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Colony Collapse Disorder

Colony Collapse Disorder

Overview
Colony collapse disorder (CCD) is a phenomenon in which worker bees from a beehive
Beehive (beekeeping)
A beehive is an enclosed structure in which some honey bee species of the subgenus Apis live and raise their young. Natural beehives are naturally occurring structures occupied by honeybee colonies, while domesticated honeybees live in man-made beehives, often in an apiary. These man-made...

 or European honey bee
European honey bee
The Western honey bee or European honey bee is a species of honey bee. The genus Apis is Latin for "bee", and mellifera comes from Latin melli- "honey" and ferre "to bear"—hence the scientific name means "honey-bearing bee"...

 colony abruptly disappear. While such disappearances have occurred throughout the history of apiculture
Beekeeping
Beekeeping is the maintenance of honey bee colonies, commonly in hives, by humans. A beekeeper keeps bees in order to collect honey and other products of the hive , to pollinate crops, or to produce bees for sale to other beekeepers...

, the term colony collapse disorder was first applied to a drastic rise in the number of disappearances of Western honey bee colonies in North America
North America
North America is a continent wholly within the Northern Hemisphere and almost wholly within the Western Hemisphere. It is also considered a northern subcontinent of the Americas...

 in late 2006. Colony collapse is significant because many agricultural crops worldwide are pollinated
Pollination
Pollination is the process by which pollen is transferred in plants, thereby enabling fertilisation and sexual reproduction. Pollen grains transport the male gametes to where the female gamete are contained within the carpel; in gymnosperms the pollen is directly applied to the ovule itself...

 by bees.
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Encyclopedia
Colony collapse disorder (CCD) is a phenomenon in which worker bees from a beehive
Beehive (beekeeping)
A beehive is an enclosed structure in which some honey bee species of the subgenus Apis live and raise their young. Natural beehives are naturally occurring structures occupied by honeybee colonies, while domesticated honeybees live in man-made beehives, often in an apiary. These man-made...

 or European honey bee
European honey bee
The Western honey bee or European honey bee is a species of honey bee. The genus Apis is Latin for "bee", and mellifera comes from Latin melli- "honey" and ferre "to bear"—hence the scientific name means "honey-bearing bee"...

 colony abruptly disappear. While such disappearances have occurred throughout the history of apiculture
Beekeeping
Beekeeping is the maintenance of honey bee colonies, commonly in hives, by humans. A beekeeper keeps bees in order to collect honey and other products of the hive , to pollinate crops, or to produce bees for sale to other beekeepers...

, the term colony collapse disorder was first applied to a drastic rise in the number of disappearances of Western honey bee colonies in North America
North America
North America is a continent wholly within the Northern Hemisphere and almost wholly within the Western Hemisphere. It is also considered a northern subcontinent of the Americas...

 in late 2006. Colony collapse is significant because many agricultural crops worldwide are pollinated
Pollination
Pollination is the process by which pollen is transferred in plants, thereby enabling fertilisation and sexual reproduction. Pollen grains transport the male gametes to where the female gamete are contained within the carpel; in gymnosperms the pollen is directly applied to the ovule itself...

 by bees.

European beekeepers observed similar phenomena in Belgium, France, the Netherlands, Greece, Italy, Portugal, and Spain, and initial reports have also come in from Switzerland and Germany
Germany
Germany , officially the Federal Republic of Germany , is a federal parliamentary republic in Europe. The country consists of 16 states while the capital and largest city is Berlin. Germany covers an area of 357,021 km2 and has a largely temperate seasonal climate...

, albeit to a lesser degree while the Northern Ireland Assembly
Northern Ireland Assembly
The Northern Ireland Assembly is the devolved legislature of Northern Ireland. It has power to legislate in a wide range of areas that are not explicitly reserved to the Parliament of the United Kingdom, and to appoint the Northern Ireland Executive...

 received reports of a decline greater than 50%. Possible cases of CCD have also been reported in Taiwan
Taiwan
Taiwan , also known, especially in the past, as Formosa , is the largest island of the same-named island group of East Asia in the western Pacific Ocean and located off the southeastern coast of mainland China. The island forms over 99% of the current territory of the Republic of China following...

 since April 2007.

The cause or causes of the syndrome are not yet understood. In 2007, some authorities attributed the problem to biotic
Biotic component
Biotic components are the living things that shape an ecosystem. A biotic factor is any living component that affects another organism, including animals that consume the organism in question, and the living food that the organism consumes. Each biotic factor needs energy to do work and food for...

 factors such as Varroa
Varroa
Varroa is a genus of parasitic mites associated with honey bees, placed in its own family, Varroidae. The genus was named for Marcus Terentius Varro, a Roman scholar who was also a beekeeper.-History and behavior:...

mites and insect diseases (i.e., pathogens including Nosema apis
Nosema apis
Nosema apis is a microsporidian, a small, unicellular parasite that mainly affects honey bees. It causes nosemosis, also called nosema, which is the most widespread of adult honey bee diseases. The dormant stage of Nosema apis is a long lived spore which is resistant to temperature extremes and...

and Israel acute paralysis virus). Other proposed causes include environmental change-related stresses, malnutrition
Malnutrition
Malnutrition is the condition that results from taking an unbalanced diet in which certain nutrients are lacking, in excess , or in the wrong proportions....

, pesticide
Pesticide toxicity to bees
Pesticides vary in their effects on bees. Contact pesticides are usually sprayed on plants and can kill bees when they crawl over sprayed surfaces of plants or other media...

s (e.g.. neonicotinoids
Neonicotinoids
Neonicotinoids are a class of insecticides which act on the central nervous system of insects with lower toxicity to mammals. Neonicotinoids are among the most widely used insecticides worldwide, but recently the uses of some members of this class have been restricted in some countries due to a...

 such as clothianidin
Clothianidin
Clothianidin is an insecticide developed by Takeda Chemical Industries and Bayer AG. Similar to thiamethoxam and imidacloprid, it is a neonicotinoid. Neonicotinoids are a class of insecticides which act on the central nervous system of insects with lower toxicity to mammals...

 and imidacloprid
Imidacloprid
Imidacloprid is a nicotine-based, systemic insecticide, which acts as a neurotoxin and belongs to a class of chemicals called the neonicotinoids. Although it is now off patent, the primary manufacturer of this chemical is Bayer CropScience,...

), and migratory beekeeping. More speculative possibilities have included both cell phone radiation and genetically modified (GM) crops
Genetically modified food
Genetically modified foods are foods derived from genetically modified organisms . Genetically modified organisms have had specific changes introduced into their DNA by genetic engineering techniques...

 with pest control
Pest control
Pest control refers to the regulation or management of a species defined as a pest, usually because it is perceived to be detrimental to a person's health, the ecology or the economy.-History:...

 characteristics.

It has also been suggested that it may be due to a combination of many factors and that no single factor is the cause. The most recent report (USDA - 2010) states that "based on an initial analysis of collected bee samples (CCD- and non-CCD affected), reports
have noted the high number of viruses and other pathogens, pesticides, and parasites present in
CCD colonies, and lower levels in non-CCD colonies. This work suggests that a combination of
environmental stressors may set off a cascade of events and contribute to a colony where
weakened worker bees are more susceptible to pests and pathogens." Applying proteomics
Proteomics
Proteomics is the large-scale study of proteins, particularly their structures and functions. Proteins are vital parts of living organisms, as they are the main components of the physiological metabolic pathways of cells. The term "proteomics" was first coined in 1997 to make an analogy with...

-based pathogen screening tools in 2010, researchers announced they had identified a co-infection of invertebrate iridescent virus
Iridoviridae
Iridoviridae are a family of viruses with double stranded DNA genomes. The name is derived from Iris the Greek goddess of the rainbow. This name was chosen because of the "rainbow like" iridescence observed in heavily infected insects and pelleted samples of invertebrate iridoviruses.-Taxonomy:The...

 type 6 (IIV-6) and the fungus Nosema ceranae
Nosema ceranae
Nosema ceranae is a microsporidian, a small, unicellular parasite that mainly affects Apis cerana, the Asiatic honey bee. It may cause nosemosis, also called nosema...

in all CCD colonies sampled. However, subsequent studies have questioned the methodology used in these proteomic experiments.

History


From 1972 to 2006, there was a dramatic reduction in the number of feral
Feral
A feral organism is one that has changed from being domesticated to being wild or untamed. In the case of plants it is a movement from cultivated to uncultivated or controlled to volunteer. The introduction of feral animals or plants to their non-native regions, like any introduced species, may...

 honey bees in the U.S. (now almost absent) and a significant though somewhat gradual decline in the number of colonies maintained by beekeepers. This decline includes the cumulative losses from all factors, such as urbanization
Urbanization
Urbanization, urbanisation or urban drift is the physical growth of urban areas as a result of global change. The United Nations projected that half of the world's population would live in urban areas at the end of 2008....

, pesticide use, tracheal
Acarapis woodi
Acarapis woodi is a mite that is an internal parasite of honey bees, originally described from the Isle of Wight. Tracheal mites are related to spiders and have eight legs. Acarapis woodi live and reproduce in the tracheae of the bees...

 and Varroa
Varroa
Varroa is a genus of parasitic mites associated with honey bees, placed in its own family, Varroidae. The genus was named for Marcus Terentius Varro, a Roman scholar who was also a beekeeper.-History and behavior:...

mites, and commercial beekeeper
Beekeeper
A beekeeper is a person who keeps honey bees for the purposes of securing commodities such as honey, beeswax, pollen, royal jelly; pollinating fruits and vegetables; raising queens and bees for sale to other farmers; and/or for purposes satisfying natural scientific curiosity...

s' retiring and going out of business. However, in late 2006 and early 2007 the rate of attrition was alleged to have reached new proportions, and the term "colony collapse disorder" began to be used to describe this sudden rash of disappearances, (sometimes referred to as Spontaneous Hive Collapse or the Mary Celeste
Mary Celeste
The Mary Celeste was an American brigantine merchant ship famous for having been discovered on 4 December 1872, in the Atlantic Ocean unmanned and apparently abandoned , despite the fact that the weather was fine and her crew had been experienced and able...

 Syndrome in the United Kingdom).

Losses had remained stable since the 1990s at 17%-20% per year attributable to a variety of factors, such as mites, diseases, and management stress. The first report of CCD was in mid-November 2006 by a Pennsylvania beekeeper overwintering
in Florida. By February 2007, large commercial migratory beekeepers in several states had
reported heavy losses associated with CCD. Their reports of losses varied widely, ranging from
30% to 90% of their bee colonies; in some cases beekeepers reported loss of nearly all of their
colonies with surviving colonies so weakened that they might no longer be viable to
pollinate or produce honey.

Losses were reported in migratory operations wintering in California,
Florida, Oklahoma and Texas. In late February, some larger non-migratory beekeepers in the mid-
Atlantic and Pacific Northwest regions also reported significant losses of more than 50%. Colony losses also were reported in five Canadian provinces, several European countries, and
countries in South and Central America and Asia. In 2010 the USDA reported that data on
overall honey bee losses for 2010 indicated an estimated 34 percent loss, which is statistically
similar to losses reported in 2007, 2008, and 2009.

Limited occurrences resembling CCD have been documented as early as 1869 and this set of symptoms has in the past several decades been given many different names (disappearing disease, spring dwindle, May disease, autumn collapse, and fall dwindle disease). Most recently, a similar phenomenon in the winter of 2004/2005 occurred, and was attributed to Varroa mites (the "Vampire Mite" scare), though this was never ultimately confirmed. Nobody has been able to determine the cause of any past appearances of this syndrome
Syndrome
In medicine and psychology, a syndrome is the association of several clinically recognizable features, signs , symptoms , phenomena or characteristics that often occur together, so that the presence of one or more features alerts the physician to the possible presence of the others...

. Upon recognition that the syndrome does not seem to be seasonally restricted, and that it may not be a "disease" in the standard sense—that there may not be a specific causative agent
Disease causative agent
The term disease causative agent usually refers to a biological agents pathogen that causes a disease. Technically, the term can also refer to a toxin or toxic chemical that causes illness such as parasites or bacteria....

—the syndrome was renamed.

There was a well documented outbreak of colony losses spreading from the Isle of Wight to the rest of the UK in 1906. In retrospect, this was attributed to a combination of factors including adverse weather, intensive apiculture leading to inadequate forage, and a new infection, the chronic bee paralysis virus.
At the time, the cause of this agricultural beekeeping problem was similarly mysterious and unknown.

Signs and symptoms


A colony which has collapsed from CCD is generally characterized by all of these conditions occurring simultaneously:
  • Presence of capped brood in abandoned colonies. Bees normally will not abandon a hive until the capped brood have all hatched.
  • Presence of food stores, both honey
    Honey
    Honey is a sweet food made by bees using nectar from flowers. The variety produced by honey bees is the one most commonly referred to and is the type of honey collected by beekeepers and consumed by humans...

     and bee pollen:
    • i. which are not immediately robbed by other bees
    • ii. which when attacked by hive
      Beehive
      A beehive is a structure in which bees live and raise their young.Beehive may also refer to:Buildings and locations:* Bee Hive, Alabama, a neighborhood in Alabama* Beehive , a wing of the New Zealand Parliament Buildings...

       pests such as wax moth
      Lesser wax moth
      Achroia grisella, the Lesser Wax Moth, is a small moth of the snout moth family , wherein it belongs to the subfamily Galleriinae. It is the only unequivocally recognized species of genus Achroia...

       and small hive beetle
      Small hive beetle
      The small hive beetle is a beekeeping pest.Endemic to sub-Saharan Africa, the small hive beetle, Aethina tumida was first discovered in the United States in 1996 and has now spread to many U.S. states including, Georgia, South Carolina, North Carolina, Pennsylvania, Ohio, Illinois, Minnesota,...

      , the attack is noticeably delayed.
  • Presence of the queen bee
    Queen bee
    The term queen bee is typically used to refer to an adult, mated female that lives in a honey bee colony or hive; she is usually the mother of most, if not all, the bees in the hive. The queens are developed from larvae selected by worker bees and specially fed in order to become sexually mature...

    . If the queen is not present, the hive died because it was queenless, which is not considered CCD.


Precursor symptoms that may arise before the final colony collapse are:
  • Insufficient workforce
    Worker bee
    A Worker bee is any female eusocial bee that lacks the full reproductive capacity of the colony's queen bee; under most circumstances, this is correlated to an increase in certain non-reproductive activities relative to a queen, as well...

     to maintain the brood that is present
  • Workforce seems to be made up of young adult
    Adult
    An adult is a human being or living organism that is of relatively mature age, typically associated with sexual maturity and the attainment of reproductive age....

     bees
  • The colony members are reluctant to consume provided feed, such as sugar syrup and protein supplement
    Dietary supplement
    A dietary supplement, also known as food supplement or nutritional supplement, is a preparation intended to supplement the diet and provide nutrients, such as vitamins, minerals, fiber, fatty acids, or amino acids, that may be missing or may not be consumed in sufficient quantities in a person's diet...

    .

North America


The National Agriculture Statistics Service reported that there were 2.44 million honey-producing hives in the United States as of February 2008, down from 4.5 million in 1980, and 5.9 million in 1947, though these numbers underestimate the total number of managed hives as they exclude several thousand hives managed for pollination contracts only, and also do not include hives managed by beekeepers owning fewer than 5 hives. This under-representation may be offset by the practice of counting some hives more than once; hives that are moved to different states to produce honey are counted in each state's total and summed in total counts.

Non-CCD winter losses as high as 50% have occurred in some years and regions (e.g., 2000-2001 in Pennsylvania
Pennsylvania
The Commonwealth of Pennsylvania is a U.S. state that is located in the Northeastern and Mid-Atlantic regions of the United States. The state borders Delaware and Maryland to the south, West Virginia to the southwest, Ohio to the west, New York and Ontario, Canada, to the north, and New Jersey to...

). Normal winter losses are typically considered to be in the range of 15-25%. In many cases beekeepers reporting significant losses of bees did not experience true CCD, but losses due to other causes.

In 2007 in the U.S., at least 24 different states as well as portions of Canada had reported at least one case of CCD. In a 2007 survey of 384 responding beekeepers from 13 states 23.8% met the specified criterion for CCD (that 50% or more of their dead colonies were found without bees and/or with very few dead bees in the hive or apiary).

In the U.S. in 2006-2007, CCD-suffering operations had a total loss of 45% compared to the total loss of 25% of all colonies experienced by non-CCD suffering beekeepers.

A 2007-2008 survey of over 19% of all colonies revealed a total loss of 35.8%. Operations that pollinated almonds lost, on average, the same number of colonies as those that did not. The 37.9% of operations that reported having at least some of their colonies die with a complete lack of bees had a total loss of 40.8% of colonies compared to the 17.1% loss reported by beekeepers without this symptom. Large operations were more likely to have this symptom suggesting that a contagious condition may be a causal factor. Sixty percent of all colonies that were reported dead in this survey died without the presence of dead bees in the hive, and thus possibly suffered from CCD.

In 2010, the USDA reported that data on
overall honey bee losses for the year indicate an estimated 34% loss, which is statistically similar to losses reported in 2007, 2008, and 2009.

Europe


According to the European Food Safety Authority (EFSA), in 2007 the United Kingdom had 274,000 hives, Italy had 1,091,630, and France 1,283,810. In 2008 the British Bee Keepers Association reported that the bee population in the United Kingdom dropped by around 30% between 2007 and 2008, and an EFSA study revealed that in Italy the mortality rate was 40-50%. However EFSA officials point out that the figures are not very reliable because before the bees started dying there was no harmonisation in the way different countries collected statistics on their bee populations. At that time (2008) the reports blamed the high death rate on the varroa mite, two seasons of unusually wet European summers, and some pesticides.

In 2010, David Aston of the British Beekeepers’ Association stated, "We still do not believe CCD (which is now better defined) is a cause of colony losses in the UK, however we are continuing to experience colony losses, many if not most of which can be explained". He feels that recent studies suggest "further evidence to the evolving picture that there are complex interactions taking place between a number of factors, pathogens, environmental, beekeeping practices and other stressors, which are causing honey bee losses described as CCD in the US".

In 2009, Tim Lovett, president of the British Beekeepers' Association, said: "Anecdotally, it is hugely variable. There are reports of some beekeepers losing almost a third of their hives and others losing none. John Chapple, chairman of the London Beekeepers' Association, put losses among his 150 members at between a fifth and a quarter. "There are still a lot of mysterious disappearances; we are no nearer to knowing what is causing them." The government's National Bee Unit continued to deny the existence of CCD in Britain; it attributes the heavy losses to the varroa mite and rainy summers that stop bees foraging for food.

Bee keepers in Scotland also reported losses for the past three years. Andrew Scarlett, a Perthshire-based bee farmer and honey packer, lost 80% of his 1,200 hives during the 2009 winter. He attributed the losses to a virulent bacterial infection that quickly spread because of a lack of bee inspectors, coupled with sustained poor weather that prevented honeybees from building up sufficient pollen and nectar stores.

In Germany, where some of the first reports of CCD in Europe appeared, and where, according to the German national association of beekeepers, 40% of the honey bee colonies died, there was no scientific confirmation; , the German media were reporting that no confirmed CCD cases seemed to have occurred in Germany.

Possible causes


The mechanisms of CCD are still unknown, but many causes have been proposed as causative agent
Disease causative agent
The term disease causative agent usually refers to a biological agents pathogen that causes a disease. Technically, the term can also refer to a toxin or toxic chemical that causes illness such as parasites or bacteria....

s; malnutrition, pathogen
Pathogen
A pathogen gignomai "I give birth to") or infectious agent — colloquially, a germ — is a microbe or microorganism such as a virus, bacterium, prion, or fungus that causes disease in its animal or plant host...

s, immunodeficiencies
Immunodeficiency
Immunodeficiency is a state in which the immune system's ability to fight infectious disease is compromised or entirely absent. Immunodeficiency may also decrease cancer immunosurveillance. Most cases of immunodeficiency are acquired but some people are born with defects in their immune system,...

, mite
Mite
Mites, along with ticks, are small arthropods belonging to the subclass Acari and the class Arachnida. The scientific discipline devoted to the study of ticks and mites is called acarology.-Diversity and systematics:...

s, fungus
Fungus
A fungus is a member of a large group of eukaryotic organisms that includes microorganisms such as yeasts and molds , as well as the more familiar mushrooms. These organisms are classified as a kingdom, Fungi, which is separate from plants, animals, and bacteria...

, pesticide
Pesticide toxicity to bees
Pesticides vary in their effects on bees. Contact pesticides are usually sprayed on plants and can kill bees when they crawl over sprayed surfaces of plants or other media...

s, beekeeping practices (such as the use of antibiotics, or long-distance transportation of beehives) and electromagnetic radiation
Electromagnetic radiation
Electromagnetic radiation is a form of energy that exhibits wave-like behavior as it travels through space...

. Whether any single factor or a combination of factors (acting independently in different areas affected by CCD, or acting in tandem) is responsible is still unknown, however most recent information suggests a combination of factors is most likely. It is likewise still uncertain whether CCD is a genuinely new phenomenon as opposed to a known phenomenon that previously only had a minor impact.

At present, the primary source of information, and the presumed "lead" group investigating the phenomenon, is the Colony Collapse Disorder Working Group, based primarily at Pennsylvania State University
Pennsylvania State University
The Pennsylvania State University, commonly referred to as Penn State or PSU, is a public research university with campuses and facilities throughout the state of Pennsylvania, United States. Founded in 1855, the university has a threefold mission of teaching, research, and public service...

. Their preliminary report pointed out some patterns but drew no strong conclusions. A survey of beekeepers early in 2007 indicated that most hobbyist beekeepers believed that starvation was the leading cause of death in their colonies while commercial beekeepers overwhelmingly believed that invertebrate pests (Varroa mites, honey bee tracheal mites, and/or small hive beetles) were the leading cause of colony mortality. A scholarly review in June 2007 similarly addressed numerous theories and possible contributing factor, but left the issue unresolved.

In July 2007, the United States Department of Agriculture
United States Department of Agriculture
The United States Department of Agriculture is the United States federal executive department responsible for developing and executing U.S. federal government policy on farming, agriculture, and food...

 (USDA) released its "CCD Action Plan", which outlined a strategy for addressing CCD consisting of four main components:
  1. survey and data collection;
  2. analysis of samples;
  3. hypothesis-driven research; and
  4. mitigation and preventative action.


In July 2009, the first annual report of the U.S. Colony Collapse Disorder Steering Committee was published. It suggested that colony collapse may be caused by the interaction of many agents in combination.

Similarly, in 2009 the CCD Working Group published a comprehensive descriptive study that concluded: "Of the 61 variables quantified (including adult bee physiology, pathogen loads, and pesticide levels), no single factor was found with enough consistency to suggest one causal agent. Bees in CCD colonies had higher pathogen loads and were co-infected with more pathogens than control populations, suggesting either greater pathogen exposure or reduced defenses in CCD bees."

The second annual Steering Committee report was released in November 2010. The group reported that although many associations, including pesticides, parasites, and pathogens have been identified throughout the course of research, "it is becoming increasingly clear that no single factor alone is responsible for [CCD]". Their findings indicated an absence of damaging levels of the parasite Nosema or parasitic Varroa mites at the time of collapse.

They did find an association of sub-lethal effects of some pesticides with CCD, including two common miticides in particular, coumaphos and fluvalinate, which are pesticides registered for use by beekeepers to control varroa mites. It was reported that studies also identified sub-lethal effects of neonicotinoids and fungicides, pesticides that may impair the bee's immune system. It is hypothesized that these pesticides impair the bee’s immune system, which leaves the bee more susceptible to bee viruses.

A large survey of healthy and CCD-affected colonies also revealed elevated levels of pesticides in wax and pollen, but the amounts of pesticides were similar in both failing and healthy hives. They also confirmed suspected links between CCD and poor colony health, inadequate diet, and long-distance transportation. Studies continue to show very high levels of pathogens in CCD-affected samples and lower pathogen levels in non-affected samples, consistent with the empirical observation that healthy honey bee colonies normally fend off pathogens. These observations have led to the hypothesis that bee declines are resulting from immune suppression.

Selective commercial breeding and lost genetic diversity in industrial apiculture


Most of the focus on CCD has been towards environmental factors. CCD is a condition recognised for greatest impact in regions of 'industrial' or agricultural use of commercially bred bee colonies. Natural breeding and colony reproduction of wild bees is a complex and highly selective process, leading to a diverse genetic makeup
Genetic diversity
Genetic diversity, the level of biodiversity, refers to the total number of genetic characteristics in the genetic makeup of a species. It is distinguished from genetic variability, which describes the tendency of genetic characteristics to vary....

 in large populations of bees, both within and between colonies. Genetic diversity
Genetic diversity
Genetic diversity, the level of biodiversity, refers to the total number of genetic characteristics in the genetic makeup of a species. It is distinguished from genetic variability, which describes the tendency of genetic characteristics to vary....

 through sexual reproduction is a significant evolutionary factor in resistance to parasites and infectious diseases. Many artificially bred species, especially domestic and agricultural species suffer from lack of genetic variation, resulting in increased risk of hereditable diseases, loss of vitality or vigour
Heterosis
Heterosis, or hybrid vigor, or outbreeding enhancement, is the improved or increased function of any biological quality in a hybrid offspring. The adjective derived from heterosis is heterotic....

, and heightened uniform susceptibility to infectious diseases. Industrial apiculture has adopted highly selective breeding programs for uniform desired traits, seasonal transportation of colonies over vast distances causes increased infectious exposures from mixing of domestic and residual wild populations, and brood incubation conditions may be stressful with respect to deficient nutrition, temperature and other basics. This combination of ecological factors, especially the host factor of loss of genetic variation and hybrid vigor, may account for the apparent multifactorial environmental 'causes' of CCD including concurrent infections.

Malnutrition


One of the patterns reported by the group at Pennsylvania State was that all producers in a preliminary survey noted a period of "extraordinary stress" affecting the colonies in question prior to their die-off, most commonly involving poor nutrition and/or drought. This is the only factor that all of the cases of CCD had in common in this report; accordingly, there is at least some significant possibility that the phenomenon is correlated to nutritional stress and may not manifest in healthy, well-nourished colonies. This is similar to the findings of a later independent survey in which small-scale beekeeping operations (up to 500 colonies) in several states reported their belief that malnutrition and/or weak colonies was the factor responsible for their bees dying in over 50% of the cases, whether the losses were believed to be due to CCD or not.

Some researchers have attributed the syndrome to the practice of feeding high-fructose corn syrup (HFCS) to supplement winter stores. The variability of HFCS may be relevant to the apparent inconsistencies of results. European commentators have suggested a possible connection with HFCS produced from genetically modified corn. If this were the sole factor involved, however, this should also lead to the exclusive appearance of CCD in wintering colonies being fed HFCS, but many reports of CCD occur in other contexts with beekeepers who do not use HFCS.

Other researchers state that colony collapse disorder is mainly a problem of feeding the bees a monoculture
Monoculture
Monoculture is the agricultural practice of producing or growing one single crop over a wide area. It is also known as a way of farming practice of growing large stands of a single species. It is widely used in modern industrial agriculture and its implementation has allowed for large harvests from...

 diet when they should receive food from a variety of sources/plants. In winter the bees are given a single food source such as corn syrup
Corn syrup
Corn syrup is a food syrup, which is made from the starch of maize and contains varying amounts of maltose and higher oligosaccharides, depending on the grade. Corn syrup is used in foods to soften texture, add volume, prevent crystallization of sugar, and enhance flavor...

 (high-fructose or other), sugar and pollen substitute. In summer they may only pollinate a single crop (e.g., almonds, cherries, or apples).

A study published in 2010 found that bees that were fed pollen from a variety of different plant species showed signs of having a healthier immune system than those eating pollen from a single species. Bees fed pollen from five species had higher levels of glucose oxidase
Glucose oxidase
The glucose oxidase enzyme is an oxido-reductase that catalyses the oxidation of glucose to hydrogen peroxide and D-glucono-δ-lactone. In cells, it aids in breaking the sugar down into its metabolites....

 than bees fed pollen from one species, even if the pollen had a higher protein content. The authors hypothesised that CCD may be linked to a loss of plant diversity.

Pathogens and immunodeficiency theories


Some researchers have commented that the pathway of propagation functions in the manner of a contagious disease
Contagious disease
A contagious disease is a subset category of infectious diseases , which are easily transmitted by physical contact with the person suffering the disease, or by their secretions or objects touched by them....

; however, there is some sentiment that the disorder may involve an immunosuppressive
Immunosuppression
Immunosuppression involves an act that reduces the activation or efficacy of the immune system. Some portions of the immune system itself have immuno-suppressive effects on other parts of the immune system, and immunosuppression may occur as an adverse reaction to treatment of other...

 mechanism, potentially linked to the aforementioned "stress" leading to a weakened immune system. Specifically, according to researchers at Pennsylvania State: "The magnitude of detected infectious agents in the adult bees suggests some type of immunosuppression". These researchers initially suggested a connection between Varroa destructor
Varroa destructor
Varroa destructor is an external parasitic mite that attacks honey bees Apis cerana and Apis mellifera. The disease caused by the mites is called varroatosis....

mite infestation and CCD, suggesting that a combination of these bee mites, deformed wing virus
Deformed Wing Virus
Deformed wing virus is an RNA virus, one of 18 known viruses affecting the honey bee, Apis mellifera. The virus was first isolated from a sample of symptomatic honeybees from Japan in the early 1980s and is currently distributed worldwide....

 (which the mites transmit) and bacteria work together to suppress immunity and may be one cause of CCD. This research group is reported to be focusing on a search for possible viral, bacterial, or fungal pathogens which may be involved.

When a colony is dying, for whatever cause, and there are other healthy colonies nearby (as is typical in a bee yard), those healthy colonies often enter the dying colony and rob its provisions for their own use. If the dying colony's provisions were contaminated (by natural or man-made toxins), the resulting pattern (of healthy colonies becoming sick when in proximity to a dying colony) might suggest to an observer that a contagious disease is involved. However, it is typical in CCD cases that provisions of dying colonies are not being robbed, suggesting that at least this particular mechanism (toxins being spread via robbing, thereby mimicking a disease) is not involved in CCD. Additional evidence that CCD is an infectious disease came from the following observations: the hives of colonies that had died from CCD could be reused with a healthy colony only if they were first treated with DNA-destroying radiation, and the CCD Working Group report in 2010 indicated that CCD-exhibiting hives tended to occur in proximity to one another within apiaries.

Varroa and Israel acute paralysis virus


According to a 2007 article, the mite
Mite
Mites, along with ticks, are small arthropods belonging to the subclass Acari and the class Arachnida. The scientific discipline devoted to the study of ticks and mites is called acarology.-Diversity and systematics:...

s Varroa destructor
Varroa destructor
Varroa destructor is an external parasitic mite that attacks honey bees Apis cerana and Apis mellifera. The disease caused by the mites is called varroatosis....

remain the world's most destructive honey bee killer due in part to the virus
Virus
A virus is a small infectious agent that can replicate only inside the living cells of organisms. Viruses infect all types of organisms, from animals and plants to bacteria and archaea...

es they carry, including deformed wing virus
Deformed Wing Virus
Deformed wing virus is an RNA virus, one of 18 known viruses affecting the honey bee, Apis mellifera. The virus was first isolated from a sample of symptomatic honeybees from Japan in the early 1980s and is currently distributed worldwide....

 and acute bee paralysis virus, which have both been implicated in CCD. Affliction with Varroa mites also tends to weaken the immune system
Immune system
An immune system is a system of biological structures and processes within an organism that protects against disease by identifying and killing pathogens and tumor cells. It detects a wide variety of agents, from viruses to parasitic worms, and needs to distinguish them from the organism's own...

 of the bees. Dr. Enesto Guzman, an entomological researcher at the University of Guelph
University of Guelph
The University of Guelph, also known as U of G, is a comprehensive public research university in Guelph, Ontario, Canada. It was established in 1964 after the amalgamation of Ontario Agricultural College, the Macdonald Institute, and the Ontario Veterinary College...

 in Canada, studied 413 Ontario
Ontario
Ontario is a province of Canada, located in east-central Canada. It is Canada's most populous province and second largest in total area. It is home to the nation's most populous city, Toronto, and the nation's capital, Ottawa....

 bee colonies in 2007-08. About 27% of hives did not survive the winter, and the Varroa
Varroa destructor
Varroa destructor is an external parasitic mite that attacks honey bees Apis cerana and Apis mellifera. The disease caused by the mites is called varroatosis....

 mite was identified as the cause in 85% of the cases. As such, Varroa mites have been considered as a possible cause of CCD, though not all dying colonies contain these mites.

In September 2007, results of a large-scale statistical RNA
RNA
Ribonucleic acid , or RNA, is one of the three major macromolecules that are essential for all known forms of life....

 sequencing
Sequencing
In genetics and biochemistry, sequencing means to determine the primary structure of an unbranched biopolymer...

 study of afflicted and unafflicted colonies were reported. RNA from all organisms in a colony was sequenced and compared with sequence databases to detect the presence of pathogens. The study used technology from 454 Life Sciences
454 Life Sciences
454 Life Sciences, is a biotechnology company based in Branford, Connecticut. It is a subsidiary of Roche, and specializes in high-throughput DNA sequencing.-History and Major Achievements:...

 developed for human genome sequencing. All colonies were found to be infected with numerous pathogens, but only the Israel acute paralysis virus (IAPV) showed a significant association with CCD: the virus was found in 25 of the 30 tested CCD colonies, and only in one of the 21 tested non-CCD colonies. Scientists pointed out that this association was no proof of causation, and other factors may also be involved in the disease or the presence of IAPV may only be a marker signifying afflicted colonies and not the actual causative agent. To prove causation, experiments are planned to deliberately infect colonies with the virus.

The IAPV was discovered in 2004, and belongs to the Dicistroviridae
Dicistroviridae
The Dicistroviridae are a family of Group IV insect-infecting viruses. Some of the insects commonly infected by dicistroviruses include aphids, leafhoppers, flies, bees, ants, silkworms.-Taxonomy:...

. It causes paralysis in bees which then die outside the hive. It can be transmitted by the mite Varroa destructor. These mites, however, were found in only half of the CCD colonies.

The virus was also found in samples of Australian honey bees. Australian honey bees have been imported into the U.S. since 2004, and until recently, it was thought possible that this is how the virus originally reached North America. Recent findings, however, reveal the virus has been present in American bees since 2002.

Recent research (2009) has found that an indicator for an impaired protein
Protein
Proteins are biochemical compounds consisting of one or more polypeptides typically folded into a globular or fibrous form, facilitating a biological function. A polypeptide is a single linear polymer chain of amino acids bonded together by peptide bonds between the carboxyl and amino groups of...

 production is common among all bees affected by CCD, a pattern consistent with IAPV infection. It is conjectured that Dicistroviridae, like the IAPV, cause degradation of the ribosome
Ribosome
A ribosome is a component of cells that assembles the twenty specific amino acid molecules to form the particular protein molecule determined by the nucleotide sequence of an RNA molecule....

s, which are responsible for protein production of cells
Cell (biology)
The cell is the basic structural and functional unit of all known living organisms. It is the smallest unit of life that is classified as a living thing, and is often called the building block of life. The Alberts text discusses how the "cellular building blocks" move to shape developing embryos....

, and that this reduced ribosomal function weakens the bees, making them more vulnerable to factors that might not otherwise be lethal.

Nosema


Some have suggested that the syndrome may be an inability by beekeepers to correctly identify known diseases such as European foulbrood or the microsporidia
Microsporidia
The microsporidia constitute a phylum of spore-forming unicellular parasites. They were once thought to be protists but are now known to be fungi. Loosely 1500 of the probably more than one million species are named now. Microsporidia are restricted to animal hosts, and all major groups of animals...

n fungus Nosema
Nosema apis
Nosema apis is a microsporidian, a small, unicellular parasite that mainly affects honey bees. It causes nosemosis, also called nosema, which is the most widespread of adult honey bee diseases. The dormant stage of Nosema apis is a long lived spore which is resistant to temperature extremes and...

. The testing and diagnosis of samples from affected colonies (already performed) makes this highly unlikely, as the symptoms are fairly well known and differ from what is classified as CCD. A high rate of Nosema infection was reported in samples of bees from Pennsylvania, but this pattern was not reported from samples elsewhere.

Mariano Higes, a scientist heading a team at a government-funded apiculture centre in Guadalajara, Spain
Guadalajara (province)
Guadalajara is a province of central/north-central Spain, in the northern part of the autonomous community of Castile-La Mancha. It is bordered by the provinces of Cuenca, Madrid, Segovia, Soria, Zaragoza, and Teruel...

, has reported that when hives of European honey bees were infected with Nosema ceranae
Nosema ceranae
Nosema ceranae is a microsporidian, a small, unicellular parasite that mainly affects Apis cerana, the Asiatic honey bee. It may cause nosemosis, also called nosema...

, a microsporidian fungus, the colonies were wiped out within eight days. Higes has extrapolated from this research to conclude that CCD is caused by N. ceranae. Higes and his team have worked on this problem since 2000, and claim to have ruled out many other potential causes. However, a 2009 comprehensive survey of CCD-affected bee populations in the United States suggested that CCD likely involves an interaction between pathogens and other stress factors. They reported that their survey found only about half of the colonies sampled, both in CCD and control populations, were infected with N. ceranae.

The primary antifungal agent
Antifungal drug
An antifungal medication is a medication used to treat fungal infections such as athlete's foot, ringworm, candidiasis , serious systemic infections such as cryptococcal meningitis, and others...

 used against Nosema is fumagillin
Fumagillin
Fumagillin is a complex biomolecule and used as an antimicrobial agent. It was isolated in 1949 from the microbial organism Aspergillus fumigatus.-In animals:...

, which has been used in a German research project to reduce the microsporidian's impact, and is mentioned as a possible remedy by the CCDWG. Higes also claims to have successfully cured colonies with fumagillin. A review of these results in the journal Nature described these results as promising, but cautioned "N. ceranae may not be to blame for all cases of colony collapse". Various areas in Europe have reported this fungus, but no direct link to CCD has yet been established.

Highly preliminary evidence of N. ceranae was recently reported in a few hives in the Merced Valley area of California (USA). The researcher did not, however, believe this was conclusive evidence of a link to CCD; "We don't want to give anybody the impression that this thing has been solved". A USDA bee scientist has similarly stated, "while the parasite Nosema ceranae may be a factor, it cannot be the sole cause. The fungus has been seen before, sometimes in colonies that were healthy". Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives, discounts it as being the cause of CCD.

In the United States, N. ceranae has been detected in honey bees from Nebraska, Wisconsin, Arkansas, New York and South Dakota using PCR of the 16S
16S ribosomal RNA
16S ribosomal RNA is a component of the 30S subunit of prokaryotic ribosomes. It is approximately 1.5kb in length...

 gene. In New York, N. ceranae was detected in 49 counties, and of the 1200 honey bee samples collected, 528 (44%) were positive for Nosema, from which, PCR
Polymerase chain reaction
The polymerase chain reaction is a scientific technique in molecular biology to amplify a single or a few copies of a piece of DNA across several orders of magnitude, generating thousands to millions of copies of a particular DNA sequence....

 analysis of 371 spore positive samples revealed 96% were N. ceranae, 3% had both N. ceranae and N. apis, and 1% had N. apis only.

Viral and fungal combination


A University of Montana and Montana State University team of scientists headed by Jerry Bromenshenk and working with the US Army’s Edgewood Chemical Biological Center published a paper in October, 2010 saying that a new DNA virus
DNA virus
A DNA virus is a virus that has DNA as its genetic material and replicates using a DNA-dependent DNA polymerase. The nucleic acid is usually double-stranded DNA but may also be single-stranded DNA . DNA viruses belong to either Group I or Group II of the Baltimore classification system for viruses...

, invertebrate iridescent virus or IIV6, and the fungus Nosema ceranae
Nosema ceranae
Nosema ceranae is a microsporidian, a small, unicellular parasite that mainly affects Apis cerana, the Asiatic honey bee. It may cause nosemosis, also called nosema...

were found in every killed colony the group studied. In their study they found that neither agent alone seemed deadly, but a combination of the virus and N. ceranae was always 100% fatal. Bromenshenk said it is not yet clear whether one condition weakens the bees enough to be finished off by the second, or whether they somehow compound the other’s destructive power. “They’re co-factors, that’s all we can say at the moment. They’re both present in all these collapsed colonies.”

Previous research, though not all, had already identified the fungus as part of the problem, and several RNA-based viruses had been detected as well. But the Army/Montana team, using a new software system developed by the military for analyzing proteins, uncovered a new DNA-based virus, and established a linkage to N. ceranae. Once the virus and the fungus were identified, the researchers tested bees in the lab. First they infected the bees with the fungus alone, and some died, though not as many as with CCD. Then they infected some with just the virus, with the same result.

When the combination of virus and fungus was used, the results appeared similar to CCD. The researchers say that the next step to test their theory will be to inoculate a colony with the two pathogens to see if it causes a colony collapse. “The real closure of the circle for us is to take the two pathogens to inoculate a colony, see it collapse, then pull out the pathogens again."

Whether this identified bee virus and its potential interaction with Nosema species is the cause or marker of CCD, is unknown. Also still not explained is the reason that the bees are never found dead in the hives but fly off at the time of death. Bromenshenk theorizes that the viral-fungal combination disrupts memory or navigating skills and the bees simply get lost. Another possibility, he said, is a kind of insect insanity. Scientists in the project emphasize that their conclusions are not the final word. They suggest that more research is still needed to determine, for example, how further outbreaks might be prevented, and how much environmental factors like heat, cold or drought might play a role. The study did not look into the role that pesticides may play, if any.

Information about the study was released to the public in a front page article in The New York Times with the heading "Scientists and Soldiers Solve A Bee Mystery". A few days later an article was published in Fortune Magazine with the title, "What a scientist didn't tell the New York Times about his study on bee deaths". Professor of entomology at Penn State University James Frazier, who is currently researching the sublethal impact of pesticides on bees, said that while Bromenshenk's study generated some useful data, Bromenshenk has a conflict of interest as CEO of a company developing scanners to diagnose bee diseases. "He could benefit financially from that if this thing gets popularized," Frazier says, "so it's a difficult situation to deal with." He adds that his own research has shown that pesticides affect bees "absolutely, in multiple ways."

Recently, the methods used to interpret the mass spectrometry data in the Bromenshenk study have been called into question, raising doubts as to whether IIV6 was ever correctly identified in any of the samples examined.

Pesticides


One of the more common general hypotheses concerns pesticide
Pesticide
Pesticides are substances or mixture of substances intended for preventing, destroying, repelling or mitigating any pest.A pesticide may be a chemical unicycle, biological agent , antimicrobial, disinfectant or device used against any pest...

s (or, more specifically, insecticide
Insecticide
An insecticide is a pesticide used against insects. They include ovicides and larvicides used against the eggs and larvae of insects respectively. Insecticides are used in agriculture, medicine, industry and the household. The use of insecticides is believed to be one of the major factors behind...

s), though several studies have found no common environmental factor
Environmental factor
Environmental factor or ecological factor or ecofactor is any factor, abiotic or biotic, that influences living organisms.- Environmental factors inducing diseases :...

s between unrelated outbreaks studied. In 2010 in the United States, the Organic Consumers
Association reported that bee colony losses were not occurring at organic beekeeping operations.

A 2010 survey reported 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen. It was disclosed that that figure represents over half of the maximum individual pesticide incidences ever reported for apiaries. It was suggested that "while exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined."

It is particularly difficult to evaluate pesticide contributions to CCD for several reasons. First, the variety of pesticides in use in the different areas reporting CCD makes it difficult to test for all possible pesticides simultaneously. Second, many commercial beekeeping
Beekeeping
Beekeeping is the maintenance of honey bee colonies, commonly in hives, by humans. A beekeeper keeps bees in order to collect honey and other products of the hive , to pollinate crops, or to produce bees for sale to other beekeepers...

 operations are mobile, transporting hives over large geographic distances over the course of a season, potentially exposing the colonies to different pesticides at each location. Third, the bees themselves place pollen
Pollen
Pollen is a fine to coarse powder containing the microgametophytes of seed plants, which produce the male gametes . Pollen grains have a hard coat that protects the sperm cells during the process of their movement from the stamens to the pistil of flowering plants or from the male cone to the...

 and honey into long-term storage, effectively meaning that there may be a delay of anywhere from days to months before contaminated provisions are fed to the colony, negating any attempts to associate the appearance of symptoms with the actual time at which exposure to pesticides occurred.

Pesticides used on bee forage are far more likely to enter the colony via the pollen stores rather than via nectar (because pollen is carried externally on the bees, while nectar is carried internally, and may kill the bee if too toxic), though not all potentially lethal chemicals, either natural or man-made, affect the adult bees: many primarily affect the brood, but brood die-off does not appear to be happening in CCD. Most significantly, brood are not fed honey, and adult bees consume relatively little pollen; accordingly, the pattern in CCD suggests that if contaminants or toxins from the environment are responsible, it is most likely to be via the honey, as it is the adults that are dying (or leaving), not the brood (though possibly effects of contaminated pollen consumed by juveniles may only show after they have developed into adults).

To date, most of the evaluation of possible roles of pesticides in CCD have relied on the use of surveys submitted by beekeepers, but it seems likely that direct testing of samples from affected colonies will be needed, especially given the possible role of systemic insecticides such as the neonicotinoid imidacloprid
Imidacloprid effects on bee population
Imidacloprid is a systemic neonicotinoid insecticide produced by the German chemical firm Bayer CropScience and sold under such trade names as Gaucho, Admire, Merit, Advantage, Confidor, Provado, and Winner. It acts as a neurotoxin and interferes with the transmission of nerve impulses in insects...

 (which are applied to the soil and taken up into the plant's tissues, including pollen and nectar), which may be applied to a crop when the beekeeper is not present. The known effects of imidacloprid on insects, including honey bees, are consistent with the symptoms of CCD; for example, the effects of imidacloprid on termite
Termite
Termites are a group of eusocial insects that, until recently, were classified at the taxonomic rank of order Isoptera , but are now accepted as the epifamily Termitoidae, of the cockroach order Blattodea...

s include apparent failure of the immune system, and disorientation.

In Europe, the interaction of the phenomenon of "dying bees" with imidacloprid has been discussed for quite some time now. It was a study from the "Comité Scientifique et Technique (CST)" which was in the center of discussion, which led to a partial ban of imidacloprid in France. The imidacloprid pesticide Gaucho was banned, in 1999 by the French Minister of Agriculture Jean Glavany
Jean Glavany
Jean Glavany is a French politician, member of the Socialist Party and former Minister.From 1981 to 1988, he was head of cabinet of President François Mitterrand . He was then Minister of Agriculture in the Plural Left government of Lionel Jospin...

, primarily due to concern over potential effects on honey bees. Consequently when fipronil
Fipronil
Fipronil is a broad spectrum insecticide that disrupts the insect central nervous system by blocking the passage of chloride ions through the GABA receptor and glutamate-gated chloride channels, components of the central nervous system. This causes hyperexcitation of contaminated insects' nerves...

, a phenylpyrazole insecticide and in Europe mainly labeled "Regent", was used as a replacement, it was also found to be toxic to bees, and banned partially in France in 2004.

In February 2007, about forty French deputies, led by UMP
Union for a Popular Movement
The Union for a Popular Movement is a centre-right political party in France, and one of the two major contemporary political parties in the country along with the center-left Socialist Party...

 member Jacques Remiller
Jacques Remiller
Jacques Remiller is a member of the National Assembly of France. He represents the Isère department, and is a member of the Union for a Popular Movement.-References:...

, requested the creation of a Parliamentary Investigation Commission on Overmortality of Bees, underlining that honey production was decreasing by 1,000 tons a year for a decade. , no investigations were yet opened. Five other insecticides based on fipronil were also accused of killing bees. However, the scientific committees of the European Union are still of the opinion "that the available monitoring studies were mainly performed in France and EU-member-states should consider the relevance of these studies for the circumstances in their country".

Around the same time French beekeepers succeeded in banning neonicotinoids, the Clinton administration permitted pesticides which were previously banned, including imidacloprid. In 2004, the Bush Administration reduced regulations further and pesticide applications increased.

In 2005, a team of scientists led by the National Institute of Beekeeping in Bologna, Italy, found pollen obtained from seeds dressed with imidacloprid contains significant levels of the insecticide, and suggested the polluted pollen might cause honey bee colony death. Analysis of maize and sunflower crops originating from seeds dressed with imidacloprid suggest large amounts of the insecticide will be carried back to honey bee colonies. Sublethal doses of imidacloprid in sucrose solution have also been documented to affect homing and foraging activity of honey bees. Imidacloprid in sucrose solution fed to bees in the laboratory impaired their communication for a few hours. Sublethal doses of imidacloprid in laboratory and field experiment
Field experiment
A field experiment applies the scientific method to experimentally examine an intervention in the real world rather than in the laboratory...

 decreased flight activity and olfactory discrimination, and olfactory learning performance was impaired.

Research in 2008 by scientists from Pennsylvania State University
Pennsylvania State University
The Pennsylvania State University, commonly referred to as Penn State or PSU, is a public research university with campuses and facilities throughout the state of Pennsylvania, United States. Founded in 1855, the university has a threefold mission of teaching, research, and public service...

 found high levels of the pesticides fluvalinate
Fluvalinate
Fluvalinate is a synthetic pyrethroid commonly used to control varroa mites in honey bee colonies....

 and coumaphos
Coumaphos
Coumaphos is a non-volatile, fat-soluble phosphorothioate with ectoparasiticide properties: it kills insects and mites. It is well known under manufacturer brand-names as a dip or wash, used on farm and domestic animals to control ticks, mites, flies and fleas...

 in samples of wax from hives, as well as lower levels of 70 other pesticides. These chemicals have been used to try to eradicate varroa mites, a bee pest that itself has been thought to be a cause of CCD. Researchers from Washington State University
Washington State University
Washington State University is a public research university based in Pullman, Washington, in the Palouse region of the Pacific Northwest. Founded in 1890, WSU is the state's original and largest land-grant university...

, under entomology professor Steve Sheppard in 2009, confirmed high levels of pesticide residue in hive wax and found an association between it and significantly reduced bee longevity.

The WSU work also focused on the impact of the microsporidia
Microsporidia
The microsporidia constitute a phylum of spore-forming unicellular parasites. They were once thought to be protists but are now known to be fungi. Loosely 1500 of the probably more than one million species are named now. Microsporidia are restricted to animal hosts, and all major groups of animals...

n pathogen Nosema ceranae
Nosema ceranae
Nosema ceranae is a microsporidian, a small, unicellular parasite that mainly affects Apis cerana, the Asiatic honey bee. It may cause nosemosis, also called nosema...

, the build-up of which was high in the majority of the bees tested, even after large doses of the antibiotic fumagillin
Fumagillin
Fumagillin is a complex biomolecule and used as an antimicrobial agent. It was isolated in 1949 from the microbial organism Aspergillus fumigatus.-In animals:...

. Penn State's Dr. Maryann Frazier said, "Pesticides alone have not shown they are the cause of CCD. We believe that it is a combination of a variety of factors, possibly including mites, viruses and pesticides."

Fipronil



Fipronil is another chemical sometimes blamed for the spread of colony collapse disorder among bees. It has been found by the Minutes-Association for Technical Coordination Fund in France that even at very low nonlethal doses for bees, the pesticide still impairs their ability to locate their hive, resulting in large numbers of forager bees lost with every pollen-finding expedition; other studies, however, have shown no acute effect on honey bees.

Fipronil is designed to eliminate insects similar to bees such as Vespula germanica and many other colonial pests by a process of toxic baiting, whereby one insect returning to the hive spreads the pesticide among the brood.

Antibiotics and miticides


Most beekeepers affected by CCD report that they use antibiotic
Antibiotic
An antibacterial is a compound or substance that kills or slows down the growth of bacteria.The term is often used synonymously with the term antibiotic; today, however, with increased knowledge of the causative agents of various infectious diseases, antibiotic has come to denote a broader range of...

s and miticides in their colonies, though the lack of uniformity as to which particular chemicals are used makes it seem unlikely that any single such chemical is involved. However, it is possible that not all such chemicals in use have been tested for possible effects on honey bees, and could therefore potentially be contributing to the CCD phenomenon.

Genetically modified crops


Some genetically modified (GM)
GMO
A GMO is a genetically modified organism.GMO may also refer to:* Gell-Mann–Okubo mass formula in particle physics* General Medical Officer, a designation for United States Army soldiers* Generalised molecular orbital theory, in chemistry...

 crops
Genetically modified food
Genetically modified foods are foods derived from genetically modified organisms . Genetically modified organisms have had specific changes introduced into their DNA by genetic engineering techniques...

 produce the natural insecticide Bt toxin
Bacillus thuringiensis
Bacillus thuringiensis is a Gram-positive, soil-dwelling bacterium, commonly used as a biological pesticide; alternatively, the Cry toxin may be extracted and used as a pesticide. B...

, which has been hypothesised to affect bees. In the scant literature on the topic, there exists no evidence of any negative effects on honey bee populations. Furthermore, CCD cases are known in areas of Europe and Canada where Bt crops are not grown, such as Switzerland.

Bee rentals and migratory beekeeping



Since U.S. beekeeper Nephi Miller
Nephi Miller
Nephi Ephraim Miller was a pioneer in the practice of migratory beekeeping. Miller gained an interest in bees as a child, while living on his father's farm. Miller was to inherit his father's farm and become a farmer, but his interest in bees grew...

 first began moving his hives to different areas of the country for the winter of 1908, migratory beekeeping has become widespread in America.

Bee rental for pollination is a crucial element of U.S. agriculture, which could not produce anywhere near its current levels with native pollinators alone. U.S. beekeepers collectively earn much more from renting their bees out for pollination than they do from honey production.

Researchers are concerned that trucking colonies around the country to pollinate crops, where they intermingle with other bees from all over, helps spread viruses and mites among colonies. Additionally, such continuous movement and re-settlement is considered by some a strain and disruption for the entire hive, possibly rendering it less resistant to all sorts of systemic disorder.

U.S. bee rental travel extent


One major U.S. beekeeper reports moving his hives from Idaho to California in January, then to apple orchards in Washington in March, to North Dakota two months later, and then back to Idaho by November—a journey of several thousand kilometres. Others move from Florida to New Hampshire or to Texas; nearly all visit California for the almond bloom in January.

Beekeepers in Europe and Asia are generally far less mobile, with bee populations moving and mingling within a smaller geographic extent (although some keepers do move longer distances, it is much less common).

This wider spread and intermingling in the U.S. has resulted in far greater losses from Varroa mite infections in recent years.

Electromagnetic radiation


Despite considerable discussion on the Internet and in the lay media, there have been few studies, published in peer reviewed scientific literature, on effects of electromagnetic field exposure on honey bees. One of the first peer-reviewed studies was published in 1981 by Gary and Westerdahl. The investigators found "no evidence that airborne invertebrates would be significantly affected during transient passage through microwaves associated with solar power satellite ground-based microwave receiving stations". No mechanism has been established by which weak radiofrequency energy can affect the behavior of insects, apart from heating effects. However, it is well-established that honey bees can detect weak static or low-frequency magnetic field
Magnetic field
A magnetic field is a mathematical description of the magnetic influence of electric currents and magnetic materials. The magnetic field at any given point is specified by both a direction and a magnitude ; as such it is a vector field.Technically, a magnetic field is a pseudo vector;...

s, which they use as one of several cues in navigation.

In 2004 an exploratory study was conducted on the non-thermal effects of electromagnetic exposure and learning. The investigators did not find any change in behavior due to RF exposure from the DECT base station operating at 1880-1900 MHz.

In 2006 investigators at the University of Landau did a pilot study on the non-thermal effects of radio frequency
Radio frequency
Radio frequency is a rate of oscillation in the range of about 3 kHz to 300 GHz, which corresponds to the frequency of radio waves, and the alternating currents which carry radio signals...

 ("RF") on honey bees (Apis mellifera carnica) and suggested that when bee hives have DECT cordless phone
Cordless telephone
A cordless telephone or portable telephone is a telephone with a wireless handset that communicates via radio waves with a base station connected to a fixed telephone line, usually within a limited range of its base station...

 base stations embedded in them, the close-range electromagnetic field
Electromagnetic field
An electromagnetic field is a physical field produced by moving electrically charged objects. It affects the behavior of charged objects in the vicinity of the field. The electromagnetic field extends indefinitely throughout space and describes the electromagnetic interaction...

 ("EMF") may reduce the ability of bees to return to their hive; they also noticed a slight reduction in honeycomb weight in treated colonies. In the course of their study, one half of their colonies broke down, including some of their controls which did not have DECT base stations embedded in them. In April 2007, news of this study appeared in various media outlets, beginning with an article in The Independent
The Independent
The Independent is a British national morning newspaper published in London by Independent Print Limited, owned by Alexander Lebedev since 2010. It is nicknamed the Indy, while the Sunday edition, The Independent on Sunday, is the Sindy. Launched in 1986, it is one of the youngest UK national daily...

, which stated that the subject of the study included mobile phone
Mobile phone
A mobile phone is a device which can make and receive telephone calls over a radio link whilst moving around a wide geographic area. It does so by connecting to a cellular network provided by a mobile network operator...

s and had related them to CCD. Though Cellular phone
Mobile phone
A mobile phone is a device which can make and receive telephone calls over a radio link whilst moving around a wide geographic area. It does so by connecting to a cellular network provided by a mobile network operator...

s were implicated by other media reports at the time, they were not covered in the study. Researchers involved have since stated that their research did not include findings on cell phones, or their relationship to CCD, and indicated that the Independent article had misinterpreted their results and created "a horror story".

In April 2011, a study conducted by a former investigator of the EPFL École Polytechnique Fédérale de Lausanne
École polytechnique fédérale de Lausanne
The École polytechnique fédérale de Lausanne is one of the two Swiss Federal Institutes of Technology and is located in Lausanne, Switzerland.The school was founded by the Swiss Federal Government with the stated mission to:...

 appeared, which stated that active mobile phones placed directly inside a beehive can induce the worker piping signal (in natural conditions, worker piping either announces the swarming process of the bee colony or is a signal of a disturbed bee colony); the author mentioned that "phones are not present in the close vicinity of honeybees in real life" and did not demonstrate what negative effect, if any, worker piping might have within a colony, nor was any link to CCD demonstrated.

In October 2011, a review study was published by the Indian government's Ministry of Environment and Forests
Ministry of Environment and Forests
The Ministry of Environment and Forests is an Indian government ministry. The Minister of Environment and Forests holds cabinet rank as a member of the Council of Ministers...

 that looked at 919 peer-reviewed scientific studies investigating impacts of EMF on birds, bees, humans, animals/wildlife, and plants.. Only 7 of the 919 studies involved honey bees, and 6 of these claimed negative effects from exposure to EMF radiation, though only one specifically demonstrated link to CCD. The review noted that according to the study titled "Impact of mobile phone on the density of Honey Bees" authored by Sainudeen Sahib (2011), once mobile phones were kept in the beehives, worker bees stopped coming to the hives after ten days. The same study also found drastic decrease in the egg production of queen bees and goes on to say that "electromagnetic radiation exposure provides a better explanation for Colony Collapse Disorder (CCD) than other theories". In view of evidence from this and several other studies, the review authors concluded: "existing literature shows that the EMRs are interfering with the biological systems in more ways than one" and recommended recognising EMF as a pollutant. However, they also noted that "these studies are not representative of the real life situations or natural levels of EMF exposure. More studies need to be taken up to scientifically establish if any, the link between the observed abnormalities and disorders in bee hives such as Colony Collapse Disorder (CCD)".

Management


the Mid-Atlantic Apiculture Research and Extension Consortium
Mid-Atlantic Apiculture Research and Extension Consortium
The Mid-Atlantic Apiculture Research and Extension Consortium , established in 1997, is a regional group focused on addressing the pest management crisis facing the beekeeping industry in the Mid-Atlantic region of the United States...

(MAAREC) offered the following tentative recommendations for beekeepers noticing the symptoms of CCD:
  1. Do not combine collapsing colonies with strong colonies.
  2. When a collapsed colony is found, store the equipment where you can use preventive measures to ensure that bees will not have access to it.
  3. If you feed your bees sugar syrup, use Fumagillin
    Fumagillin
    Fumagillin is a complex biomolecule and used as an antimicrobial agent. It was isolated in 1949 from the microbial organism Aspergillus fumigatus.-In animals:...

    .
  4. If you are experiencing colony collapse and see a secondary infection, such as European Foulbrood, treat the colonies with Terramycin, not Tylan.


Another proposed remedy for farmers of pollinated crops is simply to switch from using beekeepers to the use of native bees, such as bumble bees and mason bee
Mason bee
Mason bee is a common name for species of bees in the genus Osmia, of the family Megachilidae. They are named from their habit of making compartments of mud in their nests, which are made in hollow reeds or holes in wood made by wood boring insects....

s http://attra.ncat.org/attra-pub/nativebee.htmlhttp://www.scribd.com/doc/40824563/Alternative-Pollinators-Native-Bees. Native bees can be helped to establish themselves by providing suitable nesting locations and some additional crops the bees could use to feed from (e.g. when the pollination season of the commercial crops on the farm has ended).

A British beekeeper successfully developed a strain of bees that are resistant to varroa mites. Russian honey bees also resist infestations of varroa mites but are still susceptible to other factors associated with colony collapse disorder, and have detrimental traits that limit their relevance in commercial apiculture.

In the United Kingdom, a national bee database was set up in March 2009 to monitor colony collapse as a result of a 15% reduction in the bee population that had taken place over the previous two years. In particular, the register, funded by the Department for the Environment
Department for Environment, Food and Rural Affairs
The Department for Environment, Food and Rural Affairs is the government department responsible for environmental protection, food production and standards, agriculture, fisheries and rural communities in the United Kingdom...

 and administered by the National Bee Unit
National Bee Unit
The National Bee Unit is responsible for the delivery of the Bee Health Programmes in England and Wales. Using , a website designed to help monitor and control the spread of serious honey bee pests and diseases, the NBU consists of a team of 60-plus field-based Bee Inspectors and staff based in...

, will be used to monitor health trends and help establish whether the honey industry is under threat from supposed colony collapse disorder. Britain's 20,000 beekeepers have been invited to participate. In October 2010, David Aston of the British Beekeepers’ Association stated, ‘We still do not believe CCD is a cause of colony losses in the UK, however we are continuing to experience colony losses, many if not most of which can be explained. The approach being taken in UK beekeeping is to raise the profile of integrated bee health management, in other words identifying and trying to eliminate factors which reduce the health status of a colony. This incorporates increasing the skill level of beekeepers through training and education, raising the profile of habitat destruction and its effect of forage (nectar and pollen) availability, and of course research on the incidence and distribution of diseases and conditions in the UK together with more applied research and development on providing solutions."

Economics



The phenomenon is particularly important for crops such as almond
Almond
The almond , is a species of tree native to the Middle East and South Asia. Almond is also the name of the edible and widely cultivated seed of this tree...

 growing in California
California
California is a state located on the West Coast of the United States. It is by far the most populous U.S. state, and the third-largest by land area...

, where honey bees are the predominant pollinator and the crop value in 2006 was $1.5 billion. In 2000, the total U.S. crop value that was wholly dependent on honey bee pollination was estimated to exceed $15 billion.

Honey bees are not native to the Americas, therefore their necessity as pollinators in the U.S. is limited to strictly agricultural/ornamental uses, as no native plants require honey bee pollination, except where concentrated in monoculture
Monoculture
Monoculture is the agricultural practice of producing or growing one single crop over a wide area. It is also known as a way of farming practice of growing large stands of a single species. It is widely used in modern industrial agriculture and its implementation has allowed for large harvests from...

 situations—where the pollination need is so great at bloom time that pollinators must be concentrated beyond the capacity of native bees (with current technology).

They are responsible for pollination
Pollination
Pollination is the process by which pollen is transferred in plants, thereby enabling fertilisation and sexual reproduction. Pollen grains transport the male gametes to where the female gamete are contained within the carpel; in gymnosperms the pollen is directly applied to the ovule itself...

 of approximately one third of the United States' crop
Crop
Crop may refer to:* Crop, a plant grown and harvested for agricultural use* Crop , part of the alimentary tract of some animals* Crop , a modified whip used in horseback riding or disciplining humans...

 species, including such species as almond
Almond
The almond , is a species of tree native to the Middle East and South Asia. Almond is also the name of the edible and widely cultivated seed of this tree...

s, peach
Peach
The peach tree is a deciduous tree growing to tall and 6 in. in diameter, belonging to the subfamily Prunoideae of the family Rosaceae. It bears an edible juicy fruit called a peach...

es, soybean
Soybean
The soybean or soya bean is a species of legume native to East Asia, widely grown for its edible bean which has numerous uses...

s, apple
Apple
The apple is the pomaceous fruit of the apple tree, species Malus domestica in the rose family . It is one of the most widely cultivated tree fruits, and the most widely known of the many members of genus Malus that are used by humans. Apple grow on small, deciduous trees that blossom in the spring...

s, pear
Pear
The pear is any of several tree species of genus Pyrus and also the name of the pomaceous fruit of these trees. Several species of pear are valued by humans for their edible fruit, but the fruit of other species is small, hard, and astringent....

s, cherries
Cherry
The cherry is the fruit of many plants of the genus Prunus, and is a fleshy stone fruit. The cherry fruits of commerce are usually obtained from a limited number of species, including especially cultivars of the wild cherry, Prunus avium....

, raspberries
Raspberry
The raspberry or hindberry is the edible fruit of a multitude of plant species in the genus Rubus, most of which are in the subgenus Idaeobatus; the name also applies to these plants themselves...

, blackberries
Blackberry
The blackberry is an edible fruit produced by any of several species in the Rubus genus of the Rosaceae family. The fruit is not a true berry; botanically it is termed an aggregate fruit, composed of small drupelets. The plants typically have biennial canes and perennial roots. Blackberries and...

, cranberries
Cranberry
Cranberries are a group of evergreen dwarf shrubs or trailing vines in the subgenus Oxycoccus of the genus Vaccinium. In some methods of classification, Oxycoccus is regarded as a genus in its own right...

, watermelon
Watermelon
Watermelon is a vine-like flowering plant originally from southern Africa. Its fruit, which is also called watermelon, is a special kind referred to by botanists as a pepo, a berry which has a thick rind and fleshy center...

s, cantaloupe
Cantaloupe
"Rockmelon" redirects here, for the band see Rockmelons. See also Cantaloupe .Cantaloupe refers to a variety of Cucumis melo, a species in the family Cucurbitaceae which includes nearly all melons and squashes. Cantaloupes range in size from...

s, cucumber
Cucumber
The cucumber is a widely cultivated plant in the gourd family Cucurbitaceae, which includes squash, and in the same genus as the muskmelon. The plant is a creeping vine which bears cylindrical edible fruit when ripe. There are three main varieties of cucumber: "slicing", "pickling", and...

s and strawberries
Strawberry
Fragaria is a genus of flowering plants in the rose family, Rosaceae, commonly known as strawberries for their edible fruits. Although it is commonly thought that strawberries get their name from straw being used as a mulch in cultivating the plants, the etymology of the word is uncertain. There...

. Many but not all of these plants can be (and often are) pollinated by other insects in small holdings in the U.S., including other kinds of bees (e.g., squash bee
Squash bee
The name Squash bee is applied to two related genera of bees in the tribe Eucerini; Peponapis and Xenoglossa. Both genera are oligoleges on the plant genus Cucurbita and closely related plants...

s on cucurbits), but typically not on a commercial scale. While some farmers of a few kinds of native crops do bring in honey bees to help pollinate, none specifically need them, and when honey bees are absent from a region, there is a presumption that native pollinators may reclaim the niche, typically being better adapted to serve those plants (assuming that the plants normally occur in that specific area).

However, even though on a per-individual basis, many other species are actually more efficient at pollinating, on the 30% of crop types where honey bees are used, most native pollinators cannot be mass-utilized as easily or as effectively as honey bees—in many instances they will not visit the plants at all. Beehives can be moved from crop to crop as needed, and the bees will visit many plants in large numbers, compensating via saturation pollination
Saturation pollination
Saturation pollination is a pollination technique for agricultural crops in areas dominated by non-crop plant species that are preferred by pollinators. The technique involves keeping a larger number of bee colonies than normally maintained for honey production so as to exhaust the preferred plants...

 for what they lack in efficiency. The commercial viability of these crops is therefore strongly tied to the beekeeping
Beekeeping
Beekeeping is the maintenance of honey bee colonies, commonly in hives, by humans. A beekeeper keeps bees in order to collect honey and other products of the hive , to pollinate crops, or to produce bees for sale to other beekeepers...

 industry. In China, hand pollination of apple orchards is labor intensive, time consuming and costly.

Media


A number of documentaries have been produced in which possible causes of CCD have been explored. "Silence of the Bees" (Oct. 2007) is a part of the Nature
Nature (TV series)
Nature is a wildlife television program produced by Thirteen/WNET New York. It has been distributed to United States public television stations by the PBS television service since its debut on October 10, 1982. Some episodes may appear in syndication on many PBS member stations around the U.S. and...

television series and covers several recent investigative discoveries. The 2009 documentary Vanishing of the Bees
Vanishing of the Bees
Vanishing of the Bees is a 2009 documentary film by Hive Mentality Films & Hipfuel films, directed by George Langworthy and Maryam Henein and released in the United Kingdom on October 9. The story centers around the sudden disappearance of honey bees from beehives around the world, caused by the...

pointed to neonicotinoid pesticides as being the most likely culprit, though the experts interviewed concede that no firm data yet exists. The 2010 feature length documentary Queen of the Sun: What are the bees telling us?
Queen of the Sun
Queen of the Sun: What Are the Bees Telling Us? is a 2010 documentary film directed by Taggart Siegel. The film investigates multiple angles of the recent bee epidemic colony collapse disorder. It also explores the historical and contemporary relationship between bees and humans...

features interviews with beekeepers, scientists, farmers, and philosophers.

In popular culture


A story arc in Series 4
Doctor Who (series 4)
The fourth series of British science fiction television series Doctor Who began on 25 December 2007 with the Christmas special "Voyage of the Damned". Following the special, a regular series of thirteen episodes aired, starting with "Partners in Crime" on 5 April 2008 and ending with "Journey's End"...

 of the British science fiction television
Science fiction on television
Science fiction first appeared on a television program during the Golden Age of Science Fiction. Special effects and other production techniques allow creators to present a living visual image of an imaginary world not limited by the constraints of reality; this makes television an excellent medium...

 series Doctor Who
Doctor Who
Doctor Who is a British science fiction television programme produced by the BBC. The programme depicts the adventures of a time-travelling humanoid alien known as the Doctor who explores the universe in a sentient time machine called the TARDIS that flies through time and space, whose exterior...

referred to the disappearance of bees, culminating in "The Stolen Earth
The Stolen Earth
"The Stolen Earth" is the twelfth episode of the fourth series and the 750th overall episode of the British science fiction television series Doctor Who. The episode was written by show runner and head writer Russell T Davies and is the first of a two-part crossover story; the concluding episode is...

", where it was revealed that some bees were aliens from Melissa Majoria who created a path the Doctor could follow to find Earth and the other planets stolen by the Daleks.

See also



  • Clothianidin
    Clothianidin
    Clothianidin is an insecticide developed by Takeda Chemical Industries and Bayer AG. Similar to thiamethoxam and imidacloprid, it is a neonicotinoid. Neonicotinoids are a class of insecticides which act on the central nervous system of insects with lower toxicity to mammals...

  • Imidacloprid effects on bee population
    Imidacloprid effects on bee population
    Imidacloprid is a systemic neonicotinoid insecticide produced by the German chemical firm Bayer CropScience and sold under such trade names as Gaucho, Admire, Merit, Advantage, Confidor, Provado, and Winner. It acts as a neurotoxin and interferes with the transmission of nerve impulses in insects...

  • Pesticide toxicity to bees
    Pesticide toxicity to bees
    Pesticides vary in their effects on bees. Contact pesticides are usually sprayed on plants and can kill bees when they crawl over sprayed surfaces of plants or other media...

  • Bees and toxic chemicals
    Bees and toxic chemicals
    Bees can suffer serious effects from toxic chemicals in their environments. These include various synthetic chemicals, such as insecticides and fertilizers, as well as a variety of naturally occurring chemicals from plants, such as ethanol resulting from the fermentation of organic material...

  • Vanishing of the Bees
    Vanishing of the Bees
    Vanishing of the Bees is a 2009 documentary film by Hive Mentality Films & Hipfuel films, directed by George Langworthy and Maryam Henein and released in the United Kingdom on October 9. The story centers around the sudden disappearance of honey bees from beehives around the world, caused by the...

  • Pesticide misuse
    Pesticide misuse
    Under United States laws, pesticide misuse is the use of a pesticide in a way that violates laws regulating their use or endangers humans or the environment; many of these regulations are laid out in the Federal Insecticide, Fungicide, and Rodenticide Act...

  • Pollinator decline
    Pollinator decline
    The term pollinator decline refers to the reduction in abundance of pollinators in many ecosystems worldwide during the end of the twentieth century....

  • Diseases of the honey bee
  • Regent (insecticide)
    Regent (insecticide)
    Regent is a trademark for a broad spectrum systemic insecticide containing the active ingredient fipronil. Fipronil is an insecticide discovered and developed by Rhône-Poulenc between 1985-87. It was placed on the market in 1993. Regent's rights have been purchased by BASF. It acts by contact and...

  • Mid-Atlantic Apiculture Research and Extension Consortium
    Mid-Atlantic Apiculture Research and Extension Consortium
    The Mid-Atlantic Apiculture Research and Extension Consortium , established in 1997, is a regional group focused on addressing the pest management crisis facing the beekeeping industry in the Mid-Atlantic region of the United States...


Further reading




External links