BackgroundOver the last two winters, there have been large-scale, unexplained losses of managed honey bee (Apis mellifera L.) colonies in the United States. In the absence of a known cause, this syndrome was named Colony Collapse Disorder (CCD) because the main trait was a rapid loss of adult worker bees. We initiated a descriptive epizootiological study in order to better characterize CCD and compare risk factor exposure between populations afflicted by and not afflicted by CCD.Methods and Principal FindingsOf 61 quantified variables (including adult bee physiology, pathogen loads, and pesticide levels), no single measure emerged as a most-likely cause of CCD. Bees in CCD colonies had higher pathogen loads and were co-infected with a greater number of pathogens than control populations, suggesting either an increased exposure to pathogens or a reduced resistance of bees toward pathogens. Levels of the synthetic acaricide coumaphos (used by beekeepers to control the parasitic mite Varroa destructor) were higher in control colonies than CCD-affected colonies.Conclusions/SignificanceThis is the first comprehensive survey of CCD-affected bee populations that suggests CCD involves an interaction between pathogens and other stress factors. We present evidence that this condition is contagious or the result of exposure to a common risk factor. Potentially important areas for future hypothesis-driven research, including the possible legacy effect of mite parasitism and the role of honey bee resistance to pesticides, are highlighted.

Recent losses in honey bee colonies are unusual in their severity, geographical distribution, and, in some cases, failure to present recognized characteristics of known disease. Domesticated honey bees face numerous pests and pathogens, tempting hypotheses that colony collapses arise from exposure to new or resurgent pathogens. Here we explore the incidence and abundance of currently known honey bee pathogens in colonies suffering from Colony Collapse Disorder (CCD), otherwise weak colonies, and strong colonies from across the United States. Although pathogen identities differed between the eastern and western United States, there was a greater incidence and abundance of pathogens in CCD colonies. Pathogen loads were highly covariant in CCD but not control hives, suggesting that CCD colonies rapidly become susceptible to a diverse set of pathogens, or that co-infections can act synergistically to produce the rapid depletion of workers that characterizes the disorder. We also tested workers from a CCD-free apiary to confirm that significant positive correlations among pathogen loads can develop at the level of individual bees and not merely as a secondary effect of CCD. This observation and other recent data highlight pathogen interactions as important components of bee disease. Finally, we used deep RNA sequencing to further characterize microbial diversity in CCD and non-CCD hives. We identified novel strains of the recently described Lake Sinai viruses (LSV) and found evidence of a shift in gut bacterial composition that may be a biomarker of CCD. The results are discussed with respect to host-parasite interactions and other environmental stressors of honey bees.

Multiple mating by social insect queens increases the genetic diversity among colony members, thereby reducing intracolony relatedness and lowering the potential inclusive fitness gains of altruistic workers. Increased genetic diversity may be adaptive, however, by reducing the prevalence of disease within a nest. Honeybees, whose queens have the highest levels of multiple mating among social insects, were investigated to determine whether genetic variation helps to prevent chronic infections. I instrumentally inseminated honeybee queens with semen that was either genetically similar (from one male) or genetically diverse (from multiple males), and then inoculated their colonies with spores of Ascosphaera apis, a fungal pathogen that kills developing brood. I show that genetically diverse colonies had a lower variance in disease prevalence than genetically similar colonies, which suggests that genetic diversity may benefit colonies by preventing severe infections.

Managed honey bee colony losses are of concern in the USA and globally. This survey, which documents the rate of colony loss in the USA during the 2015-2016 season, is the tenth report of winter losses, and the fifth of summer and annual losses. Our results summarize the responses of 5725 valid survey respondents, who collectively managed 427,652 colonies on 1 October 2015, an estimated 16.1% of all managed colonies in the USA. Responding beekeepers reported a total annual colony loss of 40.5% [95% CI 39.8-41.1%] between 1 April 2015 and 1 April 2016. Total winter colony loss was 26.9% [95% CI 26.4-27.4%] while total summer colony loss was 23.6% [95% CI 23.0-24.1%], making this the third consecutive year when summer losses have approximated to winter losses. Across all operation types, 32.3% of responding beekeepers reported no winter losses. Whilst the loss rate in the winter of 2015-2016 was amongst the lowest winter losses recorded over the ten years this survey has been conducted, 59.0% (n = 3378) of responding beekeepers had higher losses than they deemed acceptable. Encuesta nacional 2015-2016 sobre pé rdidas anuales de colonias de la abeja de la miel manejada en los EE.UU Las pérdidas de colonias de abejas manejadas son preocupantes en los Estados Unidos y en el mundo. Esta encuesta, que documenta la tasa de pérdida de colonias en los EE.UU. durante la temporada 2015-2016, es el décimo informe de las pérdidas de invierno, y el quinto de las pérdidas de verano y anuales. Nuestros resultados resumen las respuestas de 5.725 encuestados válidos, quienes colectivamente manejaron 427.652 colonias el 1 de octubre de 2015, un 16.1% de todas las colonias manejadas en los Estados Unidos. Los apicultores respondieron con una pérdida total de colonias anual del 40.5% [IC del 95%: 39.8-41.1%] entre el 1 de abril de 2015 y el 1 de abril de 2016. La pérdida total de colonias de invierno fue del 26.9% [IC del 95%: 26.4-27.4%], y las de verano del 23.6% [IC del 95%: 23.0-24.1%], lo que lo convierte en el tercer año consecutivo en que las pérdidas del verano se han aproximado a las pérdidas de invierno. En todos los tipos de operaciones, el 32.3% de los apicultores que respondieron no reportaron pérdidas de invierno. Mientras que la tasa de pérdidas en el invierno de 2015-2016 fue una de las pérdidas de invierno más bajas registradas durante los diez años que se han realizado esta encuesta, el 59.0% (n = 3.378) de los apicultores que respondieron tuvieron mayores pérdidas de las que consideraban aceptables.

This study measured part of the in-hive pesticide exposome by analyzing residues from live in-hive bees, stored pollen, and wax in migratory colonies over time and compared exposure to colony health. We summarized the pesticide burden using three different additive methods: (1) the hazard quotient (HQ), an estimate of pesticide exposure risk, (2) the total number of pesticide residues, and (3) the number of relevant residues. Despite being simplistic, these models attempt to summarize potential risk from multiple contaminations in real-world contexts. Colonies performing pollination services were subject to increased pesticide exposure compared to honey-production and holding yards. We found clear links between an increase in the total number of products in wax and colony mortality. In particular, we found that fungicides with particular modes of action increased disproportionally in wax within colonies that died. The occurrence of queen events, a significant risk factor for colony health and productivity, was positively associated with all three proxies of pesticide exposure. While our exposome summation models do not fully capture the complexities of pesticide exposure, they nonetheless help elucidate their risks to colony health. Implementing and improving such models can help identify potential pesticide risks, permitting preventative actions to improve pollinator health.