Crop–noncrop spillover: arable fields affect trophic interactions on wild plants in surrounding habitats

David J. Gladbach 0 1 2 3 Andrea Holzschuh 0 1 2 3 Christoph Scherber 0 1 2 3 Carsten Thies 0 1 2 3 Carsten F. Dormann 0 1 2 3 Teja Tscharntke 0 1 2 3 Herbivory Large-scale 0 1 2 3 0 A. Holzschuh Department of Animal Ecology I, Population Ecology, University of Bayreuth, Universitatsstr. 30 , 95447 Bayreuth, Germany 1 D. J. Gladbach (&) A. Holzschuh C. Scherber C. Thies T. Tscharntke Agroecology, Department of Crop Science, Georg-August University Gottingen , Griesebachstrae 6, 37077 Gottingen, Germany 2 Communicated by Jay Rosenheim 3 C. F. Dormann Department of Computational Landscape Ecology, Helmholtz Centre for Environmental Research , UFZ, Permoserstr.15, 04318 Leipzig, Germany Ecosystem processes in agricultural landscapes are often triggered by resource availability in crop and noncrop habitats. We investigated how oilseed rape (OSR; Brassica napus, Brassicaceae) affects noncrop plants in managed systems and semi-natural habitat, using trophic interactions among wild mustard (Sinapis arvensis, Brassicaceae), rape pollen beetles (Meligethes aeneus, Nitidulidae) and their parasitoids (Tersilochus heterocerus, Ichneumonidae). We exposed wild mustard as phytometer plants in two cropland habitat types (wheat field, field margin) and three noncrop habitat types (fallow, grassland, wood margin) across eight landscapes along a gradient from simple to complex (quantified as % arable land). Both landscape and local factors affected the abundance of rape pollen beetles and parasitoids. Rape pollen beetle infestation and parasitism rates on these plants were lower in noncrop habitats and higher in wheat fields and field margins, whereas beetles and parasitoids responded differently to landscape scale parameters. We found the hypothesized spillover from OSR crop onto wild plants in surrounding habitats only for parasitoids, but not for pollen beetles. Parasitism rates were not related to landscape simplification, but benefited from increasing proportions of OSR. In contrast, rape pollen beetles benefited from simple landscape structures, presumably due to multi-annual population build-ups resulting from long-term OSR planting (as part of the crop rotation). In conclusion, we showed that spillover from cropland affects parasitism rates on related wild plants outside cropland, which has not been shown so far, but can be expected to be a widespread effect shaping noncrop food webs. - Landscape-scale patterns (sensu Turner and Gardner 1991) often affect ecosystem processes locally (Kareiva and Wennergren 1995; Hooper et al. 2005). Spatial configuration and composition of ecosystems and habitat diversity (Turner 1989) have been shown to be interwoven with land-use intensity (e.g., Wrbka et al. 2004), and may influence, as landscape effects, important trophic interactions such as biocontrol and herbivory (Gardiner et al. 2009) or pollination (Ricketts et al. 2008). Hence, both ecosystem services and dis-services (Zhang et al. 2007) in different agro-environments are promoted or constrained to various extents depending on landscape effects. Further, local effects such as habitat type and quality (habitat identity) influence diversity and population size of organisms (Matter and Roland 2002; Haynes et al. 2007; Zaller et al. 2008a). Thus, local interactions are triggered by factors such as resource availability at both the landscape and the local habitat scale. However, most studies focus either on just local effects or the distribution of only one habitat type within a landscape (Meyer et al. 2009). Only a few studies have shown the interaction of landscape and local processes and their effect on patterns of insect diversity or trophic interactions (Cushman and McGarigal 2004; Dauber et al. 2005; Schweiger et al. 2005). As a simultaneous investigation of local and landscape patterns is difficult, an experimental approach introducing the same study system in a wide range of habitats and landscapes is a suitable, but little explored technique. Here, we study the rape pollen beetle Meligethes aeneus (Fabricius 1775), which is one of the most important pest organisms in oilseed rape (OSR; Brassica napus, L.) (Buchi 2002; Alford et al. 2005). Published studies focused on pollen beetles and their parasitoids on OSR and emphasized that landscape context influences trophic interactions in cropland (e.g., Thies and Tscharntke 1999; Ricketts et al. 2008; Buchi 2002; Bianchi et al. 2006; Thies et al. 2008), whereas wild Brassicaceae have been considered only in their potential role as alternative host plants and not as a substitute resource when OSR fields are not longer available. Thus, examples of cropnoncrop spillover are almost absent (Rand et al. 2006). However, spillover may shape trophic interactions and thus we focus on the effect of cropland such as OSR on wild plants in noncrop habitats as well as in crop systems. Although existing theories predict the spillover of insects from crop to noncrop areas (Tscharntke et al. 2005; Rand et al. 2006; Rand and Louda 2006), we are not aware of studies that actually test how the huge and functionally important crop-related populations distribute across different habitats in the landscape shaping food webs, In the present study, we investigated how landscape composition affects cropnoncrop spillover and associated trophic interactions. We quantified flower herbivory by rape pollen beetles and its parasitism by an ichneumonid wasp (Nilsson 2003) in different habitat types across a gradient of landscape complexity. Spillover may vary due to the source capacity as well as the attractiveness of the destination. We hypothesize: (1) that both habitat type and landscape characteristics influence the spillover of pollen beetles (M. aeneus) and and parasitism by Tersilochus heterocerus (Thomson 1889) across the cropnoncrop interface; and (2) that increasing proportions of OSR as source habitat increases populations of specialized parasitoids more than their generalist hosts (following Thies et al. 2008), thereby affecting parasitism rates. The study was conducted after the flowering period of OSR from 1 June to 15 July 2006 in the vicinity of Gottingen, Lower Saxony, Germany (51 320N, 9 560E). The regional landscape pattern varies from intensively managed, simply structured landscapes that undergo a large inter-annual change (arable land up to 90%) to complex, extensively managed landscapes with a high proportion of near-natural, perennial habitats, (i.e., fallow, wood margin; arable land \20%). Eight landscapes, (i.e., landscape sectors) were chosen along this gradient of land-use intensity (Online Resource 1). There was no spatial correlation in the landuse gradient of the landscapes. Within each of the landscapes, we established study plots in five major habitat types (cereal field, field margin, fallow, grassland, wood margin) yielding a total of 40 plots. Field margins were chosen adjacent to cereal fields, wood margins were adjacent to cer (...truncated)