NOTICE: This is the author s version of a work that was accepted for publication in the Journal of Applied Ecology. Changes resulting from the
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1 NOTICE: This is the author s version of a work that was accepted for publication in the Journal of Applied Ecology. Changes resulting from the publishing process, such as peer review, editing, corrections or structural formatting may not be reflected in this document. Changes may have been made to this work since it was submitted for publication. A definitive version was subsequently published in the JOURNAL OF APPLIED ECOLOGY, VOL 49, ISSUE 3 (JUNE 2012). DOI: /j x 1
2 Land-use intensity drives the landscape effect on host-parasitoid interactions in agroecosystems Mattias Jonsson 1,2*, Hannah L. Buckley 3, Bradley S. Case 3, Roddy J. Hale 3, Steve D. Wratten 1 and Raphael K. Didham 4,5,6 1 Bio-Protection Research Centre, PO Box 84, Lincoln University, Lincoln 7647, New Zealand 2 Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7044, SE Uppsala, Sweden 3 Department of Ecology, PO Box 84, Lincoln University, Lincoln 7647, New Zealand 4 School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand 5 School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Australia 6 CSIRO Entomology, Centre for Environment and Life Sciences, Underwood Ave, Floreat WA 6014, Australia mattias.jonsson@ekol.slu.se; hannah.buckley@lincoln.ac.nz; bradley.case@lincoln.ac.nz; roddy.hale@lincoln.ac.nz; steve.wratten@lincoln.ac.nz; raphael.didham@uwa.edu.au * Correspondence: Mattias Jonsson, Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7044, SE Uppsala, Sweden, mattias.jonsson@ekol.slu.se, phone: , fax:
3 Habitat loss and intensification of agriculture are major drivers of global biodiversity loss 1, with important effects on species interactions 2,3 and ecosystem services such as biological control 4,5. Low parasitism rates of agricultural pests in simplified landscapes have been attributed to a lack of habitats that provide important resources for parasitoids 5,6,7. However, this could be confounded by the nearly ubiquitous correlation between decreasing diversity of landscape features and increasing intensification of agricultural land use. To tease apart the mechanisms driving landscape effects on hostparasitoid interactions we took advantage of a landscape modification gradient in New Zealand, in which landscape diversity and land-use intensity were uncorrelated. We found that rates of both primary parasitism and hyperparasitism of two important crop pests decreased with increasing land-use intensity, but were unaffected by landscape diversity. Using structural equation modeling, we identified the frequency of disturbances (insecticide application and to a lesser extent habitat disturbance) as the most important variables mediating the effect of land-use intensity on parasitism rates, whereas resource availability for parasitoids (floral resources and alternative host plants) had little effect. These results suggest that agri-environment schemes that limit the intensification of agricultural land use 8,9 will be important for the maintenance of ecosystem services in agroecosystems. Agricultural expansion modifies the environment in several ways, including destruction and fragmentation of natural habitats, reduction in habitat diversity, and increases in habitat disturbance and agrochemical application 1,10. These factors all interact to reduce species diversity and ecosystem services in agroecosystems 11,12,13. It has been shown repeatedly, for example, that parasitism of crop pests is higher in complex landscapes with high landscape diversity and a high proportion of non-crop cover, than in simplified landscapes dominated by 3
4 agriculture 4,14,15. In many agricultural landscapes these variables are strongly correlated, making it difficult to tease apart the mechanisms driving the observed relationships between landscape structure and ecosystem processes. The commonly-accepted mechanism underlying this pattern is that complex landscapes provide parasitoids with key resources, such as adult food (floral resources) and overwintering sites in proximity to the crop fields 5,6,7. While there is explicit, small-scale evidence that parasitoids use resources in non-crop habitats and then spill over into adjacent crops to parasitise pests 16,17, the hypothesis that resource availability is the key driver of landscape effects on parasitism rates remains largely untested. An alternative explanation for lower parasitism rates in landscapes dominated by agriculture is that parasitism is negatively influenced by disturbance processes, such as ploughing, harvesting and insecticide application 18,19,20, driven by increasing land-use intensification. To discriminate between the relative effects of landscape diversity and land-use intensity on host-parasitoid interactions in agroecosystems, we quantified herbivore densities and parasitism and hyperparasitism rates of two major insect pests, diamondback moth (DBM, Plutella xylostella) and aphids (grey cabbage aphid Brevicoryne brassicae and green peach aphid Myzus persicae) on brassica forage crops across 30 landscapes in New Zealand (Supplementary Fig 1). Unlike previous studies 4,14, we demonstrated using a principal component analysis (PCA) that the two major orthogonal axes of variation in land use pattern were related to independent gradients of landscape diversity (PC1) and land-use intensity (PC2) (Supplementary Table 1). This enabled us to discriminate effectively between the relative influences of landscape diversity and land-use intensity on host-parasitoid interactions. Primary parasitism rates of DBM and aphids, as well as hyperparasitism rates of aphid mummies, all decreased with increasing degree of land-use intensity, but were unaffected by landscape diversity (Figs 1, 2). The negative effect of land-use intensity was 4
5 particularly strong on aphid parasitism by Diaeretiella rapae (R 2 = 0.63, Figs 1, 2c). We used structural equation models (SEM) to test different proximate mechanisms that may explain the observed landscape effects. We hypothesized that effects of landscape diversity on hostparasitoid interactions would be mediated by resource availability (floral resources and alternative crucifer hosts; Supplementary Methods 1), land-use intensity would operate through both altered disturbance regimes (habitat disturbance and insecticide application) as well as altered resource availability (Fig. 2a). In the latter case, we hypothesized that any effects of land-use intensity that were mediated by resource availability would occur indirectly via the effect of land-use intensity on habitat disturbance, and the subsequent effect of habitat disturbance on resource availability. We found that the negative effect of land-use intensity on parasitism rates was mediated predominantly by increased frequency of insecticide application (for DBM and aphid parasitism) and to a lesser extent habitat disturbance (for aphid parasitism only), with a residual (unexplained) direct effect for aphid parasitism and hyperparasitism (Fig. 2b-d, Supplementary Tables 2-4). The only path including resource availability that was retained in any of our models described a positive indirect effect of land-use intensity on aphid parasitism via increased availability of alternative crucifer hosts in landscapes with a greater frequency of habitat disturbance; however this effect was non-significant (Fig. 2c, Supplementary Table 3). Our results suggest that land-use intensity is an important driver of the landscape effect on parasitism rates in agroecosystems, and that this effect is mediated primarily by the intensity of different types of disturbance (insecticide application and habitat disturbance, such as ploughing and harvesting). Furthermore, our study suggests that parasitoids are more sensitive to disturbance than are their herbivore hosts, and in turn hyperparasitoids are more sensitive than are primary parasitoids. This supports the theoretical prediction that higher trophic levels 5
6 should be increasingly sensitive to disturbance 18,21. To date, empirical support for this theory, in general terms, has been relatively weak 22, although it has been shown that primary parasitism rates may decrease with increasing intensity of grazing 20 and parasitoids may be sensitive to broad-spectrum insecticides 19. Our results contradict the common assumption that the negative effects of landscape simplification on parasitism rates are caused primarily by a lack of resources for parasitoids 5,6,7,23. Although empirical evidence supporting this assumption at the landscape-scale is surprisingly scant, a few studies have found parasitism rates to be positively related to the availability of some habitats in the landscape, such as forest edges or grasslands, which are known to provide resources for certain parasitoids 24,25. This disparity in conclusions about the relative importance of land-use intensity versus landscape diversity as drivers of landscape effects might simply result from a lack of effective discrimination of these processes in previous studies, or it might be that their relative importance depends on biological characteristics of the species and landscapes studied. For example, availability of a high diversity of habitat types might be more important when high overall parasitism rates are caused by the combined effects of a high diversity of parasitoids that use complementary resources 6,23. In our study, only a few species of parasitoids contributed to parasitism (Supplementary Methods 2), which may help explain the lack of importance of landscape diversity for parasitism. Alternatively, land-use intensity at the landscape level might be more important when the frequency of pesticide application and other types of disturbance are positively related to non-perennial crop cover. In our study, insecticides were more frequently applied to crops located in landscapes with high annual crop cover, but some other studies have found no such relationship 26,27. Furthermore, exotic parasitoid species may be more strongly associated with crop land than native species and the fact that all species included in 6
7 this study are exotic to New Zealand 28 could also have contributed to the importance of disturbance associated with land-use intensity. The observed effects of land-use intensity on host-parasitoid interactions were not an artefact of density-dependent responses to variation in host density 29. There was no significant relationship between host density and parasitism rate in any of the host-parasitoid systems studied (Fig. 2b-d). At the same time, though, this lack of a relationship provides no evidence that higher parasitism rates in landscapes with low land-use intensity would lead to increased pest suppression 4. Parasitism rates of aphids were probably too low (0 31 %) to have a significant effect on aphid densities, but for DBM parasitism rates were much higher ( %) and this is likely to influence DBM densities in subsequent generations. The only path including herbivore density retained in any of the SEM models was a nonsignificant negative direct effect of landscape diversity on aphid density, although the mechanism driving this relationship is unclear. In this case there was no direct relationship between parasitism rate and aphid density, so the lower aphid density in more diverse landscapes could not be attributed to increased parasitism. Aphid density was also unrelated to host-plant density, of either cultivated brassicas (landscape diversity was not related to cover of brassica fields; Supplementary Table 1) or of alternative crucifer hosts (the effect of landscape diversity was not mediated by cover of alternative crucifer hosts; Fig. 2c). We suggest that the frequency of disturbance associated with land-use intensity has been underestimated as a driver of landscape effects on ecosystem services. While we recognise that the relative importance of land-use intensity versus landscape diversity probably depends on multiple factors, including landscape structure and the identity of the species involved, the 7
8 maintenance of landscape diversity is not the only factor of critical importance for preserving ecosystem services in agroecosystems. Until we better understand the conditions under which different drivers of landscape effects operate, agri-environment schemes that decrease agricultural intensification, will be essential for maintaining ecosystem services. Implementing such schemes at the landscape scale rather than at the field scale, as currently practised 8, will improve their effectiveness. METHODS SUMMARY We conducted the study in kale (Brassica oleracea) crops grown as winter livestock feed in New Zealand. In each of 30 kale fields, aphids, parasitised aphid mummies and DBM pupae were counted within a strip that was not treated with insecticide. Primary parasitism rate of aphids was estimated by dividing the number of mummies found on the plants by the number of live aphids plus mummies. DBM pupae and aphid mummies were collected and taken to the laboratory for rearing and assessment of parasitism (for DBM pupae) and hyperparasitism rates (for DBM pupae and mummies). To quantify the pattern of land use at each site, we took aerial photographs of the landscape surrounding each field and classified the landscape within a 500-m radius of the centre of each sampling area into different land cover classes. To identify the major gradients in landscape composition among sites, we conducted a principal components analysis (PCA) on the proportion of land cover in different cover classes, a measure of landscape diversity, and the average area of annual crop fields. The PCA extracted two orthogonal axes of variation, with PC1 strongly positively correlated with cover of exotic woody vegetation and landscape diversity (we refer to PC1 as a landscape diversity gradient), while PC2 was strongly 8
9 positively correlated with cover of annual crops and the average area of annual crop fields (we refer to PC2 as a land-use intensity gradient). We identified four proximate mechanisms likely to mediate the effects of landscape diversity and land-use intensity on host-parasitoid interactions: (1) floral resources, (2) alternative crucifer hosts, (3) habitat disturbance (e.g., ploughing, harvesting or grazing), and (4) the frequency of insecticide applications. These variables were measured at a local scale within the vicinity of each site. Finally, we used structural equation modelling (SEM) 30, to discriminate the direct and indirect factors affecting host-parasitoid interactions Tilman, D. et al. Forecasting agriculturally driven global environmental change. Science 292, (2001). Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol Lett 11, 1-13 (2008). Tylianakis, J. M., Tscharntke, T. & Lewis, O. T. Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445, (2007). Thies, C. & Tscharntke, T. Landscape structure and biological control in agroecosystems. Science 285, (1999). Bianchi, F. J. J. A., Booij, C. J. H. & Tscharntke, T. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc B Biol Sci 273, (2006). Tscharntke, T. et al. Conservation biological control and enemy diversity on a landscape scale. Biol Control 45, (2008). Landis, D. A., Wratten, S. D. & Gurr, G. M. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45, (2000). Kleijn, D. & Sutherland, W. J. How effective are European agri-environment schemes in conserving and promoting biodiversity? J Appl Ecol 40, (2003). Kleijn, D. et al. Mixed biodiversity benefits of agri-environment schemes in five European countries. Ecol Lett 9, (2006). Robinson, R. A. & Sutherland, W. J. Post-war changes in arable farming and biodiversity in Great Britain. J Appl Ecol 39, (2002). Hendrickx, F. et al. How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44, (2007). Rosenlew, H. & Roslin, T. Habitat fragmentation and the functional efficiency of temperate dung beetles. Oikos 117, (2008). 9
10 Gardiner, M. M. et al. Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecological Applications 19, (2009). Thies, C., Roshewitz, I. & Tscharntke, T. The landscape context of cereal aphidparasitoid interactions. Proc R Soc B Biol Sci 272, (2005). Marino, P. C. & Landis, D. A. Effect of landscape structure on parasitoid diversity and parasitism in agroecosystems. Ecol Appl 6, (1996). Corbett, A. & Rosenheim, J. A. Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape. Ecol Entomol 21, (1996). Lavandero, B., Wratten, S. D., Shishehbor, P. & Worner, S. Enhancing the effectiveness of the parasitoid Diadegma semiclausum (Helen): Movement after use of nectar in the field. Biol Control 34, (2005). Southwood, T. R. E. Tactics, strategies and templets. Oikos 52, 3-18 (1988). Croft, B. A. Arthropod Biological Control Agents and Pesticides. (John Wiley & Sons, 1990). Kruess, A. & Tscharntke, T. Grazing intensity and the diversity of grasshoppers, butterflies, and trap-nesting bees and wasps. Conservation Biology 16, (2002). Pimm, S. L. & Lawton, J. H. Number of trophic levels in ecological communities. Nature 268, (1977). Post, D. M. The long and short of food-chain length. Trends in Ecology and Evolution 17, (2002). Tscharntke, T. et al. Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89, (2008). Bianchi, F. J. J. A., Goedhart, P. W. & Baveco, J. M. Enhanced pest control in cabbage crops near forest in The Netherlands. Landsc Ecol 23, (2008). Bianchi, F. J. J. A. et al. Landscape factors affecting the control of Mamestra brassicae by natural enemies in Brussels sprout. Agric Ecosyst Environ 107, (2005). Roschewitz, I., Thies, C. & Tscharntke, T. Are landscape complexity and farm specialisation related to land-use intensity of annual crop fields? Agric Ecosyst Environ 105, (2005). Herzog, F. et al. Assessing the intensity of temperate European agriculture at the landscape scale. European Journal of Agronomy 24, (2006). Berry, N. A., Cameron, P. J. & Walker, G. P. Integrated Pest Management for Brassicas. (Crop & Food Research, 2000). Costamagna, A. C., Menalled, F. D. & Landis, D. A. Host density influences parasitism of the armyworm Pseudaletia unipunctata in agricultural landscapes. Basic Appl Ecol 5, (2004). Kline, R. B. Principles and practice of structural equation modeling. (Guilford Press, 2005). Supplementary Information is linked to the online version of the paper at 10
11 Acknowledgements We thank the 30 land owners who gave permission to work on their farms, and provided information on insecticide input and confirmed the location of annual crops. A. Dumbleton of PGG Wrightson Ltd provided invaluable information on brassica cropping in Canterbury. I.H. Lynn and J. Barringer, Landcare Research, Lincoln, assisted with vegetation classification based on aerial photographs. S. Blyth, N. Jørgensen, J. Martin, M. Mackintosh, R. Neumegen, S. Orre, S. Sam and N. White assisted with field and laboratory work. Financial support for the study was provided by the Tertiary Education Commission, New Zealand, through the Bio-Protection Research Centre, Lincoln University, New Zealand. F. Bianchi, B. Ekbom, R.M. Ewers, A.-K. Kuusk, O. Lundin, T.A. Rand, J. Stenberg, J.M. Tylianakis and C. Winqvist provided valuable comments on previous versions of this manuscript. Author contributions All authors contributed to the design of the study; M.J. conducted the fieldwork; M.J. and B.S.C. the GIS analysis; M.J., H.L.B. and R.K.D. the statistical analysis; all authors discussed the results; M.J. and R.K.D. did the majority of the writing, but all authors edited the manuscript. Author Information Reprints and permissions information is available at The authors declare no competing financial interests. Correspondence and requests for materials should be addressed to M.J. 11
12 Figure 1 The relationship between parasitism rates and orthogonal components of landscape structure (landscape diversity and land-use intensity). The landscape diversity gradient is represented by PC1 scores and the land-use intensity gradient by the PC2 scores from a principal components analysis (PCA) (Supplementary Table 1). Parasitism of diamondback moth (DBM), and hyperparasitism of aphids are presented as arcsine-square root transformed proportions (in radians) and parasitism of aphids is presented as 4 th -root transformed proportions. Untransformed proportion parasitism of DBM was, on average, 0.68 (range: ), for aphid parasitism 0.07 (range: ) and for hyperparasitism of aphids 0.79 (range: ). The slopes of the fitted lines are the implied covariances around the sample means, derived from the SEM analyses. Figure 2 Structural equation models discriminating the direct and indirect effects of landscape diversity and land-use intensity on host-parasitoid interactions, showing (a) the full model, and the most parsimonious models for (b) parasitism of diamondback moth, (c) parasitism of aphids, and (d) hyperparasitism of aphids. The full model was the same for all three systems except that no link between floral resources and host density was present in the aphid parasitism model, because aphids do not feed on flowers. Arrows represent causal paths from predictor to response variables, and the number on each path in the parsimonious models is the value of the unstandardised partial regression coefficient, indicating whether the relationship is positive or negative. The statistical significance of individual regression coefficients is indicated by the colour of the line (black, P 0.05; dark grey, 0.05 < P 0.10; light grey P > 0.10). The thickness of the line indicates the magnitude of the standardised path coefficients (Supplementary Tables 2-4). For the four endogenous variables, squared multiple correlations (R 2 ) are given to represent the variance explained by all the associated pathways linking that variable. 12
13 Figure (a) 1.6 (b) Parasitism of diamondback moth Parasitism of diamondback moth Landscape diversity (PC1) 0.8 (c) Land-use intensification (invpc2) 0.8 (d) Parasitism of aphids Parasitism of aphids (e) Landscape diversity (PC1) (f) Land-use intensification (invpc2) 1.4 Hyperparasitism of aphids Hyperparasitism of aphids Landscape diversity (PC1) Land-use intensity (PC2) 13
14 Figure 2 (a) Full SEM model (b) Parasitism of diamondback moth 14
15 Figure 2 continued (c) Parasitism of aphids (d) Hyperparasitism of aphids 15
16 METHODS Field sites and patterns of land use. We conducted the study in kale (Brassica oleracea) crops grown as winter feed for cattle and sheep in the Canterbury region of the South Island of New Zealand. In each of 30 kale fields, the landowners allowed a strip of land at least 120 m long by 15 m wide along one side of the field to be left un-treated with insecticide (if any was applied in the surrounding area), and all insect sampling was conducted within this strip (see Supplementary Methods 3 for selection and location of fields). To quantify the pattern of land use at each site, we took aerial photographs of the landscape surrounding each field and classified the landscape within a 500-m radius of the centre of each sampling area into 14 different land cover classes (Supplementary Methods 3). We selected a 500-m scale because parasitoid species have been found to respond strongly to landscape composition at this spatial scale 14,24,31. Orthogonal gradients of landscape diversity and land-use intensity. To identify the major gradients in landscape composition among sites, we conducted a principal components analysis (PCA) in SAM 3.0 (32) on the proportion of land cover in different cover classes (with the 14 cover classes merged into four broader categories of exotic grassland, annual crops, native vegetation, and exotic woody vegetation; Supplementary Table 5), the relative distribution of land cover across all 14 cover classes (using the Q-statistic as a measure of landscape diversity; Supplementary Methods 3), and the average area of annual crop fields. The PCA extracted two orthogonal axes of variation, with PC1 strongly positively correlated with cover of exotic woody vegetation and landscape diversity, and strongly negatively correlated with exotic grassland cover (we refer to PC1 as a landscape diversity gradient), while PC2 was strongly positively correlated with cover of annual crops and the average area of annual crop fields, and moderately negatively correlated with native vegetation cover (we refer to PC2 as a land-use intensity gradient, Supplementary Table 1). Across our study sites, 16
17 landscape diversity and land-use intensity were uncorrelated, and the use of the first two orthogonal axes of variation in the PCA allowed the discrimination of the relative effects of these two variables as drivers of the landscape effect on host-parasitoid interactions. Proximate mechanisms of landscape effects on host-parasitoid interactions. From previous studies 7,17,19,20 and our own empirical observations, we identified four proximate mechanisms likely to mediate the effects of landscape diversity and land-use intensity on host-parasitoid interactions, and measured these at a local scale within the vicinity of each site (Supplementary Table 6). The effect of landscape diversity may operate through resource availability for parasitoids and herbivores, in the form of availability of (1) floral resources and (2) alternative crucifer hosts. The cover of flowering plants and of crucifers (predominantly the weed Shepherds purse, Capsella bursa-pastoris) within a 100-m radius of the centre of each transect were estimated between 19 September and 30 November 2007 by the same observer (MJ). This time of year constitutes a bottleneck in terms of resource and host availability for specialist brassica herbivores in Canterbury, when the winter feed crops have been virtually removed by grazing. The effect of land-use intensity may operate through disturbance in the form of (3) habitat disturbance (e.g., ploughing, harvest or grazing), as well as (4) the frequency of insecticide applications. We constructed an index of the intensity of habitat disturbance based on the proportion of different land cover classes within a 100-m radius of the centre of each transect, weighted by the degree of soil and vegetation disturbance in that land cover type (Supplementary Methods 4; Supplementary Table 7). We quantified the frequency of insecticide applications within the kale field outside the unsprayed sampling strip based on interviews with farmers. Insect sampling. In each field, DBM pupae were sampled once between 19 February and 5 March 2007 and aphids once between 19 March and 2 April 2007, when population densities of the different pest species were highest. Sampling was conducted along a 100 m long 17
18 transect located 8 m from the field edge, in the middle of the unsprayed strip. The number of DBM pupae (excluding empty pupal cases), live aphids and aphid mummies were counted on 25 kale plants randomly selected along each transect, with c. 4 m between sampled plants. Primary parasitism rate of aphids was estimated by dividing the number of mummies found on the plants by the number of live aphids plus mummies. DBM pupae and aphid mummies were collected (max. 5 per plant) along each transect and taken to the laboratory for rearing and assessment of parasitism (for DBM pupae) and hyperparasitism rates (for DBM pupae and mummies). We attempted to collect 100 DBM pupae and 100 mummies at each site, but in some cases a lower number was collected due to low densities and time constraints. At a few sites, the number of emerged DBM pupae, aphids or mummies found was below 10 and these sites were excluded from analyses. In all, 27 sites were analysed for DBM parasitism, 29 for aphid parasitism and 26 for aphid hyperparasitism. See Supplementary Methods 2 for densities and parasitism rates of different taxa. Discriminating the direct and indirect effects of landscape diversity and land-use intensity on host-parasitoid interactions. We used structural equation modelling (SEM) to determine the causal factors affecting host-parasitoid interactions. We hypothesized that indirect effects of landscape diversity would be mediated by resource availability (floral resources and alternative crucifer hosts), whereas land-use intensity would affect hostparasitoid interactions via both altered disturbance regimes (habitat disturbance and insecticide application) and the effect of habitat disturbance on resource availability (Fig. 2a). See Supplementary Methods 5 for more details on SEM analyses. 31 Thies, C., Steffan-Dewenter, I. & Tscharntke, T. Effects of landscape context on herbivory and parasitism at different spatial scales. Oikos 101, (2003). 32 Rangel, T.F.L.V.B., Diniz-Filho, J.A.F. & Bini, L.M. Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Global Ecol. Biogeography 15, (2006). 18
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