[1] Colony Collapse Disorder (CCD) is a poorly understood phenomenon involving the massive die-off of a beehive or bee colony. CCD is alternatively referenced as Vanishing Bee Syndrome (VBS). CCD was originally found only in colonies of the West honey bee in North America, but European beekeepers have recently claimed to be observing a similar phenomenon in Poland, Greece, Italy, Portugal and Spain, Switzerland and Germany. From 1971 to 2006 approximately half of the U.S. honey bee colonies have vanished.

Causes

The cause (or causes) of the syndrome is not yet well understood and even the existence of this disorder remains disputed. Theories include environmental change-related stresses, malnutrition, unknown pathogens, mites (Varroa mites), pesticides such as neonicotinoids, emission from cellular phones or other man made devices, and genetically modified crops.

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).

No single factor or agent of Colony Collapse Disease found, researchers suggest a combination of parasites, pathogens and pesticides as primary cause [2]

No single factor or agent emerged as a definitive cause of the phenomenon. The best hypothesis is that particular virulent combination of parasites and pathogens may interact to produce lethal consequences to the colonies in an environmental context of chronic exposure to pesticides.

Network to study causes of CCD and genomic response of bees [3]

A network of eleven countries (BEE DOC) was created in 2010 to study the effects of multiple infections and pesticides at individual bee level and at colony level. will specifically address sublethal and chronic exposure to pesticides and screen how apicultural practices affect colony health. It will tackle genomic responses towards the most important factors identified, help to prevent diseases emergence via disease resistance features, develop diagnostic tools including tools to be used at field level and focus on innovative ways of prevention and control addressing the multi-factorial causes of colony death.

A sticky paper to fight varroa mite [4]

Jeff Pettisan entomologist from the USDA Agricultural research Service, Maryland says that varroa mite infestations have become such a serious problem that maintaining bee colonies without chemical treatment is virtually impossible. Apistan—a strip that contains the chemical tau-fluvalinate is being used. Varroa, however, have begun to show resistance to the chemical.

Pettisan, looking for alternatives, introduced a sticky paper which is located beneath the hive bottom. Mites get stick to the paper and can be removed from the hive. As safe and effective chemical controls continue to be researched and developed, the sticky paper will complement Apistan in assisting beekeepers with the control of invading varroa.

Other causes of the Colony Collapse Disorder, according to Pettisan, may be an unknown virus, Bacteria, pesticides or a combination of these causes.

Genetic causes

The honey bee has a reduced number of genes which express resistance to toxics and diseases, compared with the genetic code of the fruit flies and ants. According to May Berenbaum from the University of Illinios this could make the bees more vulnerable to toxics and diseases. Berenbaum caled for improving genetic stocks of bees. He stressed the fact that supplies of animal-pollinated foods - most fruit, vegetable, and nut crops, which provide the bulk of vitamins and other necessary nutrients in our diets - may well be dramatically affected in case of further losses of hives. [5]

Decline of honeybee populations [6]

Honeybee decline is thought to be caused by a combination of factors like climate change, parasites (like the varroa mite), diseases, overexposure to pesticides and the loss of suitable habitat. Dr Dave Chandler examines naturally occurring fungi that kill the varroa mite. Varroa destructor, formerly V. jacobsoni feed on the circulatory fluid of honey bee pupae and adult bees, activate and transmit diseases, reducing bee life expectancy and causing the colony to decline.

Presently, the control of varroa is based on the use of chemical pesticides. To avoid growing mite resistance, biological control technologies, such as fungus which kill the varroa mite, could offer an alternative pest management strategy of varroa, but had a low impact on the bees and worked in the warm and dry conditions typically found in bee hives and find the best ways of applying this weapon across the hive. This includes fungal footbaths at the main entrance to hives and powder spays.

Other mite control systems [7]

Fluvalinate (Apistan strips): Fluvalinate is the active ingredient of Apistan strips. It is a synthetic pyrethroid applied as a contact miticide.
Coumaphos(CheckMite+ strips): Coumaphos is the active ingredient of CheckMite+ strips. The product is an organophosphate, applied as a contact miticide.
Sugar esters: Sugar esters (Sucrocide) in spray application Formic
Acid: Formic acid is effective against Varroa and tracheal mites (Acarapis woodi). Oxalic Acid: Oxalic acid (Oxalic acid dihydrate) should only be applied in late fall when the colony has no brood. Non Chemical Control: Traps and oils.

Diana Cox-Foster and colleagues 2007 reported a correlation between colony collapse disease and the presence of Israeli acute paralysis virus (IAPV), a highly pathogenic virus. According to Cox-Foster infected bees present paralytic-type movements and die. The researcher say, however, that the virus may not be the the sole cause of CCD, and additional stresses are needed to trigger the disease. [8]

A variety of environmental chemicals such as pesticides, found on pollen, wax, adult bees and brood may be such a trigger. [9]

Modified protein production found as primary cause of colony collapse disorder (CCD) [10]

Colony collapse disorder (CCD) made one third of US honey bees to disapear in late 2006. The researchers linked pathogens and other environmental stresses, including pesticides to the disease. However, a convincing causal relationship could not be presented.
Berenbaum and colleagues 2009 studied the gene expression of bees sampled before CCD spread, and compared it with bees from CCD colonies. The researchers found 65 transcripts as potential markers for CCD status.

The unusual ribosomal RNA fragments are possible remnants of picorna-like viral infection, including deformed wing virus and Israeli acute paralysis virus. Ribosomals are cell structures which produce proteins. The authors speculate that viruses invaded the ribosomes resulting in heavy alterations in protein synthesis in CCD colonies.

Impaired protein production reduces resistance to pesticides, fungus or bacteria infections or even malnutrition. The authors propose that these unusual ribosomal fragments establish a link to other suggested causes of CCD. These RNA fragments are the primary cause which open the door to other factors of the disease. Ribosomal fragment abundance and presence of multiple viruses are being suggested by the authors as diagnostic markers of CCD.

Increasing toxicity of miticides [11]

According to Berenbaum and colleagues honey bee mortality may occur when tau-fluvalinate and coumaphos are simultaneously present in the hive.

Both varroa mite miticides the organophosphate coumaphos (Checkmite+), and the pyrethroid tau-fluvalinate (Apistan) are lipoohilic and build up in wax structures of the hive. Honey bees may thus become exposed to both miticides as a result of repeated treatments.

The authors found a large increase in the toxicity of tau-fluvalinate in hives when coumaphos have been used before. This synergism was less accentuated whit treatment of coumaphos followed tau-fulvinate. The authors stress that the detoxification of the miticides is mediated by cytochrome P450 monooxygenase enzymes (P450s). A competition between both chemicals for access to detoxicative P450s may cause rising toxicity which would not be lethal when only one of the chemicals is present.

Symptoms of Colony Collapse Disorder [12]

Jerry Bromenshenk from Montana describes the signs of the disorder as follows: Colony Collapse Disorder (CCD) is the latest problem facing bee keepers today. Symtoms of CCD are:
1) In collapsed colonies

The complete absence of adult bees in colonies, with no or little build up of dead bees in the colonies or in front of those colonies.
The presence of capped brood in colonies.
The presence of food stores, both honey and bee bread
i.which is not immediately robbed by other bees
ii.when attacked by hive pests such as wax moth and small hive beetle, the attack is noticeably delayed.

2) In cases where the colony appear to be actively collapsing

An insufficient workforce to maintain the brood that is present.
The workforce seems to be made up of young adult bees.
The queen is present.
The cluster is reluctant to consume provided feed, such as sugar syrup and protein supplement.

Jerry Bromenshenk is a member of a team of researchers studying the disorder. He developed a questionnaire, "National Bee Loss Survey" which can be found at http://www.beesurvey.com/

Nosemosis is one of the most widespread of the adult honey bee diseases [13]

The honeybee, Apis mellifera, is undergoing a worldwide decline. It is being suggest that the worldwide decline of honeybee colonies may caused by infectious diseases together with exposure to pesticides. Vidau et al. 2011 determined the sensitivity to sublethal doses of the insecticides fipronil and thiacloprid of Nosema ceranae infected honeybee colonies. A significant increase in honeybee mortality was observed when Nosema ceranae-infected honeybees were exposed to sublethal doses of insecticides.

The authors concluded that the combination of increasing infections by Nosema ceranae together with high pesticide exposure may increase honeybee colony losses.

Microsporidia Nosema spp. infections in Chinese bumblebees [13]

Li et al 2012 report that 6,1% of Chinese bumblebees (Bombus spp.) were infected by microsporidia, notably Nosema bombi, Nosema ceranae, Nosema thomsoni, and four new putatively novel taxa: Nosema A, Nosema B-complex, Nosema C-complex and Nosema D-complex. Bumblebees are important pollinators of many economically important crops, and microsporidia infection is the most frequent disease of this important insect.

Microsporidia are restricted to animal hosts, and all major groups of animals host microsporidia. Most infect insects, but they are also responsible for common diseases of crustaceans and fish. The distinguished species of microsporidia usually infect one specific host or a related group of hosts. Several species, most of which are opportunistic, also infect humans. [14]

Energetic stress may explain Nosema spp. pathology in infected bees [15]

According to Martín-Hernández et al. 2011 Nosema ceranae is a relatively new parasite which causes a more virulent disease compared to Nosema apis infecting the honeybee for much longer. Both are obligate intracellular microsporidian parasites, consuming energy of the host. This causes an energetic stress increasing virulence observed. Caged bees, infected by Nosema ceranae presente higher mortality and sugar syrup consumption compared with those infected by Nosema apis. This was directly related to spore counts administered for infection.

Differences between both microsporidia depend on host-parasite interactions and increased energetic stress may even explain the changes in host behaviour, explained the authors. The authors report a higher prevalence of Nosema ceranae indicating advantage in the competition over Nosema apis. This may result of a better adaption to Spanish conditions. However both microsporidia may prevail in the different Spanish bioclimatic regions. [16]

Sample size and time of collection affect results of Nosema diagnosis [17]

Botías et al.2011 call for an accurate and reliable method to evaluate the presence of Nosema in honey bee. The authors stress that both sample size and the time of collection (month and day of sampling) notably affect the diagnosis.

Traver, Williams and Fell 2011 studied honeybee colony infection by Nosema ceranae during the seasons. They found that all bees sampled were infected with Nosema ceranae, and colony infection levels were the highest in April-June and lowerest in the fall and winter. [18]

Deformed Wing Virus and Varroa destructor causes honeybee losses during Winter in Switzerland [19]

Dainat et al.2011 assessed the results of different pathogens as cause of winter losses of managed honey bee colonies in Zwitzerland. The authors found that Varoa destructor and deformed wing virus reduce the life span of winter bees, and can be considered as possible mechanism for honeybee colony losses. However, neither Nosema ceranae nor acute bee paralysis virus did correlated with longevity. Expression levels of the vitellogenin gene, as a biomarker for honey bee longevity gene expression, was significantly positively correlated with acute bee paralysis virus and Nosema ceranae loads.

Queen replacement to compensate for Nosema infection of a honeybee colony [20]

Queen replacement reduces significantly the rates of Nosema infection, comparable to fumagillin treatment, say Botías and colleagues 2011. The authors explain that younger queens lay high amount of eggs which compensates losses due to infections and production of not infected eggs. However, detrimental effects of stressors such as the queenless condition, lack of brood and high infection rates were noted. The ovaries and ventriculi of queens in infected colonies were not altered by Nosema infection.

Honeybee glands as infection reservoirs of Nosema [21]

Copley and Jabaji monitored the spore presence of Nosema ceranae and Nosema apis in different gland tissues (thoracic salivary, hypopharyngeal, mandibular glands, and venom sac and glands) of Canadian honeybees. The authors found both Nosema species present in all the glands as single or mixed species, and their seasonality in the different glands tightly followed the seasonal patterns in the honeybee guts. The authors concluded that these Nosema species are not tissue specific, and samples of honeybee glands may be used to determine the extent of disease in the colony. Honeybee glands are seen as an infection reservoir.

Nosema ceranae is a microsporidian parasite known to infect Asian honey bee, Apis cerana, cross-infecting the European honey bee, Apis mellifera. Fries 2010 writes that the parasite seems to replace Nosema apis in some populations of European honey bees, despite their spores being less durable than those of N. apis, and its impact differs in different environments. [22]

Nosema ceranae may cause honey bee Colony Collapse Disorder (CCD) in Spain [23]

Higes and colleagues 2009 report that the depopulation in two Spanish colonies known as colony collapse disorder (CCD) were due to the infection by Nosema ceranae (Microsporidia), an emerging honeybee pathogen. No other significant pathogens or pesticides (neonicotinoids) were detected and the bees had not been foraging in corn or sunflower crops. The treatment with fumagillin avoided the loss of surviving weak colonies.

The microsporidia are spore-forming unicellular parasites, infesting insects crustaceans, fish and vertebrates, including in humans. Some species produce deadly infections ans some are even used as biological control of insects pests. Colony collapse disorder (or CCD) is a phenomenon in which worker bees from a beehive colony abruptly disappear. Honeybees are important pollinators of crops.

The eastern hive bee Apis cerana, were found to be infected by Nosema apis and the western hive bee Apis mellifera is susceptible to Nosema ceranae.

According to Professor Fries Nosema ceranae differs in their ultrastructure and genetics from Nosema apis. Paxton writes that Nosema ceranae jumped host from Apis cerana to Apis mellifera within the last decade. It is found nowadays in the western honey bee in North and South America, the Caribbean, across Europe and Asia [24]

Possible causes of CCD were cited such as Varroa mites and insect diseases including Nosema apis and Israel acute paralysis virus, environmental change-related stresses,malnutrition and pesticides, and migratory beekeeping. Other unproved causes were cited, such as cell phone radiation and genetically modified (GM) crops used to control pests. Some researchers suggest that the combination of many factors may finaly be the cause of the disease.

Bee disease spreads to wild bumble bees [25]

Otterstatter and Thomson in 2008 suggests that a disease caused by Crithidia bombi (a trypanosome parasite) is being spread to wild bumble bees from commercially reared bumble bees used to pollinate greenhouse crops. The Colony Collapse Disorder (CCD) of commercial bees is somehow spreading to wild bumble bees which suffer serious declines. Bees are important to pollinate greenhouse crops. Commercial bumble bees are used to pollinate tomato bell pepper, almond and a lot of berries.

Infection with Crithidia bombi causes the bees to loose their ability to distinguish between flowers that contain nectar and those that don't. They make many mistakes by visiting nectar scarce flowers and in so doing, slowly starve to death. Commercially bred bees are used in greenhouses, to pollinate, for example, tomatoes and these bees typically harbour this parasite, while wild bees do not. It is believed that the commercial bees transmitted the parasite to wild populations in some cases. they escape from the greenhouses through vents and a simple mesh could help prevent their escape. [26]

On a study in 2007 Otterstatter and Thomson found that within colonies, a bee's rate of contact with infected nestmates emerged as the only significant predictor of infection risk. The authors stress that the activity of bees, in terms of their movement rates and division of labour (e.g., brood care, nest care, foraging), do not influence risk of infection. [27]

The authors predict that the spread of C.bombi from the population of greenhouses will spread to all wild bumble bee species (Bombus spp.). A remarkably high degree of genetic diversity of C. bombi among infections was found by Schmid-Hempel and Funk 2004. The authors suggest that genetic diversification of the population of C.bombi results from strong genotypic host-parasite interactions. [28]

To control the disease the authors suggest improved management of domestic bees, such as the reduction of the parasite loads and the contact with wild bees.

High pathogen loads in collapsed honeybee colonies [29]

The winter of 2006/2007 and 2007/2008 were marked by large-scale unexplained losses of honey bee colonies. These losses of colonies were named Colony Collapse Disorder (CCD).

Vanengelsdorp and colleagues 2009 believe that CCD involves an interaction between pathogens and other stress factors. The researchers found higher loads and greater number of pathogens in CCD colonies than in healthy populations. The authors write that an increased exposure to pathogens or a reduced resistance of bees toward pathogens may be the cause of the disease.

Analysis of samples of adult bees, wax comb, pollen and brood the presence of parasites such as varroa and tracheal mites; infection by bacteria, viruses and fungi; pesticide levels; nutritional factors; and bee physiology could not specify a single factor as cause of CCD.

Pesticiddes

In this study no association between increased pesticide levels and CCD was found. In fact higher levels of the acaricide coumaphos and the pyrethroid insecticide Esfenvalerate were found in healthy colonies, compared with CCD-affected colonies.

The authors suggest that the condition may be contagious or the result of exposure to a common risk factor impairing the immune systems of the bees. The higher pathogen loads are likely to have caused CCD symptoms, however, the cause of the high number of pathogens found in the affected colonies remains unknown causes the bees to become infected with so many pathogens is still not known. The authors add that it seems that pathogens play a secondary role in the development of the disease, with evidence that the condition is contagious or the result of exposure to a common risk factor.

Further attention on monitoring parasite, pathogen and pesticide loads, as well as potential interactions among pesticide and pathogen loads are being suggested by the authors.

Bee Mortality and Bee Surveillance in Europe EFSA Report [30]

The EFSA in a 2009 report on Colony Collapse Disorder says that their review of relevant literature clearly highlights an absence of shared epidemiological indicators, common surveillance procedures and comparable populations. Trend analysis and mapping suggests some periods of higher colony loss rates, but these findings should not be over interpreted.

The FSA notes that there is a consensus amongst the scientific community that the causes of colony losses in Europe and in the United States are likely to be multifactorial (in the two aspects of this term: combination of factors at one place and different factors involved according to place and period considered). Factors implicated include beekeeping and husbandry practices (feeding, migratory beekeeping, treatments and so forth), environmental factors (climate, biodiversity, etc.), chemical factors (pesticides) or biological agents (Varroa, Nosema, etc.) which together create stress, weaken bees' defense systems allowing pests and pathogens to kill the colony (e.g. one or several parasites, viruses, etc.).

High concentrations of pesticides have rarely been identified in relation to colony losses (CCD in USA and winter colony losses in Europe) although acute events of pesticide toxicity are well described during the production season (and clearly differentiated from CCD and winter colony losses). However, the questions of possible synergistic effects of various pesticides and the effect of chronic exposure to sublethal doses of pesticides remains, and requires further investigation. Biological agents such as parasites, viruses or bacteria, alone or in combination, have clearly been identified as important factors in colony losses. Nevertheless, there is still a lack of knowledge about the exact mechanisms and/or interactions involved, this must also be addressed. Even though the multifactorial origin of colony losses is well acknowledged, the respective role of each factor as a risk or causative agent is unknown, and no hierarchy of relative threat posed by each one has been established.

There are many inconsistencies in the ways in which "colony losses" are defined, leading to confusions when reports not always refer to the same phenomenon.

European tool to monitor colony losses

The EFSA call for an appropriate tool to monitor colony losses at a European level which may provide accurate figures about colony mortality which, in turn could focus control and research activities.

- Implementation of a sustainable European network for coordination and follow-up of surveillance, and research on colony losses to underpin monitoring programmes;

- Strengthen standardization at European level by harmonization of surveillance systems, data collected and by developing common performance indicators;

- Build on the examples of best practice found in existing surveillance systems on communicable and notifiable diseases already present in some countries;

- Undertake specific studies that build on the existing work in progress to improve the knowledge and understanding of factors that affect bee health (for example stress caused by pathogens, pesticides, environmental and technological factors and their interactions) using appropriate epidemiological studies (case control and longitudinal studies);

- The set up of the coordination team at European level. This is a crucial issue and the coordination team should be organized in such a way so as to ensure its sustainability and to enable effective surveillance programme activities at the European level.

Viral infections of bees implicated in Colony Collapse Disorder [31]

Cox-Foster and colleagues 2010 found that native pollinators, like wild bees and wasps, are infected by the same viral diseases as honey bees and that these viruses are transmitted via pollen.

The scientists suspect that RNA viruses are a major contributors to Colony Collapse Disorder (CCD). RNA viruses such as deformed wing virus, sacbrood virus and black queen cell virus were detected in pollen pellets collected by bees.

The detection of RNA viruses in other pollinators, including bumble bees, solitary bees and wasps, suggests that viruses might have a deep impact on ecosystem health.

The authors stress that pollen is currently being imported into many countries to feed honey bees used in agricultural pollination, increasing the risk of a wide spread of Colony Collapse Disorder.

Fly larvae causes honeybee colony losses in North America [32]

According to John Hafernik, fly parasite Apocephalus borealis, found in honey bee hives in California and South Dakota, may be one cause of colony collapse disorder (CCD) and may easily spread to honey bee colonies throughout North America The fly deposits its eggs into a bee's abdomen which dies. After being parasitized by the fly, the bees abandon their hives at night in search for lights, walking around in circles, often with no sense of direction unable to stand up on their legs and dies. About seven days the fly larvae leaves the dead bee.

The authors of the study stress that the fungus Nosema ceranae and the deformed wing virus can often also be found infecting both bees and flies. Other studies found that the fungus and the virus are implicated in CCD. Hive abandonment is the primary characteristic of the disorder. The authors write that the parasite may disturb the normal day-night rhythm of the bees, causing them to leave the hive at night. It is also possible that they are shunned by healthy hive mates because of a chemical signal allerting other bees.

The fly parasite Apocephalus borealis is also infecting bumblebees, suggesting that it may become a new threat to honey bees.

Parasite develop complex behavioural and morphological adaptations to find a host [33]

Saul-Gershenz and Millar 2006 describe that larval aggregations of the blister beetle Meloe franciscanus, which parasitize nests of the solitary bee Habropoda pallida. The larvae agregate to a cluster formed like a female bee. Then, a chemical cue similar to the sex pheromone of the female bee is produced. Male bees are attracted by the larval aggregations, try to mate. Meanwhile the beetle larvae attach to the body of the bee, being transferred to female bees in following mating, and are then carried to the bee nest.

Hafernik and Saul-Gershenz described for the first time the cooperative behaviour and mimicry strategy in blister beetles. [34]

Pollinator of rare and endemic plants growing on dunes under threat of parasites [35]

Habropoda pallida builds single celled nests in sandy slopes along water-courses in the Mojave desert.The parasitized solitary bee Habropoda pallida is a ground-nesting bee and an important pollinator of Larrea tridentata and Astragalus lentiginosus var. borreganus at Kelso Dunes and other endemic rare and threatened plants such as Astragalus lentiginosus var. micans at Eureka Dunes, according to Saul-Gershenz. Such dune restricted plants are closely dependent on such pollinators.

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