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Interannual Landscape Changes Influence Plant–Herbivore Available online at www.sciencedirect.com Agriculture, Ecosystems and Environment 125 (2008) 266–268 www.elsevier.com/locate/agee Short communication Interannual landscape changes influence plant–herbivore–parasitoid interactions Carsten Thies a,*, Ingolf Steffan-Dewenter b, Teja Tscharntke a a Department of Agroecology, Georg-August-University, Waldweg 26, 37073 Goettingen, Germany b Department of Animal Ecology I, Population Ecology, University of Bayreuth, 95440 Bayreuth, Germany Received 17 April 2007; received in revised form 6 December 2007; accepted 21 December 2007 Available online 8 February 2008 Abstract The effects of interannual changes in landscape composition on herbivory and biological control of pollen beetles on oilseed rape were experimentally tested. Parasitism by specialized parasitoids decreased following rape crop expansion, and increased following rape crop reduction, indicating interannual dilution and crowding effects. In contrast, herbivory by rape pollen beetles did not respond to these landscape changes due to crop rotation, supporting the concept that specialist natural enemies are more affected by changing environments than their host or prey. When expansion of rape crop area between years exceeded 5% of the landscape, parasitism rates dropped below a threshold value of about 35%, below which classical biological control has rarely been reported. # 2008 Elsevier B.V. All rights reserved. Keywords: Temporal landscape changes; Spatial ecology; Trophic interactions; Biological control 1. Introduction pollen beetle populations by attacking their larvae in rape flowers. In this experimental study, changes in herbivory on Spatial and temporal landscape dynamics are particularly oilseed rape by rape pollen beetles, and their mortality due to important in agricultural landscapes owing to rotations of parasitism were analyzed in 15 crop-dominated landscapes. annual crops and changes of economic incentives by Potted oilseed rape plants were exposed in landscapes that agricultural policy. In Germany, cultivated oilseed rape showed large interannual variation in rape crop area. Local (Brassica napus) contributes to spatial and temporal populations of herbivores and parasitoids were expected to dynamics of agricultural landscape composition, and its decrease with interannually increasing rape crop area and to expansion since the 1970s was accompanied by increased increase with interannually decreasing rape crop area in the outbreaks of rape pest populations. As a consequence of landscape. increased populations of soil pathogens and nematodes during crop growing, oilseed rape is cultivated at intervals of 3–4 years, thereby resulting in a distinct dynamic of rape 2. Methods crop fields in the agricultural landscape. One of the economically most important pests on rape is the rape The experiments were performed in 15 agricultural pollen beetle (Meligethes aeneus, Coleoptera: Nitidulidae). landscapes of northern Germany, which are dominated by Three specialized parasitoids, Tersilochus heterocerus, cereals (71% of crop fields), sugar beets (12%), oilseed rape Phradis interstitialis, and P. morionellus (Hymenoptera: (8%), and maize (4%) with a mean field size of Ichneumonidae), of which the last is rare, may suppress rape 5.3 ha Æ 2.6 S.D. (N = 166 crop fields). 15 study sites located in these 15 landscapes that were characterized by an * Corresponding author. Tel.: +49 551 392359; fax: +49 551 398806. interannual expansion or a reduction of rape crop area were E-mail address: [email protected] (C. Thies). selected. The interannual changes of rape crop in the 0167-8809/$ – see front matter # 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2007.12.011 C. Thies et al. / Agriculture, Ecosystems and Environment 125 (2008) 266–268 267 agricultural landscapes were calculated as the percent the larvae (86 Æ 9 per pot) were stored in polyethylene bags difference of rape crop area cultivated in 2 consecutive years in a freezer at À22 8C. Parasitism rates were measured by (%t+1 À %t = D%). For each study site the surrounding dissection of the last instar larvae of the rape pollen beetle. proportion of rape crop area was measured in circular Plant damage caused by feeding of adult beetles was landscape sectors of 1.5-km diameter, because this land- quantified during the ripening of rape on the remaining pot scape sector could be shown to be the appropriate spatial (five rape plants) in August. The number of pods as well as scale for the studied host–parasitoid interactions (Thies the number of destroyed buds, which did not develop into et al., 2003). The percentages of non-crop area in these pods because of pollen beetle herbivory and typically landscape sectors remained unchanged and were not appeared as podless stalks were assessed. correlated to the interannual changes of rape crop Spatial autocorrelation in herbivory and parasitism was (R = À0.30; P = 0.290; N = 15 landscapes). tested in pre-analyses using Moran’s I statistics to correct for To minimize the inherent problem of landscape similarity in plant–herbivore–parasitoid interactions in comparisons that many variables change simultaneously, relation to geographic distances between sites, but no an experimental approach with potted rape crop plants, spatial autocorrelation was found (total parasitism: which have been shown to be a useful indicator to study I = À0.1564, P = 0.936; T. heterocerus parasitism: herbivory and parasitism of rape pests was used (Thies and I = À0.0957, P = 0.666; Phradis spp. parasitism: Tscharntke, 1999). These potted plants (two 30 l pots per I = À0.1532, P = 0.932; herbivory: I = 0.0009, P = 0.100). landscape, five plants per pot) had the same soil type, The effects of interannual changes of rape crop area nutrient and water availability (standardized garden soil, (%t+1 À %t = D%) on herbivory and parasitism were watered weekly), were planted with the same rape variety evaluated using simple linear regression models. Statistical (Lisonne1, Deutsche Saaten Veredelung, Lippstadt, Ger- analyses were carried out using R 2.4.0 (R Development many), and were installed in the same local environment Core Team, 2006) with normally distributed residuals. (grassy field margin strips adjacent to cereal fields) to avoid Arithmetic means Æ S.D. are given. effects of the immediate vicinity. The potted plants were exposed for one season from April to August in the center of each of the 15 landscape sectors. 3. Results Parasitism rates were analyzed during the flowering period of rape in June. All flowers of one pot (five rape The percentage of oilseed rape buds destroyed from plants) were collected. The flowers (1136 Æ 43 per pot) and feeding by adult M. aeneus was 37.1 Æ 7.4% (N =15 Fig. 1. Dependence of plant–herbivore–parasitoid interactions on the interannual changes of the percentage of rape crop area (D%) owing to crop rotation. (A) Total parasitism: Y = 45.3 À 1.7X, F = 5.07, P = 0.042, N = 15, R = À0.530; (B) Phradis spp. parasitism: Y = 23.3 À 2.4X, F = 8.61, P = 0.012, N = 15, R = À0.631; (C) Tersilochus heterocerus parasitism: Y = 39.9 À 1.1X, F = 2.93, P = 0.111, N = 15, R = À0.249; (D) Herbivory: Y = 41.4 À 0.4X, F = 2.01, P = 0.179, N = 15, R = À0.366. Arcsine square-root transformed percentage values. 268 C. Thies et al. / Agriculture, Ecosystems and Environment 125 (2008) 266–268 landscapes). Only 713.9 Æ 131.3 buds/plant developed into spatial scale. Due to crop rotation, the distance between rape pods, whereas 421.7 Æ 105.4 buds/plant were destroyed. fields in two subsequent years may be too large to be easily Total mortality of the herbivores resulting from parasitism bridged by parasitoids. However, such an increased was 44.7 Æ 19.7% (N = 15 landscapes). T. heterocerus susceptibility of natural enemies to changing composition contributed 36.1 Æ 15.5%, and Phradis spp. 18.3 Æ of crops can be hypothesized to occur mainly in weakly 14.9%. Herbivory and parasitism were not correlated with dispersing and specialized parasitoids such as T. heterocerus the current or previous year’s percentage of rape crop area and Phradis spp. (herbivory: P > 0.15; total parasitism: P > 0.20; T. hetero- Such dispersal processes at the landscape scale have not cerus parasitism: P > 0.15; Phradis spp. parasitism: been explicitly quantified so far, but appear to be essential to P > 0.15), and parasitism was not related to larval host understanding functional connectivity among habitats (Polis density (all P > 0.5). et al., 1997; Holt et al., 1999; Cronin and Reeves, 2005; Rand Total parasitism and partial parasitism by Phradis spp. et al., 2006). Similar crowding or dilution effects of specialist decreased as rape crop area (D%) increased from the first to (but not generalist) natural enemies may be expected in the second study year, and increased as rape crop area (D%) situations of habitat destruction or restoration in a more decreased, thereby indicating dilution and crowding, natural landscape context, e.g. when habitat destruction leads respectively, of the higher trophic level populations to a transient ‘‘spike’’ in predator abundance in remnant (Fig. 1A–C). For example, maximum expansion of rape habitat patches (Holt and Hochberg, 2001). crop area was 7.2% and maximum reduction of rape crop area was 8.2% of the landscape from year-to-year. In contrast, herbivory was not significantly affected by Acknowledgements interannually changing rape crop area (D%; Fig. 1D). J. Bengtsson, T.O. Crist, C.F. Dormann, D. Gabriel, B.A. Hawkins, R.D. Holt, W. van der Putten, T. Tammaru, J.M. 4. Discussion Tylianakis, K. Wiegand, and two anonymous referees are kindly acknowledged for insightful comments and/or When expansion of rape crop area between years discussions. Financial support came from the German exceeded 5% of the landscape, percent parasitism dropped Research Foundation (Deutsche Forschungsgemeinschaft) below a threshold value of about 35%, below which and the German Federal Ministry of Education and Research success in classical biological control has never been (Deutsches Bundesministerium fu¨r Bildung und Forschung; reported (Hawkins and Cornell, 1994).
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