Mickaël Henry

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.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.

Decreasing Abundance, Increasing Diversity and Changing Structure of the Wild Bee Community (Hymenoptera: Anthophila) along an Urbanization Gradient

Background Wild bees are important pollinators that have declined in diversity and abundance during the last decades. Habitat destruction and fragmentation associated with urbanization are reported as part of the main causes of this decline. Urbanization involves dramatic changes of the landscape, increasing the proportion of impervious surface while decreasing that of green areas. Few studies have investigated the effects of urbanization on bee communities. We assessed changes in the abundance, species richness, and composition of wild bee community along an urbanization gradient. Methodology/Principal Findings Over two years and on a monthly basis, bees were sampled with colored pan traps and insect nets at 24 sites located along an urbanization gradient. Landscape structure within three different radii was measured at each study site. We captured 291 wild bee species. The abundance of wild bees was negatively correlated with the proportion of impervious surface, while species richness reached a maximum at an intermediate (50%) proportion of impervious surface. The structure of the community changed along the urbanization gradient with more parasitic species in sites with an intermediate proportion of impervious surface. There were also greater numbers of cavity-nesting species and long-tongued species in sites with intermediate or higher proportion of impervious surface. However, urbanization had no effect on the occurrence of species depending on their social behavior or body size. Conclusions/Significance We found nearly a third of the wild bee fauna known from France in our study sites. Indeed, urban areas supported a diverse bee community, but sites with an intermediate level of urbanization were the most speciose ones, including greater proportion of parasitic species. The presence of a diverse array of bee species even in the most urbanized area makes these pollinators worthy of being a flagship group to raise the awareness of urban citizens about biodiversity.

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.

Large-scale trade-off between agricultural intensification and crop pollination services

Unprecedented growth in human populations has required the intensification of agriculture to enhance crop productivity, but this was achieved at a major cost to biodiversity. There is abundant local-scale evidence that both pollinator diversity and pollination services decrease with increasing agricultural intensification. This raises concerns regarding food security, as two-thirds of the worlds major food crops are pollinator-dependent. Whether such local findings scale up and affect crop production over larger scales is still being debated. Here, we analyzed a country-wide dataset of the 54 major crops in France produced over the past two decades and found that benefits of agricultural intensification decrease with increasing pollinator dependence, to the extent that intensification failed to increase the yield of pollinator-dependent crops and decreased the stability of their yield over time. This indicates that benefits from agricultural intensification may be offset by reductions in pollination serv...

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.

A Locomotor Deficit Induced by Sublethal Doses of Pyrethroid and Neonicotinoid Insecticides in the Honeybee Apis mellifera.

The toxicity of pesticides used in agriculture towards non-targeted organisms and especially pollinators has recently drawn the attention from a broad scientific community. Increased honeybee mortality observed worldwide certainly contributes to this interest. The potential role of several neurotoxic insecticides in triggering or potentiating honeybee mortality was considered, in particular phenylpyrazoles and neonicotinoids, given that they are widely used and highly toxic for insects. Along with their ability to kill insects at lethal doses, they can compromise survival at sublethal doses by producing subtle deleterious effects. In this study, we compared the bee’s locomotor ability, which is crucial for many tasks within the hive (e.g. cleaning brood cells, feeding larvae…), before and after an acute sublethal exposure to one insecticide belonging to the two insecticide classes, fipronil and thiamethoxam. Additionally, we examined the locomotor ability after exposure to pyrethroids, an older chemical insecticide class still widely used and known to be highly toxic to bees as well. Our study focused on young bees (day 1 after emergence) since (i) few studies are available on locomotion at this stage and (ii) in recent years, pesticides have been reported to accumulate in different hive matrices, where young bees undergo their early development. At sublethal doses (SLD48h, i.e. causing no mortality at 48h), three pyrethroids, namely cypermethrin (2.5 ng/bee), tetramethrin (70 ng/bee), tau-fluvalinate (33 ng/bee) and the neonicotinoid thiamethoxam (3.8 ng/bee) caused a locomotor deficit in honeybees. While the SLD48h of fipronil (a phenylpyrazole, 0.5 ng/bee) had no measurable effect on locomotion, we observed high mortality several days after exposure, an effect that was not observed with the other insecticides. Although locomotor deficits observed in the sublethal range of pyrethroids and thiamethoxam would suggest deleterious effects in the field, the case of fipronil demonstrates that toxicity evaluation requires information on multiple endpoints (e.g. long term survival) to fully address pesticides risks for honeybees. Pyrethroid-induced locomotor deficits are discussed in light of recent advances regarding their mode of action on honeybee ion channels and current structure-function studies.

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.

Phyllostomid Bat Occurrence in Successional Stages of Neotropical Dry Forests

Tropical dry forests (TDFs) are highly endangered tropical ecosystems being replaced by a complex mosaic of patches of different successional stages, agricultural fields and pasturelands. In this context, it is urgent to understand how taxa playing critical ecosystem roles respond to habitat modification. Because Phyllostomid bats provide important ecosystem services (e.g. facilitate gene flow among plant populations and promote forest regeneration), in this study we aimed to identify potential patterns on their response to TDF transformation in sites representing four different successional stages (initial, early, intermediate and late) in three Neotropical regions: México, Venezuela and Brazil. We evaluated bat occurrence at the species, ensemble (abundance) and assemblage level (species richness and composition, guild composition). We also evaluated how bat occurrence was modulated by the marked seasonality of TDFs. In general, we found high seasonal and regional specificities in phyllostomid occurrence, driven by specificities at species and guild levels. For example, highest frugivore abundance occurred in the early stage of the moistest TDF, while highest nectarivore abundance occurred in the same stage of the driest TDF. The high regional specificity of phyllostomid responses could arise from: (1) the distinctive environmental conditions of each region, (2) the specific behavior and ecological requirements of the regional bat species, (3) the composition, structure and phenological patterns of plant assemblages in the different stages, and (4) the regional landscape composition and configuration. We conclude that, in tropical seasonal environments, it is imperative to perform long-term studies considering seasonal variations in environmental conditions and plant phenology, as well as the role of landscape attributes. This approach will allow us to identify potential patterns in bat responses to habitat modification, which constitute an invaluable tool for not only bat biodiversity conservation but also for the conservation of the key ecological processes they provide.