Jean-François Odoux

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.

Territorial biodiversity and consequences on physico-chemical characteristics of pollen collected by honey bee colonies

Pollen resources may become a constraint for the honey bee in cereal farming agrosystems and thus influence honey bee colony development. This survey intended to increase knowledge on bee ecology in order to understand how farming systems can provide bee forage throughout the year. We conducted a 1-year study to investigate the flower range exploited in an agrarian environment in western France, the physico-chemical composition of honey bee-collected pollen, the territorial biodiversity visited by the bee at different periods, and the relationships between these three datasets. Palynological analyses showed the importance of maize among crop pollens and that of weeds during the food shortage period. Pollen protein varied from 16% to 29% and lipids from 7% to 24%. The contribution of different habitats to pollen harvest, was from crops (62%), woods (32%), grasslands (4%), and gardens (1%).

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.

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.

A ‘Landscape physiology’ approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats

Understanding how anthropogenic landscape alteration affects populations of ecologically- and economically-important insect pollinators has never been more pressing. In this context, the assessment of landscape quality typically relies on spatial distribution studies, but, whether habitat-restoration techniques actually improve the health of targeted pollinator populations remains obscure. This gap could be filled by a comprehensive understanding of how gradients of landscape quality influence pollinator physiology. We therefore used this approach for honey bees (Apis mellifera) to test whether landscape patterns can shape bee health. We focused on the pre-wintering period since abnormally high winter colony losses have often been observed. By exposing colonies to different landscapes, enriched in melliferous catch crops and surrounded by semi-natural habitats, we found that bee physiology (i.e. fat body mass and level of vitellogenin) was significantly improved by the presence of flowering catch crops. Catch crop presence was associated with a significant increase in pollen diet diversity. The influence of semi-natural habitats on bee health was even stronger. Vitellogenin level was in turn significantly linked to higher overwintering survival. Therefore, our experimental study, combining landscape ecology and bee physiology, offers an exciting proof-of-concept for directly identifying stressful or suitable landscapes and promoting efficient pollinator conservation.

Variations in the Availability of Pollen Resources Affect Honey Bee Health.

Intensive agricultural systems often expose honey bees (Apis mellifera L.) to large temporal variations in the availability (quantity, quality and diversity) of nutritional resources. Such nutritional irregularity is expected to affect honey bee health. We therefore tested under laboratory conditions the effect of such variation in pollen availability on honey bee health (survival and nursing physiology—hypopharyngeal gland development and vitellogenin expression). We fed honey bees with different diets composed of pollen pellets collected by honey bees in an agricultural landscape of western France. Slight drops (5–10%) in the availability of oilseed rape (Brassica napus L.) pollen resulted in significant reductions of all tested variables. Despite some variations in taxonomic diversity and nutritional quality, the pollen mixes harvested over the season had a similar positive influence on honey bee health, except for the one collected in late July that induced poor survival and nursing physiology. This period coincided with the mass-flowering of maize (Zea mays L.), an anemophilous crop which produces poor-quality pollen. Therefore, changes in bee health were not connected to variations in pollen diversity but rather to variations in pollen depletion and quality, such as can be encountered in an intensive agricultural system of western France. Finally, even though pollen can be available ad libitum during the mass-flowering of some crops (e.g. maize), it can fail to provide bees with diet adequate for their development.

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.