Predictors of Honey Bee Colony Collapse Disorder in the ......Predictors of honey bee colony collapse were analyzed using a correlational research design to determine if there is a

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.


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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


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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


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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


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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


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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


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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


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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


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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,


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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


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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


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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


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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


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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


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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).


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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


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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


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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.


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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


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


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


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


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


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


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


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.


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.


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.


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.


31

Figure 7. Location of infected (Red), Not infected (Green), and Sampling in progress (Yellow) of honey bees.


32

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