Landscapes, orchards, pesticides–Abundance of beetles (Coleoptera) in apple orchards along pesticide toxicity and landscape complexity gradients
Introduction
Apple is by far the most widely grown fruit crop in the temperate zone and following banana ranks the second in world fruit production (FAOSTAT, 2016). It accounts for 35% of the total European orchard area (1.3 million ha) with 10–14 million t of apple production per year (Eurostat, 2015). Pests cause substantial losses in apple production, which could reach up to 80–90% in some years without adequate pest control (Cross et al., 2015, Sutton et al., 2014). Naturally occurring predators and parasitoids, however, can substantially contribute to the biological control of apple pests and thus bring economic benefits to growers (Cross et al., 2015). Although numerous studies have focused on the effects of landscape composition on pests and natural enemies in annual cropping systems, considerably less attention has been paid to perennial crops such as apple (e.g. Herrmann et al., 2012; Herrmann et al., 2012; Inclán et al., 2015; Maalouly et al., 2013).
Landscape composition plays a key role in determining insect dispersal in agricultural landscapes (Bianchi et al., 2006, Chaplin-Kramer et al., 2011, Thies and Tscharntke, 1999, Veres et al., 2013). Semi-natural habitats provide shelter, reproduction and overwintering sites for agricultural insects, thus serve as sources of cyclic recolonisation of agricultural fields after soil cultivation, pesticide applications or harvest (Holland et al., 2016, Miliczky and Horton, 2005, Wissinger, 1997). Conversely, pests and their natural enemies reaching high abundances in agricultural fields can also disperse in opposite direction into semi-natural habitats (Tscharntke et al., 2012). These patterns of dispersal might show similarities but also considerable differences in perennial and annual systems. Perennial crop systems like apple orchards persist for multiple growing seasons and might offer more stable, abundant and diverse resources for insects dispersing from semi-natural habitats than arable fields. Moreover, the landscape-moderated concentration and dilution hypothesis suggests that spatial and temporal changes in habitat availability in the landscape drives the local arthropod abundances, and hence predicts that arthropods emigrating from arable fields after harvest will also concentrate in orchards (Schellhorn et al., 2015, Tscharntke et al., 2012). Thus, we presume that both natural and anthropogenic habitats can support orchard insect assemblages, with a greater contribution of undisturbed habitats. Furthermore, in general, orchards are exposed to high level of pesticides compared to arable fields (Eurostat, 2007; Roßberg, 2013), and they might be exposed to a wide range of pesticide regimes with organic and intensively managed orchards at the two endpoints (Simon et al., 2011, Dib et al., 2016). In spite of the importance of pesticides in regulating arthropod populations, most landscape-scale studies have not covered their impact or it was taken into account by using cumulative management indices, which incorporate, along with the number of pesticide treatments, the intensity of soil preparation, weed control, grazing, pruning, and harvesting (e.g. Bailey et al., 2010, Grez et al., 2013, but see Monteiro et al., 2013).
Different arthropod species and guilds respond differently to pesticide use and landscape composition. Pesticide applications may have a greater impact on natural enemies than on pests, because natural enemies have a lower level of pesticide resistance and any decline in their prey and hosts may also influence their abundance negatively (Biddinger et al., 2009; Jonsson et al., 2012; Krauss et al., 2011; Lövei et al., 1991; Markó et al., 2009; Whalon et al., 2016). On the other hand, species at higher trophic levels, such as predators and parasitoids, could be more vulnerable to habitat loss, fragmentation and isolation than those at lower levels and are therefore less able to colonise the orchards from semi-natural habitat islands and recover less rapidly after pesticide applications (Bailey et al., 2010, Herrmann et al., 2012, Holt, 1996, Tscharntke et al., 2012). Thus species traits, pesticide applications and landscape composition may interact in shaping the arthropod communities in apple orchards. Increasing pesticide pressure and landscape degradation might shift the insect communities toward pests. Conversely, with decreasing pesticide pressure and increasing amount of semi-natural habitats in the landscape insect assemblages might shift toward natural enemies.
The availability of resources necessary for pests and natural enemies vary spatially and temporally in the landscape. Resource requirements of insects (e.g. for feeding, reproduction and overwintering) and their dispersal ability (e.g. only adults can disperse over long distances) may also change during the season. Thus the temporally overlapping resources can form species-specific resource chains (Schellhorn et al., 2015). Different insect species might disperse along different resource chains, i.e. they might show species- and season-specific responses to landscape composition (Raymond et al., 2015, Schellhorn et al., 2014, Schellhorn et al., 2015). Identification of these habitat use patterns is essential for understanding how different landscape elements influence natural enemies and pests, and for gaining knowledge about how to manage landscapes and agricultural fields to maximise biocontrol services (Schellhorn et al., 2015).
Apple orchards harbour species rich and abundant beetle assemblages with several pest and predatory species (Markó et al., 1995; Sutton et al., 2014). Pests might cause damage to roots, trunk, branches, leaves, buds, flowers and fruits of apple trees, while predatory beetles, mainly coccinellids, are important contributors to the control of spider mites, aphids, psyllids and scale insects (Biddinger et al., 2009, Cross et al., 2015, Sutton et al., 2014). In this study, we tested how different landscape elements (proportion of arable fields, orchards, grasslands, human settlements, forest plantations, and semi-natural forests) and management profiles (pesticide use, weed control) can influence the abundance of coleopteran species in apple orchards throughout the growing season. We hypothesized that (i) pesticide use in apple orchards has higher impact on the abundance of predatory beetles than that of pests, (ii) semi-natural habitats in the landscape faciliate colonisation of apple orchards by predatory beetles better than agricultural fields, and (iii) beetle species show different responses to landscape composition during different periods of the season.
Section snippets
Sampling area
Twelve apple orchards with contrasting landscape context were selected as sampling sites in Szabolcs-Szatmár-Bereg County, Hungary (Supplementary Fig. 1, Table 1). In all orchards, trees were 10-years old and the main cultivar was ‘Relinda’ followed by the cv. ‘Rewena’ in some. Orchard size varied between 3.9 and 6.9 ha (mean ± S.D., 4.8 ± 0.9 ha).
Landscape composition around each orchard was estimated in a 1 km-radius circle based on CORINE land cover maps and aerial photographs using ArcGIS 10.2 (
Results
A total of 8207 individuals of 177 canopy-dwelling beetle species were collected from the studied apple orchards. The number of species varied between 30 and 55 (43 ± 10) per orchard, and the number of individuals varied between 239 and 1646 (684 ± 404). Nine species comprised 86% of the total abundance: Anthonomus pomorum (Linnaeus) (Curculionidae, 112 individuals) and Phyllobius oblongus (Linnaeus) (Curculionidae, 90) as the most abundant apple feeders; Stethorus pusillus (Herbst) (Coccinellidae,
Effects of orchard management
Our study revealed that canopy-dwelling beetle species show a guild-specific response to pesticide regimes in apple orchards. The abundance of apple feeders such as A. pomorum, P. oblongus and ‘other apple feeders’ decreased with the increasing pesticide pressure. By contrast, the abundance of predatory (H. axyridis, S. pusillus, C. septempunctata, P. quatuordecimpunctata), tourist (P. vittula) and fungivorous (C. gibbosa) beetles was unaffected by pesticide use (Fig. 2, Table 2).
Since
Conclusions
Orchards are permanent habitats that are surrounded by a variety of land-use types and exposed to high level of pesticide input. This study suggests that in commercial apple orchards pesticide use drives the abundance of beetle species with low dispersal capacity (pests), while landscape composition is the major driver of the abundance of well-dispersing beetles (mainly predatory coccinellids). For orchard colonisation by well-dispersing beetles, semi-natural habitats such as forests,
Acknowledgements
We are grateful to the growers for their cooperation during this study and to Katinka Nyisztor and Veronika Szilágyi for their assistance in field and laboratory work. We also thank Károly Vig and László Ádám for the identification of Phyllotreta vittula and Cortinicara gibbosa individuals. This study was supported by the Hungarian Scientific Research Fund (OTKA NN 101940) and by the MTA ‘Lendület’ program. A K-H. was a Bolyai and a MTA Postdoc Fellow.
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These authors equally contributed to this paper.