Microbial he humble bee has a special collapse of bee colonies. The name place in our lives. Essential describes the symptoms of diseased 1 for pollination of many plants, brood; infected cells become dis- diseases including food crops, the coloured, sunken and there is a char- provider of honey and royal acteristic smell. Adult bees are not jelly and many other products, affected. This disease has traditionally Tbees are important to the economies been treated with the antibiotic oxy- of countries and, as ecosystem tetracycline, but some bacterial strains of bees service providers, have few equals have developed resistance to this and among insects. There is a quote, often the disease is now increasing in preva- attributed to Einstein, suggesting that lence around the world. Although the if all the bees disappeared then disease was first described over 200 humans would follow within 4 years. years ago, much is still unknown about While this is perhaps an overstate- this infection. A German research team ment, a recent estimate of the has only recently discovered how the contribution of insect pollination, bacteria kill larvae, by building up to 2 mainly by bees, to agriculture was very high numbers in the gut before €153 bn. bursting into the haemocoel, causing There are many threats to bee death. survival, including the risk of disease European foulbrood (EFB) is caused caused by micro-organisms. The vast by the non-spore-forming bacterium majority of our knowledge of bee Melissococcus (=Streptococcus) plutonius. diseases focuses on the honey bee, Apis Unlike AFB, EFB usually affects mellifera, although there are actually unsealed brood, and the recently dead over 20,000 species, both stingless larvae present as watery and yellowish and stinging, from those with solitary brown cadavers twisted inside the cell. lifestyles to complex societies such as Despite the importance of EFB, the honey bee hives. disease is poorly understood, but like Viruses, fungi, protozoa and bacteria AFB, has increased in prevalence in are all known to cause infections in recent years. 3 bees, sometimes leading to collapse of Of the fungi known to infect bees, colonies, and causing serious threats species of the fungus Ascosphaera are to the bee-keeping industry. Bees have the most common. Ascosphaera apis is two distinct life forms, brood (egg, larva the causative agent of the well known and pupal stages which develop within chalkbrood disease in honey bees, so the hive) and adult. Most diseases are called because of the chalky appear- specific to just one of these life stages. ance of infected brood. Chalkbrood is While the list of diseases is quite long, usually considered a minor disease of only a few are of serious concern to bees, as is stonebrood, caused by the apiculturists. fungus Aspergillus. Bees come under attack Viruses can also cause devastation Major disease of bees in bee colonies. At least 18 types of Various evocative names, based on the viruses have been found infecting from a wide range of microbes. visual symptoms of diseased bees, are honey bees alone. Going by some  1. Sunken brood capping with holes suggests used to describe the most problematic delightfully descriptive names (e.g. American foulbrood (AFB). Zachary Huang, Michigan Travis R. Glare and Maureen diseases, for example foulbrood, sac- deformed wing virus, chronic paralysis State University, USA brood and chalkbrood. virus, acute bee paralysis, sacbrood 2. A dead larva killed by AFB usually forms a ‘false American foulbrood (AFB) is caused virus and black queen cell virus), tougue’ pointing upward. M.V. Smith, University of O’Callaghan consider the role of bee by the spore-forming bacterium Paeni- these viruses range from non-lethal to Guelph, Canada bacillus larvae. The disease was first causing significant mortality in nests. 3. Larvae showing typical European foulbrood (EFB) symptoms. These larvae show yellow streaks. M.V. Smith, diseases in the worldwide decline of described in 1769. AFB is probably One of the more interesting aspects University of Guelph, Canada the most virulent disease of honey bee of viral disease is that many infections  A honey bee (Apis mellifera) feeding. Dr John brood and is capable of causing the cause no obvious symptoms much of Brackenbury / Science Photo Library these key ecosystem providers.

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 1. Chalkbrood, whereby the larvae become mouldy with white (adult) honey bees on several continents, especially North detected in the semen of honey bee others. Some strains of bees are capable understanding of the cause of CCD, hyphae, then hardened to be similar to pieces of white chalk. This America. The sometimes startlingly high mortality rates have drones, suggesting that mating may of recognizing diseased brood well no cure will be possible, but when disease is mostly considered a stress disease, only occuring in weak, or in otherwise stressed colonies. M.V. Smith, University of Guelph, not been attributed to a particular cause. Several recent spread some disease both horizontally before it is a threat to the hive, and the factors are known, many large and Canada studies suggest that some colony collapse is caused by a and vertically. Pathogens can be remove diseased individuals. In some small mitigations can be used.  2. Close-up of the head of a larva killed by Sacbrood. M.V. Smith, combination of disease and the parasitic attentions of Varroa transmitted in bees and sometimes cases, the task of disposing of diseased The risk is that with increasing University of Guelph, Canada mites. Various studies have found that prevalence of viral in bee products, prompting many insects falls to specialist ‘undertaker pressure from civilization, bees could  3. A honey bee (Apis mellifera) with two Varroa jacobsoni mites on and protozoan diseases is higher in Varroa-infected hives countries to closely regulate the bees’ that appear to be old workers. suffer increasingly from threats and its thorax. Maryann Frazier / Science Photo Library and Varroa is thought to be capable of acting as a vector importation of bees and honey. Bees are also assisted in resisting dis- stress, including increasing prevalence  4. Coloured SEM of a Varroa sp. honey bee mite. Steve Gschmeissner for pathogenic microbes. In some cases, viral diseases that ease by propolis, present in the of disease. A better understanding of / Science Photo Library do not usually cause high mortality are rampant in hives How do bees defend plant resins collected by honey bees bee dynamics and the development with Varroa or have been associated with CCD. Israeli Acute themselves from disease? and used as a sealant in the hives. of mitigations is urgently required. the time. Kashmir bee virus can persist in bee populations Paralysis Virus (IAPV) was recently found to be the most The high density populations and Propolis is known for its antimicrobial causing no obvious symptoms, only to explode into lethal consistent indicator of CCD, as well as Kashmir bee virus conditions within the bee colony properties. Travis R. Glare & Maureen infections, possibly triggered by bee stress factors such as and Nosema spp. However, no causal link has been made (enclosed, moist, dark, poorly venti- O’Callaghan attack by the Varroa mite. Varroa mites are parasites on honey between IAPV and CCD. As with all living things, stress lated) are ideal for the outbreak What hope is there for AgResearch, Lincoln, Private Bag bees and have spread around most of the world, causing increases the susceptibility of the host to a pathogen, and and spread of disease. Fortunately, the future? 4749, Christchurch, New Zealand significant losses in hives as well acting as vectors for some if bees are under stress, disease can be more debilitating. because bees are constantly exposed With increasing prevalence of disease, (t +64 3 321 8825; e travis.glare@ viruses. Virus infections can be hard to detect and diagnose, Whether CCD is only caused by the interaction between to pathogenic micro-organisms, they unexplained disappearance of bees on agresearch.co.nz) as symptoms, if any, resemble other mortality causes. a specific stress such as Varroa and some diseases, or have evolved strategies to resist infec- some continents and the emergence widespread interaction between a number of stresses is tion. The cuticle of bees acts as a barrier of new diseases, bee populations are Emerging diseases unclear. Combinations of stresses could include multiple to penetration, and immune system- under threat. Fortunately, increasing Further reading Microbes are constantly evolving, leading to the emergence diseases. Using molecular techniques, several studies have based defence can prevent infection sophistication of research methods is Bailey, L. (1968). Honey bee pathology. of new strains with novel pathogenic abilities. For example, shown multiple diseases infecting single bees. So diseases, of many minor pathogens. However, allowing unprecedented understand- Annu Rev Entomol 13, 191–212. some honey bee diseases appear to have widened their host some of which may not normally cause death, could act the recent completion of the honey ing and insights into bee pathology Chen, Y.P. & Siede, R. (2007). Honey range in recent years. Protozoa of the genus Nosema infect together to kill. Additionally, nutritional stress can exacerbate bee genome sequence has shown that by allowing detection of cryptic bee viruses. Adv Virus Res 70, 33–80. many invertebrates, and individual species are typically the incidence of pathogens. they have only about a third of the infections, generation of epidemiolo- Cox-Foster, D.L. & others (2007). A quite limited in their host range. Nosema apis has long been number of known immunologically gical data and detailed understanding metagenomic survey of microbes in recognized as causing one of the most important diseases How do diseases spread? related genes when compared to flies of bee–pathogen interaction. With honey bee colony collapse disorder. in adult honey bees, infecting the guts of adult bees. How- How diseases spread between individuals is still largely or mosquitoes, suggesting that bees increasing understanding comes a Science 318, 283–287. ever, Nosema ceranae, thought to infect only the Asiatic or unknown. Both horizontal transmission (where viruses are rely less on individual immunity than better appreciation of the role of dis- Evans, J.D. & others (2006). Immune Eastern honey bee, Apis cerana, has recently been shown transmitted among individuals of the same generation), and most insects. ease and methods for reducing impact. pathways and defence mechanisms in to infect the European honey bee, A. mellifera. Evidence vertical transmission (where the disease is passed from Bees, in common with a number of For example, the presence of Kashmir honey bees Apis mellifera. Insect Mol Biol is emerging of recent spread of N. ceranae in honey bee queens to their offspring) are known. Modern molecular- other social insects, have well devel- bee virus has been detected in the 15, 645–656. populations around the world since around 1998. There based techniques have contributed significantly to our oped behavioural responses to combat UK, despite never being identified as Paxton, R.J. & others (2007). Nosema is ongoing risk that other highly virulent diseases of honey understanding, allowing investigation of whether pathogens disease. These behavioural responses a cause of infection in UK bees based ceranae has infected Apis mellifera in bees will emerge. are present inside eggs, and by establishing the relatedness are collectively known as hygienic on visual symptoms. This suggests a Europe since at least 1998 and may of occurrences of disease in different hives. It is obvious behaviour and include recognition and potential non-lethal role for this virus. be more virulent than Nosema apis. Bees under stress how some diseases spread; the presence of large numbers removal of diseased brood by worker Detection of virus associated with Apidologie 38, 558–565. There is still so much we don’t know about how combinations of spores, whether fungal, bacterial or protozoan, inside a bees. Bee species, and even different CCD may also lead to a cure. Wilkins, S. & others (2007). The of microbial diseases, parasites, pollution and urbanization hive will contaminate brood and/or workers that come in hives of the same species, differ in their Separating the various factors affecting incidence of honey bee pests and are affecting bees. Colony Collapse Disorder (CCD) is the contact. However, some more unusual routes have also ability to perform hygienic behaviours, bee colonies will allow the causal diseases in England and Wales. Pest name given to the recent widespread mortality of worker been demonstrated. DNA from viral pathogens has been with some colonies far superior to agents to be directly treated. Without Manage Sci 63, 1062–1068.

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