Negative effects of pesticides on wild bee communities can be buffered by landscape context

Abstract

Wild bee communities provide underappreciated but critical agricultural pollination services. Given predicted global shortages in pollination services, managing agroecosystems to support thriving wild bee communities is, therefore, central to ensuring sustainable food production. Benefits of natural (including semi-natural) habitat for wild bee abundance and diversity on farms are well documented. By contrast, few studies have examined toxicity of pesticides on wild bees, let alone effects of farm-level pesticide exposure on entire bee communities. Whether beneficial natural areas could mediate effects of harmful pesticides on wild bees is also unknown. Here, we assess the effect of conventional pesticide use on the wild bee community visiting apple (Malus domestica) within a gradient of percentage natural area in the landscape. Wild bee community abundance and species richness decreased linearly with increasing pesticide use in orchards one year after application; however, pesticide effects on wild bees were buffered by increasing proportion of natural habitat in the surrounding landscape. A significant contribution of fungicides to observed pesticide effects suggests deleterious properties of a class of pesticides that was, until recently, considered benign to bees. Our results demonstrate extended benefits of natural areas for wild pollinators and highlight the importance of considering the landscape context when weighing up the costs of pest management on crop pollination services.

Keywords: agroecosystem; apple; native bees; orchards; pest management.

Figure 1.

Bivariate relationships between surrounding natural habitat (2 km scale) and average wild bee (a) abundance and (b) species richness per transect in apple orchards in 2011 (dotted lines; N = 16) and 2012 (solid lines; N = 19). Percentage of natural area had a significant positive effect on wild bee abundance and species richness across years. Data are fitted values derived from final GLMMs, with temperature held constant at 21°C, and span the observed range of natural area for the given years.

Figure 2.

Bivariate relationships between intensity of conventional pesticide use (PUI) in 2011 and wild bee abundance (a) and species richness (e) per transect in orchards in 2011 (dotted lines) and 2012 (solid lines). PUI in 2011 had significant negative effects on wild bee species richness in both years and on abundance in 2012. Relationships between 2011 PUI and 2012 wild bee abundance (b,c,d) and species richness (f,g,h) are further separated by insecticides (dashed lines) and fungicides (solid lines) over three time periods relative to bloom: before (b,f), during (c,g) and after (d,h). Grey lines represent 95% CIs. Data are fitted values derived from final GLMMs with main effects of overall pesticide use, insecticide and fungicide use intensity included for visual representation if removed from final models; temperature and centred percentage of natural area were held constant at 21°C and 0%. Only fungicides and insecticides applied before and after bloom, respectively, showed significant (p < 0.01) negative associations with wild bee abundance and richness.

Figure 3.

Heat maps of interactions between natural habitat surrounding orchards (% natural area at 2 km radius) and intensity of conventional pesticide use (pesticide use index) in 2011 on wild bee abundance (a) and species richness (b) per transect in 2012. As percentage of natural areas surrounding orchards increased, the negative relationship between increasing pesticide use and wild bees weakened. Data are fitted values derived from final GLMMs, with temperature held constant at 21°C. Light yellow indicates highest and deep red indicates lowest wild bee abundance and species richness. Axes represent the ranges of percentage natural habitat and PUI observed in the study.