Dave Goulson

Bee declines driven by combined stress from parasites, pesticides, and lack of flowers

Conserving pollinator services for crops If pollination fails, ecosystems are eroded and we will lose reliable sources of many critical foodstuffs. Focusing on the pollination services provided by bees, Goulson et al. review the stresses bees are experiencing from climate change, infectious diseases, and insecticides. We can mitigate some of the stress on bees by improving floral resources and adopting quarantine measures, and by surveillance of bee populations. Crucially, we need to resolve the controversy surrounding prophylactic use of pesticides. Science, this issue 10.1126/science.1255957 BACKGROUND The species richness of wild bees and other pollinators has declined over the past 50 years, with some species undergoing major declines and a few going extinct. Evidence of the causes of these losses is patchy and incomplete, owing to inadequate monitoring systems. Managed honey bee stocks have also declined in North America and many European countries, although they have increased substantially in China. During this same period, the demand for insect pollination of crops has approximately tripled, and the importance of wild pollinators in providing such services has become increasingly apparent, leading to concern that we may be nearing a “pollination crisis” in which crop yields begin to fall. This has stimulated much-needed research into the causes of bee declines. Habitat loss, which has reduced the abundance and diversity of floral resources and nesting opportunities, has undoubtedly been a major long-term driver through the 20th century and still continues today. In addition, both wild and managed bees have been exposed to a succession of emerging parasites and pathogens that have been accidentally moved around the world by human action. The intensification of agriculture and increasing reliance on pesticides means that pollinators are also chronically exposed to cocktails of agrochemicals. Predicted changes in global climate are likely to further exacerbate such problems in the future. ADVANCES It has lately become clear that stressors do not act in isolation and that their interactions may be difficult to predict; for example, some pesticides act synergistically rather than additively. Both pesticide exposure and food stress can impair immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple interacting stressors is driving honey bee colony losses and declines of wild pollinators, but the precise combination apparently differs from place to place. Although the causes of pollinator decline may be complex and subject to disagreement, solutions need not be; taking steps to reduce or remove any of these stresses is likely to benefit pollinator health. Several techniques are available that have been demonstrated to effectively increase floral availability in farmland. Similarly, encouraging gardeners to grow appropriate bee-friendly flowers and to improve management of amenity grasslands can also reduce dietary stress. Retaining or restoring areas of seminatural habitat within farmland will improve nest site availability. A return to the principles of integrated pest management and avoidance of prophylactic use of agrochemicals could greatly decrease exposure of bees to pesticides. OUTLOOK Interactions among agrochemicals and stressors are not addressed by current regulatory procedures, which typically expose well-fed, parasite-free bees to a single pesticide for a short period of time. Devising approaches to study these interactions and incorporating them into the regulatory process poses a major challenge. In the meantime, providing support and advice for farmers in more sustainable farming methods with reduced pesticide use is likely to have broad benefits for farmland biodiversity. Enforcing effective quarantine measures on bee movements to prevent further spread of bee parasites is also vital. Finally, effective monitoring of wild pollinator populations is urgently needed to inform management strategies. Without this, we have no early warning system to tell us how close we may be to a pollination crisis. With a growing human population and rapid growth in global demand for pollination services, we cannot afford to see crop yields begin to fall, and we would be well advised to take preemptive action to ensure that we have adequate pollination services into the future. Multiple interacting stressors drive bee declines. Both wild and managed bees are subject to a number of important and interacting stressors. For example, exposure to some fungicides can greatly increase the toxicity of insecticides, whereas exposure to insecticides reduces resistance to diseases. Dietary stresses are likely to reduce the ability of bees to cope with both toxins and pathogens. Photo credit: DAVE GOULSON Bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined; bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites accidentally spread by humans. Climate change is likely to exacerbate these problems in the future. Stressors do not act in isolation; for example, pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple interacting stressors is driving honey bee colony losses and declines of wild pollinators, but such interactions are not addressed by current regulatory procedures, and studying these interactions experimentally poses a major challenge. In the meantime, taking steps to reduce stress on bees would seem prudent; incorporating flower-rich habitat into farmland, reducing pesticide use through adopting more sustainable farming methods, and enforcing effective quarantine measures on bee movements are all practical measures that should be adopted. Effective monitoring of wild pollinator populations is urgently needed to inform management strategies into the future.

Neonicotinoid pesticide reduces bumble bee colony growth and queen production.

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. Bumble bee colonies produce many fewer queens after exposure to a widely used insecticide. Growing evidence for declines in bee populations has caused great concern because of the valuable ecosystem services they provide. Neonicotinoid insecticides have been implicated in these declines because they occur at trace levels in the nectar and pollen of crop plants. We exposed colonies of the bumble bee Bombus terrestris in the laboratory to field-realistic levels of the neonicotinoid imidacloprid, then allowed them to develop naturally under field conditions. Treated colonies had a significantly reduced growth rate and suffered an 85% reduction in production of new queens compared with control colonies. Given the scale of use of neonicotinoids, we suggest that they may be having a considerable negative impact on wild bumble bee populations across the developed world.

REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides

Summary 1. Neonicotinoids are now the most widely used insecticides in the world. They act systemically, travelling through plant tissues and protecting all parts of the crop, and are widely applied as seed dressings. As neurotoxins with high toxicity to most arthropods, they provide effective pest control and have numerous uses in arable farming and horticulture. 2. However, the prophylactic use of broad-spectrum pesticides goes against the long-established principles of integrated pest management (IPM), leading to environmental concerns. 3. It has recently emerged that neonicotinoids can persist and accumulate in soils. They are water soluble and prone to leaching into waterways. Being systemic, they are found in nectar and pollen of treated crops. Reported levels in soils, waterways, field margin plants and floral resources overlap substantially with concentrations that are sufficient to control pests in crops, and commonly exceed the LC50 (the concentration which kills 50% of individuals) for beneficial organisms. Concentrations in nectar and pollen in crops are sufficient to impact substantially on colony reproduction in bumblebees. 4. Although vertebrates are less susceptible than arthropods, consumption of small numbers of dressed seeds offers a route to direct mortality in birds and mammals. 5. Synthesis and applications. Major knowledge gaps remain, but current use of neonicotinoids is likely to be impacting on a broad range of non-target taxa including pollinators and soil and aquatic invertebrates and hence threatens a range of ecosystem services.

An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species

Bumblebees are major pollinators of crops and wildflowers in northern temperate regions. Knowledge of their ecology is vital for the design of effective management and conservation strategies but key aspects remain poorly understood. Here we employed microsatellite markers to estimate and compare foraging range and nest density among four UK species: Bombus terrestris, Bombus pascuorum, Bombus lapidarius, and Bombus pratorum. Workers were sampled along a 1.5‐km linear transect across arable farmland. Eight or nine polymorphic microsatellite markers were then used to identify putative sisters. In accordance with previous studies, minimum estimated maximum foraging range was greatest for B. terrestris (758 m) and least for B. pascuorum (449 m). The estimate for B. lapidarius was similar to B. pascuorum (450 m), while that of B. pratorum was intermediate (674 m). Since the area of forage available to bees increases as the square of foraging range, these differences correspond to a threefold variation in the area used by bumblebee nests of different species. Possible explanations for these differences are discussed. Estimates for nest density at the times of sampling were 29, 68, 117, and 26/km2 for B. terrestris, B. pascuorum, B. lapidarius and B. pratorum, respectively. These data suggest that even among the most common British bumblebee species, significant differences in fundamental aspects of their ecology exist, a finding that should be reflected in management and conservation strategies.

Effects of neonicotinoids and fipronil on non-target invertebrates

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density

Parasite resistance mechanisms can be costly to maintain. We would therefore predict that organisms should invest in resistance only when it is likely to be required. Insects that show density–dependent phase polyphenism, developing different phenotypes at high and low population densities, have the opportunity to match their levels of investment in resistance with the likelihood of exposure to pathogens. As high population densities often precipitate disease epidemics, the high–density form should be selected to invest relatively more in resistance. We tested this prediction in larvae of the noctuid Spodoptera exempta. Larvae reared at a high density were found to be considerably more resistant to a nuclear polyhedrosis virus than those reared in isolation. A conspicuous feature of the high–density phase of S. exempta and other phase–polyphenic Lepidoptera is cuticular melanization. As melanization is controlled by the phenoloxidase enzyme system, which is also involved in the immune response, this suggests a possible mechanism for increased resistance at high population densities. We demonstrated that melanized S. exempta larvae were more resistant than non–melanized forms, independent of rearing density. We also found that haemolymph phenoloxidase activity was correlated with cuticular melanization, providing further evidence for a link between melanization and immunity. These results suggest that pathogen resistance in S. exempta is phenotypically plastic, and that the melanized cuticles characteristic of the high–density form may be indicative of a more active immune system.

Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution

The majority of species of flowering plants rely on pollination by insects, so that their reproductive success and in part their population structure are determined by insect behaviour. The foraging behaviour of insect pollinators is flexible and complex, because efficient collection of nectar or pollen is no simple matter. Each flower provides a variable but generally small reward that is often hidden, flowers are patchily distributed in time and space, and are erratically depleted of rewards by other foragers. Insects that specialise in visiting flowers have evolved an array of foraging strategies that act to improve their efficiency, which in turn determine the reproductive success of the plants that they visit. This review attempts a synthesis of the recent literature on selectivity in pollinator foraging behaviour, in terms of the species, patch and individual flowers that they choose to visit. The variable nature of floral resources necessitate foraging behaviour based upon flexible learning, so that foragers can respond to the pattern of rewards that they encounter. Fidelity to particular species allows foragers to learn appropriate handling skills and so reduce handling times, but may also be favoured by use of a search image to detect flowers. The rewards received are also used to determine the spatial patterns of searches; distance and direction of flights are adjusted so that foragers tend to remain within rewarding patches and depart swiftly from unrewarding ones. The distribution of foragers among patchy resources generally conforms to the expectations of two simple optimal foraging models, the ideal free distribution and the marginal value theorem. Insects are able to learn to discriminate among flowers of their preferred species on the basis of subtle differences in floral morphology. They may discriminate upon the basis of flower size, age, sex or symmetry and so choose the more rewarding flowers. Some insects are also able to distinguish and reject depleted flowers on the basis of ephemeral odours left by previous visitors. These odours have recently been implicated as a mechanism involved in interspecific interactions between foragers. From the point of view of a plant reliant upon insect pollination, the behaviour of its pollinators (and hence its reproductive success) is likely to vary according to the rewards offered, the size and complexity of floral displays used to advertise their location, the distribution of conspecific and of rewards offered by other plant species, and the abundance and behaviour of other flower visitors.

Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats

Many bumblebee species are declining at a rapid rate in the United Kingdom and elsewhere. This is commonly attributed to the decline in floral resources that has resulted from an intensification in farming practices. Here we assess growth of nests of the bumblebee, Bombus terrestris, in habitats providing different levels of floral resources. Experimental nests were placed out in conventional farmland, in farmland with flower-rich conservation measures and in suburban areas. Nests gained weight more quickly and attained a larger final size in suburban areas compared to elsewhere. The diversity of pollens gathered by bees was highest in suburban areas, and lowest in conventional farmland. Nests in suburban areas were also more prone to attack by the specialist bumblebee parasite Aphomia sociella, suggesting that this moth is more abundant in suburban areas than elsewhere. Overall, our results demonstrate that gardens provide a greater density and diversity of floral resources than farmland, and probably support larger populations of B. terrestris. Contrary to expectation, schemes deployed to enhance farmland biodiversity appear to have little measurable impact on nest growth of this bumblebee species. We argue that B. terrestris probably forage over a larger scale than that on which farms are managed, so that nest growth is determined by the management of a large number of neighbouring farms, not just that in which the nest is located.

Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?

Bumblebee workers vary greatly in size, unlike workers of most other social bees. This variability has not been adequately explained. In many social insects, size variation is adaptive, with different-sized workers performing different tasks (alloethism). Here we established whether workers of the bumblebee, Bombus terrestris (L.) (Hymenoptera; Apidae), exhibit alloethism. We quantified the size of workers engaging in foraging compared to those that remain in the nest, and confirmed that it is the larger bees that tend to forage (X ± SE thorax widths 4.34 ± 0.01 mm for nest bees and 4.93 ± 0.02 mm for foragers). We then investigated whether large bees are better suited to foraging because they are able to transport heavier loads of food back to the nest. Both pollen and nectar loads of returning foragers were measured, demonstrating that larger bees do return with a heavier mass of forage. Foraging trip times were inversely related to bee size when collecting nectar, but were unrelated to bee size for bees collecting pollen. Overall, large bees brought back more nectar per unit time than small bees, but the rate of pollen collection appeared to be unrelated to size. The smallest foragers had a nectar foraging rate close to zero, presumably explaining why foragers tend to be large. Why might larger bees be better at foraging? Various explanations are considered: larger bees are able to forage in cooler conditions, may be able to forage over larger distances, and are perhaps also less vulnerable to predation. Conversely, small workers are presumably cheaper to produce and may be more nimble at within-nest tasks. Further research is needed to assess these possibilities. ©2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species

Honey bees, Apis mellifera, use short-lived repellent scent marks to distinguish and reject flowers that have recently been visited by themselves or by siblings, and so save time that would otherwise be spent in probing empty flowers. Conversely, both honey bees and bumblebees, Bombus spp., can mark rewarding flowers with scent marks that promote probing by conspecifics. We examined detection of recently visited flowers in a mixed community of bumblebees foraging on comfrey, Symphytum officinale, in southern England. When foraging among inflorescences on a plant, three abundant species of Bombus probed fewer inflorescences more than once than would be expected from random foraging. Bees frequently encountered inflorescences but departed without probing them for nectar. Examination of the incidence of such rejections in the two most common species, B. terrestris and B. pascuorum, revealed that the low incidence of multiple probing visits was due to two factors: bees both foraged systematically and selectively rejected inflorescences that they had previously visited. When presented with inflorescences of known history, bees selectively rejected those that had been recently visited by themselves or by conspecifics compared with randomly selected inflorescences. They were also able to distinguish inflorescences that had been visited by other Bombus species. Bees were unable to distinguish and reject inflorescences from which the nectar had been removed artificially. We conclude that these Bombus species are probably using scent marks left by previous visitors. The significance of deposition and detection of interspecific scent marks for competitive interactions between species is discussed. Copyright 1998 The Association for the Study of Animal Behaviour.