The use of probiotics, essential oils and fatty acids in the control of American foulbrood and other bee diseases (Review)

Journal of Apicultural Research

Volume 55, Issue 5, 5 December 2016, Pages 386-395

[El uso de los probióticos, aceites esenciales y ácidos grasos en el control de la loque americana y otras enfermedades de la abeja]

Kuzyšinová, K.^a, 

Mudroňová, D.^b , 

Toporčák, J.^a, 

Molnár, L.^a, 

Javorský, P.^c

 

^a  Clinic for Birds and Exotic Animals, University of Veterinary Medicine and Pharmacy, Košice, Slovakia
^b  Department of Microbiology and Immunology, University of Veterinary Medicine and Pharmacy, Košice, Slovakia
^c  Institute of Animal Physiology, Slovak Academy of Sciences, Košice, Slovakia

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Abstract

American foulbrood is one of the most serious honey bee brood diseases. The treatment of this disease is banned in EU countries. Affected hives must instead be burned, which leads to considerable economic losses. The use of antibiotic therapy in countries which permit this therapy is disputable with regard to its low effectiveness, development of resistant bacterial strains, and residues in honey bee products. Because of the above mentioned, alternative methods of prevention or therapy of American foulbrood have been considered. They are based mostly on substances of natural origin that neither affect adversely the honey bee products nor put some load on the environment. Such substances include for example probiotics, prebiotics, fatty acids, plant essential oils, and other plant materials. These substances are commonly used in prevention or treatment of a whole range of diseases of farm and pet animals and have also recently been used in bee-keeping. © 2016 International Bee Research Association.

Author keywords

American foulbrood; essential oils; fatty acids; probiotics

ISSN: 00218839 CODEN: JACRASource Type: Journal Original language: English

DOI: 10.1080/00218839.2016.1252067Document Type: Review

Publisher: Taylor and Francis Ltd

Funding details

Funding number	Funding sponsor	Acronym
1/0358/16	Scientific Grant Agency	VEGA
1/0858/16	Scientific Grant Agency	VEGA

Funding text

The study was financially supported by the Slovak Scientific Agency VEGA [projects number 1/0858/16, 1/0358/16].

References (91)

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• 
  1

  Albo, G.N., Henning, C., Ringuelet, J., Reynaldi, F.J., De Giusti, M.R., Alippi, A.M.
  

  Evaluation of some essential oils for the control and prevention of American Foulbrood disease in honey bees
  (2003) Apidologie, 34 (5), pp. 417-427. Cited 28 times.
  

  • View at Publisher
• 
  2

  Alippi, A.M.
  Ensayos de Campo para la evaluar efectividad de algunos aceites esenciales [Field trials for evaluation of some essential oils efficiency]
  (2001) Vida Apicola, 108, pp. 41-46.
  

  •  
• 
  3

  Alippi, A.M., Aguilar, O.M.
  

  Unique DNA fingerprint patterns of Paenibacillus larvae subsp. larvae strains
  (1998) Journal of Apicultural Research, 37 (4), pp. 273-280. Cited 21 times.
  

  • View at Publisher
• 
  4

  Alippi, A.M., Albo, G.N., Leniz, D., Rivera, I., Zanelli, M.L., Roca, A.E.
  

  Comparative study of tylosin, erythromycin and oxytetracyline to control American foulbrood of honey bees
  (1999) Journal of Apicultural Research, 38 (3-4), pp. 149-158. Cited 31 times.
  

  • View at Publisher
• 
  5

  Alippi, A.M., Reynaldi, F.J.
  

  Inhibition of the growth of Paenibacillus larvae, the causal agent of American foulbrood of honeybees, by selected strains of aerobic spore-forming bacteria isolated from apiarian sources
  (2006) Journal of Invertebrate Pathology, 91 (3), pp. 141-146. Cited 39 times.
  doi: 10.1016/j.jip.2005.12.002
  

  • View at Publisher
• 
  6

  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
  (1996) Journal of Herbs, Spices and Medicinal Plants, 4 (2), pp. 9-16. Cited 40 times.
  doi: 10.1300/J044v04n02_03
  

  • View at Publisher
• 
  7

  Markowicz Bastos, D.H., Barth, O.M., Rocha, C.I., Da Silva Cunha, I.B., De Oliveira Carvalho, P., Silva Torres, E.A., Michelan, M.
  

  Fatty acid composition and palynological analysis of bee (Apis) pollen loads in the states of São Paulo and Minas Gerais, Brazil
  (2004) Journal of Apicultural Research, 43 (2), pp. 35-39. Cited 18 times.
  

  • View at Publisher
• 
  8

  Baudoux, D.
  Antiviral and antimicrobial properties of essential oils
  (2000) Positive Health, 55.
  http://www.positivehealth.com/article/aromatherapy/antiviral-and-antimicrobial-properties-of-essential-oils
  

  •  
• 
  9

  Bednář, M., Fraňková, V., Schindler, J., Souček, A., Vávra, J.
  (1996) Lékařská mikrobiologie, p. 558. Cited 17 times.
  Prague: Marvil
  

  •  
• 
  10

  Benatti, P., Peluso, G., Nicolai, R., Calvani, M.
  

  Polyunsaturated fatty acids: Biochemical, nutritional and epigenetic properties
  (2004) Journal of the American College of Nutrition, 23 (4), pp. 281-302. Cited 218 times.
  

  • View at Publisher
• 
  11

  Bomba, A., Nemcová, R., Mudroňová, D., Guba, P.
  

  The possibilities of potentiating the efficacy of probiotics
  (2002) Trends in Food Science and Technology, 13 (4), pp. 121-126. Cited 61 times.
  doi: 10.1016/S0924-2244(02)00129-2
  

  • View at Publisher
• 
  12

  Bomba, A., Strojný, L., Nemcová, R., Mudroňová, D.
  Probiotics for farm animals
  (2012) Lactic acid bacteria–Microbiological and functional aspects, pp. 633-670. Cited 2 times.
  Lahtinen S., Ouwehand A., Salminen S., von Wrigth A., (eds), Boca Raton: CRC press, Taylor & Francis Group
  

  •  
• 
  13

  Boudegga, H., Boughalleb, N., Barbouche, N., Hamouda, M.H.B., Mahjoub, M.E.
  

  In vitro inhibitory actions of some essential oils on Ascosphaera apis, a fungus responsible for honey bee chalkbrood
  (2010) Journal of Apicultural Research, 49 (3), pp. 236-242. Cited 4 times.
  http://www.ibra.org.uk/downloads/20100623-1/download
  doi: 10.3896/IBRA.1.49.3.02
  

  • View at Publisher
• 
  14

  Calder, P.C.
  

  Polyunsaturated fatty acids, inflammation, and immunity
  (2001) Lipids, 36 (9), pp. 1007-1024. Cited 453 times.
  

  • View at Publisher
• 
  15

  Canganella, F., Balsamo, R.
  Isolation and selection of probiotic microorganisms with antagonistic activities against Paenibacillus larvae and Paenibacillus alvei
  (2008) Proceedings of International Probiotic Conference, Probiotics for the 3rd Millenium, p. 28.
  High Tatras, Slovakia:
  

  •  
• 
  16

  Carson, C.F., Mee, B.J., Riley, T.V.
  

  Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy
  (2002) Antimicrobial Agents and Chemotherapy, 46 (6), pp. 1914-1920. Cited 388 times.
  doi: 10.1128/AAC.46.6.1914-1920.2002
  

  • View at Publisher
• 
  17

  Chaibi, A., Ababouch, L.H., Belasri, K., Boucetta, S., Busta, F.F.
  

  Inhibition of germination and vegetative growth of Bacillus cereus T and Clostridium botulinum 62A spores by essential oils
  (1997) Food Microbiology, 14 (2), pp. 161-174. Cited 71 times.
  doi: 10.1006/fmic.1996.0075
  

  • View at Publisher
• 
  18

  Chesson, A.
  Probiotics and intestinal mediators
  (1993) Principles of pig science, pp. 197-214.
  Cole M., Wisemm J., Varley M.A., (eds), Loughborough: Nottingham University Press
  

  •  
• 
  19

  Čokášová, D., Siegfried, L., Strojný, L., Bomba, A.
  Probiotiká [Probiotics]
  (2009) Slovenský Veterinársky Časopis, pp. 156-157.
  

  •  
• 
  20

  Delcenserie, V., Martel, D., Lamoureux, M., Amiot, J., Boutin, Y., Roy, D.
  

  Immunomodulatory effects of probiotics in the intestinal tract
  (2008) Current Issues in Molecular Biology, 10 (1), pp. 37-54. Cited 177 times.
  http://www.horizonpress.com/cimb/v/v10/05.pdf
  

  • View at Publisher
• 
  21

  Dilika, F., Bremner, P.D., Meyer, J.J.M.
  

  Antibacterial activity of linoleic and oleic acids isolated from Helichrysum pedunculatum: A plant used during circumcision rites
  (2000) Fitoterapia, 71 (4), pp. 450-452. Cited 73 times.
  doi: 10.1016/S0367-326X(00)00150-7
  

  • View at Publisher
• 
  22

  Dorman, H.J.D., Deans, S.G.
  

  Antimicrobial agents from plants: Antibacterial activity of plant volatile oils
  (2000) Journal of Applied Microbiology, 88 (2), pp. 308-316. Cited 1749 times.
  doi: 10.1046/j.1365-2672.2000.00969.x
  

  • View at Publisher
• 
  23

  Drobníková, V.
  (1983) Tlmení moru včelího plodu, p. 29.
  Prague: Ústav vědeckotechnických informací pro zemědelství
  

  •  
• 
  24

  Evans, J.D., Lopez, D.L.
  

  Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae)
  (2004) Journal of Economic Entomology, 97 (3), pp. 752-756. Cited 66 times.
  

  • View at Publisher
• 
  25

  (2002) Guidelines for the evaluation of probiotics in food
  London, Ontario:
  

  •  
• 
  26

  Feldlaufer, M.F., Knox, D.A., Lusby, W.R., Shimanuki, H.
  Antimicrobial activity of fatty acids against Bacillus larvae, the causative agent of American foulbrood disease
  (1993) Apidologie, 24, pp. 90-99.
  

  •  
• 
  27

  Feldlaufer, M.F., Pettis, J.S., Kochansky, J.P., Stiles, G.
  

  Lincomycin hydrochloride for the control of American foulbrood disease of honey bees
  (2001) Apidologie, 32 (6), pp. 547-554. Cited 17 times.
  

  • View at Publisher
• 
  28

  Forsgren, E., Olofsson, T.C., Vásquez, A., Fries, I.
  

  Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae
  (2010) Apidologie, 41 (1), pp. 99-108. Cited 92 times.
  doi: 10.1051/apido/2009065
  

  • View at Publisher
• 
  29

  Fuller, R.
  

  Probiotics in man and animals.
  (1989) Journal of Applied Bacteriology, 66 (5), pp. 365-378. Cited 2434 times.
  

  • View at Publisher
• 
  30

  Fuller, R.
  The effect of probiotics on the gut microbiology of farm animals
  (1992) The lactic acid bacteria, pp. 171-192.
  Wood B.J.B., (ed), London: Elsevier Appl. ScL
  

  •  
• 
  31

  Fuselli, S.R., Gende, L.B., Garcia de la Rosa, S.B., Eguaras, M.J., Fritz, R.
  Short communication. Inhibition of Paenibacillus larvae subsp. larvae by the essential oils of two wild plants and their emulsifying agents
  (2005) Spanish Journal of Agricultural Research, 3, pp. 220-224.
  

  •  
• 
  32

  Fuselli, S.R., De La Rosa, S.B.G., Gende, L.B., Eguaras, M.J., Fritz, R.
  

  Antimicrobial activity of some Argentinian wild plant essential oils against Paenibacillus larvae larvae, causal agent of American foulbrood (AFB)
  (2006) Journal of Apicultural Research, 45 (1), pp. 2-7. Cited 20 times.
  

  • View at Publisher
• 
  33

  Genersch, E.
  

  American Foulbrood in honeybees and its causative agent, Paenibacillus larvae
  (2010) Journal of Invertebrate Pathology, 103 (SUPPL. 1), pp. S10-S19. Cited 112 times.
  doi: 10.1016/j.jip.2009.06.015
  

  • View at Publisher
• 
  34

  Hornitzky, M.A.Z.
  (2001) Literature review of chalkbrood a fungal disease of honey bees, p. 17. Cited 10 times.
  Barton, ACT: Rural Industries Research and Development Corporation, Australia
  

  •  
• 
  35

  Hornitzky, M.A.Z.
  (2003) Fatty acids–An alternative control strategy for honey bee diseases, p. 23. Cited 4 times.
  Barton, ACT: Rural Industries Research and Development Corporation, Australia
  

  •  
• 
  36

  Isman, M.B.
  

  Plant essential oils for pest and disease management
  (2000) Crop Protection, 19 (8-10), pp. 603-608. Cited 1003 times.
  doi: 10.1016/S0261-2194(00)00079-X
  

  • View at Publisher
• 
  37

  Javed, H., Erum, S., Tabassum, S., Ameen, F.
  An overview on medicinal importance of Thymus vulgaris
  (2013) Journal of Asian Scientific Research, 3, pp. 974-982. Cited 5 times.
  

  •  
• 
  38

  Johnson, B.R., Synk, W., Jasper, W.C., Mussen, E.
  

  Effects of high fructose corn syrup and probiotics on growth rates of newly founded honey bee colonies
  (2014) Journal of Apicultural Research, 53 (1), pp. 165-170. Cited 2 times.
  http://www.ibra.org.uk/downloads/20140221_17/download
  doi: 10.3896/IBRA.1.53.1.18
  

  • View at Publisher
• 
  39

  Juhás, Š., Bukovská, A., Čikoš, Štefan, Czikková, S., Fabian, D., Koppel, J.
  

  Anti-inflammatory effects of Rosmarinus officinalis essential oil in mice
  (2009) Acta Veterinaria Brno, 78 (1), pp. 121-127. Cited 14 times.
  http://vfu-www.vfu.cz/acta-vet/archives/volume78/pdf/200978010121.pdf
  doi: 10.2754/avb200978010121
  

  • View at Publisher
• 
  40

  Jump, D.B.
  

  The biochemistry of n-3 polyunsaturated fatty acids
  (2002) Journal of Biological Chemistry, 277 (11), pp. 8755-8758. Cited 363 times.
  doi: 10.1074/jbc.R100062200
  

  • View at Publisher
• 
  41

  Kabara, J.J.
  

  Antimicrobial agents derived from fatty acids
  (1984) Journal of the American Oil Chemists' Society, 61 (2), pp. 397-403. Cited 45 times.
  doi: 10.1007/BF02678802
  

  • View at Publisher
• 
  42

  Kardono, L.B.S., Tsauri, S., Padmawinata, K., Pezzuto, J.M., Douglas Kinghorn, A.
  

  Cytotoxic constituents of the bark of Plumeria rubra collected in Indonesia
  (1990) Journal of Natural Products, 53 (6), pp. 1447-1455. Cited 67 times.
  

  • View at Publisher
• 
  43

  Kaštel', R., Revajová, V., Magic, D., Pistl, J., Levkut, M., Bindas, L'., Šajbidor, J., (...), Horváth, M.
  

  Effect of oil containing n-3 polyunsaturated fatty acids (PUFA) on the immune response and growth factors in piglets
  (1999) Acta Veterinaria Hungarica, 47 (3), pp. 325-334. Cited 9 times.
  

  • View at Publisher
• 
  44

  Kevan, S.D., Nasr, M.E., Kevan, P.G.
  Natural oils and other substances for mite control in honey bees
  (1999) Hivelights, 12, pp. 15-16.
  

  •  
• 
  45

  Kinsella, J.E., Lokesh, B., Stone, R.A.
  

  Dietary n-3 polyunsaturated fatty acids and amelioration of cardiovascular disease: Possible mechanisms
  (1990) American Journal of Clinical Nutrition, 52 (1), pp. 1-28. Cited 513 times.
  
• 
  46

  Klouček, P., Flesar, J., Kokoska, L., Nedorostová, L., Titera, D.
  Activity of essentials oils vapor phase against Paenibacillus larvae
  (2008) Planta Medica, 74, p. 1038.
  

  •  
• 
  47

  Komissar, A.
  Bitter wormwood for treating nosema
  (2008) Bee Talk, 4, p. 3.
  

  •  
• 
  48

  Kuzyšinová, K., Mudroňová, D., Toporčák, J., Nemcová, R., Molnár, L., Mad'ari, A., Vaníková, S., (...), Kožár, M.
  

  Testing of inhibition activity of essential oils against Paenibacillus larvae - The causative agent of American foulbrood
  (2014) Acta Veterinaria Brno, 83 (1), pp. 9-12. Cited 3 times.
  http://actavet.vfu.cz/pdf/201483010009.pdf
  doi: 10.2754/avb201483010009
  

  • View at Publisher
• 
  49

  Laird, K., Phillips, C.
  

  Vapour phase: A potential future use for essential oils as antimicrobials?
  (2012) Letters in Applied Microbiology, 54 (3), pp. 169-174. Cited 35 times.
  doi: 10.1111/j.1472-765X.2011.03190.x
  

  • View at Publisher
• 
  50

  Lambert, R.J.W., Skandamis, P.N., Coote, P.J., Nychas, G.-J.E.
  

  A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol
  (2001) Journal of Applied Microbiology, 91 (3), pp. 453-462. Cited 948 times.
  doi: 10.1046/j.1365-2672.2001.01428.x
  

  • View at Publisher
• 
  51

  Lilly, D.M., Stillwell, R.H.
  

  Probiotics: Growth-promoting factors produced by microorganisms
  (1965) Science, 147 (3659), pp. 747-748. Cited 406 times.
  

  • View at Publisher
• 
  52

  Máchová, M., Rada, V., Huk, J., Smékal, F.
  Development of probiotics for bees
  (1997) Apiacta, 22, pp. 99-111.
  

  •  
• 
  53

  Maistrello, L., Lodesani, M., Costa, C., Leonardi, F., Marani, G., Caldon, M., Mutinelli, F., (...), Granato, A.
  

  Screening of natural compounds for the control of nosema disease in honeybees (Apis mellifera)
  (2008) Apidologie, 39 (4), pp. 436-445. Cited 30 times.
  doi: 10.1051/apido:2008022
  

  • View at Publisher
• 
  54

  Manning, R.
  

  Fatty acids in pollen: A review of their importance for honey bees
  (2001) Bee World, 82 (2), pp. 60-75. Cited 36 times.
  

  • View at Publisher
• 
  55

  Marcus, A.J.
  

  The eicosanoids in biology and medicine
  (1984) Journal of Lipid Research, 25 (13), pp. 1511-1516. Cited 46 times.
  

  • View at Publisher
• 
  56

  Mathe, A.
  Essential oils as phytogenic feed additives (PFA)
  (1996) 27th International Symposium on Essential Oils: Essential oil symposium Proceeding, pp. 315-321.
  University of Veterinary Medicine, Vienna, Austria:
  

  •  
• 
  57

  Matsuzaki, T., Chin, J.
  

  Modulating immune responses with probiotic bacteria
  (2000) Immunology and Cell Biology, 78 (1), pp. 67-73. Cited 167 times.
  doi: 10.1046/j.1440-1711.2000.00887.x
  

  • View at Publisher
• 
  58

  Mezzoug, N., Elhadri, A., Dallouh, A., Amkiss, S., Skali, N.S., Abrini, J., Zhiri, A., (...), Idaomar, M.
  

  Investigation of the mutagenic and antimutagenic effects of Origanum compactum essential oil and some of its constituents
  (2007) Mutation Research - Genetic Toxicology and Environmental Mutagenesis, 629 (2), pp. 100-110. Cited 49 times.
  doi: 10.1016/j.mrgentox.2007.01.011
  

  • View at Publisher
• 
  59

  Miguel, M.G., Duarte, J., Figueiredo, A.C., Barroso, J.G., Pedro, L.G.
  

  Thymus carnosus Boiss.: Effect of harvesting period, collection site and type of plant material on essential oil composition
  (2005) Journal of Essential Oil Research, 17 (4), pp. 422-426. Cited 10 times.
  

  • View at Publisher
• 
  60

  Miyagi, T., Peng, C.Y.S., Chuang, R.Y., Mussen, E.C., Spivak, M.S., Doi, R.H.
  

  Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States
  (2000) Journal of Invertebrate Pathology, 75 (1), pp. 95-96. Cited 95 times.
  doi: 10.1006/jipa.1999.4888
  

  • View at Publisher
• 
  61

  Mudroňová, D., Toporčák, J., Nemcová, R., Gancarčíková, S., Hajdučková, V., Rumanovská, K.
  

  Lactobacillus sp. as a potential probiotic for the prevention of Paenibacillus larvae infection in honey bees
  (2011) Journal of Apicultural Research, 50 (4), pp. 323-324. Cited 2 times.
  www.ibra.org.uk/autologin
  doi: 10.3896/IBRA.1.50.4.11
  

  • View at Publisher
• 
  62

  Nedorostova, L., Kloucek, P., Kokoska, L., Stolcova, M., Pulkrabek, J.
  

  Antimicrobial properties of selected essential oils in vapour phase against foodborne bacteria
  (2009) Food Control, 20 (2), pp. 157-160. Cited 103 times.
  doi: 10.1016/j.foodcont.2008.03.007
  

  • View at Publisher
• 
  63

  Nemcová, R.
  Kritéria výberu laktobacilov pre probiotické účely [Criteria for the selection of lactobacilli for probiotic purposes]
  (1997) Veterinary Medicine–Czech, 42, pp. 19-27.
  

  •  
• 
  64

  Ouwehand, A.C., Kirjavainen, P.V., Shortt, C., Salminen, S.
  

  Probiotics: Mechanisms and established effects
  (1999) International Dairy Journal, 9 (1), pp. 43-52. Cited 232 times.
  doi: 10.1016/S0958-6946(99)00043-6
  

  • View at Publisher
• 
  65

  Parker, R.B.
  Probiotics, the other half of the antibiotic story
  (1974) Animal Nutrition and Health, 29, pp. 4-8.
  

  •  
• 
  66

  Paster, N., Menasherov, M., Ravid, U., Juven, B.
  

  Antifungal activity of oregano and thyme essential oils applied as fumigants against fungi attacking stored grain
  (1995) Journal of Food Protection, 58 (1), pp. 70-75. Cited 57 times.
  

  • View at Publisher
• 
  67

  Ptaszyńska, A.A., Borsuk, G., Zdybicka-Barabas, A., Cytryńska, M., Małek, W.
  

  Are commercial probiotics and prebiotics effective in the treatment and prevention of honeybee nosemosis C?
  (2016) Parasitology Research, 115 (1), pp. 397-406. Cited 4 times.
  link.springer.de/link/service/journals/00436/index.htm
  doi: 10.1007/s00436-015-4761-z
  

  • View at Publisher
• 
  68

  Rada, V., Havlík, J., Flesar, J.
  (2009) Biologicky aktivní látky ve výživě včel, p. 52.
  Výzkumný ústav živočíšne výroby; Prague: Czech Republic
  

  •  
• 
  69

  Rafiei, M., Rajaei, H.
  

  Structural and developmental studies on oil producing reproductive organs in lime (Citrus aurantifolia Swingle)
  (2007) Journal of Biological Sciences, 7 (6), pp. 848-853. Cited 3 times.
  

  • View at Publisher
• 
  70

  Ratledge, C., Wilkinson, S.G.
  An overview of microbial lipids
  (1988) Microbial Lipids, 1, pp. 3-22.
  

  •  
• 
  71

  Reiche, R., Martin, K., Mollmann, U., Hentschel, E.J.
  Beitrag zur klärung der resistenz der bienenlarven gegen den erreger der Amerikanischen faulbrut Paenibacillus (vorher Bacillus) larvae [Contribution to the clarification of the resistance of the bee larvae against the causative agent of the American Foulbrood Paenibacillus (previously Bacillus) larvae] (White 1906)
  (1996) Apidologie, 27, pp. 296-297.
  

  •  
• 
  72

  Rejnič, J., Haragsim, O., Rekoš, J.
  (1990) Včelárstvo, p. 249.
  Príroda: Bratislava
  

  •  
• 
  73

  Reynaldi, F.J., Albo, G.N., Alippi, A.M.
  

  Effectiveness of tilmicosin against Paenibacillus larvae, the causal agent of American Foulbrood disease of honeybees
  (2008) Veterinary Microbiology, 132 (1-2), pp. 119-128. Cited 10 times.
  doi: 10.1016/j.vetmic.2008.04.034
  

  • View at Publisher
• 
  74

  Reynaldi, F.J., De Giusti, M.R., Alippi, A.M.
  

  Inhibition of the growth of Ascosphaera apis by Bacillus and Paenibacillus strains isolated from honey
  (2004) Revista Argentina de Microbiologia, 36 (1), pp. 52-55. Cited 26 times.
  

  • View at Publisher
• 
  75

  Rickli, M., Guerin, P.M., Diehl, P.A.
  

  Palmitic acid released from honeybee worker larvae attracts the parasitic mite Varroa jacobsoni on a servosphere
  (1992) Naturwissenschaften, 79 (7), pp. 320-322. Cited 42 times.
  doi: 10.1007/BF01138711
  

  • View at Publisher
• 
  76

  Rinderer, T.E., Rothenbuhler, W.C., Gochnauer, T.A.
  

  The influence of pollen on the susceptibility of honey-bee larvae to Bacillus larvae
  (1974) Journal of Invertebrate Pathology, 23 (3), pp. 347-350. Cited 31 times.
  doi: 10.1016/0022-2011(74)90100-1
  

  • View at Publisher
• 
  77

  Rothenbuhler, W.C.
  

  Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood
  (1964) Animal Behaviour, 12 (4), pp. 578-583. Cited 162 times.
  

  • View at Publisher
• 
  78

  Rustan, A.C., Drevon, C.A.
  (2000) Fatty acids: Structures and properties. Encyclopedia of Life Sciences. Cited 3 times.
  London: Nature Publishing
  

  •  
• 
  79

  Sammataro, D., Finley, J., Leblanc, B., Wardell, G., Ahumada-Segura, F., Carroll, M.J.
  

  Feeding Essential oils and 2-heptanone in sugar syrup and liquid protein diets to honey bees (Apis mellifera L.) as potential varroa mite (Varroa destructor) controls
  (2009) Journal of Apicultural Research, 48 (4), pp. 256-262. Cited 3 times.
  doi: 10.3896/IBRA.1.48.4.05
  

  • View at Publisher
• 
  80

  Shimanuki, H., Knox, D.A., Feldlaufer, M.F.
  Honey bee disease interactions: The impact of chalkbrood on other honey bee brood diseases
  (1992) American Bee Journal, 132, pp. 735-736. Cited 6 times.
  

  •  

View all 91 references

  Mudroňová, D.; Department of Microbiology and Immunology, University of Veterinary Medicine and Pharmacy, Košice, Slovakia; email:dagmar.mudronova@uvlf.sk
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