Since 2006 the rate of honey bee colony failure has increased significantly. As an aid to testing hypotheses for the causes of colony failure we have developed a compartment model of honey bee colony population dynamics to explore the impact of different death rates of forager bees on colony growth and development. The model predicts a critical threshold forager death rate beneath which colonies regulate a stable population size. If death rates are sustained higher than this threshold rapid population decline is predicted and colony failure is inevitable. The model also predicts that high forager death rates draw hive bees into the foraging population at much younger ages than normal, which acts to accelerate colony failure. The model suggests that colony failure can be understood in terms of observed principles of honey bee population dynamics, and provides a theoretical framework for experimental investigation of the problem.
Citation: Khoury DS, Myerscough MR, Barron AB (2011) A Quantitative Model of Honey Bee Colony Population Dynamics. PLoS ONE 6(4): e18491. https://doi.org/10.1371/journal.pone.0018491
Editor: James A. R. Marshall, University of Sheffield, United Kingdom
Received: September 27, 2010; Accepted: March 9, 2011; Published: April 18, 2011
Copyright: © 2011 Khoury et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by The School of Mathematics and Statistics, The University of Sydney. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
A honey bee colony is a population of related and closely interacting individuals that form a highly complex society. The population dynamics of this group is complicated, because the fates of individuals within it are not independent, and an individual's lifespan is strongly influenced by their role in the colony. To aid exploration of honey bee population dynamics here we describe a simple mathematical representation of how the social regulation of worker division of labour can influence the longevity of individual bees, and colony growth. The model also allows simulation of how demographic disturbances can impact colony growth, or contribute to colony failure.
The life cycle of individual bees in the hive is well understood. Worker bees enter the population from eggs laid by the queen, and the existing population of workers raise a proportion of these eggs to adulthood . It takes three weeks for worker bees to develop from eggs to adults , but their lifespan as adults is strongly influenced by their behavioural role in the colony. Survival of bees in the protected hive environment is high, but the survival of forager bees is much lower . The average foraging life of a bee has been estimated as less than seven days, because of the many risks and severe metabolic costs associated with foraging . As a consequence of this it might be expected that a bee's overall lifespan would be strongly influenced by the age at which she commenced foraging.
The division of labour among worker bees in a colony is age dependent: typically young adults work within the hive on colony maintenance tasks and brood care (nursing), but change to foraging tasks when they are older , . This process of behavioural development is sensitive to social feedback. If there is a decline in the number of foragers, hive bees accelerate their behavioural development and begin foraging precociously to compensate , . Similarly, if there is a surfeit of foragers and a lack of nurses, bees can reverse their behavioural development and switch back from foraging to nursing roles , . The pheromonal mechanism mediating this ‘social inhibition’ of foraging has been identified . Old forager bees transfer ethyl oleate to young hive bees via trophallaxis, which delays the age at which they begin foraging .
As a consequence of this social regulation of division of labour, one would predict an interaction between the composition of the colony workforce, and longevity of individual bees. If social inhibition is reduced and bees initiate foraging when young they would be expected to have an overall reduced lifespan (since foraging is associated with such high mortality), and therefore have less time to contribute to colony growth. Here we present a simple mathematical model that allows a formal exploration of how a loss of foragers and reduced social inhibition might impact colony growth.
This issue is salient because of the current concern over globally declining bee populations. Since 2006 beekeepers worldwide have reported elevated rates of colony losses , , . Since 2006 the average overwinter loss of honey bee colonies in the United States has exceeded 30% consistently , and elevated colony losses have been reported across Europe, the Middle East and Japan . The impact of the parasitic mite Varroa destructor is certainly a major factor behind the global increase in colony failure rates , , , , but other stressors include various bee diseases (but especially Nosema sp.), changes in bee management practice , factors related to climate change and seasonal shifts  and pesticide exposure , , , , . These have all been linked to colony failure.
Extreme cases of mysterious mass colony death where there is no clear causal agent have become known as colony collapse disorder, or CCD . Diagnostic of this syndrome are vacant hives containing dead brood and food stores but few or no adult bees, suggesting very rapid catastrophic depopulation . Surveys of pathogens associated with colony collapse events have identified many disease organisms present , , , , and several newly described bee pathogens have been linked with CCD , , but at the time of writing no definite single agent has been identified as the cause of CCD. The current prevailing opinion is that colony collapse is not a result of a single new causal factor . The problem is considered multicausal and may reflect the outcome of an accumulation of stressors on a honey bee colony , .
CCD has focused attention on the problem of colony failure, and the many stressors now impacting colony survival. It is clear that while an enormous amount is know about honey bee sociobiology, comparatively little is know about the social responses of bees to population stresses on a colony. The presented model explores how varying the rate of forager bee mortality might impact colony growth, which may be a useful tool to aid research into the complex problem of colony failure.
Materials and Methods
Constructing a demographic model to explore the process of colony failure: the hypothesis
We hypothesise that colony failure occurs when the death rate of bees in the colony is unsustainable. At this point normal social dynamics break down, it becomes impossible for the colony to maintain a viable population, and the colony will fail.
We hypothesise that any factor that causes an elevated forager death rate will reduce the strength of social inhibition, resulting in a precocious onset of foraging behaviour in young bees . Because foraging is high-risk , precocious foraging shortens overall bee lifespan. Precocious foragers are also less effective and weaker than foragers that have made the behavioural transition at the normal age , . Consequently, as the mean age of the foraging force decreases forager death rates increase further, which accelerates the population decline. A precocious onset of foraging reduces the population of hive bees engaged in brood care. This reduces colony brood rearing capacity, and the population crashes. A similar hypothesis has been proposed to explain the impact of Nosema ceranae on colonies , but we argue this hypothesis is applicable to any factor that chronically elevates forager bee death rates. We explore this hypothesis using the following simple mathematical model.
A mathematical model allows us to explore the effects of different factors and forces on the population of the hive in a quantitative way. Such a model has the potential to make predictions for the outcome of various manipulations, and to allow a preliminary exploration of the problem before investing in experimental work.
We construct a simple compartment model for the worker bee population of the hive (Fig. 1). Our model only considers the population of female workers since males (drones) do not contribute to colony work. Let H be the number of bees working in the hive and F the number of bees who work outside the hive, referred to here as foragers. We assume that all adult worker bees can be classed either as hive bees or as foragers, and that there is no overlap between these two behavioural classes , . Hence the total number of adult worker bees in the colony is N = H+F.
Figure 1. Elements of honey bee social dynamics considered by our model.
Eggs laid by the queen are reared as brood that eclose three weeks later as adult bees. Adult bees work in the hive initially before becoming foragers. Our model considers the death rate of adult bees within the hive to be negligible, but forager death rate is a parameter varied in our simulations. We assume the amount of brood reared is influenced by the size of the colony (number of hive and forager bees) and that the rate at which bees transition from hive bees to forager bees is influenced by the number of foragers to represent the effect of social inhibition.
Our model does not consider the impact of brood diseases on colony failure, however we believe our approach is still useful because many cases of colony failure and CCD are not caused by brood diseases , , . Hive bees eclose from pupae and mature into foragers. Death rates of adult hive bees in a healthy colony are extremely low as the environment is protected and stable. We assume that the death rate of hive bees is negligible. Workers are recruited to the forager class from the hive bee class and die at a rate m. Let t be the time measured in days. Then we can represent this process as a differential equation model:(1)(2)The function E(H,F) describes the way that eclosion depends on the number of hive bees and foragers. The recruitment rate function R(H,F) models the effect of social inhibition on the recruitment rate.
It is known that the number of eggs reared in a colony (and hence the eclosion rate) is related to the number of bees in the hive. Big colonies raise more brood , , . The nature of this dependence is not known, however. We assume that the maximum rate of eclosion is equivalent to the queen's laying rate L and that the eclosion rate approaches this maximum as N (the number of workers in the hive) increases. In the absence of other information we use the simplest function that increases from zero for no workers and tends to L as N becomes very large:(3)Here w determines the rate at which E(H,F) approaches L as N gets large. Figure 2 shows E(H,F) as a function of N for a range of values of w.
Figure 2. Plot of the eclosion function E(h,F) = LN/(w+N) where N = H+F for different values of w.
The solid line has w = 4000; the dashed line, w = 10 000 and the dash-dot line, w = 27 000.
We write the recruitment function as(4)The first term represents the maximum rate that hive bees will become foragers when there are no foragers present in the colony. The second term represents social inhibition and, in particular, how the presence of foragers reduces the rate of recruitment of hive bees to foragers. We have assumed that social inhibition is directly proportional to the fraction of the total number of adult bees that are foragers, such that a high fraction of foragers in the hive results in low recruitment. In the absence of any foragers new workers will become foragers at a minimum of four days after eclosing , so an appropriate choice for the rate of uninhibited transition to foraging is = 0.25. We chose = 0.75 since this factor implies that a reversion of foragers to hive bees would only occur if more than one third of the hive are foragers. We also chose L = 2000 as the daily laying rate of the queen  and w = 27,000.
Analysis of the model
The equations (1) and (2) with the functions (3) and (4) were analysed using standard linear stability analysis and phase plane analysis .
The model has a globally stable steady state (H0,F0) where(5)when(6)Otherwise the state with no adult bees is an attractor and the hive population goes to zero.
Figure 3 shows phase plane solutions for a low death rate, m = 0.24, when the populations tend to a positive steady state, and a higher death rate m = 0.40, when the population goes extinct. In each case the solution rapidly approaches the line F = JH so that the ratio of hive bee numbers to forager numbers is close to being constant. The population size adjusts more slowly to either a positive steady state or to zero. Figure 4 shows the decline of a doomed population as a function of time (dotted line). If the foragers become less able and more likely to die as they get younger then the decline will be more rapid (solid line).
Figure 3. Phase plane diagrams of solutions to the model for different values of m.
Each line on the diagrams represents a solution trajectory, giving the number of foragers F and the number of hive bees H. As time t increases the solutions change along the trajectory in the direction of the arrows. In (a) m = 0.24 and the populations tend to a stable equilibrium population, marked by a dot. In (b), m = 0.40 there is no nonzero equilibrium and the hive populations collapses to zero. Parameter values are L = 2000, = 0.25, = 0.75 and w = 27 000.
Figure 4. The effect of inefficient precocious foraging on population decline.
This plot shows the time course of colony decline when all foragers perform equally well (dashed line) and when precocious foragers die faster than mature foragers (solid line). The effect of precocious foraging is modeled by replacing the death rate m by m = ml R2/(2+R2) whenever R<0 where R is the recruitment rate of foragers given in eqn (4). Parameter values are L = 2000, = 0.25, = .75, w = 27 000, ml = 0.6 and 2 = 0.059.
Figure 5 is a bifurcation diagram, which shows that for low values of the forager death rate m there are large numbers of bees in the colony, but once m passes a critical value the colony population cannot support itself and the colony fails.
Figure 5. The dependence of the colony population at equilibrium on the death rate of foragers.
For this set of parameter values, when the death rate m exceeds 0.355, the only stable equilibrium population is zero. Parameter values are the same as Figure 3.
Figure 6 shows how the average age at commencement of foraging and the average age at death depend on the forager death rate m. The model predicts that at a higher death rate the forager population will be smaller and also made up of younger bees.
We compared results from the model to experimental observations of Rueppell et al . We used the observed flightspan [the number of days bees were observed foraging 33], to estimate the death rate of foragers since m is the reciprocal of flightspan. With these values of m we used the model to calculate the average age of onset of foraging (AAOF) and the lifespan of worker bees for each colony and compared these model values to observed results. These observed and calculated results are shown in Table 1. Even with the somewhat rough estimates of parameters, the model matches the observational data well for average age at onset of foraging, although it is slightly high for worker lifespan. Nevertheless, given that the model is a very simple representation of honey bee demographics, the results are encouraging.
Results and Discussion
Our model clarifies how forager death rate influences colony population, and suggests that very rapid population decline can result from chronically high forager death rates. The model emphasizes the role social feedback mechanisms within the honey bee colony may play in colony failure, and suggests that colony failure can be explored as both a sociobiological as well as an epidemiological question.
The model proposes a bifurcation point in the death rate parameter such that when death rate is below a critical threshold, colony population reaches an equilibrium point determined by model parameters, but when forager death rate is sustained above the threshold, colony population declines to zero and the colony fails. This bifurcation point represents the point at which the colony cannot maintain brood production at a rate sufficient to replace losses of forager bees in the field. The model suggests that if a high forager death rate is sustained, colony population decline can be rapid (Fig. 4) since the social consequences of high forager losses accelerate colony failure. When forager death rate is high, nurse bees begin foraging precociously (Fig. 6). While this restores the proportion of foragers in the population, it shortens the overall lifespan of adult bees (Fig. 6) and reduces the time each bee can contribute to colony growth and brood production. This reduces the brood-rearing capacity of the colony. Since precocious foragers are less effective and resilient than normal foragers ,  forager death rate increases further, the pressure on colony population is compounded and the rate of colony decline is increased (Fig. 4).
In our simulations the bifurcation point was m = 0.355 which would imply that if the average duration of bees' foraging lives is reduced to just 2.8 days of foraging, and if this population stress is sustained colonies are likely to fail. In healthy colonies bees survive about 6.5 days of foraging on average , therefore our model predicts that chronic stressors that reduce the forager survival by approximately two thirds will place a colony at risk. Exploration of the model suggested that a high forager death rate in isolation would not cause colony failure, rather colony failure is caused by the social consequences resulting from a high forager death rate driving a decline in brood rearing alongside sustained forager losses.
The importance of forager longevity for equilibrium colony size has also been recognised by earlier modeling approaches , , but the function of these earlier models was to simulate patterns of growth observed in real colonies, whereas the modeling approach that we use here is a more abstract representation of colony population dynamics and its purpose is to explore why forager death rate has such a strong influence on population size.
The model that we present here is very simple and focuses on the effect of varying forager death rate on brood and adult bee population dynamics. We have also constructed and explored more complicated models which include, for example, the effects of stored food in the hive and the effects of the presence of brood on bee behaviour, but we found that this leaner model was the most revealing and conceptually useful. The aim of this model is simply to provide a basic theoretical understanding of colony dynamics in an idealised state. We have not considered seasonal and climatic variation in queen egg laying rate and forager mortality rate, but these elements could be incorporated as elaborations of the basic model.
Does the current simplistic model usefully represent colony social dynamics and the process of colony failure? In some ways, simulations from the model effectively mimic the performance of natural colonies. The model predicts that from any initial starting population of hive bees and foragers, colonies move towards an equilibrium point by rapidly establishing a stable and consistent proportion of nurses and foragers (Fig. 3) while the total population size adjusts more slowly until the equilibrium point is reached. These simulations reflect experimental observations . Colonies constructed with either no foragers, or 100% foragers rapidly adjusted the proportions of foragers and hive bees to values closer to those seen in normal hives , , . When colonies are experimentally depleted of foragers they rapidly restore the ratio of hive bees to forager bees by accelerating the behavioural development of hive bees , but adjustments in colony size occurred more slowly. The model also predicted worker age at onset of foraging and lifespans that were a reasonable match to observed experimental data (Table 1).
While the current model suggests how social processes might contribute to colony failure, in its current form the model does not capture all features associated with the very dramatic colony failure observed in cases of CCD. Rapid population decline is one key characteristic of CCD. The rate of decline is not precisely defined  and may vary between cases, but the amount of abandoned brood found in CCD colonies suggests a very large drop in population within a few weeks . The model predicts rapid initial declines in colony population (Fig. 4), but the current model does not effectively represent the absolute colony abandonment, which is also diagnostic of CCD . Our simulations take about 200 days to reach close to zero population (Fig. 4). The current model does not consider factors that might accelerate the terminal decline of a honey bee colony once the population becomes small. Colonies with small populations are not able to thermoregulate effectively, which will weaken or kill developing brood , . Stressed colonies will cannibalise developing larvae , which will further reduce brood production and accelerate colony failure. Stressed colonies will sometimes abscond when the remaining bees and the queen leave the hive box altogether. It seems likely that population decline will accelerate once colony population becomes small, but this process has not been well studied experimentally.
One of the mysterious aspects of CCD is the abandonment of brood by adult bees . Our model suggests that this may occur because as populations dwindle, bees make the transition from hive bees to become foragers. Whether this extreme failure of division of labour would occur in natural colonies is not known, but experimental evidence has shown that the response of bees to various stressors is to change behaviour from brood care to foraging , . This suggests that when bees are starving or diseased or face other factors that shorten their individual lifespan, the motivation to forage overrides the motivation to attend to brood. In CCD cases the amount of brood left abandoned would suggest that this total collapse of normal division of labour must occur quite rapidly. Rigorous experimental observation of this process is needed urgently to understand how CCD compares to less dramatic cases of colony failure.
The model that we have presented focuses attention on forager death rate and the social consequences of this as a driver of colony failure. If brood production and the eclosion rate are too low to support a sustained level of forager losses then a colony will fail. One inference from this understanding is that factors that affect the survival of both brood and adult bees could leave colonies particularly vulnerable to collapse. Examples of such factors would be the mite Varroa destructor, which affects both brood and forager survival ,  and Nosema infections , both of which are known causes of colony failure , , . The model also predicts that treatment strategies to restore failing colonies should focus on preventing precocious foraging to extend the useful lifespan of adult bees in the colony, and boosting brood production to restore the colony to a point at which recruitment into the population is sufficient to sustain ongoing forager losses.
Experimental testing of the model predictions will hopefully yield a better understanding of the process of catastrophic colony failure, and how best to intervene to restore failing colonies.
Conceived and designed the experiments: ABB MRM DSK. Performed the experiments: DSK. Analyzed the data: DSK. Contributed reagents/materials/analysis tools: MRM. Wrote the paper: ABB MRM.
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ARS Honey Bee Health and Colony Collapse Disorder
Honey bees are a critical link in U.S. agricultural production. Pollination by managed honey bee colonies adds at least $15 billion to the value of U.S. agriculture annually through increased yields and superior-quality harvests. But managed honey bees have come under serious pressures from many different stresses, which has resulted in beekeepers losing many colonies.
One problem plaguing honey bees since 2006 has been Colony Collapse Disorder (CCD), which is a syndrome specifically defined as a dead colony with no adult bees and with no dead bee bodies but with a live queen, and usually honey and immature bees, still present. CCD is not a general term that covers all managed honey bee colonies that are lost due to any reason. No scientific cause for CCD has been proven. Most research has pointed to a complex of factors being involved in the cause of CCD, and possibly not all of the same factors or the same factors in the same order are involved in all CCD incidents.
But CCD is far from the only major threat to the health of honey bees and the economic stability of commercial beekeeping in the United States. In fact, the number of managed colonies that beekeepers have reported losing specifically from CCD has been waning since 2010. But the beekeeping industry continues to report losing a high percentage of their colonies each year to other causes.
Major factors threatening honey bee health can be divided into four general areas: parasites and pests, pathogens, poor nutrition, and sublethal exposure to pesticides. In reality though, these factors tend to overlap and interact with one another, which complicates issues. In addition, there are other issues that have impacts on honey bee health such as the narrow genetic base of honey bees in the United States.
The Agricultural Research Service (ARS), USDA's in-house scientific research agency, is striving to enhance overall honey bee health and improve bee management practices by studying honey bee diseases and parasites and how best to control them, as well as basic honey bee biology and genetics. ARS scientists also are working on projects as diverse as studying the biological interaction of simultaneous exposure to sublethal amounts of pesticides and infection by nosema fungi to long-term storage of honey bee semen to preserve genetic resources. In addition, ARS researchers are cooperating with other Federal agencies and State departments of agriculture, universities, and private companies in a variety of projects to improve honey bee health.
Why Should the Public Care About What Happens to Honey Bees?
About one mouthful in three in our diet directly or indirectly benefits from honey bee pollination. Commercial production of many high-value and specialty crops like almonds and other tree nuts, berries, fruits and vegetables depend on pollination by honey bees. These are the foods that give our diet diversity, color, and flavor.
Honey bees are not native to the New World; they were brought here from Europe in the 1500s and 1600s by colonists. But many of our crops also came from the Old World and evolved in the same places as honey bees. There are native pollinators in the United States, but honey bees are more prolific and easier to manage, especially on a commercial level for pollination of a wide variety of crops. Almonds, for example, are almost completely dependent on honey bees for pollination. In California, the almond industry makes use of almost three-quarter of all managed honey bee colonies in the United States, brought from all over the country during one short window of time in January and February each year.
Honey Bee Health Problems
Parasites and pests: Varroa mites (Varroa destructor) are essentially a modern honey bee plague. The Varroa mite has been responsible for the deaths of massive numbers of honey bee colonies since its arrival in the United States in 1987. A native of Asia, Varroa normally parasitizes the Asian honey bee, Apis cerana, which is a different species from the European or western honey bee, Apis mellifera, on which this country primarily depends for crop pollination.
Varroa mites directly damage honey bees by attaching and sucking the bees’ equivalent of blood (hemolymph fluid) somewhat like ticks. They also indirectly damage honey bees because, similarly to mosquitos, Varroa mites also transmit an array of pathogenic viruses to honey bees such as deformed wing virus.•
Beekeepers have identified Varroa mites as their single most serious problem causing colony losses today.
Small hive beetles, native to sub-Saharan Africa, were first found in the United States in 1996 and had spread to 30 States by 2014. Large beetle populations are able to lay enormous numbers of eggs. These eggs develop quickly and result in rapid destruction of unprotected combs in a short time. If large populations of beetles are allowed to build up, even strong colonies can be overwhelmed in a short time.
Wax moths arrived in the United States in 1998 in Florida. This can be a very destructive insect pest, damaging beeswax comb, comb honey, and bee-collected pollen. Wax moths are rarely the initial cause of colony failure but can overcome weak colonies.
Pathogens: Since the 1980s, many new exotic pathogens that infect honey bees have been found in this country. These include deformed wing virus, paralytic viruses such as Israeli acute paralysis virus, which was first found in 2004, European foulbrood bacteria, and Nosema ceranae fungi, which arrived in 2005. They have all become major problems for U.S. honey bees and beekeepers.
Poor nutrition: Honey bees’ natural diet comes primarily from nectar and pollen gathered from a wide variety of flowers. Insufficient or incomplete nutrition has come to be recognized as an essential factor that weakens the honey bee’s immune systems and is likely to make bees more susceptible to all of the other problems troubling them today.
As demand for pollination services grows, bee colonies often are kept for more time on sites in a mono-crop environment before being moved directly to the next mono-crop area. As more and more land is lost to urbanization and suburbanization, it also means a loss of habitat with a diverse mix of nutritious bee forage plants. In addition, when it comes to helping bee colonies survive the winter and droughts, both times when nectar supplies can be scarce for bees, beekeepers often provide an artificial diet. Scientists are still trying to perfectly duplicate a bee’s natural pollen/nectar diet for those times of the year when good forage is not available.
Pesticides: The U.S. Environmental Protection Agency (EPA) has strict regulations to protect managed honey bee colonies form incidents of pesticide misuse in formulation or application. Tips and complaints alleging pesticide-related bee incidents may be reported to State or tribal authorities or directly to the EPA Office of Pesticide Programs, firstname.lastname@example.org, National Pesticide Information Center: http://pi.ace.orst.edu/erep/ or https://www.epa.gov/compliance/guidance-inspecting-alleged-cases-pesticide-related-bee-incidents.
Sublethal pesticide effects: A survey of honey bee colonies conducted in 2010 by ARS researchers looked at 170 pesticides or their residues in honey bees, beeswax, and pollen. The data showed no consistent pattern of pesticide that differed between healthy and CCD-affected colonies. The most commonly found pesticide in the study was coumaphos, which is used by beekeepers to treat honey bees for Varroa mites.
The pesticide class neonicotinoids (for example, clothianidin, thiamethoxam, and imidacloprid) has been accused of damaging or killing honey bees or being the cause of CCD even when the exposure is below the level expected to be toxic. The nicotine-based neonicotinoids were developed in the mid-1990s in large part because they showed reduced toxicity to wildlife compared with previously used organophosphate and carbamate insecticides.
The scientific data about the impact of pesticides and neonicotinoids in particular at environmentally and agriculturally realistic levels is mixed. Some findings have shown that neonicotinoids have sublethal effects on honey bees at or below approved doses and exposures. Documenting such sublethal effects is very difficult due to the many factors that can influence individual situations in field studies and during grower use including timing of use, health and nutritional state of the bees, total mix of pesticides, pathogens and parasites present, crop type, weather during the growing season, and accumulation of pesticides from year to year. Other studies have indicated that healthy colonies appear not to be impacted.•
While these four areas are easy to categorize on paper, in reality these factors often may overlap or interact with one another. Honey bees might be able to survive many of these problems if the problems occurred one at a time. But when they hit in any of a wide variety of combinations, the result can weaken and overcome the honey bee colony’s ability to survive.
ARS Research Directions
ARS is focused on directly improving the health of managed honey bees by finding ways to mitigate the impacts of pathogens, pests, and pesticides and enhancing bee nutrition and management. Agency scientists are also working on projects that take a bigger-picture view toward helping honey bees. This includes developing better knowledge about areas such as gut microbes and their interactions with honey bee immune systems, preservation and expansion of honey bee genetic diversity, and evaluating the effect of land management practices on bees to assure better productivity of pollinators.
For more information about ARS honey bee research programs, see ARS National Program #305 Action Plan [2013-2018]
ARS News about Honey Bees
Bacterial Imbalances Can Mean Bad News for Honey Bees
ARS Research Leads to Better Understanding of Bee Health August 2, 2016
USDA Scientists and Beekeepers Swap Colonies to Better Bees June 21, 2016
Bees Abuzz Over Rapini February 17, 2016
USDA Research Identifies Factors for Faster Commercial Honey Bee Queen Failure February 10, 2016
New ARS Bee Genebank Will Preserve Genetic Diversity and Provide Breeding Resources January 26, 2016
Camelina Cover Crops a Boon for Bees November 19, 2015
Newly Named Bacteria Help Honey Bee Larvae Thrive May 6, 2015
Research Shows Honey Bee Diseases Can Strike in All Seasons February 5, 2015
Colony Collapse Disorder: An Incomplete Puzzle
Agricultural Research magazine July 2012
Colony Collapse Disorder: A Complex Buzz
Agricultural Research magazine May/June 2008
Pathogen Loads Higher in Bee Colonies Suffering from Colony Collapse Disorder August 12 , 2009
Honey Bees with Colony Collapse Disorder Show their Genes August 24, 2009
Still Seeking a Cause of Colony Collapse Disorder May 5, 2008
Imported Bees Not Source of Virus Associated with Colony Collapse Disorder November 19, 2007
Genetic Survey Finds Association Between CCD and Virus September 6, 2007
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Best Recommendation for Beekeepers
Since little is known for sure about the cause(s) of CCD, mitigation must be based on improving general honey bee health and habitat and countering known mortality factors by using best management practices. This includes supplemental feeding in times of nectar/pollen scarcity.
Best Recommendations for the Public
The best action the public can take to improve honey bee survival is not to use pesticides indiscriminately. In particular, the public should avoid applying pesticides during mid-day hours, when honey bees are most likely to be out foraging for nectar and pollen on flowering plants.
In addition, the public can plant pollinator-friendly plants-plants that are good sources of nectar and pollen such as red clover, foxglove, bee balm, joe-pye weed, and other plants. (For more information, visit www.nappc.org.)
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Recent ARS Honey Bee Scientific Publications
Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator, New Phytologist, September 2017
Limited impacts of truck-based ultra-low-volume applications of mosquito adulticides on mortality in honey bees (Apis mellifera), Bulletin of Entomological Research, April 2017
Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites, Bee World, April 2017
Sublethal Effects of Imidacloprid on Honey Bee Colony Growth and Activity at Three Sites in the U.S., PLoS One, December 2016
Honey bee gut microbial communities are robust to the fungicide Pristine® consumed in pollen, Apidologie, Nov 2016
Transcriptomic and functional resources for the Small Hive Beetle Aethina tumida, a worldwide parasite of honey bees, Genomics Data, September 2016
Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide Imidacloprid and the organophosphate Acaricide Coumaphos, Journal of Insect Physiology, June 2016
Parasaccharibacter apium, gen. nov., sp. nov., Improves Honey Bee (Hymenoptera: Apidae) Resistance to Nosema, Journal of Economical Entomology, February 2016
Multiyear survey targeting disease incidence in US honey bees, Apidologie, May 2016
The effects of Imidacloprid and Varroa destructor on the survival and health of European honey bees, Apis mellifera,Insect Science, May 2016
Population growth of Varroa destructor (Acari: Varroidae) in honey bee colonies is affected by the number of foragers with mites, Experimental and Applied Acarology, May 2016
The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions, MBio, April 2016
Colony failure linked to low sperm viability in honey bee (Apis mellifera) queens and an exploration of potential causative factors, PLoS One, February 2016
Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements, Apidologie, August 2015
Prevalence and reproduction of Tropilaelaps mercedesae and Varroa destructor in concurrently infested Apis mellifera colonies, Apidologie, May 2015
Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health and Colony Collapse Disorder (CCD), PLoS Pathogens, July 2014
Functionality of Varroa-Resistant Honey Bees (Hymenoptera: Apidae) When Used for Western U.S. Honey Production and Almond Pollination, Journal of Economic Entomology, April 2014
The microbial communities associated with honey bee (Apis mellifera) foragers, PLoS One, March 2014
Finding the missing honey bee genes: lessons learned from a genome upgrade, BMC Genomics, January 2014
Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae, PLoS One, July 2013
Pathogen webs in collapsing honey bee colonies, PLoS One, August 2012
Pesticide exposure in honey bees results in increased levels of the gut pathogen, Naturwissenschaften, February 2012
Predictive markers of honey bee colony collapse, PLoS One, February 2012
Coordinated responses to honey bee decline in the USA, Apidologie, May-June 2010
High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health, PLoS One, March 2010
Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis, Journal of Economic Entomology, October 2010
Changes in gene expression relating to colony collapse disorder in honey bees, Apis mellifera, Proceedings of the National Academy of Sciences, October 2009
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ARS Honey Bee Research Laboratories
U.S. Honey Bee Losses
The total number of managed honey bee colonies has decreased from 5 million in the 1940s to about 2.66 million today, according to a USDA-National Agricultural Statistics Service (NASS) survey. There are many factors that may have contributed to this long-term slide, a number of them economic or cultural through the 1980s. These may have included a drop in the number of farms, especially small farms after World War II, accompanied by increasing opportunities for off-farm jobs for farm wives who often sold honey and honey products. In addition, drops in prices of honey started the downward slide in the number of colonies. In the late 1980s, the onset of Varroa mites and other bee health issues played a role in another drop in numbers of managed colonies. Typical average annual losses jumped to about 15-22 percent of managed colonies.
When Colony Collapse Disorder (CCD) began to be reported in 2006/2007, annual losses of honey bee colonies rose again. CCD has since waned, but high losses have continued, averaging about 30 percent. It is not known if this is because beekeepers are better at ascribing losses to particular causes, if causes have shifted, or if other factors have changed.
There has been a recent increase in the overall total number of managed honey bee colonies. This is being driven mostly by an increasing demand for almond pollination, which is tightly clustered in just a few weeks in late January and early February. California almond acreage grew to 1,020,000 in 2014, up 5 percent from 2013. In 2010, it was 810,000 acres - a 2 percent increase from 2008’s 795,000 acres. Almond growers are the largest single users of honey bee pollination and need the colonies all in a short period of time.
To meet the increasing demand, beekeepers are splitting hives and buying more queens to create more colonies, which ends up with greater total numbers of colonies. But they are still losing higher percentages of their colonies now than they were 10 years ago before CCD and all the other bee health problems surfaced. The two numbers are different measures: total colonies vs. percent loss.
Survey Reports Latest Honey Bee Losses
For honey bee colony loss survey results after 2015, please go to USDA/NASS
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In October 2006, some beekeepers began reporting losses of 30-90 percent of their hives. While colony losses are not unexpected, especially over the winter, this magnitude of losses was unusually high.
The main symptom of CCD is very low or no adult honey bees present in the hive but with a live queen and no dead honey bee bodies present. Often there is still honey in the hive, and immature bees (brood) are present. Varroa mites, a virus-transmitting parasite of honey bees, have frequently been found in hives hit by CCD.
This is not the first time that beekeepers are being faced with unexplained losses. The scientific literature has several mentions of honey bee disappearances-in the 1880s, the 1920s, and the 1960s. While the descriptions sound similar to CCD, there is no way to know for sure if those problems were caused by the same agents as CCD.
There have also been unusual colony losses before. In 1903, in the Cache Valley in Utah, 2000 colonies were lost to an unknown "disappearing disease" after a "hard winter and a cold spring." More recently, in 1995-96, Pennsylvania beekeepers lost 53 percent of their colonies without a specific identifiable cause.
In June 2007, ARS and the National Institute of Food and Agriculture (NIFA), USDA's extramural research grants agency, co-chaired a workshop of scientists and stakeholders to develop a Colony Collapse Disorder Action Plan. This plan identified areas where more information was needed and developed a research priority list for additional research projects related to finding the cause/causes of CCD.
Cell Phones and CCD
Despite a great deal of attention having been paid to the idea, neither cell phones nor cell phone towers have been shown to have any connection to CCD or poor honey bee health.
Originally, the idea was provoked by the media making a connection between CCD and a very small study done in Germany. But that study looked at whether a particular type of base station for cordless phones could affect honey bee homing systems. However, despite all the attention that this study has received, the base station has nothing to do with CCD. Stefan Kimmel, the researcher who conducted the study and wrote the paper, e-mailed The Associated Press to say that there is "no link between our tiny little study and the CCD-phenomenon ... Anything else said or written is a lie."
In addition, apiaries are often located in rural areas, where cell phone coverage can be spotty. This makes cell phones or cell towers unlikely culprits.
In addition, apiaries are often located in rural areas, where cell phone coverage can be spotty. This makes cell phones or cell towers unlikely culprits.
Research from ARS and other institutions has provided new management recommendations that beekeepers have begun to adopt. For example, it is now recommended that beekeepers feed honey bees more protein during times of nectar shortage such as during times of drought or in the winter. As part of this, ARS has developed a new bee diet, Megabee, now available to beekeepers. The feeding of supplemental nutrients may help to decrease winter colony losses.
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In 2008, Germany revoked the registration of the neonicotinoid clothianidin for use on seed corn after an incident that resulted in the die-off of hundreds of nearby honey bees colonies. Investigation into the incident revealed that the die-off was caused by a combination of factors, including the failure to use a polymer seed coating known as a "sticker": weather conditions that resulted in late planting of corn while nearby canola crops were in bloom, attracting honey bees; use of a particular type of air-driven equipment used to sow the seeds, which blew clothianidin-laden dust off the seeds and into the air as the seeds were ejected from the machine into the ground; dry and windy conditions at the time of planting, which blew the dust into the nearby canola fields where honey bees were foraging; and a higher application rate than had been authorized was used to treat for a severe root worm infestation.
ARS researchers also have been analyzing samples from healthy and CCD-struck colonies and applying a variety of stressors from the four categories of possible causes to colonies in hopes of provoking a colony response that duplicates CCD.
While a number of potential causes have been championed by a variety of researchers and interest groups, none of them have stood up to detailed scrutiny. Every time a claim is made of finding a "smoking gun," further investigation has not been able to make the leap from a correlation to cause-and-effect. Other times, not even a scientific correlation has been demonstrated in the study claiming to have found "the cause" of CCD.
Researchers have concluded that no one factor is the cause of CCD. Most likely, CCD is caused by multiple factors. It is not possible to know at this time if all CCD incidents are due to the same set of factors or if the factors follow the same sequence in every case.
Studies are being conducted by ARS scientists and collaborators to look at the combined impact of two or more factors on honey bees-most recently the impact of exposure to the neonicotinoid imidacloprid and Nosema. While the dual exposure indicated some sublethal effects on individual honey bees, the overall health of the colony did not show an adverse effect.
Annual Reports of CCD Research Progress
2012 CCD Progress Report
2011 CCD Progress Report
2010 CCD Progress Report
2009 CCD Progress Report
2007-2008 CCD Progress Report
For more information, contact:
Kim Kaplan, Agricultural Research Service
Office of Communications,
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