by Sofia Croppi and Erik Tihelka. No.16 August 2020
Beekeeping belongs among the oldest agricultural activities of man. Since at least 9,000 years before the present, humans have regularly collected honey and wax, an avocation that later developed into true beekeeping as we know it today. The long history of human interest in the life of honey bees is documented in ancient manuscripts such as Columella’s (4 – c. 70 AD) monumental work De re rustica, which also includes vivid descriptions of honey bee diseases. In the aforementioned book, Columella discusses, among others, disorders and diseases such as starvation, dysentery, poisoning from plants, and possibly also conditions that we know today as European and American foulbrood, and tracheal mite infestation. However, it was not until much later that the earliest scientific enquiries into the causes of foulbrood were first made.
The first use of the word ‘foulbrood’ has been traced back to the German apiculturist and clergyman Adam Gottlob Schirach (1724 – 1773) in 1769 [1]. Schirach argued that the disease is caused by malnutrition and by a disorder of the queen that causes her to lay brood the wrong way into the cell. Thus, in 2020, 251 years have elapsed since the first modern attempt at explaining foulbrood in bees, albeit retrospectively a somewhat naïve one.
Looking back at the history of bee diseases before the age of modern veterinary medicine offers us a unique insight into the history of beekeeping but understanding how our ancestors dealt with this serious disease can also be inspiring for organic beekeepers today. In this article, we briefly examine the history of American and European foulbrood in central European apiculture at the turn of the 19th and 20th centuries as viewed through the lens of the beekeeping press of the time.
American foulbrood, also abbreviated to AFB, is a disease of honey bees that hardly requires an introduction. The causative agent of AFB is the destructive Gram-positive, spore-forming, rod-shaped bacterium Paenibacillus larvae. The equally destructive European foulbrood, EFB, is caused by the Gram-positive Melissococcus pluton which, unlike the former, affects open brood. It was not until 1885 that Cheshire and Cheyne demonstrated that the causative agent of the latter disease is the bacterium Bacillus alvei, which was subsequently reclassified as Melissococcus pluton [2],[3]. The disease became known as European foulbrood, since it was first described in Europe. The causative agent of American foulbrood, Paenibacillus larvae, was not discovered until 1907 in the USA, but despite their somewhat misleading names both diseases have a cosmopolitan distribution [4]. Before this date, beekeepers had to rely largely on their intuition and trial-and-error to combat the disease.
Early beekeeping authors used terms such as “foulbrood”, “bee plague”, “brood decay”, or “sour disease” interchangeably, while others developed specific nomenclatural systems. For example, Jan Dzierżon (1811 – 1906), the influential Polish beekeeper and one of the first modern European beekeepers to use a movable frame hive, distinguished between two types of foulbrood – ‘mild and curable’ which affected open brood (possibly European foulbrood) and ‘malignant and incurable’ foulbrood which affected capped and uncapped brood, (possibly American foulbrood [5], but it is possible that other non-infectious conditions were included under these umbrella terms as well. The fact that foulbrood used to be defined so vaguely and that it was probably used to refer to several different diseases of the brood presented a massive complication, for it was hardly possible to study the disease without clearing the problem of naming it first. Today it is often impossible to know whether the authors were dealing with American or European foulbrood, or if they encountered a totally different condition, especially when their descriptions are brief. An overview of diseases, at least passingly similar to American and European foulbrood, is given in Tab. 1.
| Disease | Similarities to Foulbrood | Differences from Foulbrood |
| Sacbrood. | Discoloured larvae, perforated capping, unpleasant smell. | Pupal stage never effected infected larvae show clear segmentation. The dead larvae have a raised head infected larva appears baggy-like, if punctured a watery fluid escape dried scales can be easily removed from the cell. |
| Chalkbrood. | Perforated cappings. | Diseased larvae become white to grey and chalky in appearance mummies can easily be removed affected larvae never rope. |
| “Half-moon syndrome”. | Discoloured larvae unpleasant smell. | Many eggs in one cell drone brood in worker cells affected larvae do not rope. |
| Brood dying from malnutrition. | Discoloured and decaying brood, perforated capping. | Symptoms similar to European foulbrood. |
| Brood dying from cold. | If not removed quickly by bees the dead brood decays, becomes discoloured and produces an unpleasant smell. | Symptoms similar to foulbrood. |
Enigmatic causes
Many conflicting ideas about the possible causes of foulbrood have been voiced throughout the last 250 years. Reverend Schirach, who coined the disease’s name in the mid-18th century, attributed foulbrood to malnutrition and the queen placing bee eggs head inwards into the cells. Numerous authors after him, proposed their own hypotheses, a selection of which is provided in Tab. 2.
| Author | Cause |
| Schirach (1769) | Malnutrition and placing bee larvae head inwards into the cells |
| Leuckhart (1860) | Fungi |
| Muhlfeld (1868) | Parasitic wasp, genus ichneumon |
| Preuss (1868) | Fungus, genus Cryptococcus |
| Geilen (1868) | Bees bringing decaying matter home from animal corpses |
| Lambrecht (1870) | Fermentation of bee bread |
| Hallier (1870) | Fungi |
| Cornallia (1870) | Fungus, genus Cryptococcus |
| Fischer (1871) | Malnutrition |
Due to the wide range of conditions historically considered under foulbrood, it should not be surprising that the disease was traditionally thought to have many causes. A popular explanation in the latter half of the 19th century claimed that a combination of malnutrition and neglect of the brood by nurse bees could result in foulbrood (9). Some believed that foulbrood outbreaks coincided with the honeydew flow and that honeydew can contains pathogenic fungi that may cause the disease (10). Others thought that foulbrood was caused by insufficient protein in the bee’s diet (11) and some observed that foulbrood was especially prevalent in years with poor honey yields (12). Others even believed that foulbrood resulted from “poisoned honey” (13) pointing to the plant Daphne mezereum as the possible culprit (14,15). While this plant is indeed poisonous to humans, similar effects have not been reported in bees. Moreover, poisoning by toxic nectar or pollen typically affects the adult bee population and not the brood alone (16).
Similarly, it was claimed that “foul” or “fermented” honey and pollen could be the cause of foulbrood (14 – 17). Honey and pollen collected in late autumn can start fermenting during the winter and in spring beekeepers often found conspicuous moulds overgrowing the combs. But could fermenting honey and pollen cause foulbrood? The Prussian beekeeper Emil Hilbert designed an experiment in 1878 in which he fed two strong colonies with fermented honey and pollen. The colonies weakened quickly, losing a considerable portion of the adult population and much of their brood died. In 20 days, all that what was left of the two colonies was just the queen surrounded by a small cohort of workers. However, the experimental feeding failed to induce foulbrood symptoms. Hilbert therefore concluded that fermenting honey and pollen could not be the sole cause of foulbrood (18).
Another oft-cited hypothesis was that foulbrood outbreaks are triggered by cold spells that cause the brood to die; it was suspected that if a beekeeper inspects his hive too frequently the brood may succumb to the cold. Likewise, frosty nights in early spring may cause large amounts of brood to die and if the bees don’t remove all the dead brood in time, a foulbrood outbreak may result (11, 19). To prevent brood from dying when inspections had to be done on cold days, some placed a hot brick onto the bottom board to compensate for the lost heat (17).
The Czech beekeeper and priest Ferdinand Liška carried out a series of experiments on air circulation inside the hive in the 1870s. He concluded that CO2-rich air leaves the hive only very slowly and that bees must therefore fan vigorously to facilitate gas exchange between the hive and its surroundings. He used several anecdotal observations of other beekeepers and of himself to suggest that foulbrood is caused by “foul” or “depleted” air. When bee brood dies, due to cold for instance, it would undergo a process of decay that would presumably produce various poisonous gases responsible for the characteristic smell associated with foulbrood. Liška advised that a well-ventilated hive can best prevent the disease (9).
By the 1880s, some French beekeepers came to believe that the disease was caused by “foul” water. It was advised that beekeepers provide their colonies with clean water and change it daily. Some boiled the water and added thyme twigs. According to reports from the time, these measures were very efficient in some cases (20). The traditional practice of adding thyme twigs to water is certainly very interesting, since essential oils and extracts from thyme have been shown to possess strong antimicrobial properties against P. larvae in laboratory trials (21, 22).
By the end of the 19th century, most beekeepers came to believe that foulbrood was in fact a microbe-borne disease (17, 23) Janklo (15) wrote in 1905: “The most frequent cause of bacteria is with greatest certainty the uncleanness of the bee’s dwelling and the air in the beehive. Hives that are not ventilated well can cause foulbrood, because foul air provides ideal conditions for bacterial life. These then start to swirl and multiply as soon as they find a dead larva in the comb.”
Beekeepers in the 19th century believed that mismanagement and various mistakes on behalf of the beekeeper could contribute to a foulbrood outbreak. Several authors, starting with Schirach in 1769, have emphasised the role of malnutrition in the development of the disease. This view seems to be corroborated by recent findings. Malnourished bees are indeed more susceptible to disease (24b -26). When P. larvae is ingested, it resides in the bee larval gut and competes with the developing bee for food (27). If food is plentiful, the larvae will most probably develop normally, pupate, and excrete the pathogen during development. But if food is in short supply, P. larvae will eventually kill the larva and produce typical AFB symptoms (28). Therefore, the old observation that foulbrood and bee nutrition are linked seems to be based on truth.
The location of the hive was thought to play an important role in foulbrood outbreaks. Beehives located in shaded and damp places were supposedly more likely to develop foulbrood. Beekeepers were advised to keep their apiaries clean and pick up any dead bees. Beekeeping tools had to be cleaned frequently, beehives kept well-ventilated, the combs changed frequently, and the colonies kept strong all year around to prevent foulbrood (15, 29). Another widespread belief claimed that foulbrood outbreaks only occur when the weather is unfavourable; a cold spell would first kill larvae and if not cleaned quickly the condition would soon spread to the rest of the brood (30). The bee genotype was another factor taken into account. Some beekeepers observed that Italians (A. m. ligustica) were especially susceptible to the disease compared to the native dark honey bees (A. m. mellifera).
Surprisingly, early writings from the middle of the 19th century indicate that foulbrood was originally not very prevalent. In 1840, the Czech beekeeper and clergyman Josef Stern called foulbrood a “rare disease” (13). The Prussian bee journal Eichstadt Bienenzeitung in 1868 published an account of a local beekeeper that kept bees since his early childhood but never came across foulbrood until one of his colleagues purchased a movable frame hive (31). In Germany, there was a popular saying “Dzierzonstöcke, Faulbrutstöcke”(30) which very roughly translates as “Dzierżon hives, foulbrood thrives”, referring to Jan Dzierżon’s early movable frame hive. The observation that many beekeepers only started experiencing problems with foulbrood when they switched from primitive straw and log hives to modern movable frame hives is surprisingly prevalent in apicultural literature of the timeas well as the claim that early on, affected colonies would often recover spontaneously (13)
Caution is needed when interpreting these observations. It is possible that since before the introduction of movable comb hives beekeepers were hardly able to inspect their colonies, they would rarely see foulbrood and therefore considered it a rare disease. But perhaps the prevalence of foulbrood during the 19th century before the introduction of movable frame hives was, at least in central Europe, lower than today. Foulbrood is absent or present at very low levels across much of Africa where intensive beekeeping is not practised and where beekeepers replenish their stock from captured swarms (33). Likewise, studies in New Zealand have demonstrated that the prevalence of American foulbrood in feral colonies is low (34).
Do we have any hard data to show how prevalent foulbrood was in Europe in the past? Quantitative surveys of bee diseases provide valuable data for understanding the historical development of bee health, but studies of this kind are rare over the past 250 years. In Bohemia (western historical region of the present day Czech Republic), the State Federation of Beekeeping Societies (SFBSB, Zemské ústředí včelařských spolků pro Čechy) acted as a union of several hundreds of smaller beekeeping clubs so that over 85% of Bohemian beekeepers were affiliated with the Federation. The SFBSB monitored honey bee losses between 1936 and 1941 by sending out questionnaires to its local constituent organisations (35). Although the survey does not capture the state of honey bee health before the introduction of ‘modern’ beekeeping practices, its scale and age make it of a special interest nonetheless. Between 1936 and 1941, reported annual colony mortality averaged 8.1% (2.1% – 23%; Tab. 3). High loses were experienced during the war years when winter feed was scarce, so the figure is likely an overestimate of what the normal bee mortality rates would be like. In either way, an 8.1% colony loss rate is almost half the colony mortality beekeepers in Austria, Czech Republic, Slovakia, Poland, Germany, Switzerland and Slovenia are experiencing today, at least based on data collected by the COLOSS between 2008 and 2016 (36-38). Although caution should be exercised when comparing these two bee health surveys since they used different methodologies, it should also be pointed out that central Europe is still enjoying one of the lowest colony mortality rates on the continent (36). Assuming that beekeepers were faithful in reporting their colony losses, then during the five years of the SFBSB survey, foulbrood incidence was low and accounted for merely 1% of colony losses. The leading causes of colony death were the so-called ‘obstipatio apium’ and ‘obstipatio pollinaris’ (syndromes associated with dysentery and loss of adult workers, respectively), nosematosis, and tracheal mite disease. All in all, the results of this historical and indeed rather unique bee survey show that bee losses were probably much lower before the introduction of Varroa, and that foulbrood was not a major contributor of colony mortality at the time.
| Year | 1936 | 1937 | 1938 | 1939 | 1940 | 1941 | Average |
| Winter mortality | 1.6% | 2.9% | 1.6% | 1.4% | 21.5% | 10.5% | 6.7% |
| Total losses | 2.1% | 4.0% | 2.3% | 2.3% | 23.0% | 14.9% | 8.1% |
Why did pre-modern beekeepers experience low foulbrood incidence? This could have been due to the beekeepers restocking capturing wild swarms, which are subject to higher selection pressures than managed colonies and so are presumably more resistant to the disease (39). Studies in New Zealand confirmed that wild colonies have lower P. larvae spore loads than managed colonies (40). Traditional skep beekeepers would often kill their best colonies in autumn to extract honey and this barbaric practice possibly prevented the build-up of spores in hive material. Another factor that may have aided the presumed resistance or tolerance to foulbrood was that in the past, colonies were seldom treated by beekeepers, placing them under stronger selective pressures. Consequently, colonies were under a much higher pressure to develop resistance compared with today (39). Old apiaries were small and dispersed (41) reducing the likelihood of bees drifting or robbing and exchanging pathogens; this limited the transmission of foulbrood and would probably lead pathogens to evolve avirulence (39). Moreover, before movable frame hives became widespread in Europe in the mid-19th century, beekeepers could not transfer combs between hives which probably significantly limited the spread of the disease. Beekeepers allowed and encouraged their colonies to swarm because before the introduction of modern queen rearing methods and advances in making splits, swarming used to be the only way beekeepers could multiply their stocks. Swarming probably decreases the spore load of individual colonies and thus lowers the chance of a foulbrood outbreak (42,43). Before the invention of the honey extractor in 1865, beekeepers in Europe had to extract honey either by immersing honeycombs into warm water or by using presses. Both methods damaged the comb to the extent that it could not be reused. This meant that bees had to draw fresh comb every year, likely reducing the pathogen load.
Janko (15) cites two ways of foulbrood transition: primary and secondary. Primary transmission, as he called it, occurs when the bees themselves bring pathogens into their hive. Secondary transmission occurs when the apiculturist brings the pathogen with contaminated beekeeping equipment. Some beekeepers believed that foulbrood could be transmitted by wax moths (20). An interesting note regarding the transmission of foulbrood was made by McLain (44). He suggested that the causative agent of foulbrood may be transmitted via the beekeeper’s contaminated clothes. He also observed that the disease spreads in the direction of the prevailing wind. This caused him to believe that wind could play an important role in transmitting foulbrood as well. Today it is understood that most beekeeping equipment, perhaps with the exception of the hive tool, plays a negligible role in foulbrood transmission, but the observation of foulbrood spreading downwind may be associated with the direction of drifting bees (6).
Even in the 19th century, many beekeepers relied on some form of a quarantine system for their colonies. Quarantine zones were set up as soon as unhealthy colonies were detected to protect the uninfected ones. Foulbrood positive hives would be carried to a separate apiary, far away from healthy stock. To prevent cross-contamination, beekeepers had to use dedicated tools and clothes for work at the quarantined colonies (15). Once a quarantine was established, the treatment could start. Many different treatment methods were designed in the past but unfortunately few empirical studies were carried out to test their efficiency.
Before the discovery and widespread introduction of antiseptics in the 1860s, it was apparently widely believed that hives with bees that suffered from foulbrood should be emptied and let to air for two years. It was believed that like this the disease would “leave the hive” (14). Later, many practitioners of beekeeping recognised that in order to avoid infection in the future, the hive and the associated tools must be disinfected. One recipe suggested that hives should be washed with 10% sulphuric acid, rinsed thoroughly with water, and then placed into a pre-heated oven for several hours. Meanwhile frames with dead brood were to be burned and dead bees buried. The soil in front of the hive had to be dug up and sprinkled with 10% sulphuric acid (31). Some suggested that there is no need to burn all the combs, but the beekeepers should manually remove dead larvae from the cells and then return them into the hive. Some beekeepers even summoned birds to clean their frames of dead bees. Not all beekeepers were willing to burn their equipment or spend long hours cleaning the combs and so some took this advice more lightly than others, which undoubtedly helped amplify and even spread the disease further.
In Britain, Frank Richard Cheshire (1833?–1894) suggested mixing phenol with sugar water in a 1:500 ratio and feeding the resulting solution to diseased colonies (40). The effects of the treatment have been disputed, some beekeepers reported that the procedure was totally inefficient, and later various alleged improvements were made to the method (45). However, more recent studies have shown that phenolic phytochemicals do display strong antimicrobial activities against P. larvae (46).
Others recommended feeding colonies with a mixture of salicylic acid or beta naphthol with sugary water in a 1:1,000 ratio. Emil Hilbert made extensive experiments with using salicylic acid to treat foulbrood and constructed a burner to evaporate the acid. The burner was loaded with 0.5-1g of salicylic acid powder, ignited, and placed into the hive. After all acid evaporated, the bees were fed with honey or sugar mixed with more salicylic acid in a 1:935 ratio. The whole procedure was then repeated five times. The chemical was apparently nontoxic to young brood. Formic acid and thymol were also endorsed. These treatments were reportedly the most efficient if the disease was only in its infancies, late-stage foulbrood was difficult to treat (8, 10, 12, 47).
Different variants of the shook swarm method were also popular. This approach involves the transfer of adult bees into a new disinfected hive, while leaving the old combs and brood behind (13). The old hive was then burned or disinfected thoroughly with phenol and formaldehyde. The combs from old hive were immersed in a 4% formaldehyde solution for 24 hours. The wax was then extracted and sold for industrial uses. Beekeepers were warned not to reuse wax from infected colonies (15, 29, 48). Indeed, P. larvae spores are heat-resistant and survive when wax is boiled in water. Only when left at 120°C for half hour and under pressure are all spores killed (49).
Some beekeepers observed that replacing the queen may help cure the disease (50,70) but it is more likely that the alleviation of disease symptoms was due to brood interruption resulting from queen replacement rather than the superior qualities of the new queen.
Interestingly, some traditional European beekeepers during the 19th century believed that foraging on certain plants such as spiraea shrubs, poplar trees, and other conifers could help colonies suffering from foulbrood to overcome the disease. Some beekeepers that had colonies with advanced foulbrood noticed that their colonies recovered spontaneously after foraging on willow trees (12,51). This observation is likewise interesting, since laboratory studies have found that the pollen of some plants contains saturated fatty acids that have antimicrobial properties against P. larvae and M. pluton (52). Plants with pollen high in these bioactive compounds have been highlighted as potentially important resources for honey bee self-medication (53).
Not everyone believed, however, that foulbrood can be efficiently cured. Some held the opinion that no efficient treatment exists and advocated the destruction of all affected colonies by burnin (17,54).
Although beekeeping law has its origins in the ancient world, few restrictions regarding bee diseases were in place in Europe during the 19th century. It was not until 1914 that American and European foulbrood became notifiable veterinary diseases under the Austro-Hungarian law (55). When a beekeeper suspected American or European foulbrood in his colonies, he had to notify the mayor. He would then call a veterinarian or a beekeeping expert who would inspect the colonies and decide on the next steps. A sample of the infected comb would be sent for laboratory analysis. All diseased colonies were quarantined; moving the hives or selling bee products was strictly prohibited. If the disease was severe and affected many colonies, the bees had to be killed with sulphur and the hives and equipment stored away carefully so they would not be come into contact by forager bees from other uninfected apiaries. If the progression of the disease was mild, the shook swarm method would be used. Contaminated materials had to be either burned or disinfected where possible. Failure to comply with the law would result in a fine ranging from 1 to 1,000 Austro- Hungarian Krones (i.e. €4 to €8,180 in 2019 value) or into imprisonment for 1 day to 3 years (56).
Some of the traditional methods of foulbrood treatment, namely moving colonies to self-medicate on certain plants or providing extracts of aromatic plants may find a surprising resonance with organic beekeepers today. It would be interesting to speculate that our ancestors took advantage of the antimicrobial and anti-AFB properties of fatty acids and essential oils of plants long before they have been re- discovered and studied empirically in the several past decades. Perhaps it is time to re-examine the traditional practices of European beekeepers in a new light.
We thank Ioannis Anagnostopoulos for valuable comments on an earlier version of this manuscript.
Sofia Croppi was first introduced to beekeeping by her mother as a teenager. Her interest in bees was furthered through her passion for veterinary medicine and ecological sustainability thanks to a number of collaborations that brought her closer to apiological research. She is currently collaborating with the Food and Agriculture Organization of the United Nations (FAO) in Rome to study antimicrobial resistance in bees. Sofia will be commencing her studies at the Veterinary School of the University of Bristol in September 2020.
Erik Tihelka comes from a family with a long tradition of beekeeping managing 40 colonies in the Kutná hora region of the Czech Republic. The key focus of their beekeeping is apitourism and public outreach regarding bee conservation. He is interested in integrating molecular data and fossil evidence to elucidate questions in insect evolution. Erik will be commencing his studies in evolutionary biology at the University of Bristol in the Fall of 2020.
REFERENCES
[1] SCHIRACH, A. G. Histoire naturelle de la reine des abeilles [The Natural History of the Queen of the Bees]. Amsterdam: B. Vlam, 1769, p. 56. [2] CHESHIRE, F. R., CHEYNE, W. W. The pathogenic history and the history under cultivation of a new bacillus (B Alvei), the cause of a disease of the hive bee hitherto known as foul brood. Journal of the Royal Microscopical Society 5(4), pp. 581–601, 1885. [3] BAILEY, L., Collins, M. D. Reclassification of ‘Streptococcus pluton’ (White) in a new genus Melissococcus, as Melissococcus pluton nom. rev.; comb. nov. Journal of Applied Microbiology 53(2), pp. 215-217, 1982. [4] WHITE, G. F. The cause of American foulbrood. Circular, US Department of Agriculture, Bureau of Entomology 94(1), pp. 1-44, 1907. [5] Dzierzon, J. 1882. Rational Bee-Keeping. Houlston & Sons, London. [6] GOODWIN, M. Elimination of American Foulbrood Disease without the use of Drugs. Wellington: National Beekeepers ́ Association of Nez Zealand, 2013, 115 p. [7] WHITE, G. F. The bacteria of the apiary with special reference to bee disease. Technical Series, US Department of Agriculture, Bureau of Entomology 14(1), pp. 1- 50, 1906. [8] PHILLIPS, E. F., WHITE, G. F. Historical notes on the causes of bee diseases. Bulletin, US Department of Agriculture, Bureau of Entomology 98(1), pp. 1-96, 1912. [9] LIŠKA, P. F. Morovina a hniloplod, neboli zhoubné následky nedýchatelného a otráveného vzduchu v oule [Brood putrefaction and foulbrood, or the consequences of depleted and foul air in the beehive]. Prague: self-published, 1876, 62 p. [10] KEBRLE, J. Zpráva o XXIV. valném sjezdu německých a rakouských včelařů v Praze od 7-11. Září 1879 [A Report from the German beekeeping congress held in Prague, 7th-11th September 1879]. Český včelař 13(6), pp. 86-90, 1880. [11] ANON. Z dějin rozprav o hniloplodu [History of foulbrood]. Včela brněnská 24(8), pp. 103-106, 1890. [12] WARNKER, V. J. T. K otázce hniloplodu [On the foulbrood question]. Včela brněnská 20(11), pp. 161-164, 1886. [13] STERN, J. Krátké ponaučení o včelařství [A Short Treatise on Beekeeping]. Brno: František Gastl, 1840, p. 33. [14] KODYM, F. S. Kniha včelařská hlavně dle Dzierzona [The Book of Beekeeping, Based Mainly on Dzierzon]. Prague: Bedřich Rohlíček, 1857, pp. 261-262. [15] JANKO, J. Jak předejíti a vyléčiti hniloplod? [How to prevent and cure foulbrood?]. Koleč: První český včelařský závod v Kolči, 1905, 11 p. [16] BUTLER, C. G. Bee paralysis, May sickness etc. Bee World 24(1), pp. 3-7, 1943. [17] ŠABACKÝ, F. Něco ze včelařství [Some notes on apiculture]. Včela brněnská 22(2), pp. 174-175, 1885 [18] HILBERT, E. Jaké úkazy pozorujeme u včelstva, jehož zásoby medu a pelu zakysaly? A může-li případ takový způsobiti hnilobu plodu? [What kinds of symptoms develop in colonies fed with fermented honey and pollen show? And could this be the cause of foulbrood?]. Český včelař 7(10), pp. 154-155, 1878. [19] MACNER, H. Zkušenosti o hnilobě plodu nabyté v Písku r. 1870 [Experiences pertaining to the foulbrood outbreak in Písek in 1870]. Včelař 5(10), p. 79, 1871. [20] HLINECKÝ, M. Osvědčený prostředek proti hniloplodu [An effective foulbrood cure]. Český včelař 12(6), pp. 90-92, 1888. [21] ALIPPI, A. M., RINGUELET, J. A., CERIMELE, E. L., RE, M. S., HENNING, C. P. Antimicrobial activity of some essential oils against Paenibacillus larvae, the causal agent of American foulbrood disease. Journal of Herbs, Spices & Medicinal Plants, 4(2), pp. 9-16, 1996. [22] KUZYŠINOVÁ, K., MUDROŇOVÁ, D., TOPORČÁK, J., NEMCOVÁ, R., MOLNÁR, L., MAĎARI, A., KOŽÁR, M. Testing of inhibition activity of essential oils against Paenibacillus larvae – the causative agent of American foulbrood. Acta Veterinaria Brno, 83(1), pp. 9-12, 2014. [23] KOVÁŘ, V. Příspěvek ku theorii o hnilobě plodu [Contribution to the theory of foulbrood]. Český včelař 9(8-9), pp. 108-110, 1875. [24] ALAUX, C., DUCLOZ, F., CRAUSER, D., LE CONTE, Y. Diet effects on honeybee immunocompetence. Biology Letters rsbl20090986, 2010. [25] FOLEY, K., FAZIO, G., JENSEN, A. B., HUGHES, W. O. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. Journal of Invertebrate Pathology 111(1), p. 68-73, 2012. [26] DI PASQUALE, G., SALIGNON, M., LE CONTE, Y., BELZUNCES, L. P., DECOURTYE, A., KRETZSCHMAR, A., … ALAUX, C. Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PloS One 8(8), e72016, 2013. [27] BAILEY, L., Ball, B. V. Honey Bee Pathology. London: Academic Press, 1991, p. 37. [28] BAILEY, L. Melissococcus pluton, the cause of European foulbrood of honey bees (Apis spp.). Journal of Applied Microbiology 55(1), pp. 65-69, 1983. [29] KOLRUS, J. P. Krátká rukojeť moudrého včelaření [A Brief Handbook of Rational Beekeeping]. Prague: Karel Bellmann, 1863, pp. 98-100. [30] BAUMAN, J. Hniloba plodu [Foulbrood]. Český včelař 10(9), pp. 140-141, 1886. [31] PREUSS. Das Wesen der bosartigen Faulbrut besteht in einem mikroskopischen Pilze, Cryptococeus alvearis. Sie kann verhutet und geheilt werden [The nature of the malignant foulbrood consists in a microscopic fungus, Cryptococeus alvearis. It can be combated and cured]. Eichstadt Bienenzeitung 24(19), pp. 225-228, 1868. [32] KRULICH, V. Něco ze včelaření našich předků [Some notes on beekeeping of our ancestors]. Český včelař 31(8), pp. 116-119, 1897. [33] Hussein M.H. (2000) Beekeeping in Africa, Apiacta 1, 32–48.; Fries I., Raina S. (2003) American Foulbrood and African Honey Bees (Hymenoptera: Apidae), J. Econ. Entomol. 96, 1641–1646. [34] GOODWIN, R. M., HOUTEN, A. T., PERRY, J. H. Incidence of American foulbrood infections in feral honey bee colonies in New Zealand. New Zealand Journal of Zoology 21(3), pp. 285-287, 1994. [35] Nepraš J. (ed) (1941). – Zpráva zemského ústředí včelařských spolků pro Čechy v roce 1935 (Annual Report of the State Federation of Beekeeping Societies for Bohemia for 1941). [in Czech]. Prague, State Federation of Beekeeping Societies for Bohemia. Dietemann, V., Pirk, C. W. W., & Crewe, R. (2009). Is there a need for conservation of honeybees in Africa?. Apidologie, 40 (3), 285-295. [36] BRODSCHNEIDER, R., GRAY, A., ZEE, R. VAN DER, ADJLANE, N., BRUSBARDIS, V., CHARRIÈRE, J.-D., CHLEBO, R., COFFEY, M.F., CRAILSHEIM, K., DAHLE, B., DANIHLÍK, J., DANNEELS, E., GRAAF, D.C. DE, DRAŽIĆ, M.M., FEDORIAK, M., FORSYTHE, I., GOLUBOVSKI, M., GREGORC, A., GRZĘDA, U., HUBBUCK, I., TUNCA, R.İ., KAUKO, L., KILPINEN, O., KRETAVICIUS, J., KRISTIANSEN, P., MARTIKKALA, M., MARTÍN-HERNÁNDEZ, R., MUTINELLI, F., PETERSON, M., OTTEN, C., OZKIRIM, A., RAUDMETS, A., SIMON-DELSO, N., SOROKER, V., TOPOLSKA, G., VALLON, J., VEJSNÆS, F., WOEHL, S. Preliminary analysis of loss rates of honey bee colonies during winter 2015/16 from the COLOSS survey. Journal of Apicultural Research 55(5), pp. 375-378 (2016). [37] ZEE, R. VAN DER, PISA, L., ANDONOV, S., BRODSCHNEIDER, R., CHARRIÈRE, J.-D., CHLEBO, R., COFFEY, M.F., CRAILSHEIM, K., DAHLE, B., GAJDA, A., GRAY, A., DRAZIC, M.M., HIGES, M., KAUKO, L., KENCE, A., KENCE, M., KEZIC, N., KIPRIJANOVSKA, H., KRALJ, J., KRISTIANSEN, P., HERNANDEZ, R.M., MUTINELLI, F., NGUYEN, B.K., OTTEN, C., ÖZKIRIM, A., PERNAL, S.F., PETERSON, M., RAMSAY, G., SANTRAC, V., SOROKER, V., TOPOLSKA, G., UZUNOV, A., VEJSNÆS, F., WEI, S., WILKINS, S. Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008–9 and 2009– 10. Journal of Apicultural Research 51(1), pp. 100-114, 2012. [38] ZEE, R. VAN DER, BRODSCHNEIDER, R., BRUSBARDIS, V., CHARRIÈRE, J.-D., CHLEBO, R., COFFEY, M.F., DAHLE, B., DRAZIC, M.M., KAUKO, L., KRETAVICIUS, J., KRISTIANSEN, P., MUTINELLI, F., OTTEN, C., PETERSON, M., RAUDMETS, A., SANTRAC, V., SEPPÄLÄ, A., SOROKER, V., TOPOLSKA, G., VEJSNÆS, F., GRAY, A. Results of international standardised beekeeper surveys of colony losses for winter 2012–2013: analysis of winter loss rates and mixed effects modelling of risk factors for winter loss. Journal of Apicultural Research 53(1), 19-34, 2014. [39] SEELEY, T. D., TARPY, D. R., GRIFFIN, S. R., CARCIONE, A., DELANEY, D. A. A survivor population of wild colonies of European honeybees in the northeastern United States: investigating its genetic structure. Apidologie 46(5), pp. 654-666, 2015. [40] GOODWIN, R. M., HOUTEN, A. T., PERRY, J. H. Incidence of American foulbrood infections in feral honey bee colonies in New Zealand. New Zealand Journal of Zoology 21(3), pp. 285-287, 1994. [41] BAILEY, L. The Effect of the Number of Honey Bee Colonies on their Honey Yields and Diseases. Ilford: Central Association of Bee-Keepers, 1984, 16 p. [42] DUNHAM, W. E., KING, P. E. Treating Colonies Affected with American Foulbrood with a Bacteriological Verificaton. Journal of Economic Entomology 27(3), pp. 601-607, 1934. [43] MUNAWAR, M. S., RAJA, S., WAGHCHOURE, E. S., BARKAT, M. Controlling American Foulbrood in honeybees by shook swarm method. Pakistan Journal of Agricultural Research 23(1-2), pp. 3-58, 2010. [44] MCLAIN, N. W. Report on experiments in apiculture. Report of the Commissioner of Agriculture for 1886. Washington: Government Printing Office, 1887, pp. 583-591. [45] SCHRÖTER, K. O nové léčbě plodmoru [About a new foulbrood cure]. Včela brněnská 22(9), pp. 137-138, 1888. [46] MĂRGHITAŞ, L., DEZMIREAN, D., CHIRILĂ, F., FIŢ, N., BOBIŞ, O. Antibacterial activity of different plant extracts and phenolic phytochemicals tested on Paenibacillus larvae bacteria. Scientific Papers Animal Science and Biotechnologies 44, pp. 94-99, 2011. [47] ANON, J. R. Domácí zprávy včelařsé: z okolí Prahy [Regional beekeeping news: Prague]. Český včelař 11(1), pp. 13-14, 1878. [48] ŠPAČEK, F. Kterak léčím hniloplod [My foulbrood treatment method]. Český včelař 9(7), pp. 92-93, 1875. [49] MACHOVÁ, M (1993) Resistance of Bacillus larvae in beeswax. Apidologie 24(1), pp. 25-31, 1993. [50] CHESHIRE, F. E. Queen and eggs containing Bacillus alvei— foul brood? British Bee Journal 12(152), pp. 276-277, 1884. [51] TADMAN, J. Medical herbs for bees – an experiment. The Australasian Beekeeper 115(5), pp. 450-451, 2014. 54 LOVEČEK, J. (ed.) Řehoř Mendl včelařem [Gregor Mendel as a Beekeeper]. Olomouc: Kroužek lidových včelařských výzkumníků v Olomouci, 1964, 23 p. 55 SCHÖNFELD, A. Nemoci a nákazy včel [Honey Bee Diseases]. Kladno: Svaz zemských ústředí včelařských spolků v ČSR, 1938, p. 56. 56 ADAMEC, F. Zákon o nákazách včelího plodu [Bee Brood Disease Act]. Brno: Zemský ústřední spolek včelařský v Brně, 1914, 30 p. 52 MANNING, R. Fatty acids in pollen: a review of their importance for honey bees. Bee World, 82(2), pp. 60-75, 2001 53 TIHELKA, E. The immunological dependence of plant-feeding animals on their host’s medical properties may explain part of honey bee colony losses. Arthropod-Plant Interactions 12(1), pp. 57-64, 2018.
