{"id":392,"date":"2018-07-24T17:19:18","date_gmt":"2018-07-24T17:19:18","guid":{"rendered":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/chapter\/5-4-the-mysterious-case-of-colony-collapse-disorder\/"},"modified":"2018-07-26T18:38:32","modified_gmt":"2018-07-26T18:38:32","slug":"5-4-the-mysterious-case-of-colony-collapse-disorder","status":"publish","type":"chapter","link":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/chapter\/5-4-the-mysterious-case-of-colony-collapse-disorder\/","title":{"raw":"5.4 The Mysterious Case of Colony Collapse Disorder","rendered":"5.4 The Mysterious Case of Colony Collapse Disorder"},"content":{"raw":"\n

Andrew T. Wood<\/h2>\n

Colony Collapse Disorder or CCD has decimated the honeybee population. Most scientists agree that it is caused by a combination of factors ranging from the environment, climate change, unknown viruses, and other pathogens. If CCD is not resolved, it will severely damage a multi-billion dollar food industry.<\/h5>\n[caption id=\"attachment_179\" align=\"aligncenter\" width=\"595\"]\"Honeybee Figure 1. A European Honeybee (Apis mellifera) gathers nectar from a flower.
\nPhotograph by James Petts, 2014. CC BY-SA 2.0.[\/caption]\n

Since 2009, the population of <\/span>Apis mellifera<\/span>, or the honeybee (Figure 1), has been in continuous decline. Scientists are unsure of what is causing the decline, called <\/span>Colony Collapse Disorder (CCD)<\/span><\/a>, but many researchers hypothesize it stems from numerous factors ranging from the misuse of <\/span>pesticide<\/span><\/a>s<\/span> to <\/span>RNA<\/span><\/a> viruses.<\/span>1,2,3,4,5,6<\/sup><\/span> Diminished populations of honeybees can have a large impact on the quantity of crops produced and the global economy.<\/span>1,3,4,6,7<\/sup><\/span> While there are many possible causes of CCD, microbes, pollutants, and stress factors are the three biggest influences that have contributed to the decline of honeybees.<\/span>\n[caption id=\"attachment_180\" align=\"aligncenter\" width=\"1000\"]\"Global Figure 2. Distribution of the honeybee (Apis melifera).
\nWhile native to Europe, Asia, and Africa, the European Honeybee can now be found around the world.
\nCourtesy of Semhur, 2011. CC BY-SA 2.0.[\/caption]\n

Scientists are searching for possible causes of CCD on a microbial level due to the lack of clear indicators on a larger magnitude scale. While CCD only explains a small proportion of losses, it is prevalent in numerous independent populations. The three most researched groups of microbes are viruses, bacteria, and fungi.<\/span>8<\/sup><\/span> <\/span>Virus<\/span><\/a>es<\/span> can change honeybees at the cellular level by altering <\/span>DNA<\/span><\/a> and RNA strands. Scientists have documented around twenty positive RNA viruses, and these viruses can \"affect the morphology, physiology, and behavior of bees and have been widely associated with weak and dying <\/span>colonies<\/span><\/a> both historically and recently\".<\/span>8<\/sup><\/span> As a result, it is possible an unknown virus has affected the bees\u2019 cognitive function and inhibited them from returning to the hive.<\/span>9<\/sup><\/span> Healthy bees also attempt to save the hive by removing the infected bees.<\/span>8<\/sup><\/span>\n

Bacteria<\/span><\/a> have the advantage of being highly infectious and target the weak and young bees.<\/span>8<\/sup><\/span> Well known diseases such as the American and European <\/span>foul brood disease<\/span><\/a> infect and kill the <\/span>larvae<\/span><\/a>, but are less hindering towards adults.<\/span>4<\/sup><\/span> Tests have concluded that adults carry lower levels of these infectious bacteria.<\/span>8<\/sup><\/span> A bacterial infection would explain the quick spread of disease within a colony. Lastly, infected bees do not return to the hive, thus an infection would be undetected in the healthy bees.<\/span>\n[caption id=\"attachment_181\" align=\"aligncenter\" width=\"1024\"]\"Colony Figure 3.
\nImage courtesy of Giulia De Rossi, 2014. CC BY-SA 4.0.
\nSunflower photo by Stan Shebs, 2008. CC BY-SA 3.0.
\nPeach rose photo by Scott Wylie, 2009. CC BY 2.0.
\nCosmos photo by Magnus Manse, 2013. CC BY 2.0.
\nWhite rose photo by Scott Wylie, 2009. CC BY 2.0.
\nYellow tidy tips photo by Alan Vernon, 2010. CC BY 2.0.
\nVarroa mites photo by Robert Engelhardt, 2005. Public Domain.
\nMicrograph of microorganisms by Richard Muir, 1927. CC BY 4.0.
\nPhorid fly photo by Inna Strazhnik, 2014. CC BY 2.0.
\nHoney bee photo by Karunakar Rayker, 2010. CC BY 2.0.[\/caption]\n

Fungi also have many ways of spreading around the colony and killing larvae.<\/span>8<\/sup><\/span> Fungi can spread both vertically and horizontally. Vertically would be the queen passing it her brood during reproduction, whereas horizontally, hive mates transfer the fungi to each other by their close approximations within the hive. Bees have evolved to try to combat this spread, but their methods may sometimes cause more harm than good. For example, hives can produce special worker bees that \u201crecognize larvae infected with chalkbrood <\/span>fungus<\/span><\/a> earlier in the disease process than workers from typical colonies, and subsequently remove the larvae before spore maturation\".<\/span>8<\/sup><\/span> Other less specialized workers remove the dead from the hive or eat them in an attempt to rid the colony of <\/span>pathogen<\/span><\/a>s<\/span>.<\/span>8<\/sup><\/span> This is problematic because diseases can spread from the dead to the living when the worker bees eat them or come into contact with them. One possible reason why bees leave the hive is because workers detect the sickness and send them away to die. However, the queen is rarely sick and that may point to a horizontal disease path.<\/span>2<\/sup><\/span>\n

Other stressors have also been known to affect bee health. Scientists are becoming more interested in the interaction of the environmental factors which include <\/span>habitat<\/span><\/a> loss and <\/span>climate change<\/span><\/a>. Climate change may impact organization levels of bee hierarchy by \u201cchanging the temporal activity of bees\u201d.<\/span>7<\/sup><\/span> Plant <\/span>biodiversity<\/span><\/a> in many regions of the world has changed due to the introduction of foreign plants, pathogens, and other species of insects.<\/span>7<\/sup><\/span> Some foreign plants were introduced to provide better resources for the bees. Other plants and bees have been introduced into the region and have caused new pathogens to come into contact with native honeybees.<\/span>7<\/sup><\/span> Transplanted bees have an extremely difficult time adjusting to their new environment. Bees have to constantly move from location to location to <\/span>pollinate<\/span><\/a> crops around the United States, and as more colonies die, the healthy colonies must work harder to pollinate<\/span>8 <\/sup><\/span>(Figure 4). Lastly, the interaction of the foreign objects with the indigenous species can cause diseases to pass and mutate.<\/span>\n[caption id=\"attachment_182\" align=\"aligncenter\" width=\"1024\"]\"Gradual Figure 4. Reported Annual Honeybee Losses in the U.S.
\nAnnual surveys conducted by the U.S. Department of Agriculture and collaborators show that since the winter of 2006\/2007, honeybee mortality has remained above the level that beekeepers consider economically sustainable (18.9%).
\nData from Kim Kaplan, 2006-2014.[\/caption]\n

Human made chemicals are also detrimental to the health of honeybees.<\/span>3,4,6,10<\/sup><\/span> The <\/span>Environmental Protection Agency (EPA)<\/span><\/a> has tested the <\/span>active ingredient<\/span><\/a>s<\/span> in nearly all chemical compounds and they have deemed these compounds safe for use in mass application. Many of the benign chemicals in <\/span>insecticide<\/span><\/a>s<\/span> may not be entirely harmless. This is because they are considered non-active and do not face the same rigors of testing by the EPA. These \u2018inactive\u2019 chemicals may harm honeybees as well as other insects. They may also \u201calter honeybee <\/span>gene<\/span><\/a> expression for detoxification pathways and may down-regulate gene products\u201d<\/span>10<\/sup><\/span> and \u201calter physiological functions, immune responses, and detoxification functions in the host bees rendering them more susceptible to pathogens and pesticides\u201d.<\/span>10 <\/sup><\/span>The physical and mental health risks involved with these chemicals can either make bees sick through pathogens or can slowly kill them, and may also lead to higher mortality rates of future generations.<\/span>10<\/sup><\/span>\n

Researching the causes of Colony Collapse Disorder is important because bees increase the yield of 96% of the crops that require animal pollination, and 75% of all crops that require insect pollination.<\/span>7<\/sup><\/span> The global annual economic value of insect pollination was estimated at 153 billion Euros in 2005<\/span>7<\/sup><\/span> (190.4 billion U.S. Dollars).<\/span><\/span> Without honeybees to pollinate wild plants and cultivated crops, the global food industry would have to use artificial means for pollination and this would vastly increase the price of food products.<\/span>1,3,4,7<\/sup><\/span> Honeybees are essential if humans hope to continue producing cheap food and food byproducts. In conclusion, honeybees are important to the humans because they affect the success of so many products used in our daily needs. Remedying Colony Collapse Disorder is imperative to ensure honeybee survival.<\/span>\n[caption id=\"attachment_183\" align=\"aligncenter\" width=\"1024\"]\"Beekeeper Figure 5. A beekeeper inspects a honeybee hive at a cherry farm in South Wales. Honeybees are often moved from farm to farm in order to pollinate crops.
\nPhotograph by Nick Pitsas, 2007. CC BY 3.0.[\/caption]\n

\n

References<\/h4>\n
    \n
  1. Associated Press. (20017, May). Declining Honeybees a \u2018threat\u2019 to Food Supply. MSNBC.<\/span><\/li>\n
  2. Dainat, B., et al. (2012). Colony collapse disorder in Europe. Environmental Microbiology Reports. 123-125<\/span><\/li>\n
  3. Holland, Jennifer (2013, May 10). The Plight of the Honeybee. National Geographic. <\/span><\/li>\n
  4. Plumer, Brad (2013, May 3). Why are bees dying? The U.S. and Europe have different theories. The Washington Post.<\/span><\/li>\n
  5. Van Engelsdorp, D., et al. (2009). Colony Collapse Disorder: A Descriptive Study. Plos One. 4.8:1-17.<\/span><\/li>\n
  6. Walsh, Bryan (2013, May 7). Beepocalypse Redux: Honeybees Are Still Dying \u2014 and We Still Don't Know Why. Time.<\/span><\/li>\n
  7. Potts, S., et al. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution. 25.6:345-353.<\/span><\/li>\n
  8. Evans, J.D., & Schwarz, R.S. (2011). Bees brought to their knees: microbes affecting honey bee health. Trends in Microbiology. 19.12:614-620.<\/span><\/li>\n
  9. Bromenshenk, J., et al. (2010). Iridovirus and Microsporidian Linked to Honey Bee Colony Decline. Plos One. 5(10):1-11<\/span><\/li>\n
  10. Berry, J.A., et al. (2013). Field-Level Sublethal Effects of Approved Bee Hive Chemicals on Honey Bees (Apis mellifera L). Plos One. 8(10):1-7<\/span><\/li>\n
  11. Petts, James. (2014). [Photograph of honeybee gathering nectar]. Retrieved from <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY-SA 2.0.<\/span><\/a><\/li>\n
  12. S\u00e9mhur. 2011. [Map of the distribution of Apis melifera, the European Honeybee]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. \u00a9 S\u00e9mhur. <\/span>CC BY-SA 2.0<\/span><\/a>.<\/span> <\/span><\/li>\n
  13. Kaplan, Kim. (2006-2014). Annual Survey Reports on U.S. Honey Bee Losses. U.S. Department of Agriculture. <\/span><\/li>\n
  14. CSIRO (Pitsas, Nick). (2007). CSIRO ScienceImage 6807 Dr Denis Anderson of CSIRO Entomology examining in a hive at a cherry farm near Young New South Wales. [Photograph]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>.<\/span> \u00a9 CSIRO. <\/span>CC BY 3.0<\/span><\/a>.<\/span><\/li>\n
  15. De Rossi, Giulia. (2014). [Diagram describing possible causes of Colony Collapse Disorder]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. \u00a9 DensityDesign Research Lab. <\/span>CC BY-SA 4.0<\/span><\/a>.<\/span><\/li>\n
  16. Shebs, Stan. (2008). [Photograph of sunflower]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>CC BY-SA 3.0.<\/span><\/a> <\/span><\/li>\n
  17. Wylie, Scott. (2009). [Photograph of peach rose]. Retrieved from <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY 2.0. <\/span><\/a><\/li>\n
  18. Manske, Magnus. (2013). [Photograph of cosmos flower]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>CC BY 2.0.<\/span><\/a><\/li>\n
  19. Wylie, Scott. (2009). [Photograph of white rose]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>CC BY 2.0.<\/span><\/a><\/li>\n
  20. Vernon, Alan. (2010). [Photograph of yellow coastal tidy tips flower]. Retrieved from<\/span> <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY 2.0.<\/span><\/a><\/li>\n
  21. Kika De La Garza Subtropical Agricultural Research Center. (2005). [Photograph of varroa mite]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>Public Domain.<\/span><\/a><\/li>\n
  22. Muir, Richard. (1927). [Micrograph of microorganisms]. Retrieved from <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY 4.0.<\/span><\/a><\/li>\n
  23. Strazhnik, Inna. (2014). [Photograph of phorid fly]. Retrieved from <\/span>Phorid.net.<\/span><\/a> <\/span>CC BY 2.0.<\/span><\/a> <\/span><\/li>\n
  24. Rayker, Karunakar. (2010). Honey Bee Macro. [Photograph]. Retrieved from <\/span>FlickrCommons<\/span><\/a>. <\/span>CC BY 2.0.<\/span><\/a><\/li>\n<\/ol>\n\n","rendered":"

    Andrew T. Wood<\/h2>\n

    Colony Collapse Disorder or CCD has decimated the honeybee population. Most scientists agree that it is caused by a combination of factors ranging from the environment, climate change, unknown viruses, and other pathogens. If CCD is not resolved, it will severely damage a multi-billion dollar food industry.<\/h5>\n
    \"Honeybee<\/p>\n

    Figure 1. A European Honeybee (Apis mellifera) gathers nectar from a flower.
    \nPhotograph by James Petts, 2014. CC BY-SA 2.0.<\/p>\n<\/div>\n

    Since 2009, the population of <\/span>Apis mellifera<\/span>, or the honeybee (Figure 1), has been in continuous decline. Scientists are unsure of what is causing the decline, called <\/span>Colony Collapse Disorder (CCD)<\/span><\/a>, but many researchers hypothesize it stems from numerous factors ranging from the misuse of <\/span>pesticide<\/span><\/a>s<\/span> to <\/span>RNA<\/span><\/a> viruses.<\/span>1,2,3,4,5,6<\/sup><\/span> Diminished populations of honeybees can have a large impact on the quantity of crops produced and the global economy.<\/span>1,3,4,6,7<\/sup><\/span> While there are many possible causes of CCD, microbes, pollutants, and stress factors are the three biggest influences that have contributed to the decline of honeybees.<\/span><\/p>\n

    \"Global<\/p>\n

    Figure 2. Distribution of the honeybee (Apis melifera).
    \nWhile native to Europe, Asia, and Africa, the European Honeybee can now be found around the world.
    \nCourtesy of Semhur, 2011. CC BY-SA 2.0.<\/p>\n<\/div>\n

    Scientists are searching for possible causes of CCD on a microbial level due to the lack of clear indicators on a larger magnitude scale. While CCD only explains a small proportion of losses, it is prevalent in numerous independent populations. The three most researched groups of microbes are viruses, bacteria, and fungi.<\/span>8<\/sup><\/span> <\/span>Virus<\/span><\/a>es<\/span> can change honeybees at the cellular level by altering <\/span>DNA<\/span><\/a> and RNA strands. Scientists have documented around twenty positive RNA viruses, and these viruses can “affect the morphology, physiology, and behavior of bees and have been widely associated with weak and dying <\/span>colonies<\/span><\/a> both historically and recently”.<\/span>8<\/sup><\/span> As a result, it is possible an unknown virus has affected the bees\u2019 cognitive function and inhibited them from returning to the hive.<\/span>9<\/sup><\/span> Healthy bees also attempt to save the hive by removing the infected bees.<\/span>8<\/span>\n<\/p>\n

    Bacteria<\/span><\/a> have the advantage of being highly infectious and target the weak and young bees.<\/span>8<\/sup><\/span> Well known diseases such as the American and European <\/span>foul brood disease<\/span><\/a> infect and kill the <\/span>larvae<\/span><\/a>, but are less hindering towards adults.<\/span>4<\/sup><\/span> Tests have concluded that adults carry lower levels of these infectious bacteria.<\/span>8<\/sup><\/span> A bacterial infection would explain the quick spread of disease within a colony. Lastly, infected bees do not return to the hive, thus an infection would be undetected in the healthy bees.<\/span><\/p>\n

    \"Colony<\/p>\n

    Figure 3.
    \nImage courtesy of Giulia De Rossi, 2014. CC BY-SA 4.0.
    \nSunflower photo by Stan Shebs, 2008. CC BY-SA 3.0.
    \nPeach rose photo by Scott Wylie, 2009. CC BY 2.0.
    \nCosmos photo by Magnus Manse, 2013. CC BY 2.0.
    \nWhite rose photo by Scott Wylie, 2009. CC BY 2.0.
    \nYellow tidy tips photo by Alan Vernon, 2010. CC BY 2.0.
    \nVarroa mites photo by Robert Engelhardt, 2005. Public Domain.
    \nMicrograph of microorganisms by Richard Muir, 1927. CC BY 4.0.
    \nPhorid fly photo by Inna Strazhnik, 2014. CC BY 2.0.
    \nHoney bee photo by Karunakar Rayker, 2010. CC BY 2.0.<\/p>\n<\/div>\n

    Fungi also have many ways of spreading around the colony and killing larvae.<\/span>8<\/sup><\/span> Fungi can spread both vertically and horizontally. Vertically would be the queen passing it her brood during reproduction, whereas horizontally, hive mates transfer the fungi to each other by their close approximations within the hive. Bees have evolved to try to combat this spread, but their methods may sometimes cause more harm than good. For example, hives can produce special worker bees that \u201crecognize larvae infected with chalkbrood <\/span>fungus<\/span><\/a> earlier in the disease process than workers from typical colonies, and subsequently remove the larvae before spore maturation”.<\/span>8<\/sup><\/span> Other less specialized workers remove the dead from the hive or eat them in an attempt to rid the colony of <\/span>pathogen<\/span><\/a>s<\/span>.<\/span>8<\/sup><\/span> This is problematic because diseases can spread from the dead to the living when the worker bees eat them or come into contact with them. One possible reason why bees leave the hive is because workers detect the sickness and send them away to die. However, the queen is rarely sick and that may point to a horizontal disease path.<\/span>2<\/span>\n<\/p>\n

    Other stressors have also been known to affect bee health. Scientists are becoming more interested in the interaction of the environmental factors which include <\/span>habitat<\/span><\/a> loss and <\/span>climate change<\/span><\/a>. Climate change may impact organization levels of bee hierarchy by \u201cchanging the temporal activity of bees\u201d.<\/span>7<\/sup><\/span> Plant <\/span>biodiversity<\/span><\/a> in many regions of the world has changed due to the introduction of foreign plants, pathogens, and other species of insects.<\/span>7<\/sup><\/span> Some foreign plants were introduced to provide better resources for the bees. Other plants and bees have been introduced into the region and have caused new pathogens to come into contact with native honeybees.<\/span>7<\/sup><\/span> Transplanted bees have an extremely difficult time adjusting to their new environment. Bees have to constantly move from location to location to <\/span>pollinate<\/span><\/a> crops around the United States, and as more colonies die, the healthy colonies must work harder to pollinate<\/span>8 <\/sup><\/span>(Figure 4). Lastly, the interaction of the foreign objects with the indigenous species can cause diseases to pass and mutate.<\/span><\/p>\n

    \"Gradual<\/p>\n

    Figure 4. Reported Annual Honeybee Losses in the U.S.
    \nAnnual surveys conducted by the U.S. Department of Agriculture and collaborators show that since the winter of 2006\/2007, honeybee mortality has remained above the level that beekeepers consider economically sustainable (18.9%).
    \nData from Kim Kaplan, 2006-2014.<\/p>\n<\/div>\n

    Human made chemicals are also detrimental to the health of honeybees.<\/span>3,4,6,10<\/sup><\/span> The <\/span>Environmental Protection Agency (EPA)<\/span><\/a> has tested the <\/span>active ingredient<\/span><\/a>s<\/span> in nearly all chemical compounds and they have deemed these compounds safe for use in mass application. Many of the benign chemicals in <\/span>insecticide<\/span><\/a>s<\/span> may not be entirely harmless. This is because they are considered non-active and do not face the same rigors of testing by the EPA. These \u2018inactive\u2019 chemicals may harm honeybees as well as other insects. They may also \u201calter honeybee <\/span>gene<\/span><\/a> expression for detoxification pathways and may down-regulate gene products\u201d<\/span>10<\/sup><\/span> and \u201calter physiological functions, immune responses, and detoxification functions in the host bees rendering them more susceptible to pathogens and pesticides\u201d.<\/span>10 <\/sup><\/span>The physical and mental health risks involved with these chemicals can either make bees sick through pathogens or can slowly kill them, and may also lead to higher mortality rates of future generations.<\/span>10<\/sup><\/span>\n<\/p>\n

    Researching the causes of Colony Collapse Disorder is important because bees increase the yield of 96% of the crops that require animal pollination, and 75% of all crops that require insect pollination.<\/span>7<\/sup><\/span> The global annual economic value of insect pollination was estimated at 153 billion Euros in 2005<\/span>7<\/sup><\/span> (190.4 billion U.S. Dollars).<\/span><\/span> Without honeybees to pollinate wild plants and cultivated crops, the global food industry would have to use artificial means for pollination and this would vastly increase the price of food products.<\/span>1,3,4,7<\/sup><\/span> Honeybees are essential if humans hope to continue producing cheap food and food byproducts. In conclusion, honeybees are important to the humans because they affect the success of so many products used in our daily needs. Remedying Colony Collapse Disorder is imperative to ensure honeybee survival.<\/span><\/p>\n

    \"Beekeeper<\/p>\n

    Figure 5. A beekeeper inspects a honeybee hive at a cherry farm in South Wales. Honeybees are often moved from farm to farm in order to pollinate crops.
    \nPhotograph by Nick Pitsas, 2007. CC BY 3.0.<\/p>\n<\/div>\n

    \n

    References<\/h4>\n
      \n
    1. Associated Press. (20017, May). Declining Honeybees a \u2018threat\u2019 to Food Supply. MSNBC.<\/span><\/li>\n
    2. Dainat, B., et al. (2012). Colony collapse disorder in Europe. Environmental Microbiology Reports. 123-125<\/span><\/li>\n
    3. Holland, Jennifer (2013, May 10). The Plight of the Honeybee. National Geographic. <\/span><\/li>\n
    4. Plumer, Brad (2013, May 3). Why are bees dying? The U.S. and Europe have different theories. The Washington Post.<\/span><\/li>\n
    5. Van Engelsdorp, D., et al. (2009). Colony Collapse Disorder: A Descriptive Study. Plos One. 4.8:1-17.<\/span><\/li>\n
    6. Walsh, Bryan (2013, May 7). Beepocalypse Redux: Honeybees Are Still Dying \u2014 and We Still Don’t Know Why. Time.<\/span><\/li>\n
    7. Potts, S., et al. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution. 25.6:345-353.<\/span><\/li>\n
    8. Evans, J.D., & Schwarz, R.S. (2011). Bees brought to their knees: microbes affecting honey bee health. Trends in Microbiology. 19.12:614-620.<\/span><\/li>\n
    9. Bromenshenk, J., et al. (2010). Iridovirus and Microsporidian Linked to Honey Bee Colony Decline. Plos One. 5(10):1-11<\/span><\/li>\n
    10. Berry, J.A., et al. (2013). Field-Level Sublethal Effects of Approved Bee Hive Chemicals on Honey Bees (Apis mellifera L). Plos One. 8(10):1-7<\/span><\/li>\n
    11. Petts, James. (2014). [Photograph of honeybee gathering nectar]. Retrieved from <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY-SA 2.0.<\/span><\/a><\/li>\n
    12. S\u00e9mhur. 2011. [Map of the distribution of Apis melifera, the European Honeybee]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. \u00a9 S\u00e9mhur. <\/span>CC BY-SA 2.0<\/span><\/a>.<\/span> <\/span><\/li>\n
    13. Kaplan, Kim. (2006-2014). Annual Survey Reports on U.S. Honey Bee Losses. U.S. Department of Agriculture. <\/span><\/li>\n
    14. CSIRO (Pitsas, Nick). (2007). CSIRO ScienceImage 6807 Dr Denis Anderson of CSIRO Entomology examining in a hive at a cherry farm near Young New South Wales. [Photograph]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>.<\/span> \u00a9 CSIRO. <\/span>CC BY 3.0<\/span><\/a>.<\/span><\/li>\n
    15. De Rossi, Giulia. (2014). [Diagram describing possible causes of Colony Collapse Disorder]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. \u00a9 DensityDesign Research Lab. <\/span>CC BY-SA 4.0<\/span><\/a>.<\/span><\/li>\n
    16. Shebs, Stan. (2008). [Photograph of sunflower]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>CC BY-SA 3.0.<\/span><\/a> <\/span><\/li>\n
    17. Wylie, Scott. (2009). [Photograph of peach rose]. Retrieved from <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY 2.0. <\/span><\/a><\/li>\n
    18. Manske, Magnus. (2013). [Photograph of cosmos flower]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>CC BY 2.0.<\/span><\/a><\/li>\n
    19. Wylie, Scott. (2009). [Photograph of white rose]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>CC BY 2.0.<\/span><\/a><\/li>\n
    20. Vernon, Alan. (2010). [Photograph of yellow coastal tidy tips flower]. Retrieved from<\/span> <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY 2.0.<\/span><\/a><\/li>\n
    21. Kika De La Garza Subtropical Agricultural Research Center. (2005). [Photograph of varroa mite]. Retrieved from <\/span>Wikimedia Commons<\/span><\/a>. <\/span>Public Domain.<\/span><\/a><\/li>\n
    22. Muir, Richard. (1927). [Micrograph of microorganisms]. Retrieved from <\/span>Wikimedia Commons.<\/span><\/a> <\/span>CC BY 4.0.<\/span><\/a><\/li>\n
    23. Strazhnik, Inna. (2014). [Photograph of phorid fly]. Retrieved from <\/span>Phorid.net.<\/span><\/a> <\/span>CC BY 2.0.<\/span><\/a> <\/span><\/li>\n
    24. Rayker, Karunakar. (2010). Honey Bee Macro. [Photograph]. Retrieved from <\/span>FlickrCommons<\/span><\/a>. <\/span>CC BY 2.0.<\/span><\/a><\/li>\n<\/ol>\n","protected":false},"author":23485,"menu_order":4,"template":"","meta":{"_candela_citation":"false","CANDELA_OUTCOMES_GUID":"","pb_show_title":"on","pb_short_title":"","pb_subtitle":"","pb_authors":[],"pb_section_license":""},"chapter-type":[47],"contributor":[],"license":[],"class_list":["post-392","chapter","type-chapter","status-publish","hentry","chapter-type-standard"],"part":370,"_links":{"self":[{"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/chapters\/392","targetHints":{"allow":["GET"]}}],"collection":[{"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/chapters"}],"about":[{"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/wp\/v2\/types\/chapter"}],"author":[{"embeddable":true,"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/wp\/v2\/users\/23485"}],"version-history":[{"count":1,"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/chapters\/392\/revisions"}],"predecessor-version":[{"id":486,"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/chapters\/392\/revisions\/486"}],"part":[{"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/parts\/370"}],"metadata":[{"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/chapters\/392\/metadata\/"}],"wp:attachment":[{"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/wp\/v2\/media?parent=392"}],"wp:term":[{"taxonomy":"chapter-type","embeddable":true,"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/pressbooks\/v2\/chapter-type?post=392"},{"taxonomy":"contributor","embeddable":true,"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/wp\/v2\/contributor?post=392"},{"taxonomy":"license","embeddable":true,"href":"https:\/\/courses.lumenlearning.com\/suny-monroe-environmentalbiology\/wp-json\/wp\/v2\/license?post=392"}],"curies":[{"name":"wp","href":"https:\/\/api.w.org\/{rel}","templated":true}]}}