Causes of Colony Collapse Disorder

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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.


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.

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 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.

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.

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.