Robyn M. Underwood

Colony Collapse Disorder: A Descriptive Study

Background Over 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 Findings Of 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/Significance This 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.

A Survey of Honey Bee Colony Losses in the U.S., Fall 2007 to Spring 2008

Background Honey bees are an essential component of modern agriculture. A recently recognized ailment, Colony Collapse Disorder (CCD), devastates colonies, leaving hives with a complete lack of bees, dead or alive. Up to now, estimates of honey bee population decline have not included losses occurring during the wintering period, thus underestimating actual colony mortality. Our survey quantifies the extent of colony losses in the United States over the winter of 2007–2008. Methodology/Principal Findings Surveys were conducted to quantify and identify management factors (e.g. operation size, hive migration) that contribute to high colony losses in general and CCD symptoms in particular. Over 19% of the countrys estimated 2.44 million colonies were surveyed. A total loss of 35.8% of colonies was recorded; an increase of 11.4% compared to last year. Operations that pollinated almonds lost, on average, the same number of colonies as those that did not. The 37.9% of operations that reported having at least some of their colonies die with a complete lack of bees had a total loss of 40.8% of colonies compared to the 17.1% loss reported by beekeepers without this symptom. Large operations were more likely to have this symptom suggesting that a contagious condition may be a causal factor. Sixty percent of all colonies that were reported dead in this survey died without dead bees, and thus possibly suffered from CCD. In PA, losses varied with region, indicating that ambient temperature over winter may be an important factor. Conclusions/Significance Of utmost importance to understanding the recent losses and CCD is keeping track of losses over time and on a large geographic scale. Given that our surveys are representative of the losses across all beekeeping operations, between 0.75 and 1.00 million honey bee colonies are estimated to have died in the United States over the winter of 2007–2008. This article is an extensive survey of U.S. beekeepers across the continent, serving as a reference for comparison with future losses as well as providing guidance to future hypothesis-driven research on the causes of colony mortality.

A survey of honey bee colony losses in the United States, fall 2008 to spring 2009

Summary This study records the third consecutive year of high winter losses in managed honey bee colonies in the USA. Over the winter of 2008–9 an estimated 29% of all US colonies died. Operations which pollinated Californian almond orchards over the survey period had lower average losses than those which did not. Beekeepers consider normal losses to be 17.6%, and 57.9% of all responding beekeepers suffered losses greater than that which they considered to be acceptable. The proportion of operations with the Colony Collapse Disorder (CCD) symptom of “no dead bees in the colony or apiary” decreased in this period as compared to the previous years. The proportion of colonies dying from apparently manageable conditions, however, such as starvation or a weak condition in the fall increased as compared to previous surveys.

Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera

The effect of using acaricides to control varroa mites has long been a concern to the beekeeping industry due to unintended negative impacts on honey bee health. Irregular ontogenesis, suppression of immune defenses, and impairment of normal behavior have been linked to pesticide use. External stressors, including parasites and the pathogens they vector, can confound studies on the effects of pesticides on the metabolism of honey bees. This is the case of Varroa destructor, a mite that negatively affects honey bee health on many levels, from direct parasitism, which diminishes honey bee productivity, to vectoring and/or activating other pathogens, including many viruses. Here we present a gene expression profile comprising genes acting on diverse metabolic levels (detoxification, immunity, and development) in a honey bee population that lacks the influence of varroa mites. We present data for hives treated with five different acaricides; Apiguard (thymol), Apistan (tau-fluvalinate), Checkmite (coumaphos), Miteaway (formic acid) and ApiVar (amitraz). The results indicate that thymol, coumaphos and formic acid are able to alter some metabolic responses. These include detoxification gene expression pathways, components of the immune system responsible for cellular response and the c-Jun amino-terminal kinase (JNK) pathway, and developmental genes. These could potentially interfere with the health of individual honey bees and entire colonies.

A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010

Summary This study records the fourth consecutive year of high winter losses in managed honey bee (Apis mellifera) colonies in the USA. Over the winter of 2009–2010, US beekeepers responding to this survey lost an average of 42.2% of their colonies, for a total loss of 34.4%. Commercial beekeepers (those operating more than 500 colonies) experienced lower total losses as compared to sideline and backyard beekeepers. Similarly, operations that maintained colonies in more than one state and operations that pollinated almond orchards over the survey period had lower total losses than operations either managing colonies in one state exclusively or those not pollinating almonds. On average beekeepers consider acceptable losses to be 14.5%, and 65% of all responding beekeepers suffered losses in excess of what they considered acceptable. The proportion of operations that experienced losses and reported having no dead bees in their colonies or apiaries was comparable to that reported in the winter of 2008–2009. Manageable conditions, such as starvation and a weak condition in the fall were the leading self-identified causes of mortality as reported by all beekeepers. Commercial beekeepers were, however, less likely to list such manageable causes, instead listing poor queens, mites, and pesticides most frequently as the self-identified causes of mortality in their operations.

Standard Epidemiological Methods to Understand and Improve Apis Mellifera Health

Summary In this paper, we describe the use of epidemiological methods to understand and reduce honey bee morbidity and mortality. Essential terms are presented and defined and we also give examples for their use. Defining such terms as disease, population, sensitivity, and specificity, provides a framework for epidemiological comparisons. The term population, in particular, is quite complex for an organism like the honey bee because one can view “epidemiological unit” as individual bees, colonies, apiaries, or operations. The population of interest must, therefore, be clearly defined. Equations and explanations of how to calculate measures of disease rates in a population are provided. There are two types of study design; observational and experimental. The advantages and limitations of both are discussed. Approaches to calculate and interpret results are detailed. Methods for calculating epidemiological measures such as detection of rare events, associating exposure and disease (Odds Ratio and Relative Risk), and comparing prevalence and incidence are discussed. Naturally, for beekeepers, the adoption of any management system must have economic advantage. We present a means to determine the cost and benefit of the treatment in order determine its net benefit. Lastly, this paper presents a discussion of the use of Hills criteria for inferring causal relationships. This framework for judging cause-effect relationships supports a repeatable and quantitative evaluation process at the population or landscape level. Hills criteria disaggregate the different kinds of evidence, allowing the scientist to consider each type of evidence individually and objectively, using a quantitative scoring method for drawing conclusions. It is hoped that the epidemiological approach will be more broadly used to study and negate honey bee disease.

The effects of temperature and dose of formic acid on treatment efficacy against Varroa destructor (Acari: Varroidae), a parasite of Apis mellifera (Hymenoptera: Apidae).

In order to decrease the variability of formic acid treatments against the honey bee parasite the varroa mite, Varroa destructor, it is necessary to determine the dose-time combination that best controls mites without harming bees. The concentration × time (CT) product is a valuable tool for studying fumigants and how they might perform under various environmental conditions. This laboratory study is an assessment of the efficacy of formic acid against the varroa mite under a range of formic acid concentrations and temperatures. The objectives are 1) to determine the effect of temperature and dose of formic acid on worker honey bee and varroa mite survival, 2) to determine the CT50 products for both honey bees and varroa mites and 3) to determine the best temperature and dose to optimize selectivity of formic acid treatment for control of varroa mites. Worker honey bees and varroa mites were fumigated at 0, 0.01, 0.02, 0.04, 0.08, and 0.16 mg/L at 5, 15, 25, and 35 °C for 12 d. Mite and bee mortality were assessed at regular intervals. Both mite and bee survival were affected by formic acid dose. Doses of 0.08 and 0.16 mg/L were effective at killing mites at all temperatures tested above 5 °C. There was a significant interaction between temperature, dose, and species for the CT50 product. The difference between the CT50 product of bees and mites was significant at only a few temperature-dose combinations. CT product values showed that at most temperatures the greatest fumigation efficiency occurred at lower doses of formic acid. However, the best fumigation efficiency and selectivity combination for treatments occurred at a dose of 0.16 mg/L when the temperature was 35 °C.

Short-Term Fumigation of Honey Bee (Hymenoptera: Apidae) Colonies with Formic and Acetic Acids for the Control of Varroa destructor (Acari: Varroidae)

Abstract Controlling populations of varroa mites is crucial for the survival of the beekeeping industry. Many treatments exist, and all are designed to kill mites on adult bees. Because the majority of mites are found under capped brood, most treatments are designed to deliver active ingredients over an extended period to control mites on adult bees, as developing bees and mites emerge. In this study, a 17-h application of 50% formic acid effectively killed mites in capped worker brood and on adult bees without harming queens or uncapped brood. Neither acetic acid nor a combined treatment of formic and acetic acids applied to the West Virginia formic acid fumigator was as effective as formic acid alone in controlling varroa mites. In addition, none of the treatments tested in late summer had an effect on the late-season prevalence of deformed wing virus. The short-term formic acid treatment killed >60% of varroa mites in capped worker brood; thus, it is a promising tool for beekeepers, especially when such treatments are necessary during the nectar flow.

Indoor Winter Fumigation with Formic Acid for Control of Acarapis woodi (Acari: Tarsonemidae) and Nosema Disease, Nosema sp.

ABSTRACT Indoor fumigation of honey bees, Apis mellifera L., with formic acid to control varroa mites, Varroa destructor Anderson & Trueman, allows simultaneous fumigation of multiple colonies with little labor input and good efficacy. Several experiments were designed to test the efficacy of formic acid as a treatment for honey bee mites, Acarapis woodi (Rennie) (Acari: Tarsonemidae), and nosema disease, Nosema sp., indoors in winter. The objectives of this study were 1) to determine the efficacy of formic acid fumigation for honey bee mite control by using both the thoracic slice and live dissection methods and 2) to determine whether indoor fumigation can reliably prevent the buildup of nosema disease in overwintering honey bee colonies. Indoor winter fumigation of honey bee colonies with formic acid was effective in killing a high percentage of honey bee mites but did not significantly reduce the proportion of bees with infested tracheae over the duration of the experiments. Thus, the method used to determine the efficacy of the treatment affected the results. Under conditions of relatively low or decreasing levels of nosema, fumigation tended to suppress the mean abundance of nosema spores relative to the controls. In three separate fumigation experiments using a range of formic acid concentrations, there was no statistical difference between the buildup or maintenance of nosema spore mean abundance over the winter in bees from formic acid fumigated colonies compared with untreated controls. However, fumigation with formic acid during winter at a low concentration for extended periods significantly suppressed spore buildup of mixed populations of nosema (Nosema apis and Nosema ceranae) in 1 yr.

Effects of release pattern and room ventilation on survival of varroa mites and queens during indoor winter fumigation of honey bee colonies with formic acid

This study examined the effects of indoor fumigation with formic acid on survival of honey bee, Apis mellifera L. (Hymenoptera: Apidae), queens and varroa mites (Varroa destructor Anderson and Trueman (Acari: Varroidae)). A relationship between cumulative formic acid concentration and varroa mite mortality was established for colonies subjected to high-concentration fumigation while held indoors at 2–4 °C during winter. We also examined the effects of the formic acid release pattern and room ventilation rate on queen loss and treatment efficacy during fumigation. Two experiments were conducted in a wintering building. In both experiments, room air had higher formic acid concentrations than hive air. In experiment 1, 50% and 95% of mites were killed when exposed to in-hive concentration × time combinations of 49 ppm × days (CT50 product) and 111 ppm × days (CT95 product), respectively. No queen loss was observed under either the increasing- concentration or constant high concentration fumigation pattern. I...