Pesticide hazard, floral resource availability and natural enemies interactively drive the fitness of bee species depending on their crop fidelity.

Pesticides, loss of floral resources and parasitism are considered drivers of wild bee decline in agroecosystems, but their interactions are poorly understood under field conditions. Negative impacts are predicted to vary across species of distinct crop fidelity because of the associated consequences for pesticide exposure and dependence on wild flowers. We experimentally established populations of two solitary bee species in apple orchards with distinct pesticide hazard and flower availability in surrounding landscapes. The number of nesting females, their reproduction and offspring survival and parasitism rate were tracked throughout apple bloom. We show that in the solitary bee Osmia cornuta, which showed a strong preference to forage in apple orchards, the number of females remaining at nesting sites towards the end of apple bloom and the overall reproductive success of the released bees declined with pesticide hazard. In contrast, the closely related Osmia bicornis, which showed a lower preference for apple, was not affected by pesticide use in orchards. Floral resource distribution furthermore modulated parasitism rates in both species: while large amounts of locally available resources reduced offspring parasitism, it increased with relatively higher food availability in the landscapes surrounding focal orchards, probably due to the bees foraging on a larger scale and thus longer periods during which nests remained unattended. Our findings provide novel insights into the complex interplay of pesticide exposure, flower availability and parasitism risk driving population dynamics of bees in agroecosystems. They show that in particular the most reliable crop pollinator species are especially harmed by high pesticide use in crops. Our study underpins the key role of reducing pesticide risks for pollinators through effective regulation of potentially hazardous agrochemicals and the promotion of alternative pest regulation approaches along with conserving and restoring flower-rich habitats to sustain pollinator populations in agroecosystems.