Crop pollination from native bees at risk from agricultural intensification

Abstract

Ecosystem services are critical to human survival; in selected cases, maintaining these services provides a powerful argument for conserving biodiversity. Yet, the ecological and economic underpinnings of most services are poorly understood, impeding their conservation and management. For centuries, farmers have imported colonies of European honey bees (Apis mellifera) to fields and orchards for pollination services. These colonies are becoming increasingly scarce, however, because of diseases, pesticides, and other impacts. Native bee communities also provide pollination services, but the amount they provide and how this varies with land management practices are unknown. Here, we document the individual species and aggregate community contributions of native bees to crop pollination, on farms that varied both in their proximity to natural habitat and management type (organic versus conventional). On organic farms near natural habitat, we found that native bee communities could provide full pollination services even for a crop with heavy pollination requirements (e.g., watermelon, Citrullus lanatus), without the intervention of managed honey bees. All other farms, however, experienced greatly reduced diversity and abundance of native bees, resulting in insufficient pollination services from native bees alone. We found that diversity was essential for sustaining the service, because of year-to-year variation in community composition. Continued degradation of the agro-natural landscape will destroy this "free" service, but conservation and restoration of bee habitat are potentially viable economic alternatives for reducing dependence on managed honey bees.

Fig 1.

(a) Total estimated pollen deposition by native bees ± SE in 2001 on ON, OF, and CF farms. The gray line indicates pollen deposition for production of marketable fruit. (b) Native bee diversity (circles) and abundance (triangles) ± SE in 2001.

Fig 2.

(a) Cumulative estimated mean pollen deposition per flower for ON (open circles), OF (filled circles), and CF (filled inverted triangles) in 2001 based on individual means in d. The gray line indicates pollen deposition threshold. 1, H. tripartitus; 2, Bombus californicus; 3, Peponapis pruinosa; 4, Bombus vosnesenskii; 5, Melissodes lupina, robustior, stearnsi, or tepida timberlakei; 6, H. farinosus; 7, Lasioglossum (Evylaeus) spp. (n = 4); 8, L. (Dialictus) spp. (n = 4); 9, H. ligatus; 10, L. mellipes or titusi; 11, Hylaeus rudebeckiae, stevensi, or conspicuus; 12, Agapostemon texanus. (b) Mean visits per flower day ± SE for each bee species (order and symbols as above) at each farm type. (c) Median pollen deposition per visit with quartiles for females (open squares) and males (filled squares) of each bee species. (d) Estimated mean pollen deposition per flower day ± SE by each bee species on each farm type.

Fig 3.

(a) Abundance of each bee species at watermelon during 2000 (black bars) and 2001 (gray bars). Stars indicate significant differences from expectation (Freeman–Tukey deviates). Species are in rank order of contribution to pollination service in 2001 (see Fig. 2 legend); because selected groups were lumped in 2000, s (small striped) includes 1, 9, and 10, and t (tiny black) includes 8, 11, and C. nanula (not observed in 2001). Anthophora urbana (13) was also observed only in 2000. (b) Means ± SE of cumulative pollen deposition for ON farms in 2000 (black with solid line) and 2001 (gray with dashed line). Numbers and letters refer to species identity as above.