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Running head: PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
Predictors of Honey Bee Colony Collapse Disorder in the Central Valley
Henry Rabas
California State University, Sacramento
Course: ENVS 190
May 15, 2019
Advisor: Dr. Singh
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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Abstract
Over the last 15 years, beekeepers in the United States and other parts of the world have reported
a high loss of honey bees from their hives. Honey bees are disappearing from hives leaving only
a few worker bees and the queen bee behind in the hive. Researchers do not yet know the
specific conditions that lead to colony loss or why this is mysterious phenomenon, named the
Colony Collapse Disorder, is occurring. Honey bee losses have been blamed on a multitude of
threats such as habitat loss, pesticides, viruses, diet, and the loss of genetic diversity. A literature
review of peer-reviewed journal articles and government documents was conducted to generate a
list of potential predictor variables. Predictors of honey bee colony collapse were analyzed using
a correlational research design to determine if there is a relationship between predictor variables
and the presence of colony collapse. The results from the broad collection of data suggested that
a single predictor variable may not be enough to cause colony collapse. The results showed that a
combination of stressors can weaken hive health and, if left unchecked, can lead to bee colony
collapse.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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Table of ContentsAbstract............................................................................................................................................2Introduction......................................................................................................................................4Background and Goal ......................................................................................................................6
Approach......................................................................................................................................7Significance .....................................................................................................................................7Literature Review ............................................................................................................................8
Economic Value...........................................................................................................................9California Statistics ................................................................................................................10Almonds .................................................................................................................................11Almond pollination fees .........................................................................................................11Floriculture .............................................................................................................................12Jobs.........................................................................................................................................13
Honeybee Threats ......................................................................................................................13Pesticides ................................................................................................................................13GMO.......................................................................................................................................15Parasites and bacteria .............................................................................................................16Genetics ..................................................................................................................................18Stress ......................................................................................................................................19Climate Change ......................................................................................................................20Nutrition. ................................................................................................................................21
Solutions.....................................................................................................................................23Policy .........................................................................................................................................23
Conclusion .....................................................................................................................................26Figures ...........................................................................................................................................28References......................................................................................................................................32
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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Introduction
Honey bees are an important global species due to the ecological and economical services
that honey bees provide to the world. One-third of all food consumed in the United States is
pollinated by pollinators such as honey bees (California Department of Food and Agriculture
[CDFA], 2013). The economic value that pollinators, such as bees, provide to the world has been
estimated at 153 billion dollars per year and produces a total surplus loss between 190 to 310
billion dollars (Gallai, Salles, Settele, & Vaissiere, 2009). Animal species pollinators are
responsible for pollinating 78 to 94 percent of all plants, depending on the plant’s geographic
location (Ollerton, Winfree, & Tarrant, 2011).
However, according to the United States Department of Agriculture (USDA), since the
mid-2000s, beekeepers have been reporting an annual loss of 30 to 90 percent of honey bees
from their hives (“Colony collapse disorder: An incomplete puzzle,” 2017). Despite these
statistics, researchers and environmental scientists do not know what the exact causes of the
collapse are. Honey bees are quickly disappearing from hives all over the United States and in
other parts of the world and researchers in the United States have started to call this mysterious
phenomenon the Colony Collapse Disorder (CCD). CCD occurs when most of the worker bees
leave the nest and do not come back, leaving only the queen bee and few worker bees behind
(Caldararo, 2015).
Research of American honey bee (Apis mellifera) colonies has revealed that the exact
causes of CCD are not known; however, researchers have found that CCD syndrome may be
caused by several factors working synergistically (Farooqui, 2013). Recently, Paudel,
Mackereth, Hanley, and Qin (2015) discovered that there are specific threats that honey bee
pollinators are facing such as habitat loss, pesticides, viruses, diet, and the loss of genetic
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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diversity. Given the significant role that pollinators play in maintaining ecosystem services and
the economic value that pollinators contribute, a world without bees would struggle to feed the
rising world population. Bees are an important species and play a significant role in other species
wellbeing and survival. Interdisciplinary knowledge between researchers, policymakers, farmers,
and environmental groups is needed to stop CCD from occurring.
According to the agricultural statistics review, a report published in 2013 by the
California Department of Food and Agriculture (CDFA, 2013), California produces more food
than any other state in the United States. California is ranked as the number one state in the U.S.
by the dollar value of the agricultural products grown in California (CDFA, 2013). California is
also one of only five places in the world that has a unique Mediterranean-like climate which is
ideal for agricultural production (CDFA, 2013). The California Central Valley is an agricultural
hub and is responsible for producing over half of all the fruits, vegetables, and nuts grown in the
United States (CDFA, 2013). California is also responsible for producing the majority (99%) of
all the almonds, artichoke, dates, dried plums, figs, garlic, kiwifruit, olives, olive oil, pistachios,
raisins, grapes, and walnuts, grown in the United States (CDFA, 2013). In 2012 Almonds were
ranked as the number one nut and fruit crop produced in California, and the production of
almonds generate close to 4 billion dollars in revenue (CDFA, 2013). The success of agricultural
production in California Central Valley can be attributed to climate, fertile soil, and pollinators,
such as the honey bee. California’s number one cash crop, almonds, are exclusively pollinated by
honey bees and without natural pollinators, the diversity and quantity of crops grown in the
California Central Valley would not be possible.
For this thesis, I will examine and attempt to identify the predictors of honey bee colony
collapse in the California Central Valley. To do so, a discussion of the background and goal of
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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the research will be provided. Following, a literature review will provide an overview of the
current literature on the topic. A discussion of proposed methodology will be provided along
with a discussion of results. Finally, this thesis will provide a conclusion discussion of the
findings and make recommendations for future research.
Background and Goal
In recent years, various honey bee colonies across the United States have suffered from
colony collapse disorder (CCD). Environmentally, between 67% and 96% flowering plants in the
wild need to be pollinated by animal pollination, such as bees (Ollerton et al., 2011). In regard to
economics, globally, between 235 and 577 billion dollars’ worth of annual food production is
dependent on pollinators, such as the honey bee. In California alone, honey bees as pollinators
are a 7.6-billion-dollar industry and almond orchards in California grow more than 80% of the
worlds almond supply (Medina, 2014). Additionally, 75% of the world's food crops depend, at
least in part, on pollination. However, recently, honey bee colonies have been impacted and
collapsed due to a variety of reasons including the use of pesticides, presence of diseases,
parasites, mites, pathogens, virus’ and even suburban sprawl. Climate changes have also been
identified as threats to the bee colonies due to increased occurrences of severe drought, floods,
and fires.
The goal of this study is to answer the research question: What is the relationship
between specific predictor variables and the honey bee colony collapse disorder in Central
Valley? Specifically, the researcher aims to examine predictors related to climate, nutrition,
habitat, and human imposed factors that impact the honey bee colony collapse. The methodology
to be used will be a quantitative correlational design to determine if a relationship exists between
the predictor variables and the colony collapse. Application of the findings will allow an
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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understanding of what specific factors predicate honey bee colony collapses so that changes can
be made. Potential significance and outcomes include increasing the bee colony size, increasing
pollination and, as a result, food production such as almonds, providing important dietary
sources of vitamins and minerals to humans, and implementation of new policies at state and
federal levels.
Approach
To achieve the goals discussed, a literature review of over twenty peer-reviewed journal
articles and research government documents will be conducted using a correlational research
design to predict if the specific variables caused colony collapse. To do so, a list of predictor
variables will be generated based on past peer-reviewed journal articles research specific to the
topic. Upon identification, predictor variables will be analyzed in relation to the colony collapse
outcome. Relationships will be examined for each predictor variable individually as well as
together to determine if any of the predictor variables interact with others in relation to the
collapse.
Significance
The proposed study aims to provide input and suggestions for action at various levels
including for the bee farmers, food farmers, and local/federal government policy. By
understanding the specific predictors of bee colony collapse disorder (CCD) in the California
Central Valley, recommendations can be made to assist bee farmers with properly raising and
maintaining bee colonies. In addition, food farmers (for example, almond orchards) may be able
to implement actions to reduce the exposure of certain predictors (e.g. pesticides) that are found
to have caused the collapse. Finally, environmental policy actions may result, and the local, state
and federal government become more aware of the specific factors that cause honey bee colony
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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collapse. While recognizing the negative impact that results from the colony collapse is
important to engage action, there needs to be an understanding of the specific factors that lead to
the collapse to avoid future collapses from occurring.
Literature Review
In the winter of 2006, honey beekeepers across the United States began reporting a high
number of bee colony losses. Beekeepers were finding some of their hives completely empty of
adult honey bees with no dead bees present to account for the losses, it looked as though the bees
had simply left the hives and disappeared (Stokstad, 2007). At the time, it was estimated that 20
to 30 percent of all beehives in the U.S. were affected by the phenomena that scientists named as
Colony Collapse Disorder (CCD). Beekeepers suspected the collapse may be attributed to
multiple factors, but the direct cause of CCD was not known (Watanabe, 2008). According to
Bekić, Jeločnik, and Subić (2014), before CCD there were at least twenty other instances of
honey bee colony collapses on record; however, the large bee colony losses that occurred
between 1960 and 2006 were all found to be caused by various parasitic diseases. CCD is
different from previously recorded honey bee losses because there is no evidence of dead bees
around or inside the hive and hives have ample amount of food left for bees to consume (Bekić et
al., 2014). Per Bekić et al. (2014), large beekeeper operations in the United States that were
experiencing CCD were reporting losses of 50 to 90 percent of their honey bees. However, CCD
is not unique to the U.S. as the same phenomena of bee colony collapse is occurring in Europe,
the Middle East, South America, and other parts of the world (Watanabe, 2008).
According to Caldararo (2015), honey bees face many disruptions and threats such as
lack of food, disease, and viruses. Goodrich (2019) argued that additional research is needed to
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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assess threats to honey bees to improve bee colony health. According to Goodrich (2019), more
research is also needed to study the economic impact of threats to honey bee colonies.
Economic Value
According to research by Bauer and Wing (2010), the world is facing a shortage of
managed pollinators, such as the honey bee, which may adversely affect the economy and can
lead to global food insecurity. Both in the United States and the rest of the world, managed
honey bee colonies have been declining since the 1960s. Managed bee colonies have decreased
from over 0.25 colonies per hectare in 1960 to just 0.06 colonies per hectare in the United States
and from 0.22 colonies per hectare to 0.16 colonies per hectare in the rest of the world (Figure
1), indicating an alarming decline in honey bee abundance (Food and Agriculture Organization
of the United Nations, 2010). Bauer and Wing (2010) used computer-aided equilibrium
modeling to determine what direct and indirect effect a pollinator shortage will have on food
production and the economy.
Bauer and Wing (2010) argued that declines in the world bee population due to CCD
have been disruptive to economic growth and may limit people’s access to enough nutritious
food, particularly in countries where agriculture makes up a large portion of the country’s
economy, such as West Africa. Per Bauer and Wing (2010), there are three trends that indicate
that a future pollinator shortage is occurring. Bauer and Wing (2010) indicated there is an
increase in crops that require bee pollinators; the abundance of managed bees is declining, and
the demand for pollinators is increasing. Additionally, another indicator of bee pollinator
shortage is the increase in bee pollination rental prices, brought on by high demand from almond
growers in California and the Pacific Northwest (Bauer & Wing, 2010). Bauer and Wing (2010)
reported that government assistance programs will need to be implemented to increase bee
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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pollinator abundance, both for managed bees and bees in the wild, to meet market demand.
According to Bauer and Wing (2010), fruits and nuts depend the most on bee pollinators and
thus will be the most affected by a bee shortage.
The equilibrium model Bauer and Wing (2010) used evaluated changes in global revenue
that were directly and indirectly affected by a decline in bee pollinators and estimated losses to
be around 334 billion dollars to the economy. The research also revealed that due to demand for
certain crops, such as fruits and nuts, the total revenue of those crops increased when supply
decreased, which benefited producers but hurt the economy (Bauer & Wing, 2010).
Furthermore, Bauer and Wing (2010) argued that the equilibrium approach to assessing changes
in revenue is a more comprehensive approach for calculating losses because the equilibrium
method considers both direct and indirect effects of pollinator losses. However, to establish a
more accurate result of total economic losses due to a decline in bee pollinators, a better
understanding of crops total dependency for managed bee pollinators would need to be more
thoroughly studied (Bauer & Wing, 2010). Therefore, understanding what factors are leading to
CCD may assist with reducing the honey bee shortage and thereby reduce economic losses long-
term.
California Statistics. According to the 2012-2013 California Agricultural Statistics
Review, a government report that tracks and ranks revenue generate by agriculture, California is
the top-grossing agricultural state in the United States (Figure 2). California produces almost half
of all the fruits, nuts, and vegetables that are grown in the United States (CDFA, 2013). In
addition to leading the way in agricultural production, California is also the nation’s largest
exporter of agricultural commodities and generated 16.87 billion dollars in revenue in 2011
alone. Many of the agricultural commodities, such as almonds, dates, plums, kiwifruit, olives,
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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pistachios, raisins, grapes, and walnuts, are exclusively produced in California and exported
globally (CDFA, 2013). There are over 400 agricultural commodities produced in California, the
top 20 crop and livestock commodities were valued at 35.8 billion dollars in 2011 and of those
20 highest producing commodities, 11 generated over 1 billion U.S. dollars each (CDFA, 2013).
Bekić et al. (2014) caution that the reduction in world bee colonies will directly affect crop
prices and yield and disrupt world trade.
Almonds. Of all the top producing commodities on the list, almonds were ranked as the
second highest commodity and brought in 3.87 billion dollars in revenue, only second to milk
production which was valued at 7.68 billion dollars (CDFA, 2013). The report also shows that
revenue from almond production has increased from 0.74 billion in 2001 to 3.87 billion dollars
in 2011, indicating the high economic importance of this commodity to the California economy.
Most almonds produced in the U.S. are produced in the California Central Valley; Fresno, Kern,
and Stanislaus counties, where some of the highest reports of Colony Collapse Disorder have
been reported. According to CDFA (2013), in addition to almond production, of the top 20
grossing commodities in California in 2011, seven of the commodities require bee pollination
during bloom season (Figure 3). In addition to tracking agricultural revenue in California, the
report also tracked notable decreases in cash receipts. According to the report, half of the top ten
decreases in California cash receipts in 2011 were fruit trees which are dependent on honey bee
pollinators for cross-pollination and honey, produced by bees. Without pollinators such as honey
bees, the production of top-grossing commodities such as almonds, grapes, berries
(strawberries), flowers and foliage, avocados, and honey would not be possible.
Almond pollination fees. Honey bee pollination fees in the U.S. have been on the rise
for the last few decades due to high demand from California almond growers and decreasing bee
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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colony size and supply (Goodrich, 2019). According to Goodrich (2019), fees for pollination
services have been increasing because bee colony sizes have been declining for the last few
decades due to CCD. According to the Bee Informed Partnership Winter Loss Survey, a survey
that tracks bee colony mortality rates over winter, both large and small commercial bee
pollination outfitters have experienced a high percentage of bee mortality rates over winter when
bees are most vulnerable (Goodrich, 2019).
While pollination prices have increased over the last few decades due to a reduced
number of bee colonies, Goodrich (2019) argued that prices may also be influenced by other
factors. According to Goodrich (2019), research shows that the number of bee colonies that
almond growers use to pollinate almond blossoms has almost doubled since 1973. In other
words, the standards for the number of bees a hive should contain has almost doubled for almond
production (Goodrich, 2019). Goodrich (2019) argued that this increase in demand from almond
growers has decreased the supply of beehives to other agricultural markets. Per Goodrich (2019),
Colony Collapse Disorder is being blamed for reduced bee abundance; however, Goodrich
(2019) argued that bee colony strengths need to be considered when calculating the total number
of bee colonies. Therefore, in order to address concerns such as those raised by Goodrich (2019),
it is important for future studies to examine the specific factors that lead to CCD.
Floriculture. In addition to almond production, California is also leading the nation in
floriculture crop sales revenue. California floriculture revenue was estimated at over 1 billion
dollars in 2011 and amounted to almost 25% of wholesale flower agriculture produced in the
U.S. (CDFA, 2013). According to the California Department of Food and Agriculture, 2012-
2013 report, California also leads the nation in annuals, garden plants, and potted flowers which
are all primarily pollinated by honey bees. According to the California Department of Food and
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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Agriculture 2012-2013 report, all the data used to generate the value of agricultural goods was
derived from government published sources, such as Department of Commerce, United States
Trade Commission, Canadian import data, Economic Research Service, and Agricultural
Marketing Service publications (CDFA, 2013).
Jobs. According to a report compiled by Assembly Committee on Jobs and Economic
Development, and the Economy, California agriculture was responsible for almost 1.4 million
jobs in 2013 and agriculture contributes over 36 thousand jobs to the economy annually (Medina,
2014). In addition, most of the agricultural jobs and job growth in California are occurring in the
Central Valley where bee hives have experienced some of the highest cases of Colony Collapse
Disorder. Many of the agricultural products that are produced in California and the jobs that
depend on those products would not be possible without bee pollinators. Per the report, 25.4
million acres of land in California is used for agriculture and California produced two-thirds of
all the fruit and nuts and one-third of all the vegetables in the U.S. in 2012 (Medina, 2014).
California economy and jobs are heavily dependent on agriculture and agriculture is deeply
dependent on natural pollinators such as honey bees (Medina, 2014). Almost 60% percent of all
the fruits and nuts that the U.S. exports are produced in California and, while most nuts are wind
pollinated, fruit trees need bee pollinators to reproduce (Medina, 2014). California is the largest
producer of almonds in the world and over 80% of all the almonds produced in the world are
grown in California. The revenue and jobs that almond production contributes to California are
staggering and without bees to pollinate almond flowers, almond production would collapse.
Honeybee Threats
Pesticides. There is a growing global concern that pesticide use in agriculture is a
contributing factor to CCD (Hladik, Vandever, & Smalling, 2016). However, according to
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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Hladik et al. (2016), little research has been done to show how land management practices affect
wild bee colonies. Insects, such as bees, are important environmental indicators and provide
many ecosystem services (Hladik et al., 2016). According to Hladik et al. (2016), land
management practices such as modification of landscapes and the use of pesticides in agriculture
can expose pollinators to stress and harmful chemicals that persist in the environment. Hladik et
al. (2016) sampled both wild native grassland bee populations and commercial wheat bee
colonies over a two-year period from 2013 to 2014 on a bimonthly basis to compare detection
frequencies of pesticides collected from grassland and wheat field bees (Figure 4). In total, there
were 18 different pesticides detected in both populations of bees, with thiamethoxam being the
most prominent pesticide found in 46% of the samples that were tested (Hladik et al., 2016).
Thiamethoxam is a powerful insecticide used in agriculture to control insect feeding; bees
encounter thiamethoxam through pollen and nectar (Hladik et al., 2016). According to Hladik et
al. (2016), bees exposed to thiamethoxam experience reduced locomotion and can become
disoriented outside of the hive. In addition to thiamethoxam, several other toxic insecticides,
fungicides, and herbicides were detected in bee samples at levels that were harmful to bees
(Hladik et al., 2016).
Honey bee deaths linked to the use of pesticides is a global problem when bees become
exposed to pesticides through contaminated pollen, honey, and water (Kasiotis,
Anagnostopoulos, Anastasiadou, & Machera, 2014). Kasiotis et al. (2014) analyzed honey bees,
bee pollen, and honey collected from infected beehives throughout Greece to see if honey bee
deaths could be attributed to the use of pesticides. Honey bees encounter pesticides when
pesticides are sprayed and drift through the air and land on crops; bees that encounter those crops
then transport the pollen into beehives contaminating the pollen and honey in the beehive
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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(Kasiotis et al., 2014). Other ways that bees are exposed to pesticides occur when bees touch the
fluid that oozes from the pores of plants that have been sprayed with pesticides, and through
consuming pesticide contaminated surface (Kasiotis et al., 2014). Kasiotis et al. (2014) sent 71
samples of dead honey bees, honey, and pollen collected between 2011 and 2013 from
beekeepers throughout Greece to the Benaki Phytopathological Institute laboratory to test for
pesticide residue. According to Kasiotis et al. (2014), using the multiresidue sampling method,
over 70 percent of the honey bees, 40 percent of pollen, and 0.1 percent of honey samples tested
positive for pesticide residue. Out of all the honey bee samples analyzed, 50 percent of the
samples tested positive for clothianidin, a chemical pesticide used that can be lethal to bees when
the pesticide is ingested (Kasiotis et al., 2014). However, according to Kasiotis et al. (2014), the
concentration levels of clothianidin pesticide recovered from the dead bees sampled would not
be enough alone to cause sudden death to bees. But if bees encountered other chemical
compounds that exist in nature, such as on pollen, plants or in water, the chemicals could have a
synergetic effect that could be deadly to bees (Kasiotis et al., 2014).
In a similar pesticide study, Penn State researchers have found over 171 different
pesticide residues in honey bee wax, pollen, and nectar (Watanabe, 2008). However, according
to Watanabe (2008), while pesticides can affect bee health, the Connecticut Agricultural Station
in New Haven was unable to conclude that pesticides and herbicides alone were the direct cause
of CCD (Watanabe, 2008).
GMO. In addition to threats from pesticides, bees are also exposed to pollen from plants
from genetically modified organisms (GMO), and Bekić et al. (2014) argued that the effects of
GMO pollen may be harmful to bees. According to Bekić et al. (2014), the effects that
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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genetically modified plants have on bees have not been researched enough to rule out as a cause
of CCD and more research is needed to determine if GMO’s are harmful to bees.
Parasites and bacteria. According to Watanabe (2008), one of the threats that
honeybees face are parasites, such as mites, which feed on bee blood and inhibit bees from
breathing by injecting deadly bacteria into the bee. Parasites such as microsporidia can also
infect bee digestive systems and weaken the immune system, either killing the bee or
significantly shortening their life (Watanabe, 2008). Nosema ceranae is another parasite that
causes damage to bee organs and digestive system in adult honey bees and has been shown to
decrease the life expectancy of bees by 25 to 58 percent (Bekić et al., 2014). Nosema parasites
cause bees to become disoriented during flight and inhibit bees from gathering honey and pollen,
leading to starvation (Bekić et al., 2014). Additionally, Bekić et al. (2014) argued that other
diseases such as foulbrood and varroa can spread in beehives when beekeepers purchase bees
infected with the virus or use contaminated equipment from unsterilized wax.
In addition to attacks from parasites, bees are also exposed to a variety of harmful
chemicals that are in the environment, such as pesticides and herbicides which can further
weaken bees’ immune system, making bees more susceptible to diseases (Watanabe, 2008).
According to Watanabe (2008), a study was conducted to find out if a virus was causing CCD
and honeybees from infected bee colonies were tested for microbial infections and over eight
different bacteria species were identified in the study (Watanabe, 2008). Per Watanabe (2008),
out of the eight bacteria that scientists discovered in bees, only one bacterium, Israely acute
paralysis virus (IAPV), was believed to contribute to CCD. The IAPV bacteria discovered in
bees was believed to originate in Israel and the same bacteria was also found in Australian and
Israel bees in 2004 (Watanabe, 2008).
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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Another theory of how the bacteria entered the U.S. is through the small hive beetle that
may have been carrying the IAPV bacteria (Watanabe, 2008). The third theory that Watanabe
(2008) proposed was that IAPV bacteria entered the U.S. as a virus carried by the royal jelly, a
jelly that is sometimes used by beekeepers to attract a queen bee into a hive. In addition to the
three discussed theories of how the deadly IAPV bacteria was introduced, studies also discovered
dead cockroaches in beehives that were infected by IAPV. To test if IAPV bacteria caused
cockroaches to die, researchers removed IAPV bacteria from dead cockroaches and injected non-
infected cockroaches with the IAPV bacteria and those cockroaches died within four days,
indicating IAPV bacteria was a probable cause of mortality (Watanabe, 2008).
However, according to the U.S. Department of Agriculture Bee Research Laboratory in
Beltsville, Maryland, IAPV bacteria can be found in both healthy and sick beehives, indicating
that there may be different strains and strengths of the disease (Watanabe, 2008). Sequencing
DNA from healthy and infected bees may one day provide researchers with the evidence needed
to determine the cause of CCD. However, for now, bacteria found in affected bees is just one of
many threats believed to have caused CCD (Watanabe, 2008). According to Bekić et al. (2014),
diseases over time can weaken bee colonies by reducing bee colony size and strength, making
bees more vulnerable to other threats that exist in the environment. While the exact cause of
CCD is unknown, the timing of viruses discovered in infected bee hives is strongly correlated to
beehive collapse (Bekić et al., 2014).
While most researchers studying CCD are trying to figure out how bees are getting sick
and dying, Jay Evans, a geneticist with the USDA bee laboratory in Maryland, is asking how
bees are surviving (Zakaib, 2011). The USDA Bee Research Laboratory where Evans works is
separating bee genome DNA from other genetic material found in bee colonies to see what other
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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organisms, such as bacteria, fungi, and viruses, are present in the DNA (Zakaib, 2011). The goal
of the research was to do an inventory of all non-bee DNA to see how bees are affected by the
disease at a molecular level and if any of the non-bee DNA found in the hive might be working
synergistically to negatively impact bee health (Zakaib, 2011). According to Zakaib (2011),
genetic researchers have discovered that some bees have genes that are more resilient in fighting
off diseases. For example, strands of a particular RNA can booster a bee’s immune system and
make bees more resilient against viruses (Zakaib, 2011). According to Zakaib (2011), identifying
bee genes that make bees less susceptible to diseases can be used by geneticists to help bees fight
threats at a molecular level. However, it is important to also know the specific factors that are
leading to CCD in order to understand how to make bees less susceptible but also reduce the
threats leading to CCD overall.
According to Caldararo (2015), bees are social animals capable of developing
mechanisms that give bees the ability to recognize behavior to avoid exposure to infection that
would lead to mortality, such as Colony Collapse Disorder (CCD). Per Caldararo (2015), empty
beehives may be a result of a bee’s response to an emerging disease agent that has invaded the
hive. Caldararo (2015) argued that, like humans, bees form complex social societies and can
detect when they are in mortal danger and have developed response mechanisms that may cause
bees to abandon an infected bee colony hive. Per Caldararo (2015), a bee abandoning a beehive
could be likened to a human avoiding a person that has been infected with a deadly disease such
as the plague. Therefore, more research is needed to examine the factors leading to CCD to
reduce the dangers currently affecting bee colonies.
Genetics. While the demand for pollination services from honeybees has drastically
increased globally, honey bee genetic variability has been declining and individual bee genotype
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
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are becoming like one another (Bekić et al., 2014). According to Bekić et al. (2014), most of the
queen bees bred in the United States for pollination come from a small number of queen bees,
significantly reducing the genetic diversity and making queen bees more vulnerable to diseases
and pests.
Stress. According to Ahn, Xie, Riddle, Pettis, and Huang (2012), one of the biggest
stresses that bees face is long distance travel. Long distance transportation of honeybees from
Florida to California can have an adverse effect on honey bee physiology (Ahn et al., 2012).
Commercial bee operations transport bee colonies throughout the U.S. to pollinate crops that
grow in different seasons and regions; crops such as almonds, cherries, plums, apples, and
avocados (Goodrich, 2019). Ahn et al. (2012) argued that travel influences how living
organisms’ function and the effects of travel on bees are poorly understood. Per Goodrich
(2019), beekeepers that transport bees over long distances experience higher bee mortality rates
than beekeepers that operate locally. Additionally, bees that participate in multiple pollination
markets are exposed to more deadly chemicals such as pesticides and herbicides than bees that
pollinate fewer varieties of crops locally (Goodrich, 2019).
According to Ahn et al. (2012), studies show that bees exposed to long-distance transport
have less developed food glands, which may inhibit the bee’s ability to nurse their young.
Physiological and behavioral changes caused by stress from traveling have also been shown to
affect juvenile hormone (JH) levels, a hormone responsible for regulating reproduction and
development in bees; however, according to Ahn et al. (2012), in their study of seven and 17-day
old bees, there was no significant difference in JH hormone levels between bees that were
transported and bees that were not. Additionally, Ahn et al.’s (2012) research study focused on
the effects of travel on younger bees and it is possible that older bees may be affected differently.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
20
Climate Change. Monitoring of bee colonies has revealed that climate changes, such as
prolonged droughts, heat waves, and flooding, is a serious threat to honey bees (Flores et al.,
2019). Flores et al. (2019) conducted a study of six bee colonies in 2016 and nine colonies in
2017 to assess the effects of climate change on bee colonies and discovered that bees were food
stressed. Prolonged droughts with high temperatures and little precipitation result in shorter
bloom flowering seasons, which means less pollen and nectar for bees to turn into honey; in
other words, food (Flores et al., 2019). Electronic dataloggers were used in the study to remotely
monitor bees throughout the flowering season to assess bee populations, larvae, and the amount
of honey in beehives (Flores et al., 2019). Researchers counted the number of adult bees and
weighted the amount of honey and pollen in hives and found that there was a lack of food stores
(Flores et al., 2019). According to Flores et al. (2019), the pollen and honey that bees collect
during the flowering season are used as primary sources of energy to feed the brood and maintain
adult bee health. Without adequate storage of food, honeybees become food-stressed and can
cause the bees to starve and lead to colony collapse disorder (Flores et al., 2019).
In another study, researchers studied how more frequent extreme weather, due to climate
change has affected bee mortality. According to Dalmon, Peruzzi, Conte, Alaux, and Pioz
(2019), extreme cold or hot temperatures can increase bee mortality rates and expose bees to
more diseases. To determine how bees were affected by temperature, rearing bees were exposed
to six different temperature treatments that ranged between 59- and 110-degrees Fahrenheit
(Dalmon et al., 2019). Dalmon et al. (2019) found that bees exposed to both high and low
temperatures increased bee mortality rates and bees that were exposed to a temperature of 110
degrees Fahrenheit for over an hour, experienced the highest mortality rates. Dalmon et al.
(2019) reported that prolonged exposure to extreme cold or hot temperatures, due to climate
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
21
change, can shorten bees’ lifespan and lead to colony collapse. However, while bee mortality
rates increased at temperatures between 99 to 110 degrees Fahrenheit, viral load levels also
decreased by 8 to 17-fold, due to heat stunned protein cells that impede viral cell replication
(Dalmon et al., 2019). According to Dalmon et al. (2019), temperature has been used to treat
virus-infected plants such as the ringspot virus found in roses bushes and should be studied
further to determine if temperature can be used as a tool to control the spread of viral infections
in bee colonies.
Nutrition. Honeybees are exposed to a plethora of threats during their lifetime that can
cause CCD, and according to Bekić et al. (2014), poor nutrition has been reported in all cases of
colony collapse. Bekić et al. (2014) argued that honey bees need a more diverse diet that
provides bees with better nutrition, such as pollen and nectar from a variety of plants. Honey
bees rely on the pollen and nectar from a variety of flowering plants to supply bees with the
nutrition they need; however, managed bees are primarily exposed to a monoculture that fails to
meet bees’ nutritional requirements (Bekić et al., 2014). According to Bekić et al. (2014), bees
used for commercial pollination have a poorer immune system than bees that forage on a variety
of plants.
According to Naug (2009), another reason for colony collapse in the United States is due
to pollinator habitat loss and foraging behavior. Naug (2009) used data from the National
Resources Inventory (NRI), a survey of national resources, to analyze land use data for the
United States and found that states with the most developed land had the least amount of honey
harvest per bee colony. Naug (2009) argued that declines in bee colonies may be explained by
examining bee habitats and foraging behavior. As stated by Naug (2009), honey bees become
infected by a microscopic fungus called Nosema spores that develop in bees’ guts and are passed
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
22
on to other bees through contact with infected spores. Bees infected by Nosema disease live
shorter lives, do not usually produce offspring, and exhibit high levels of hunger (Naug, 2009).
According to Naug (2009), Nosema disease causes honey bees to become food-stressed, have
less energy than healthy honey bees, and leave the hive to forage for food. However, because
bees infected by Nosema disease have less fitness than healthy bees, activities that require high
energy, such as flying in cool weather, are more difficult (Naug, 2009). Naug (2009) reported
that loss of habitat in the United States due to urbanization has decreased suitable foraging areas
for bees and infected honey bees may not have enough energy to return to their hive from
extended foraging trips. Naug (2009) used data from the National Agricultural Statistics to
estimate the number of working honey bee colonies in each state in the United States and the
amount of honey each bee colony produced, then compared those numbers to the NRI land use
data. According to Naug (2009), decreases in honey bee colony populations in the United States
have decreased significantly from the 1980s to 2007 (Figure 5). The decrease in honey bee
colony populations correlates with land coverage changes that occurred during the same period
that saw reductions in cropland, pastures, and free-range land in the United States (Naug, 2009).
Additionally, Naug’s (2009) data showed that states with the highest amount of open land, such
as Nebraska, New Mexico, and the Dakotas, had the lowest reported colony losses (Figure 6).
While land use and honey yield can be used to estimate bee abundance, Naug (2009) cautions
that the formula he used does not consider mistakes that could occur from some hives being
counted multiple times in different states, due to transportation of managed honey bees for
pollination purposes, beekeepers splitting bee colonies that survive to start new colonies, and the
number of bees from beekeepers with fewer than five hives. According to Naug (2009), suitable
honey bee habitat plays an important role in bee colony size and abundance and increases the
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
23
rate of survival for bees foraging for food. Nevertheless, bees are exposed to many threats
during their lives that can cause declines in bee colonies which lead to colony collapse in honey
bees (Naug, 2009).
Solutions
There are many threats that have been identified to cause CCD and finding a solution has
been elusive. While the cause of CCD has yet to be determined, organizations such as ZomBee
Watch, a citizen organization that tracks honey bee parasites, has developed a novel idea to
discover how bees are becoming infected and dying. ZomBee Watch launched in 2012 and is
funded by the AWS Education Grant award, to document the location of infected bees in the
United States (Nugent, 2018). The goal of the project is to document the locations (Figure 7) of
infected bees by having regular citizens report signs of infections observed on dead honey bees.
This is important because hive abandonment is a major indicator of CCD and this could help
researchers identify the symptoms of bees that have left the hive to determine the cause of CCD
(Nugent, 2018).
Policy
To stop the spread of infections and diseases in bees, in 1992 the U.S. Congress passed
the Honeybee Act, which prevented bees from being transported into the U.S. (Watanabe, 2008).
However, in 2005, pressure from California almond growers that wanted more bees for almond
pollination forced Congress to create an exemption to the 1992 Honeybee Act which allowed
bees from Australia into the United States. According to Watanabe (2008), the policy exception
to allow bees from Australia into the United States may have been how the IAPV bacteria was
first introduced into U.S. bee populations. In a similar fashion, to combat the spread of disease to
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
24
honey bees, royal jelly was banned from being imported into China in 2002 because royal jelly
was shown to cause bacterial infections that killed bee larvae (Watanabe, 2008).
While there are many Federal policies and regulations that create conditions, which
support beekeepers, land use policies tend to favor private landowner and state rights over
migratory honeybee beekeeper rights (Durant, 2019). According to Durant (2019), there are
mechanisms in place that restrict beekeepers from accessing floral resources, which has a
negative effect on bee health. Between 2015 and 2018, Durant (2019), interviewed 41
commercial beekeepers, 12 research scientist, and 8 county, state, federal employees in the
Midwest where over 45 percent of U.S. honey is produced and to discovered why the amount of
honey produced by bee colonies has drastically decreased. According to Durant (2019), land use
conflicts between beekeepers and private landowners, environmental groups, and policy-makers
have led to changes and restriction in bee foraging laws and thus reduced suitable bee foraging
areas. As a result, beekeepers had to switch to manmade pollen and commercial pollination
events to supplement bee nutrition, which has decreased bee health (Durant, 2019). Durant
(2019) indicated that current land management policies in the U.S. have created barriers for
commercial beekeepers and thus bee production in the U.S. has been declining.
Another hurdle for beekeepers in the U.S. is that current Environmental Protection
Agency (EPA) guidelines regarding the use of pesticides do not follow the precautionary
principle; in other words, pesticides in use are labeled safe until proven harmful (Durant, 2019).
Per Durant (2019), there is a system of organization in policy making that prioritizes the needs of
agricultural industries, landowners, and agrochemical companies over beekeepers, by
incentivizing land management practices that exclude beekeepers from resources. Furthermore,
federal policies such as the 2005 Energy Policy Act, that prioritizes renewable energy standards
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
25
and the 2007 Energy Independence Act, which promotes the use of corn to produce ethanol, have
substituted nutritious bee forage acreage with less nutritious monoculture crops, such as corn, to
make biofuel (Durant, 2019).
Additionally, the Conservation Reserve Program, a USDA Farm service agency, differs
between wild bees and honey bees and classifies honey bees as nonnative or invasive species in
the United States, because honey bees were originally brought to the U.S. from Eurasia (Durant,
2019). Durant (2019) argued that unfavorable land policies have driven many commercial honey
beekeepers out of business or to turn to commercial pollination events which are proven to
decrease bee health and increase mortality among honey bees. However, the relationship
between commercial beekeepers and agricultural production is a double edge sword, due to the
prevalence of pesticides in agriculture and beekeeper’s dependence on the agriculture industry to
survive (Durant, 2019). Durant (2019) stressed the importance of open dialogue and
communication between growers, landowners, and beekeepers so that bee mortalities due to
pesticides use can be avoided and access to forage is arranged.
While USDA actions and policy may not always prioritize beekeeper rights over
agricultural and landowner needs, according to Vanegas (2017), in 2006 the USDA moved
quickly to ban the use of neonicotinoid, a group of pesticides known to cause CCD. Vanegas
(2017), argues that after CCD was discovered in 2006 the USDA and EPA worked together to
develop the Federal Insecticide, Fungicide, and Rodenticide Act, which assessed the ecological
risk to bees and other pollinators and banned the use of many high-risk pesticides harmful to
bees. However, in 2012 despite previous legislation banning the use of high-risk pesticide, the
EPA approved several pesticides that were considered high risk, despite the pesticides being
harmful to pollinators (Vanegas, 2017). According to Vanegas (2017), the EPA argued that the
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
26
pesticides that the EPA approved would not cause unreasonable harm to pollinators and that the
economic and social benefits derived from said pesticides outweighed the harm that would result
to pollinators. Consequently, the action was challenged in courts by the Pollinator Stewardship
Council and overturned, indicating the high importance pollinators play in society (Vanegas,
2017). The EPA has the difficult job of overseeing issues of many stakeholders and balancing the
benefits and disadvantages of the policies the EPA manages (Vanegas, 2017).
Conclusion
The importance of bees to the ecosystem and people is immeasurable, a world without
bee pollination is not sustainable and the importance of bees to the world economy and food
production is too great to estimate (Bekić et al., 2014). In the United States, honey bees are
responsible for every third bite of food people consume (CDFA, 2013) and contribute over 334
billion dollars in revenue annually to the global economy (Conservation work for honey bees,
2017). A single colony of bees can pollinate 3 million flowers each day (Bekić et al., 2014).
Since the discovery of Colony Collapse Disorder in 2006, 30 to 90 percent of honey bees
have vanished from beekeepers hives in the United States (“Colony collapse disorder: An
incomplete puzzle,”, 2017). Despite these statistics, researchers and environmental scientists
have not been able to identify the exact cause of colony collapse. While numerous theories exist
on the causes of CCD syndrome, researchers and scientist have yet to identify the direct link that
causes the disorder.
Many scientist and researchers believe that CCD is caused by several factors working
synergistically (Farooqui, 2013). In this literature review, several causes of CCD were proposed
and discussed to determine how specific threats affect honey bee pollinators. The specific threats
that were discussed and honey bee pollinators are facing, such as pesticides, diseases, genetically
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
27
modified organisms, parasites and bacteria, genetic variation, stress, climate change, and
nutrition, were evaluated to determine why CCD is occurring. While many proposed causes of
CCD discussed were prevalent in managed honey bee populations, no single one cause could be
identified to have caused CCD on its own. However, there were several causes of CCD that were
mentioned more often by scientist and researchers during the course of the literature review, such
as the threats of pesticides and diseases. Most of the literature from researchers and scientists
around the world proposed different examples of threats to bees that could cause CCD.
However, the effects that agricultural use of pesticides and diseases have on bees was discussed
or mentioned unanimously by researchers and scientists as a factor of CCD. While many studies
proposed scenarios with threats that could cause CCD, no one study successfully attributed CCD
to a single specific threat.
While many causes of CCD were discussed, a more comprehensive literature review
should be completed to determine if particular threats, such as pesticides and diseases, are
entirely to blame for causing CCD or if novel areas of research, such as genes or the effects that
pollen and nectar from genetically modified plants have on bees, are to blame for the collapse. A
systematic review of metanalysis should be performed to determine which threats pose the
greatest danger to bees so that remaining research can be used to fill the gaps. Furthermore, there
is a level of consensus among researchers and scientists that more initiatives and policy need to
be developed to limit bees from human threats to understand why CCD is occurring.
Additionally, people must study how the relationship between people and bees has changed over
time to determine what has made bees more vulnerable to emerging threats. The synergetic effect
of factors driving honey bee losses need to be considered and quantified so that best practices
and more comprehensive policies can be developed to eliminate threats leading to CCD.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
28
Figures
Figure 1. Managed bee colonies for bee pollinator-dependent harvested acre of land (1961-2008). Source: Food and Agriculture Organization of the United Nations (2010).
Figure 2. Top 5 agricultural revenue ranked states in the United States in 2011.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
29
Figure 3. Top 20 agricultural commodities in California in 2011.
Figure 4. Frequencies of pesticides collected from grassland in 2013 and 2014 and wheat field in 2014.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
30
Figure 5. Number of managed honeybee colonies in the United States.
Figure 6. Changes in land types; (a) cropland, (b) pasture, (c) rangeland, and (d) developed land.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
31
Figure 7. Location of infected (Red), Not infected (Green), and Sampling in progress (Yellow) of honey bees.
PREDICTORS OF HONEY BEE COLONY COLLAPSE DISORDER…
32
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