Colony Collapse Disorder: Cause and Effect
A CAUSAL ANALYSIS OF OBSERVED DECLINES IN MANAGED HONEY BEES (APIS MELLIFERA) (2014)
- CONCLUSION: A causal analysis methodology was introduced to bee experts at a workshop, in which a problem was defined within a temporal and spatial scale. Experts used a set of causal criteria against which evidence was logically evaluated. Thirty-nine candidate causes were put forth as potential causes of reduced survivability since 2006 of commercial bees used in the California almond industry. Based on the weight-of-evidence against each criterion, candidate causes were categorized as being probable, possible, or unlikely. Due to lack of information and data, several candidate causes were categorized as indeterminate. The parasitic mite Varroa destructor plus viruses was judged to be a “probable cause,” while nutrient deficiency was judged to be a “possible cause” of the reduced survival probability of commercial honey bee colonies in the California almond scenario since approximately 2006. Neonicotinoid pesticides were judged to be “unlikely” as the sole cause of this reduced survival probability, although they could possibly be a contributing factor. The duration of the workshop was insufficient to complete the analysis for all the identified candidate causes (Table 1).
- The causal analysis presented here represents a general agreement among the workshop experts, but it is not a formal consensus, and dissenting opinions were expressed on a variety of topics. The results of this analysis should be considered preliminary, because many data gaps remain, especially surrounding environmental factors and beekeeping practices that may potentially affect colony survival but for which the consistency of evidence is “indeterminate” (Table 2). Moreover, it is likely that multiple causes, rather than one single cause, are responsible for the reduced survival of commercial honey bee colonies. The number of potential causes and the likelihood that they are interacting complicates the design of future research investigations. However, a better understanding of these causes can lead to the development of methods to better manage honey bees in commercial beekeeping operations.
CAUSES OF POLLINATOR DECLINES AND POTENTIAL THREATS
- CONCLUSIONS: Just as different species of pollinators differ in the degree to which their diversity and populations have declined, the causes that underlie decline vary widely. Some mortality is particularly important in a narrow range of pollinators; in managed pollination systems, there is clear evidence of reductions in pollinator numbers caused by introduced parasites and pathogens. The evidence indicates that these agents of mortality also could operate in wild pollinator declines. Other causes of mortality affect a cross-section of pollinators (albeit to different extents); habitat degradation and habitat loss, in their many manifestations, have contributed to declines in many vertebrate and invertebrate pollinators.
DOCUMENTING PERSISTENCE OF MOST EASTERN NORTH AMERICAN BEE SPECIES (HYMENOPTERA: APOIDEA: ANTHOPHILA) TO 1990–2009 (2011)
- ABSTRACT: The status of wild bees, the major group of pollinators in most biomes, has gained recognition as an important ecological and economic issue. Insufficient baseline data and taxonomic expertise for this understudied group has hindered efforts to assess the conservation status of the majority of wild bee species. To more objectively address their current conservation status, we drew upon museum collections and the expertise of melittologists (biologists studying non-Apis bees) to compile a complete list of bee species for eastern North America, discriminating those which have and have not been detected during the past 20 years. The vast majority (95% of about 770 eastern North American bee species) have been found again, at least once since 1990. The remaining 37 species were rarely collected before 1990 as well. Some may truly be at risk (or lost). Others are undoubtedly data deficient due to inadequate knowledge of their biology or hosts, or the geographic regions and local habitats where they occur.
- Distributional and ecological patterns among these missing species are discussed. Most were recorded in the region only from peripheral areas or areas known to be undersampled by recent collectors, such as the southeastern United States. Others are characterized by specialized life histories or they cannot be identified routinely in the absence of taxonomic revisions. Clearly, most eastern North American bee species have persisted until recent times, with no evidence of widespread recent extinctions. An absence of well-documented global extinctions of bee species does not warrant complacency regarding pollinator conservation, as our qualitative method does not lend itself to documenting range contractions, range fragmentation, or declines in abundance and species richness in local bee communities.
BEE HEALTH IN EUROPE: AN OVERVIEW (2012)
- Research shows that the main cause of honey bee colony losses is Varroa, a parasite found in almost every apiary in Europe. The “Deutsche Bienenmonitoring” project showed that honey bee losses are correlated with Varroa infection, a conclusion similar to that described in the Journal of Apicultural Research’s special issue “Colony Losses”. While the issue’s authors have a variety of opinions, most pinpoint Varroa and other diseases as key factors. High overwinter colony losses in Europe generally involve damage caused by the mite.
- Researchers have also identified environmental issues such as habitat loss, reduced biodiversity and insufficient amounts of high quality nectar and pollen as major factors affecting bee health. Changes in land use and crop management as well as the traditional farming and forestry practices that provided rich habitats lead to a lack of biodiversity. Bee foraging is also compromised by society’s efforts to “neaten” landscapes by removing wild flowers and weeds from lawns, parks, and farms.
- Pesticide use is often assumed to damage bee health. And while single poisoning events linked to spray application have been reported in many countries, they do not seem to cause widespread colony losses. When pesticide-linked incidents do happen, it’s usually because of product misuse or due to farmer ignorance of product labels combined with poor communication with beekeepers.
- Evidence also suggests that a drop in managed honey bee colonies in Europe may simply be linked to a decline in beekeeping. While there’s little information on the economics of beekeeping in Europe, the activity is widely considered unprofitable when carried out on a small scale as a hobby or secondary activity.
HISTORICAL CHANGES IN NORTHEASTERN US BEE POLLINATORS RELATED TO SHARED ECOLOGICAL TRAITS (2012)
- ABSTRACT: Pollinators such as bees are essential to the functioning of terrestrial ecosystems. However, despite concerns about a global pollinator crisis, long-term data on the status of bee species are limited. We present a long-term study of relative rates of change for an entire regional bee fauna in the northeastern United States, based on >30,000 museum records representing 438 species. Over a 140-y period, aggregate native species richness weakly decreased, but richness declines were significant only for the genus Bombus. Of 187 native species analyzed individually, only three declined steeply, all of these in the genus Bombus. However, there were large shifts in community composition, as indicated by 56% of species showing significant changes in relative abundance over time.
- Traits associated with a declining relative abundance include small dietary and phenological breadth and large body size. In addition, species with lower latitudinal range boundaries are increasing in relative abundance, a finding that may represent a response to climate change. We show that despite marked increases in human population density and large changes in anthropogenic land use, aggregate native species richness declines were modest outside of the genus Bombus. At the same time, we find that certain ecological traits are associated with declines in relative abundance. These results should help target conservation efforts focused on maintaining native bee abundance and diversity and therefore the important ecosystems services that they provide.
STATUS REVIEW OF THREE FORMERLY COMMON SPECIES OF BUMBLE BEE IN THE SUBGENUS BOMBUS (2008)
- CONCLUSION: There are a number of threats facing bumble bees, any of which may be leading to the decline of these species. The major threats to bumble bees include: spread of pests and 34 diseases by the commercial bumble bee industry, other pests and diseases, habitat destruction or alteration, pesticides, invasive species, natural pest or predator population cycles, and climate change.
- In the case of these bumble bees, several lines of evidence implicate introduced disease as the most likely cause of the declines of Bombus sensu stricto in North America. Firstly, the fact that other bumble bee species persist and thrive in areas where members of the subgenus Bombus sensu stricto in North America are declining suggests a more specific cause for vulnerability of this particular subset of our bumble bee fauna. Secondly, instead of a gradual decline over decades, as has been documented with British bumble bee populations (Williams et al. 2007), these bumble bees went from being widespread and commonly found to rare or absent within a relatively short period of time (about 7-10 years) throughout much or all of their previous ranges. A third factor indicating disease is the timing of the declines. The earliest declines were observed with B. occidentalis in western North America in the late 1990s; this is the same time that commercially raised B. occidentalis populations were exhibiting problems with Nosema bombi (Velthius and van Doorn 2006). Several years later, scientists began to notice B. affinis and B. terricola populations declining in eastern North America.
- The fact that the bumble bees in decline are all closely related suggests that there could be genetic susceptibility to certain disease strains exhibited by bumble bees in the subgenus Bombus sensu stricto, or shared behavioral traits that increase their susceptibility to certain pests or parasites (Otterstatter and Whidden 2004). Declines from threats other than disease that are listed in this review would have likely impacted species across a broader range of bumble bee subgenera (Williams et al. 2007). Recent discoveries of isolated populations may indicate the existence of remnant populations of bumble bees that were either not exposed to the disease through geographic isolation or were resistant to the disease.
Disease and Pathogens
DISEASE ASSOCIATIONS BETWEEN HONEYBEES AND BUMBLEBEES AS A THREAT TO WILD POLLINATORS (2014)
- ABSTRACT: Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops. Honey bees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high impact pathogens and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumble bees (Bombus spp.) are in global decline, one cause of which may be pathogen spillover from managed pollinators like honey bees, or commercial colonies of bumble bees. In our study, a combination of infection experiments with landscape scale field data indicates that honey bee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic Nosema ceranae is linked between honey bees and bumble bees, with honey bees having higher DWV prevalence, and sympatric bumble bees and honey bees sharing DWV strains; Apis is therefore the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.
MULTIYEAR SURVEY TARGETING DISEASE INCIDENCE IN US HONEY BEES (2016)
- ABSTRACT: The US National Honey Bee Disease Survey sampled colony pests and diseases from 2009 to 2014. We verified the absence of Tropilaelaps spp., the Asian honey bee (Apis cerana), and slow bee paralysis virus. Endemic health threats were quantified, including Varroa destructor, Nosema spp., and eight honey bee viruses. Varroa loads varied across years, with annual fall peaks; Nosema peaked January to April. Migratory beekeepers had significantly lower Varroa prevalence (84.9 vs. 97.0 %) and loads (3.65 ± 0.28 vs. 5.99 ± 0.22) than stationary operations, while Nosema was more prevalent (59.9 vs. 46.7 %) in migratory colonies. Since 2010, chronic bee paralysis virus prevalence doubled annually. We detected strong positive relationships between V. destructor and Varroa-transmitted viruses, between Nosema and Lake Sinai virus 2, and a positive relationship across several viral pathogens of bees. The results provide a disease baseline to help identify drivers of poor bee health.
THE GERMAN BEE MONITORING PROJECT: A LONG TERM STUDY TO UNDERSTAND PERIODICALLY HIGH WINTER LOSSES OF HONEY BEE COLONIES (2010)
- CONCLUSION: A panel of factors have been analyzed for their role in winter losses of honey bee colonies in Germany. Among all these factors, infestation with Varroa destructor turned out to play the key role. Based on the results presented it is safe to state that Varroa destructor is the dominant killer of honey bee colonies during winter. In addition to high varroa infestation levels, DWV and ABPV infections in autumn significantly lower the winter survival of honey bee colonies as do old queens heading overwintering colonies. That a weak colony has not the best chance to survive the winter is rather trivial but the fact that we observed such winter losses due to colony weakness shows that beekeepers still winter weak colonies. It is safe to assume that these identified factors are not specific for winter losses in Germany but that these results have wider implications.
- Varroa destructor, viral infections, old queens, colony weakness for sure are also responsible for winter losses in many other European regions and may be even in parts of North-America.
Global Honey Bee Viral Landscape Altered by a Parasitic Mite (2012)
- ABSTRACT: Emerging diseases are among the greatest threats to honey bees. Unfortunately, where and when an emerging disease will appear are almost impossible to predict. The arrival of the parasitic Varroa mite into the Hawaiian honey bee population allowed us to investigate changes in the prevalence, load, and strain diversity of honey bee viruses. The mite increased the prevalence of a single viral species, deformed wing virus (DWV), from ~10 to 100% within honey bee populations, which was accompanied by a millionfold increase in viral titer and a massive reduction in DWV diversity, leading to the predominance of a single DWV strain. Therefore, the global spread of Varroa has selected DWV variants that have emerged to allow it to become one of the most widely distributed and contagious insect viruses on the planet.
SPECIES RICHNESS DECLINES AND BIOTIC HOMOGENISATION HAVE SLOWED DOWN FOR NW-EUROPEAN POLLINATORS AND PLANTS (2013)
- CONCLUSION: Europe has some of the world's most intensively managed landscapes, but in recent decades cropland expansion has decelerated and even been partially reversed throughout large parts of the continent (EEA, European Environmental Agency 2012). Moreover, increased public awareness of the consequences of biodiversity loss has led to increased investment in measures to counteract the most negative impacts of industrial pollution (EEA, European Environment Agency 2011), habitat destruction and agricultural intensification (EEA, European Environment Agency 2010). Furthermore, farm payments have led to conversion of cropland into restored conservation or agri-environmental management areas (Kleijn & Sutherland 2003; EEA, European Environment Agency 2010). For such substantial investments to be continued, we need evidence to assess their effectiveness. Our work helps fill that gap.
- While we document declines in species richness and increases in biotic homogenisation in most groups and taxa in the mid 20th century, during earlier periods of accentuated loss of natural habitat (Haines-Young et al. 2003; Van Eetvelde & Antrop 2009; EEA, European Environment Agency 2010; FAO, Food & Agriculture Organization of the United Nations 2012), and of less investment in conservation (Kleijn & Sutherland 2003), we find strong indications that many of these problems have been ameliorated in the most recent two decades since 1990.
- The species assemblages remaining in these countries will likely continue to bear the marks of past declines for a long time; yet they remain diverse and contain considerable numbers of specialist and rare species. Thus, while other drivers may also contribute to the increase in richness in comparatively species-poor regions (e.g. climate), the slowing of rates of biodiversity loss (and particularly of biotic homogenisation) during recent decades constitutes a positive sign indicating that, at least in regions where large land-use changes leading to natural habitat loss have nearly stopped, conservation efforts may be paying off.
NEONICOTINOIDS IN BEES: A REVIEW ON CONCENTRATIONS, SIDE-EFFECTS AND RISK ASSESSMENT (2012)
- ABSTRACT: Neonicotinoid insecticides are successfully applied to control pests in a variety of agricultural crops; however, they may not only affect pest insects but also non-target organisms such as pollinators. This review summarizes, for the first time, 15 years of research on the hazards of neonicotinoids to bees including honey bees, bumble bees and solitary bees. The focus of the paper is on three different key aspects determining the risks of neonicotinoid field concentrations for bee populations: (1) the environmental neonicotinoid residue levels in plants, bees and bee products in relation to pesticide application, (2) the reported side-effects with special attention for sublethal effects, and (3) the usefulness for the evaluation of neonicotinoids of an already existing risk assessment scheme for systemic compounds. Although environmental residue levels of neonicotinoids were found to be lower than acute/chronic toxicity levels, there is still a lack of reliable data as most analyses were conducted near the detection limit and for only few crops.
- Many laboratory studies described lethal and sublethal effects of neonicotinoids on the foraging behavior, and learning and memory abilities of bees, while no effects were observed in field studies at field-realistic dosages. The proposed risk assessment scheme for systemic compounds was shown to be applicable to assess the risk for side-effects of neonicotinoids as it considers the effect on different life stages and different levels of biological organization (organism versus colony). Future research studies should be conducted with field-realistic concentrations, relevant exposure and evaluation durations. Molecular markers may be used to improve risk assessment by a better understanding of the mode of action (interaction with receptors) of neonicotinoids in bees leading to the identification of environmentally safer compounds.
Effect on Pollination
DELIVERY OF CROP POLLINATION SERVICES IS AN INSUFFICIENT ARGUMENT FOR WILD POLLINATOR CONSERVATION (2015)
- ABSTRACT: 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.
EFFECTS OF DECREASES OF ANIMAL POLLINATORS ON HUMAN NUTRITION AND GLOBAL HEALTH: A MODELLING ANALYSIS (2015)
- METHODS: We assembled a database of supplies of 224 types of food in 156 countries. We quantified nutrient composition and pollinator dependence of foods to estimate the size of possible reductions in micronutrient and food intakes for different national populations, while keeping calorie intake constant with replacement by staple foods. We estimated pollinator-decline-dependent changes in micronutrient-deficient populations using population-weighted estimated average requirements and the cutpoint method. We estimated disease burdens of non-communicable, communicable, and malnutrition-related diseases with the Global Burden of Disease 2010 comparative risk assessment framework.
- FINDINGS: Assuming complete removal of pollinators, 71 million (95% uncertainty interval 41–262) people in low-income countries could become newly deficient in vitamin A, and an additional 2·2 billion (1·2–2·5) already consuming below the average requirement would have further declines in vitamin A supplies. Corresponding estimates for folate were 173 million (134–225) and 1·23 billion (1·12–1·33). A 100% decline in pollinator services could reduce global fruit supplies by 22·9% (19·5–26·1), vegetables by 16·3% (15·1–17·7), and nuts and seeds by 22·1% (17·7–26·4), with significant heterogeneity by country. In sum, these dietary changes could increase global deaths yearly from non-communicable and malnutrition-related diseases by 1·42 million (1·38–1·48) and disability-adjusted life-years (DALYs) by 27·0 million (25·8–29·1), an increase of 2·7% for deaths and 1·1% for DALYs. A 50% loss of pollination services would be associated with 700 000 additional annual deaths and 13·2 million DALYs.
- Declines in animal pollinators could cause significant global health burdens from both non-communicable diseases and micronutrient deficiencies.