inside the (means1 SE). Means labeled by different numbers respresent experimental exclosures compared to control locations significant differences at the a 0.05 level (Tukey’s HSD tests with no exclosure (Table 2, Fig. 3). In addition, the effect evaluated differences among all area and matrix combinations). of the exclosures on clover biomass differed according to 2 clover habitat area. In plots with 16 m of clover habitat, In July, the densities of herbivore species were collec- clover biomass did not differ strongly between exclosures 2 tively influenced by all three main effects, clover area, clover and controls. In plots with 64 m of clover habitat, fragmentation, and matrix composition (Appendix 1). however, clover biomass was 1.4 times higher inside the Three of the five herbivore species displayed a trend exclosures. Thus herbivores had strong effects on clover towards higher density in the plots with greater clover biomass in larger patches of clover. Herbivory effects on area (Halticus bractatus, Lygus lineolaris, Empoasca fabae ; clover biomass were unrelated to matrix composition and habitat fragmentation. Fig. 5), though this trend was significant only for Halticus bractatus (Appendix 2). Densities of this species were 3.2 Based on a multiple regression analysis, the differences in 2 biomass between the exclosures and controls (exclosure times greater in plots with 64 compared to 16 m of clover biomass Á control biomass) were not significantly related to habitat. Conversely, Therioaphis trifolii density was 3.5 the July densities of any of the herbivore species (Table 3). times higher in the latter plots. Matrix composition However, there was a positive relationship between the significantly affected the densities of both Therioaphis difference in biomass and the density of Empoasca fabae in trifolii and Agallia constricta (Appendix 2). Therioaphis August (Table 3, Fig. 4). The August densities of all other trifolii densities were 5.8 times higher in clover habitat insect species were unrelated to the difference in biomass embedded within the bare-ground matrix. Agallia constricta between exclosures and controls. For the August data, a exhibited the opposite response; densities were twice as high regression model including all of the herbivore species in clover habitat within the grass matrix. Finally, fragmen- explained 26.6% of the variation in the biomass differential tation did not significantly affect the July densities of any among plots (based on the r2 value). Despite the apparent single herbivore species. In August, herbivore densities were effects of Empoasca fabae on clover biomass, we found not collectively influenced by any of the experimental no relationship between total herbivore density and the factors (Appendix 1). With regard to the effect of clover biomass differential in July (biomass differential habitat area, however, all of the herbivore species individu- 0.5 2 1.121 (density) 64.823, n 30, p 0.585, r ally exhibited the same trends that were observed in July. 0.011) or August (biomass differential 10.102 (den- sity)0.5 Á 43.323, n 30, p 0.287, r2 0.04). Table 2. Results from a profile ANOVA on effects of herbivore exclosure, habitat area, matrix composition, and habitat fragmenta- Table 1. ANOVA results on the effects of habitat area, habitat tion on clover biomass. Significant results at the a 0.05 level are fragmentation and matrix composition on clover biomass in control shown in bold. locations. Significant results at the a 0.05 level are shown in bold. Source DF F p Source DF F p Exclosure 1 7.178 0.014 Area 1 0.054 0.819 Exclosure Area 1 5.256 0.032 Matrix 1 3.026 0.096 Exclosure Matrix 1 1.036 0.320 Fragmentation 1 1.068 0.313 Exclosure Fragmentation 1 0.028 0.868 Area Matrix 1 9.544 0.005 Exclosure Area Matrix 1 1.862 0.186 Area Fragmentation 1 0.094 0.763 Exclosure Area Fragmentation 1 0.512 0.482 Matrix Fragmentation 1 0.090 0.767 Exclosure Matrix Fragmentation 1 0.828 0.373 Area Matrix Fragmentation 1 0.439 0.514 Exclosure Area Matrix Fragmentation 1 0.168 0.686 Error 22 Error 22
1480 210 300
Bare, continuous 200 Bare, fragmented
) Grass, continuous -2 140 100 Grass, fragmented
0
70 -100
-200
0 -300 Biomass differential (residuals) Biomass differential (g m -400 01234567 -2 -70 Square root (no. m ) Large Small Habitat area Figure 4. Relationship between the density of Empoasca fabae and the effect of herbivores on clover biomass. The effect of herbivores Figure 3. Differences in clover biomass between herbivore on clover biomass was measured as the difference in clover biomass exclosures and control locations (biomass inside exclosures Á between herbivore exclosures and control locations (biomass inside control biomass, means1 SE). Results from a profile ANOVA exclosure Á control biomass). To indicate the effect of Empoasca (Table 2) showed that the effect of herbivore exclusion on biomass fabae alone on clover biomass, the residuals from a model was greater in plots with 64 m2 of clover habitat than in plots with including all of the herbivores except Empoasca fabae were 16 m2 of clover habitat. regressed against the density of Empoasca fabae (biomass differ- ential [residuals] 38.26 (Empoasca fabae density)0.5 Á 114.21, n 30, r2 0.219). Exclosure and pesticide effects on clover exclosures and controls to differences in the intensity of Our experimental test for enclosure effects on clover herbivory. Thus, herbivory was much stronger in plots with biomass revealed no difference between controls and the greater clover area. Similar findings of insect herbivory ‘leaky’ exclosures (0.00890.427 g m 2, mean difference 2 increasing with increasing patch area have been reported in of ln(g m ) 995% CI, t9 0.466, p 0.652), which other systems (e.g. understory herbs, forest fragments; allowed insects to move freely in or out of the exclosures. In O¨ sterga˚rd and Ehrle´n 2005, Valladares et al. 2006). Unlike addition, clover biomass did not differ between exclosures 2 clover area, the fragmentation of clover habitat and sprayed with pesticide solution (82.498.4 g m , mean9 composition of the matrix had no effects on herbivory. 1 SE) and exclosures sprayed with water (79.696.1 g m 2; F1,18 0.003, p 0.955). Habitat-structure effects on herbivore densities and herbivory Discussion The strong effect of habitat area on herbivory may be partly Our study shows that herbivore damage to red clover was explained by the collective effects of habitat area on influenced by the area of clover habitat. We found a herbivore densities. Densities of three of the five herbivore substantial difference in clover biomass between exclosures species (Halticus bractatus, Lygus lineolaris and Empoasca and open controls in plots with 64 m2 of clover habitat, but fabae) increased with increasing clover area, whereas two no such difference in biomass in plots with 16 m2 of clover herbivore species (Therioaphis trifolii and Agallia constricta) habitat. Because we found no exclosure effects on clover exhibited negative responses to increasing clover area (these biomass, we attribute differences in clover biomass between responses were statistically significant only for Halticus
Table 3. Results from multiple regression analyses examining the relationships between the densities of each herbivore species in July and August and the clover biomass differential (biomass inside exclosure Á biomass outside exclosure). Densities were square-root transformed. Significant results at the a 0.05 level are shown in bold.
Herbivore species July August
Coefficient t p Coefficient t p
Agallia constricta 3.990 0.400 0.693 5.490 1.153 0.735 Empoasca fabae 2.434 0.303 0.764 39.112 2.634 0.015 Therioaphis trifolii 0.843 0.119 0.906 10.791 1.148 0.260 Lygus lineolaris 10.841 0.507 0.617 8.444 0.468 0.644 Halticus bractatus 14.733 1.124 0.272 5.545 0.679 0.504
July: r2 0.101. August: r2 0.266.
1481 Bare, continuous Bare, fragmented Grass, continuous Grass, fragmented
Agallia constricta 120 Grass > Bare 50 (p < 0.001) 40 80 30 40 20 10 0 0 Empoasca fabae 30 30 20 20 10 10 0 0
Small > Large Therioaphis trifolii ) 50
-2 2500 (p = 0.005) 2000 Bare > Grass 40 1500 (p= 0.002) 30 1000 20 500 10 0 0 Density (no. m Lygus lineolaris 25 10 20 8 15 6 10 4 5 2 0 0 Halticus bractatus 50 100 40 Large > Small 80 30 (p = 0.001) 60 20 40 10 20 0 0 Large Small Large Small Habitat area Habitat area July August
Figure 5. Effects of habitat area, habitat fragmentation, and matrix composition on the densities of Agallia constricta, Empoasca fabae, Therioaphis trifolii, Lygus lineolaris and Halticus bractatus (means1 SE). After finding that the densities of the herbivore species were collectively influenced by the experimental factors in July, but not August (based on MANOVAs), the July data was further analyzed by performing separate ANOVAs for each herbivore species (Quinn and Keough 2002). Significant results at the a 0.05 level are listed in the figure. bractatus and Therioaphis trifolii). Positive densityÁarea are likely for species exhibiting area-dependent immigration relationships in herbivorous insects are traditionally thought and perimeter-dependent emigration (Hamba¨ck and Eng- to result from increased rates of immigration into and (or) lund 2005). An alternative explanation for the negative decreased rates of emigration out of large host-plant patches responses of Therioaphis trifolii and Agallia constricta to in order to maximize feeding efficiency (the resource increasing clover area is that predation pressure on these concentration hypothesis; Root 1973). Given that all of species was higher in plots with large clover subplots. the herbivore species appeared to strongly prefer the clover Reductions in habitat area are often expected to have habitat over the grass matrix (all exhibited much higher stronger adverse effects on predators than on their prey densities in clover; Haynes unpubl.), this hypothesis may (Holt et al. 1999, Tscharntke and Brandl 2004). One major explain the positive responses of Halticus bractatus, Lygus consequence of this effect is that reducing the area of habitat lineolaris and Empoasca fabae to increasing clover area. Even could potentially lead to outbreaks of herbivores and plant among habitat-specialist species, however, negative densityÁ destruction (With et al. 2002). If predation was responsible area relationships, like we report for Therioaphis trifolii and for the negative densityÁarea relationships of Therioaphis Agallia constricta, are not atypical. In a meta-analysis, trifolii and Agallia constricta, this effect was not sufficient to Hamba¨ck and Englund (2005) found that various aphid, have a cascading influence on clover biomass. leafhopper and planthopper species exhibited densityÁarea For herbivores that forage in multiple habitat types, relationships ranging from slightly negative to slightly densities may often be elevated in patches of the focal positive. Negative densityÁarea relationships, they showed, habitat type that border matrix habitat types that provide
1482 supplementary or complementary resources (Dunning et al. subplots were closer to clover-matrix edges, on average, than 1992, Haynes et al. 2007). Consistent with this hypothesis, in large clover subplots (16 m2), the lack of competitors at we found that Agallia constricta, a polyphagous leafhopper the cloverÁbare-ground boundary would likely be more which feeds on both forbs and grasses, exhibited higher beneficial to clover in small clover subplots. A review by densities in clover habitat embedded within grass matrix Haynes and Cronin (2004) found that matrix composition compared to bare-ground matrix. The more-specialized, often influences the quality (e.g. plant size, tissue nitrogen legume-feeding aphid, Therioaphis trifolii, showed the content) of focal patches of vegetation by altering competi- opposite response to matrix composition; densities were tion between plants in the patch and the matrix or by higher in clover within bare-ground matrix. The higher altering nutrient subsidies across the patch edge. densities of aphids in clover habitat embedded within bare- ground matrix may be the result of a reluctance to move over bare ground. The planthopper Prokelisia crocea,a Species-specific impacts of herbivores monophagous herbivore of the grass Spartina pectinata, displays a similar distributional pattern. The planthopper The density of only one herbivore species, Empoasca fabae, reaches higher densities in host-plant patches bordered by was significantly related to the difference in clover biomass mudflats than in patches bordered by non-host grasses between exclosures and controls. The biomass differential because the rate of emigration from patches in mudflats is (exclosure biomass Á control biomass) increased with much lower (Haynes and Cronin 2003, Cronin 2007, increasing density of Empoasca fabae in August, explaining Reeve et al. 2008). Despite the effects of matrix composi- approximately one fifth of the variation in the biomass tion on herbivore densities in our system, matrix composi- differential among plots (Fig. 3). This greater importance of tion did not influence levels of herbivory. The lack of effects Empoasca fabae is likely due to the feeding habits of this of matrix composition on herbivory may be explained by species. Unlike many other hemipterans which are sheath the fact that neither Agallia constricta nor Therioaphis trifolii feeders (stylet tips are sealed into a plant’s vascular cell using appeared to strongly affect clover biomass. a sheath composed of hardened saliva), Empoasca spp. feed Like matrix composition, habitat fragmentation did not by rupturing plant cells with a unique form of stylet affect levels of herbivory. The collective densities of movement, secreting saliva, and then sipping the contents herbivore species were influenced by habitat fragmentation, of damaged cells (reviewed by Backus et al. 2005). but no single species was strongly affected by this factor. Consequently, Empoasca fabae and its congeners are The lack of clear fragmentation effects may be partially especially likely to cause hopperburn, a type of damage that results in tip-wilting, leaf yellowing, and plant stunting explained by the fact that the scale of fragmentation in this (reduced growth). Stunting caused by Empoasca fabae is a study was likely small relative to the dispersal abilities of major cause of reduced yield in legume forage crops in three of the five herbivore species. The leafhoppers Agallia North America (Backus et al. 2005). constricta and Empoasca fabae and the plant bug Lygus Empoasca fabae was likely the most damaging herbivore lineolaris are sufficiently mobile that the fragmentation of in our clover agroecosystem, but spatial variation in levels of clover habitat probably did little to improve access to herbivory can not be understood solely on the basis of the resources in the matrix (Fleischer et al. 1988, Hoffman and spatial distribution of this species. Although our experiment Hogg 1992, B. Schroeder pers. comm.). For Halticus revealed that the effects of herbivores on clover biomass bractatus, however, it is conceivable that fragmentation were much stronger in plots with more clover area, densities increased the ability to forage both in clover and the matrix of Empoasca fabae were only slightly higher in these plots. since a large percentage of adult females are wingless (Day One possible explanation for the disproportionately high 1991). Similarly, most Theroaphis trifolii adults were reduction in clover biomass in plots with large clover wingless in July and August (92% and 100% of captured subplots is that increased clover habitat area had positive adults). Thus, rates of movement of this habitat-specialist effects on the densities of three of the five dominant herbivore among clover subplots were likely substantially herbivores (Empoasca fabae, Lygus lineolaris and Halticus reduced by the fragmentation of clover habitat. bractatus) in both July and August. Densities of Halticus bractatus, for example, were 1.9 and 3.2 times higher in large than in small clover subplots in July and August, Competition between clover and matrix vegetation respectively. Furthermore, although the multivariate re- sponse of all five herbivore species in August to habitat area Our results also showed that clover biomass was influenced was not significant, the consistently positive effects of clover by an interactive effect of clover habitat area and composi- habitat area on the densities of Empoasca fabae, Lygus tion of the matrix. Clover biomass was highest in plots with lineolaris and Halticus bractatus likely explains the impor- less clover area and bare-ground matrix. Given that we tance of habitat area in influencing levels of herbivory. did not see interactive effects of area and matrix on herbivore densities, this effect was probably not a result of herbivory. It is more likely that the observed differences in Conclusions clover biomass resulted because of competition between clover plants and grass in the matrix, particularly along Our findings support the view that the area of a focal clover-matrix edges. In plots with bare-ground matrix, habitat (e.g. crop) is an important factor influencing clover plants near the edges of subplots may have exhibited herbivore densities and herbivore damage (Root 1973) increased growth due to reduced competition for water or as well as the concept that the practice of planting in large nutrients. Because clover plants in small (4 m2) clover monocultures may ensure continued high losses of crop
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1485 1486 Appendix 1
Results from MANOVAs on the effects of habitat area, matrix composition, and habitat fragmentation on the collective densities of the five herbivore species. Densities were square-root transformed. Significant results at the a 0.025 level are shown in boldface.
Source July August
Wilk’s l DF F p Wilk’s l DF F p
Area 0.351 5, 18 6.657 0.001 0.539 5, 18 3.084 0.035 Matrix 0.318 5, 18 7.724 B0.001 0.696 5, 18 1.571 0.218 Fragmentation 0.500 5, 18 3.593 0.020 0.649 5, 18 1.946 0.136 Area Matrix 0.787 5, 18 0.974 0.460 0.693 5, 18 1.598 0.211 Area Fragmentation 0.799 5, 18 0.903 0.501 0.874 5, 18 0.519 0.759 Matrix Fragmentation 0.815 5, 18 0.818 0.553 0.744 5, 18 1.238 0.332 Area Matrix Fragmentation 0.642 5, 18 2.004 0.127 0.801 5, 18 0.896 0.505
Appendix 2
Results from univariate ANOVAs examining effects of habitat area (A), matrix composition (M), and habitat fragmentation (F) on the densities of each herbivore species in July. Densities were square-root transformed. Significant results at the a 0.025 level are shown in boldface.
Source DF Agallia constricta Empoasca fabae Therioaphis trifolii Lygus lineolaris Halticus bractatus
FpFpF pFpF p
A 1, 22 0.424 0.522 0.362 0.643 9.486 0.005 2.736 0.112 13.143 0.001 M 1, 22 24.393 B0.001 0.864 0.363 12.941 0.002 0.035 0.854 0.021 0.886 F 1, 22 3.457 0.076 0.274 0.606 0.847 0.367 2.490 0.129 0.224 0.641 A M 1, 22 0.057 0.813 1.391 0.251 2.651 0.118 0.377 0.546 0.734 0.401 A F 1, 22 2.232 0.149 3.171 0.089 0.435 0.516 0.914 0.350 0.615 0.441 M F 1, 22 2.145 0.157 1.504 0.233 0.026 0.873 0.824 0.374 0.045 0.835 A M F 1, 22 0.015 0.903 0.010 0.922 0.642 0.432 4.287 0.050 3.726 0.067