Open access peer-reviewed chapter

Biological Control of Honey Bee Diseases and Pests

Written By

Mehtap Usta

Submitted: 31 July 2023 Reviewed: 29 September 2023 Published: 27 November 2023

DOI: 10.5772/intechopen.1003750

From the Edited Volume

Melittology - New Advances

Muhammad Asif Aziz

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Abstract

Beekeeping makes significant contributions to both the agricultural economy and crop production through pollination. Protecting the health of honey bees is of critical importance. It is evaluated that in an environment without bees, crop production may decrease by 47%. Many factors in the beekeeping sector negatively affect honey production. Among these reasons, microorganism-induced diseases as well as organism-induced diseases and hazards are at the forefront. Various strategies are used to protect the health of honey bees. However, pests and diseases are still not prevented. The most important of these are chemicals due to their widespread use. These products jeopardize both bee health and bee product quality. Methods using biological materials, which are more environmentally friendly than chemical control, should be preferred. Among these methods, biological control method stands out. As a result, the use of biological products as an alternative is critical for both the health of the organisms and the elimination of residues. The use of microorganisms and their products as biological control agents in the protection of bee health will be an important step in this regard.

Keywords

  • biological control
  • honey bee
  • honey bee diseases
  • honey bee health
  • microbiology

1. Introduction

Honey bee growth stages can provide an ideal setting for a variety of disease causes and pests. For this reason, many pathogens and pests can cause disease in honey bees [1]. However, due to rapid global movement, commerce of bees, bee products, and beekeeping supplies between continents and nations, bee illnesses quickly spread to all countries [2]. Similarly, the rapid spread of diseases and pests within the country is an important factor in migratory beekeeping [3]. One of the most significant challenges delaying the growth of beekeeping and restricting production efficiency in Turkey is honey bee illnesses and pests [4]. Bee illnesses generate major losses in Turkish beekeeping, and it is impossible to establish if medications are used on purpose. Furthermore, the environmental damage caused by the usage of chemical pesticides is enormous. As a result, new ecologically friendly solutions for bee illnesses and pests should be employed and developed [5]. Bee illnesses are classed as adult or brood diseases based on the source of the disease (bacterial, fungal, viral, parasitic, or protozoan) or the host where the disease occurs (adult or larva).

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2. Honey bee diseases

2.1 Bacterial diseases

American foulbrood is a deadly and widespread brood disease in honey bee larvae that causes them to die and stink. The disease is caused by a spore-forming bacteria called Paenibacillus larvae subsp. larvae. Dr. GF White was the first to identify it in 1906 [6]. Paenibacillus larvae subsp. larvae is a gram-positive bacteria that causes no illness in adult bees since its spores are harmful to the larvae. Bacterial spores delivered to larvae through food cause illness [7]. It is easily disseminated and can cause considerable losses in bees because of bacterial transmission. The infected honeycomb sample delivered from Pınarhisar area of Kırklareli in 1947 was the first official record and definite diagnosis of the illness in Turkey. A detailed investigation done in Turkey in 1991 discovered that this condition is seen in nearly every location [1]. The safest and most successful way to tackle this illness, which must be notified in Turkey, is to fully burn the sick colonies [3]. Aside from that, no biological control agent has been produced. However, research into this condition continues [8, 9, 10].

European foulbrood is another foulbrood disease that occurs across the world and also in Turkey except in New Zealand. This name was given because the first studies on the disease were carried out in Europe [11]. The causative agent of the disease is a gram (+) bacterium called Melissococcus pluton, which does not form spores [12, 13]. It is accompanied by certain secondary microorganisms. Paenibacillus alvei, Bacillus laterosporus, Achromobacter euridice, Enterococcus faecalis, and Enterococcus faecium are the strains [7, 13]. The harmful bacteria enter the digestive tract of bee larvae via the food delivered by the feeder bees. After the pup enters the pupal stage, bacteria that settle in the larva’s digestive tract mature in the gut, and the disease agent is discharged into the honeycomb with excrement. While the worker bees clear these leftovers from the comb cells, they spread the sickness to the healthy larvae. This illness has no effect on adult bees that are carriers [14, 15]. The first line of defense against the illness is to keep the hives healthy. Because the illness is most damaging in weak hives [16]. Because the appearance of European foulbrood is directly related to colony stress, behaviors that may cause stress in the colonies should be avoided [11]. In the battle against this disease, the tactic of destruction is also applied. A product for use as a biological control approach has yet to be created.

Septicemia is a disease of adult honey bees caused by the bacterium Pseudomonas aeruginosa (=Pseudomonas apiseptica). Pseudomonas apiseptica is a gram (−) and non-spore forming bacterium [17]. In nature, this bacteria may be found in damp soils, plants, stagnant water, and marshes. Pseudomonas apiseptica causes disease by entering the bee’s respiratory (tracheal) system and then spreading to the circulatory fluid in numerous ways. The disease is seen in hives with no air and high humidity [1, 14]. There are no known bee breeds or lines that are resistant to septicemia. There is currently no therapeutic approach for the condition. The illness is avoided by locating the apiary in a dry, clean, sunny location, providing the essential feedings, and reducing stressors for the bees [15].

2.2 Viral diseases

There are about 20 viruses that cause disease in adult bees. Some of these viruses are more dangerous than others, such as sacbrood virus, wingless bee virus (DWV), and chronic and acute bee paralysis virus (CBPV and ABPV) [18]. Some of these viruses cause harm because they are transmitted by mites. In the signs of viral disease, it can be shown that the bodies of the bees are hairless, shiny and oily. Furthermore, its legs and wings twitch regularly. Because the liquids in the honey stomach cannot be discharged, the honey stomach’s abdomen swells. They are unable to fly since their wings have been shattered [4, 7, 19]. Precautions for viral diseases are often regarded as physical precautions. Precautions include maintaining the hives in wet areas, positioning supports 30–40 cm above the ground, and replacing the queen bee [20]. In Turkey, viral investigations are largely diagnostic; no biological preparation that may be used to treat illnesses has been created [21, 22, 23, 24].

2.3 Fungal diseases

Chalkbrood disease is a puppy illness caused by the fungus Ascosphaera apis [25]. It was discovered in Turkey in 1988. According to 1989 study, the illness was found in all regions of Turkey, and according to research performed in the Southern Marmara Region, the sickness was found in 25% of the hives [26, 27, 28].

Aspergillus flavus is the most common cause of stone disease. The causative agents are sometimes Aspergillus fumigatus or other Aspergillus species. The color of Aspergillus flavus is yellow green, while Aspergillus fumigatus is gray green. These fungi are found in both soil and plants. It infects both young and mature bees. This fungus also infects other insects, animals, birds, and people [1, 29, 30]. By transporting sick combs to healthy colonies and feeding the bees tainted honey, fungal infections can be transferred to other bees. Fungal illnesses can emerge as a result of factors like as inadequate hive ventilation, excessive moisture content, and loss of bees’ natural gut flora owing to antibiotic usage [17]. Because human ingestion of honey from infected hives causes carcinogenic consequences, these honeys and combs must be destroyed [4]. The best way to prevent fungal illnesses is to destroy sick bees, honeycombs, completely clean the hives, and replace the queen bee.

2.4 Protozoan diseases

Nosema disease is one of the adult bee diseases caused by the protozoan Nosema apis [17]. Zander originally identified Nosema apis spores in Germany in 1909. Except for Central Africa, it has spread practically everywhere [14]. The first report of Nosema apis infection in Turkey occurred in 1952, and the disease was first diagnosed in 1986 [29]. Nosema is a prevalent ailment in Turkey, particularly in the Marmara and Black Sea regions, and it should be addressed. The primary signs of the condition include wing separation, abdominal swelling, loss of sting reflexes, inability to fly, and crawling on the ground [31]. In the therapy, bees are given medications containing Fumagillin in addition to syrup. Preventive actions should be implemented to keep the illness under control [32].

A disease identical to Nosema was discovered in the eastern honey bee Apis cerana in 1996, giving rise to the term Nosema ceranae. Little is known about the impact of this disease and its progression in Asia today. Until recently, it was considered that this chemical was exclusively found in the eastern honey bee, Apis cerana. However, for the first time, Chinese researchers reported finding Nosema ceranae in the western honey bee Apis mellifera in Taiwan in 2005. Nosema ceranae was discovered in the western honey bee Apis mellifera in Spain. While Nosema losses in Spain were 10% in 2000, they quickly grew to 20%, 30%, and eventually 88% in 2004. Nosema ceranae was also discovered to be the cause of large-scale bee losses in Spain during the summer of 2005. Furthermore, incidents in the apiaries, such as very severe Varroa infestation and bees fleeing their hives totally, have been documented [33, 34].

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3. Honey bee pests

Trache mite (Acarapis woodi) is an internal parasitic mite that lives in worker bees’ respiratory tracts. It is sometimes found in queen bees and drones. Rennie initially discovered Acarapis woodi in England in 1921. The mite first discovered in England and Scotland moved to Europe, Australia, New Zealand, Asia, America, and South Africa. In Turkey, there is no information or research on the occurrence of tracheal mites [35]. Trache mite-infected bees exhibit symptoms similar to Nosema, chemical poisoning, and other diseases that induce paralysis in bees. As a result, the final diagnosis should be made after the infected bees have been checked in the laboratory [20]. Fumigant medications with the active components bromopropylate, menthol, and formic acid are used to treat the condition.

The bee mite (Varroa destructor) is a highly hazardous external parasite that feeds on the larvae, pupae, and adults of the honey bee (Apis mellifera L.), multiplying fast and causing mass bee mortality. Apis cerana, the Indian and Far Eastern bee, is the primary host of Varroa. Apis cerana has developed a natural defensive mechanism against Varroa as a result of living with the parasite for many years, and no pesticides are required to control the parasite [36]. It was discovered that Varroa was present in 35% of the hives in the Southern Marmara Region and 41% of the hives in Turkey [29, 30]. The optimal temperature for Varroa development is 34°C. The formation and propagation of Varroa; genetic variables, the appropriateness of colony circumstances, the amount of brood area, and the colony’s Varroa infection rate. The sex and race of the larva on which it develops are also important in Varroa reproduction [37]. Because synthetic chemicals can harm human health by leaving residues in honey and beeswax, and mites develop resistance to these drugs, the use of natural licensed drugs such as formic acid, lactic acid, and oxalic acid, as well as essential oils such as thymol, has recently begun in the control of Varroa. The most extensively utilized biological control strategy is to feed the hive honeycombs containing drone cells. Because Varroa favors male brood eyes, it places its eggs in them. These frames are removed from the hive when the eyes have closed, lowering the Varroa population [37].

Honeycomb moths have two species, one giant Galleria mellonella and one tiny Achroia grisella, and they frequently do severe damage in weak colonies. The giant honeycomb moth is the more dangerous of the two. The adult honeycomb moth, which is only dangerous during the larval stage of its life, lives in the bush [3]. In the world and also in Turkey, various chemical substances (paradichlorobenzene, ethylene dibromide, sulfur dioxide, acetic acid, calcium cyanide, methylbromide, etc.), physical applications (heating, cooling), and biological applications (Bacillus thuringiensis bacteria) are used in pest control studies [26]. The addition of the bacterium Bacillus thuringiensis, which is applied as a biological control, to the basic honeycombs is applied in different countries and this application is not yet done in Turkey.

Bee diseases and pests are one of the most serious issues impeding the growth of beekeeping. As a result, beekeepers must be knowledgeable with the signs and features of the most prevalent parasites and illnesses in bees, as well as the ways for battling them. Unconscious and incorrect procedures will result in economic losses as well as the spread of the illness to healthy colonies. Care should be made to combat infections in a timely and effective way. It should not be forgotten that any chemically utilized substance will harm human health by leaving residues in honey and beeswax [1, 2, 3].

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4. Biological control

Biological control is the use of other living creatures to lower pest numbers rather than chemicals to reduce pest populations. It is the labor done to maintain pest populations beneath the economic harm threshold by employing organisms that live in farmed plants and control pests and weeds [27]. Harry Scott Smith coined the phrase “biological control” during a 1919 conference of the Pacific Slope Branch of the American Association of Economic Entomologists in Scottford, California. Biological control methods as we know them now first appeared in the 1870s. During this decade, Missouri State Entomologist C. V. Riley and Illinois State Entomologist W. LeBaron pioneered the use of parasitoids for crop pest management in the United States. Charles V. Riley sent the first international shipment of an insect as a biological control agent to France in 1873 to aid in the fight against the predatory mite “Tyroglyphus phylloxera,” the “vine phylloxera” (Daktulosphaira vitifoliae), which is damaging grapevines in France. Following the founding of the Department of Entomology in 1881, the United States Department of Agriculture (USDA) began research in the subject of classical biological management [28].

This section will discuss the use of microorganisms, in addition to the use of several biological control approaches.

Biological control bacteria infect insects through their digestive systems. Bacillus thuringiensis is a soil-borne bacteria that is employed against Lepidoptera (moths and butterflies), Coleoptera (insects), and Diptera (flies). Farmers get the bacteria in dry or packaged form, which is combined with water and sprayed onto sensitive plants such as fruit trees. Some Bacillus thuringiensis bacterial genes have been inserted into some GMOs, causing the plant to manufacture bacterium toxins, which are a form of protein. These repel insect pests, reducing the need for pesticides. If pests develop resistance to these crops, Bacillus thuringiensis will become obsolete in organic farming. The bacteria Paenibacillus popilliae, which causes white spot illness, has been discovered to be useful in the management of the Japanese beetle by destroying its larvae. It is a host-specific bacteria that causes no damage to vertebrates or other invertebrates [38, 39].

Baculoviridae viruses are species-specific and have been found to be beneficial in biological control. Lymantria dispar multicapsid nuclear polyhedrosis virus, for example, has been used to spray extensive woods in North America where Lymantria dispar dispar (gypsy moth) larvae cause significant defoliation. The viruses it consumes kill the moth, and its rotting stems shed viral particles on the leaves, infecting additional larvae [40, 41]. According to the literature, Baculoviruses used in biological control have not been used in terms of honey bee health [42].

In terms of bee health, fungus, bacteria and bacterial products are mostly used. The use of biological control agents; predators, parasitoids or pathogens to control pests can be considered as suitable options. Biocontrol agents are expected to manage the population of bee pests without causing harmful effects on honey bees and without contaminating valuable bee products.

Fungus applications have been used more especially in mite control. In this context, Metarhizium anisopliae and Beauveria bassiana are the fungal species used in the literature [43, 44, 45]. Applications with the fungus were tested both in the laboratory and in the field. While successful results were obtained in the laboratory (85–100%), the results in the field were not very favorable due to the negative effect of conidia and the effect of different external conditions. In the laboratory, the day of death varies between 5 and 10 days depending on the type of fungus [44, 46, 47].

In honey bee pests, wax moth (Galleria mellonella) is the biggest pest. There are not many studies using microorganisms or their products in the control of wax moth [48]. In one of the nine different strains used in studies with Bacillus thuringiensis in the literature, after 3 days 50–83.3% success was achieved. Studies on these bacteria and their products are still ongoing. In addition, other entomopathogenic microorganisms (fungi, nematodes, etc.) have been tried on the wax moth, but no results have been obtained as an effective agent [49, 50, 51, 52, 53].

As a result of the study with Steinernema riobrave and Heterorhabditis indica nematode species, 76–94% results were obtained in 19 weeks. Although the rate seems to be high, it is not very suitable for effective use because the application time is too long [54].

Although even 100% results are obtained in laboratory application, the same efficiency cannot be obtained in field application. However, for field application, both the use of nematodes and the use of fungi need to be further developed [42, 55, 56].

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5. Harmful effects of pesticides on bees

Many research have been conducted on the impact of pesticides on bees. Some chemicals have been found to create aberrations in bee communication. For example, it was discovered that when a deadly amount of parathion was administered to bees, the bees made errors in determining the direction and distance to the location of the nutrients [57]. Gels et al. investigated the effects of lawn pesticides on the bumblebee Bombus impatiens Cresson. The study discovered that after applying Imidacloprid in the form of granules and sprays, it is innocuous to bees in the event of irrigation, but has a detrimental effect on colony viability in the absence of irrigation [58]. Many research have identified the harmful effects of neonicotinoid group medications on honey bees, although the effect of low dosages of these chemicals on bee behavior is not entirely known, according to El Hassani et al. [59]. Under controlled laboratory circumstances, researchers administered acetamiprid and thiamethoxam orally and topically to bees and discovered that acetamiprid was more effective on bee movements than thiamethoxam, although this impact was not different from the control group [59]. According to Johnson et al. [60], pesticides reduce honey bee products, particularly wax production. Researchers also discovered that a combination of chemicals, rather than a single pesticide, had an impact on honeybee health [60]. Doğaroğlu claimed that Turkey holds an important place in the world of beekeeping due to its diverse ecological circumstances and honey bee races and ecotypes, and that our local bee breeds should be safeguarded [61]. The effects of thiametoxam, a popular pesticide in Turkey, on wasps (Vespa sp.) were studied. According to the findings of the study, the prescribed amount and diluted concentrations of the pesticide diminish the life span of wasps and kill bees [61].

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6. Biological control for harmful insects and diseases

Bacteria, fungi, viruses, protozoa, and nematodes are examples of entomopathogens utilized in biological insect control. Protozoa and nematodes are investigated in independent categories with their own names in certain publications. However, only a small number of them are utilized in pest control [62]. Entomopathogens are naturally occurring pathogens that attack, infect, and occasionally kill insects. Many entomopathogens are mass-produced and sold as “biological insecticides.” Bacillus thuringiensis is one of the most well-known, and it has been employed successfully against a wide range of insect species. Entomopathogens are often administered by combining them with common spraying instruments or irrigation water. Because these commercially generated entomopathogens are usually species-specific, they may be utilized safely in biological management. Unfortunately, these preparations account for just around 2–5% of the global pharmaceutical industry [63]. Studies on this topic are ongoing, and it has been discovered that numerous entomopathogenic species provide promising results in biological control. On the other hand, it should be attempted to boost their efficiency by developing ideal microhabitats for naturally occurring entomopathogens.

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7. Conclusion

Pollinators, especially honey bees, are in many respects almost keystone species for the ecosystem, but pesticides, whose use has increased significantly in recent years, have become a threat to honey bees and other pollinators. The toxicity of pesticides on honey bees has been scientifically proven by laboratory research. Under natural conditions, honey bees are exposed to the synergistic effect of multiple pesticides rather than a single pesticide as in laboratory studies. As a result, although it is not possible to compare the findings obtained under laboratory conditions with those obtained under natural conditions, it is sufficient to grasp the current situation. Predators, parasitoids and/or microbial biopesticides have the potential to be used against honey bee pests.

In general, these biocontrol agents are better applied within well-planned integrated pest management programmes to control pests than used alone.

The development of more specific and effective biocontrol agents is particularly will be even more needed in situations such as climate change, which can greatly affect honey bees.

In addition, the microorganisms and their products to be used for cost-effective honey bee pest control are of constant importance. Furthermore, the correct application methods of microbial products need to be further developed to ensure the sustainable release and thus long-term use of these microorganisms.

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Conflict of interest

The authors declare no conflict of interest.

References

  1. 1. Tutkun E, İnci A. Bal arısı Zararlıları, Hastalıkları ve Tedavi Yöntemleri (Teşhisten Tedaviye). Demircioğlu Matbaacılık; 1992. pp. 1-154
  2. 2. Öztürk Aİ. Balarısı hastalıkları. Muğla’da Tarım. 2001;1(5):57-59
  3. 3. Gülpınar V. Bal arısı hastalık ve zararlıları. Teknik Arıcılık. 2005;87:2-7
  4. 4. Doğaroğlu M. Modern Arıcılık Teknikleri, Trakya Üniversitesi Ziraat Fakültesi, Tekirdağ. 1999;s:241-279
  5. 5. Aydın L, Çakmak İ, Güleğen E, Korkut M. Güney Marmara Bölgesi arı hastalıkları ve zararlıları anket sonuçları. Uludağ Arıcılık Dergisi. 2003;3(1):37-40
  6. 6. Hansen H, Brodsgaard CJ. American foulbrood: A review of its biology, diagnosis and control. Bee World. 1999;80(1):5-23
  7. 7. Zeybek H. Arı Hastalıkları ve Zararlıları. T.K.B Hayvan Hastalıkları Arastırma Müdürlügü. Etlik, Ankar; 1991;96 s.;S:36-53
  8. 8. Özkırım A, Keskin N, Kürkçüoğlu M, Başer KHC. Evaluation of some essential oils as alternative antibiotics against American foulbrood agent Paenibacillus larvae on honey bees Apis mellifera L. Journal of Essential Oil Research. 2012;24(5):465-470
  9. 9. Karaoğlu ŞA, Bıyık S, Nisbet C, Akpınar R, Bozdeveci A, Suyabatmaz Ş, et al. Use of Dicranum polysetum extract against Paenibacillus larvae causing American Foulbrood under in vivo and in vitro conditions. International Microbiology. 2023;1(1):1-15
  10. 10. Farghaly DS, Nafea E, Altammar K, Kadada HMED. Antimicrobial activity of some honey bee products treated in controlling the American foulbrood, Paenibacillus larva. Egyptian Journal of Chemistry. 2023;66(3):351-358
  11. 11. Öztürk Aİ. Balarılarında yavru çürüklüğü hastalıklarının kontrolü ve mücadelesi. TYUAP Ege- Marmara Dilimi 2000 Yılı Hayvancılık Bilgi Alışveriş Toplantısı Bildirileri; 25-27 Nisan 2000; Menemen-İzmir
  12. 12. Bailey L, Ball BV. Honey bee pathology. In: Chapter 10 The Treatment of Bee Diseases. London, UK: Academic Press; 1991. pp. 132-153
  13. 13. Russenova N, Parvanov P. European foulbrood disease—aetiology, diagnostics and control. Trakia Journal of Sciences. 2005;3(2):10-16
  14. 14. Genç F, Dodoloğlu A. Arıcılığın temel esasları. Atatürk Üniv. Ziraat Fak. Ders Yayınları No:166, s.338. Erzurum; 2002
  15. 15. Öder E. Türkiye’de yaygın bal arısı hastalıkları, parazitleri ve zararlıları. Teknik Tavukçuluk Dergisi. 1990;67:21-26
  16. 16. Sönmez R, Altan Ö. Teknik Arıcılık. Ege Üniversitesi Ziraat Fakültesi Yay. No:499, E.Ü. Basımevi. Sayfa 181-204. Bornova/İzmir; 1992
  17. 17. Shimanuki H, Knox DA. Diagnosis of Honey Bee Diseases. U.S. Department of Agriculture, Agriculture Handbook 2000: No. AH–690. 61 pp
  18. 18. Kevan PG, Hannan MA, Ostiguy N, Guzman E. A summary of the varroa-virus disease complex in honeybees. American Bee Journal. 2006;146:694-697
  19. 19. Genç F. Bal Arılarında Koloni Performansını Etkileyen Faktörler. Teknik Arıcılık. 1990;27:18-26
  20. 20. Öncüer C, Benlioğlu K. Balarısı Zararlıları, Hastalıkları ve Zehirlenmeleri. Adnan Menderes Üniversitesi Yayınları. Yayın no: 3. Aydın. 1998
  21. 21. Eroglu GB. Detection of honey bee viruses in Vespula germanica: Black queen cell virus and Kashmir bee virus. Biologia. 2023;78(9):3
  22. 22. Kalayci G, Cagirgan AA, Kaplan M, Pekmez K, Beyazit A, Ozkan B, et al. The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Üniversitesi Veteriner Fakültesi Dergisi. 2020;26(5):671-677
  23. 23. Çakmak İ, Çakmak SS. Beekeeping and recent colony losses in Turkey.Uludağ Arıcılık Dergisi. 2016;16(1):31-48
  24. 24. Utkan NG, Eroğlu GB. Molecular identification of microbial pathogens in honey bees from Amasya. Uludağ Arıcılık Dergisi. 2023;23(1):93-104
  25. 25. Betts AD. Fungus diseases of bees. Bee World. 1932;40:156
  26. 26. Kumova U, Korkmaz A. Depolanan peteklerin büyük mum güvesine (Galleria mellonella L.) karşı korunması üzerine bir araştırma. Teknik Arıcılık. 2002;77:19-23
  27. 27. Van Driesche R, Bellows TS Jr. Biological Control. Boston/Dordrecht/London: Springer Science & Business Media; Kluwer Academic Publishers; 2012. pp. 3-7
  28. 28. Heimpel G, Mills N. Biological control and invasion biology. In: Biological Control: Ecology and Applications. Cambridge: Cambridge University Press; 2017. pp. 21-45
  29. 29. Tutkun E. İlkbaharda en çok görülen bal arısı hastalık ve zararlıları. Teknik Arıcılık. 2000;67:6-8
  30. 30. Çakmak İ, Aydın L, Güleğen AE. Güney Marmara Bölgesinde balarısı zararlı ve hastalıkları. Uludağ Arıcılık Dergisi. 2003;3(2):33-35
  31. 31. Aydın L, Çakmak İ, Güleğen E, Wells H. Honeybee Nosema disease in the Republic of Turkey. Journal of Apicultural Research. 2005;44(4):196-197
  32. 32. Aydın L, Güleğen E, Çetinbaş H. Bursa yöresi bal arılarında Nosema apis (Zander, 1909)‘in yaygınlığı. Bültendif. 2001;17:6-8
  33. 33. Civan M. Nosema ceranae hastalığı. Uludağ Arıcılık Dergisi. 2006;6(3):91-92
  34. 34. Higes M, Martín R, Meana A. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology. 2006;92(2):93-95
  35. 35. Güleğen AE. Bal arılarında trake akarı (Acarapis woodi). Uludağ Arıcılık Dergisi. 2002;1(2):27-29
  36. 36. Kaftanoğlu O. Türkiye arıcılığının genel yapısı ve temel sorunları- II: Varroa jacobsoni ve kontrol yöntemleri. Uludağ Arıcılık Dergisi. 2002;2(2):4-6
  37. 37. Kumova U. In: Aydın L, Çakmak İ, Güneş N, editors. Varroa ile mücadele yöntemleri. II. Marmara Arıcılık Kongresi Bildiri Kitabı. Bursa: Uludağ Üniv. Basımevi; 2004. pp. 83-131
  38. 38. Valtierra-de-Luis D, Villanueva M, Berry C, Caballero P. Potential for Bacillus thuringiensis and other bacterial toxins as biological control agents to combat dipteran pests of medical and agronomic importance. Toxins. 2020;12(12):773
  39. 39. Sauka DH, Benintende GB. Bacillus thuringiensis: General aspects. An approach to its use in the biological control of lepidopteran insects behaving as agricultural pests. Revista Argentina de Microbiología. 2008;40(2):124-140
  40. 40. Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS. Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology. 2015;132:1-41
  41. 41. Grzywacz D. Basic and applied research: Baculovirus. In: Microbial Control of Insect and Mite Pests. Academic Press; 2017. pp. 27-46
  42. 42. Abou-Shaara HF, Staron M. Present and future perspectives of using biological control agents against pests of honey bees. Egyptian Journal of Biological Pest Control. 2019;29(1):1-7
  43. 43. García-Fernández P, Santiago-Álvarez C, Quesada-Moraga E. Pathogenicity and thermal biology of mitosporic fungi as potential microbial control agents of varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of honey bee, Apis mellifera (Hymenoptera: Apidae). Apidologie. 2008;39:662-673
  44. 44. Kanga LHB, James RR, Boucias DG. Hirsutella thompsonii and Metarhizium anisopliae as potential microbial control agents of varroa destructor, a honey bee parasite. Journal of Invertebrate Pathology. 2002;81:175-184
  45. 45. Shaw KE, Davidson G, Clark SJ, Ball BV, Pell JK, Chandler D, et al. Laboratory bioassays to assess the pathogenicity of mitosporic fungi to varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of the honeybee, Apis mellifera. Biological Control. 2002;24:266-276
  46. 46. Meikle WG, Mercadier G, Girod V, Derouane F, Jones WA. Evaluation of Beauveria bassiana (Balsamo) Vuillemin (Deuteromycota: Hyphomycetes) strains isolated from varroa mites in southern France. Journal of Apicultural Research. 2006;45:219-220
  47. 47. Meikle WG, Mercadier G, Holst N, Nansen C, Girod V. Duration and spread of an entomopathogenic fungus, Beauveria bassiana (Deuteromycota: Hyphomycetes), used to treat varroa mites (Acari: Varroidae) in honey bee (Hymenoptera: Apidae) hives. Journal of Economic Entomology. 2007;100:1-10
  48. 48. Burges HD. Control of wax moths: Physical, chemical and biological methods. Bee World. 1978;59:129-138
  49. 49. Abou-Shaara HF. Evaluation of non-chemical traps for management of wax moth populations within honey bee colonies. Journal of Agricultural and Urban Entomology. 2017;33:1-9
  50. 50. Bombelli P, Howe CJ, Bertocchini F. Polyethylene bio-degradation by caterpillars of the wax moth Galleria mellonella. Current Biology. 2017;27:R292-R293
  51. 51. Benzina F, Oulebsir-Mohandkaci H, Belaid M, Irnatene H, Mammeri S. Isolation of entomopathogenic bacteria from larvae of a lepidopteran specie; Galleria mellonella and study of their insecticidal effect. Agricultural Forestry. 2017;63:59-68
  52. 52. Kwadha CA, Ong’amo GO, Ndegwa PN, Raina SK, Fombong AT. The biology and control of the greater wax moth, Galleria mellonella. Insects. 2017;8:61
  53. 53. Serebrov VV, Gerber ON, Malyarchuk AA, Martemyanov VV, Alekseev AA, Glupov VV. Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. The Biological Bulletin. 2006;33:581
  54. 54. Ellis JD, Spiewok S, Delaplane KS, Buchholz S, Neumann P, Tedders WL. Susceptibility of Aethina tumida (Coleoptera: Nitidulidae) larvae and pupae to entomopathogenic nematodes. Journal of Economic Entomology. 2010;103:1-9
  55. 55. Shapiro-Ilan DI, Morales-Ramos JA, Rojas MG, Tedders WL. Effects of a novel entomopathogenic nematode-infected host formulation on cadaver integrity, nematode yield, and suppression of Diaprepes abbreviatus and Aethina tumida. Journal of Invertebrate Pathology. 2010;103:103-108
  56. 56. Cuthbertson AGS, Mathers JJ, Blackburn LF, Powell ME, Marris G, Pietravalle S, et al. Screening commercially available entomopathogenic biocontrol agents for the control of Aethina tumida (coleoptera: Nitidulidae) in the UK. Insects. 2012;3:719-726
  57. 57. Polat B, Özüiçli M, Cetin H, Aydın L. Pestisit Kullanımının Bal Arısı Sağlığına ve Ürünlerine Etkisi. Journal of Research in Veterinary Medicine. 2020;39(2):128-134
  58. 58. Gels JA, Held DW, Potter DA. Hazards of insecticides to the bumble bees Bombus impatiens (Hymenoptera: Apidae) foraging on flowering white clover in turf. Journal of Economic Entomology. 2002;95(4):722-728
  59. 59. El Hassani AK, Dacher M, Gary V, Lambin M, Gauthier M, Armengaud C. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Archives of Environmental Contamination and Toxicology. 2008;54:653-661
  60. 60. Johnson RM, Ellis MD, Mullin CA, Frazier M. Pesticides and honey bee toxicity–USA. Apidologie. 2010;41(3):312-331
  61. 61. Doğaroğlu T. Small hive beetle Aethina tumida (Coleoptera: Nitidulidae) and it’s importance for beekeeping. Hayvansal Üretim (Journal of Animal Production). 2015;56(1):80-82
  62. 62. Vega FE. The use of fungal entomopathogens as endophytes in biological control: A review. Mycologia. 2018;110(1):4-30
  63. 63. Ridgway RL, Inscoe MN. Mass-reared naturel enemies for pest control: Trends and challenges. In: Ridgway RL, Hoffmann MP, Inscoe MN, Glenister CS, editors. Mass-Reared Naturel Enemies: Application, Regulation, and Needs. Vol. 1. Lanham, Maryland: Thomas Say Publications in Entomology, Entomological Society of America; 1998. pp. 185-201

Written By

Mehtap Usta

Submitted: 31 July 2023 Reviewed: 29 September 2023 Published: 27 November 2023