Fabrice Requier

A Common Pesticide Decreases Foraging Success and Survival in Honey Bees

Bad News for Bees Neonicotinoid insecticides were introduced in the early 1990s and have become one of the most widely used crop pesticides in the world. These compounds act on the insect central nervous system, and they have been shown to be persistent in the environment and in plant tissues. Recently, there have been controversial connections made between neonicotinoids and pollinator deaths, but the mechanisms underlying these potential deaths have remained unknown. Whitehorn et al. (p. 351, published online 29 March) exposed developing colonies of bumble bees to low levels of the neonicotinoid imidacloprid and then released them to forage under natural conditions. Treated colonies displayed reduced colony growth and less reproductive success, and they produced significantly fewer queens to found subsequent generations. Henry et al. (p. 348, published online 29 March) documented the effects of low-dose, nonlethal intoxication of another widely used neonicotinoid, thiamethoxam, on wild foraging honey bees. Radio-frequency identification tags were used to determine navigation success of treated foragers, which suggested that their homing success was much reduced relative to untreated foragers. Honey bees cannot find their way home after exposure to sublethal doses of a widely used insecticide. Nonlethal exposure of honey bees to thiamethoxam (neonicotinoid systemic pesticide) causes high mortality due to homing failure at levels that could put a colony at risk of collapse. Simulated exposure events on free-ranging foragers labeled with a radio-frequency identification tag suggest that homing is impaired by thiamethoxam intoxication. These experiments offer new insights into the consequences of common neonicotinoid pesticides used worldwide.

Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds.

In intensive farmland habitats, pollination of wild flowers and crops may be threatened by the widespread decline of pollinators. The honey bee decline, in particular, appears to result from the combination of multiple stresses, including diseases, pathogens, and pesticides. The reduction of semi-natural habitats is also suspected to entail floral resource scarcity for bees. Yet, the seasonal dynamics and composition of the honey bee diet remains poorly documented to date. In this study, we studied the seasonal contribution of mass-flowering crops (rapeseed and sunflower) vs. other floral resources, as well as the influence of nutritional quality and landscape composition on pollen diet composition over five consecutive years. From April to October, the mass of pollen and nectar collected by honey bees followed a bimodal seasonal trend, marked by a two-month period of low food supply between the two oilseed crop mass-flowerings (ending in May for rapeseed and July for sunflower). Bees collected nectar mainly from crops while pollen came from a wide diversity of herbaceous and woody plant species in semi-natural habitats or from weeds in crops. Weed species constituted the bulk of the honey bee diet between the mass flowering crop periods (up to 40%) and are therefore suspected to play a critical role at this time period. The pollen diet composition was related to the nutritional value of the collected pollen and by the local landscape composition. Our study highlights (1) a food supply depletion period of both pollen and nectar resources during late spring, contemporaneously with the demographic peak of honey bee populations, (2) a high botanical richness of pollen diet, mostly proceeding from trees and weeds, and (3) a pollen diet composition influenced by the local landscape composition. Our results therefore support the Agri-Environmental Schemes intended to promote honey bees and beekeeping sustainability through the enhancement of flower availability in agricultural landscapes.

ECOBEE: a tool for long-term honey bee colony monitoring at the landscape scale in West European intensive agroecosystems

Summary In Central Western France, as in many other areas, traditional apiculture has been replaced by more intensive practices to compensate for colony losses and current decreasing honey yields. One neglected aspect concerns the choice by professional beekeepers of apiary sites in intensive agrosystems, with regard to landscape features, a choice which appears to be largely empirical. ECOBEE is a colony monitoring scheme specifically intended to provide beekeepers and researchers with basic ecological data on honeybees in intensive agrosystems, as well as colony population dynamics. ECOBEE was launched in 2008 as a long-term ecological project with three specific aims: 1. to monitor seasonal and inter-annual population dynamic parameters of honeybee colonies in a heterogeneous farming system; 2. to provide relevant and robust datasets to test specific hypotheses about bees such as the influence of landscape planning, agricultural inputs or human pressure; and 3. to offer opportunities for assessing the effectiveness of agro-environmental schemes or the effects of changes in agricultural policies on honey bee wellbeing. Here we present an overview of ECOBEE, the type of datasets collected over the first four years of monitoring, and their possible application and use. We found that colony dynamics were largely influenced by the phenology of the main mass-flowering crops foraged by bees, namely oilseed rape and sunflowers. Furthermore, we detected a sharp food shortage period in late spring between the flowering of oilseed rape and sunflowers, possibly temporarily constraining colony sustainability. We further discuss the research perspectives offered by ECOBEE, especially with regard to spatial ecotoxicology.

Distance from forest edge affects bee pollinators in oilseed rape fields

Wild pollinators have been shown to enhance the pollination of Brassica napus (oilseed rape) and thus increase its market value. Several studies have previously shown that pollination services are greater in crops adjoining forest patches or other seminatural habitats than in crops completely surrounded by other crops. In this study, we investigated the specific importance of forest edges in providing potential pollinators in B. napus fields in two areas in France. Bees were caught with yellow pan traps at increasing distances from both warm and cold forest edges into B. napus fields during the blooming period. A total of 4594 individual bees, representing six families and 83 taxa, were collected. We found that both bee abundance and taxa richness were negatively affected by the distance from forest edge. However, responses varied between bee groups and edge orientations. The ITD (Inter-Tegular distance) of the species, a good proxy for bee foraging range, seems to limit how far the bees can travel from the forest edge. We found a greater abundance of cuckoo bees (Nomada spp.) of Andrena spp. and Andrena spp. males at forest edges, which we assume indicate suitable nesting sites, or at least mating sites, for some abundant Andrena species and their parasites (Fig. 1). Synthesis and Applications. This study provides one of the first examples in temperate ecosystems of how forest edges may actually act as a reservoir of potential pollinators and directly benefit agricultural crops by providing nesting or mating sites for important early spring pollinators. Policy-makers and land managers should take forest edges into account and encourage their protection in the agricultural matrix to promote wild bees and their pollination services.

Pesticide risk assessment in free-ranging bees is weather and landscape dependent

The risk assessment of plant protection products on pollinators is currently based on the evaluation of lethal doses through repeatable lethal toxicity laboratory trials. Recent advances in honeybee toxicology have, however, raised interest on assessing sublethal effects in free-ranging individuals. Here, we show that the sublethal effects of a neonicotinoid pesticide are modified in magnitude by environmental interactions specific to the landscape and time of exposure events. Field sublethal assessment is therefore context dependent and should be addressed in a temporally and spatially explicit way, especially regarding weather and landscape physiognomy. We further develop an analytical Effective Dose (ED) framework to help disentangle context-induced from treatment-induced effects and thus to alleviate uncertainty in field studies. Although the ED framework involves trials at concentrations above the expected field exposure levels, it allows to explicitly delineating the climatic and landscape contexts that should be targeted for in-depth higher tier risk assessment.

The carry‐over effects of pollen shortage decrease the survival of honeybee colonies in farmlands

1. Many studies have reported honeybee colony losses in human-dominated landscapes. While bee floral food resources have been drastically reduced over past decades in humandominated landscapes, no field study has yet been undertaken to determine whether there is a carry-over effect between seasonal disruption in floral resource availability and high colony losses. 2. We investigated if a decline in the harvest of pollen by honeybees in spring affected managed honeybee colony dynamics (brood size, adult population and honey reserves) and health (Varroa mite loads and colony survival) throughout the beekeeping season. 3. A decline in pollen harvest was associated with a direct reduction in brood production, leading to a negative effect on the adult population size later in the season, and lower honey reserves before the onset of winter. Furthermore, the decline in pollen harvest negatively impacted the health of the colony, resulting in higher Varroa mite loads and higher seasonal and winter colony losses. 4. Early-warning signs of these carry-over effects were identified, showing that preferential investment in honey reserves instead of brood production early in the season increased the decline in pollen harvest and its associated carry-over effects. 5. Synthesis and applications. The results suggest that the decline in pollen harvest may have been overlooked as a cause of pollen shortage and associated bee colony losses. Strategies to avoid such losses in intensive farmland systems include (i) limiting or avoiding honey harvests in spring, (ii) monitoring colonies for early-warning signals of colony failure and (iii) increasing the amount of floral resources available through wise land-use management.

3D Tracking of Honeybees Enhanced by Environmental Context

This paper summarizes an approach based on stereo vision to recover honeybee trajectories in 3D at the beehive entrance. The 3D advantage offered by stereo vision is crucial to overcome the rough constraints of the application (number of bees, target dynamics and light). Biologists have highlighted the close scale influence of the environment on bees dynamics. We propose to transpose this idea to enhance our tracking process based on Global Nearest Neighbors. Our method normalizes track/observation association costs that are originally not uniformly distributed over the scene. Therefore, the structure of the scene is needed in order to compute relative distances with the targets. The beehive and especially the flight board is the referent environment for bees, so we propose a method to reconstruct the flight board surface from the noisy and incomplete disparity maps provided by the stereo camera.

Towards an integrated species and habitat management of crop pollination

Pollination deficits are widespread in current agriculture, so improving management for crop pollination is critical. Here we review the two most common management approaches to enhance crop pollination, species and habitat management, by providing referenced lists of successful examples. We pinpoint that these approaches have been studied in isolation from each other, with little discussion on potential synergies and trade-offs between them. The potential costs of species management (e.g., loss of biodiversity due to biological invasion), as well as the potential benefits to managed pollinator species from habitat restoration, are rarely quantified. An integrative approach to crop pollination should be implemented, accounting for the cost and benefits (including those beyond crop production) and interactions of species and habitat management.

An expert-assisted citizen science program involving agricultural high schools provides national patterns on bee species assemblages

Ecology studies often require large datasets. The benefits of citizen science for collecting such datasets include the extension of spatial and temporal scales, and cost reduction. In classical citizen science, citizens collect data and send them directly to scientists. This may not be possible for the many biological groups for which specimen identification is difficult and requires high-level expertise. Here we report the results of an expert-assisted citizen science program where teachers from 20 French agricultural high schools collected bees, which were identified to species level by a panel of expert bee taxonomists. Overall the dataset included 70 collections (year × sampling site combinations) that resulted in 4574 specimens belonging to 195 species. We analysed this dataset using data freely available at a national scale on agriculture intensity and landscape composition. We found that species richness increased with increasing proportion of herbaceous semi-natural elements; species dominance decreased with increasing crop diversity; the proportion of above ground nesting species and specimens increased as the intensity of agricultural practices decreased. Comparing the results obtained with identification to species level and those obtained with higher taxa or parataxonomic approaches, we found that the loss of taxonomic resolution resulted in the non-significance of some results on the effects of environmental variables on bee assemblage-level attributes. Our study suggests that identification to species level is of great importance to detect the effects of global change on bees and that an expert-assisted citizen science paradigm could provide relevant results to guide conservation measures at a national scale.

Predictive systems models can help elucidate bee declines driven by multiple combined stressors

Bee declines are driven by multiple combined stresses, making it exceedingly difficult to identify experimentally the most critical threats to bees and their pollination services. We highlight here the too often ignored potential of mechanistic models in identifying critical stress combinations. Advanced bee models are now available as open access tools and offer an unprecedented opportunity for bee biologists to explore bee resilience tipping points in a variety of environmental contexts. We provide general guidelines on how to run bee models to help detect a priori critical stress combinations to be targeted in the field. This so-called funnel analysis should be performed in tight conjunction with the recent development of large-scale field monitoring programs for bee health surveillance.