American foulbrood – a dangerous bacterial honey bee disease
MICHAŁ SCHULZ
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie, ul. Akademicka 13, 20-950ALEKSANDRA ŁOŚ
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w LubliniePATRYCJA SKOWRONEK
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w LublinieADAM STANISZEWSKI
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w LublinieBARTŁOMIEJ IWAŃSKI
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w LublinieŁUKASZ WÓJCIK
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w LublinieANETA STRACHECKA
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w LublinieAbstrakt
Honeybees are exposed to many threats including a bacterial disease called American foulbrood (AFB). The AFB disease is caused by Paenibacillus larvae bacteria, which infects the brood at an early stage of development and leads to the death of the whole colony. Foulbrood bacteria are common in the environment, but neglected apiaries and non-sterilized beekeeping equipment are believed to be the main source of infection. This disease is rapidly spreading, and due to the prohibition on the use of antibiotics in the EU, there is no effective method of treatment. The only way to protect against the appearance of foulbrood in the apiary is prevention activity based on a good knowledge about the mechanisms of infection.
Słowa kluczowe:
zgnilec złośliwy, AFB, Paenibacillus larvae, bakterioza, obszar zapowietrzonyBibliografia
Albo G.N., Henning C., Ringuelet J., Reynaldi F.J., De Giusti M.R., Alippi A.M., 2003. Evaluation of some essential oils for the control and prevention of American Foulbrood disease in honey bees. Apidologie 34(5), 417–427, https://doi.org/10.1051/apido:2003040.
Al-Fattah M.A.A., El-Awady M., Gelan M.I., Barakat O.S., 2010. Microbiological and molecular diagnosis of American foulbrood in honeybee (Apis mellifera L.) colonies. Arab. J. Biotech. 13(1), 1–12.
Alippi A.M., 1995. Detection of Bacillus larvae spores in Argentinian honeys by using a semi-selective medium. Microbiología. Sem. 11, 343–350.
Alippi A.M., Reynaldi F.J., 2006. 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. J. Invertebr. Pathol. 91(3), 141–146, https://doi.org/ 10.1016/j.jip.2005. 12.002.
Alippi A.M., Ringuelet J.A., Cerimele E.L., Re M.S., Henning C.P., 1996. Antimicrobial activity of some essential oils against Paenibacillus larvae, the causal agent of American foulbrood disease. J. Herbs. Spices Med. Plants. 4(2), 9–16.
Antúnez K., Harriet J., Gende L., Maggi M., Eguaras M., Zunino P., 2008. Efficacy of natural propolis extract in the control of American Foulbrood. Vet. Microbiol. 131(3–4), 324–331, https://doi.org/10.1016/j.vetmic.2008.04.011.
Arredondo D., Castelli L., Porrini M.P., Garrido P.M., Eguaras M.J., Zunino P., Antúnez K., 2018. Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Benef. Microbes. 9(2), 279–290, https://doi. org/10. 3920/BM2017.0075.
Ash C., Priest F.G., Collins M.D., 1994. Paenibacillus gen. nov. Validation of the Publication of New Names and New Combinations Previously Effectively Published Outside the IJSB. Int. J. Syst. Bacteriol. 44, 852–853.
Bailey L., 1968. Honey bee pathology. Annu. Rev. Entomol. 13(1), 191–212.
Bíliková K., Wu G., Šimúth J., 2001. Isolation of a peptide fraction from honeybee royal jelly as a potential antifoulbrood factor. Apidologie 32(3), 275–283.
Brødsgaard C.J., Ritter W., Hansen H., 1998. Response of in vitro reared honey bee larvae to various doses of Paenibacillus larvae larvae spores. Apidologie 29(6), 569–578, https://doi.org/10.1051/apido:19980609.
Chantawannakul P., Dancer B.N., 2001. American foulbrood in honey bees. Bee World 82(4), 168–180.
Chorbiński P., 2004. Zwalczanie grzybicy otorbielakowej pszczoły miodnej. Życie Wet. 79(11), 613–615.
Crane E., 1990. Bees and beekeeping: science, practice and world resources. Heinemann Newnes, Oxford.
Cuthbertson A.G.S., Brown M.A., 2009. Issues affecting British honey bee biodiversity and the need for conservation of this important ecological component. Int. J. Environ. Sci. Technol. 6(4), 695–699, https://doi.org/10.1007/BF03326110.
De Rycke P.H., Joubert J.J., Hosseinian S.H., Jacobs F.J., 2002. The possible role of Varroa de-structor in the spreading of American foulbrood among apiaries. Exp. Appl. Acarol. 27(4), 313–318, https://doi.org/10.1023/A:1023392912999.
Djukic M., Brzuszkiewicz E., Fünfhaus A., Voss J., Gollnow K., Poppinga L., Daniel R., 2014. How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS One, 9(3), e90914, https://doi.org/10.1371/journal.pone.0090914.
Dsouza M., Taylor M.W., Turner S.J., Aislabie J., 2014. Genome-based comparative analyses of Antarctic and temperate species of Paenibacillus. PloS One, 9(10), e108009, https://doi.org/10.1371/journal.pone.0108009.
Engel P., Moran N.A., 2013. Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes 4(1), 60–65.
Evans J.D., Schwarz R.S., 2011. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol. 19(12), 614–620, https://doi.org/10.1016/j.tim.2011.09.003.
Flesar J., Havlik J., Kloucek P., Rada V., Titera D., Bednar M., Kokoska L., 2010. In vitro growth-inhibitory effect of plant-derived extracts and compounds against Paenibacillus larvae and their acute oral toxicity to adult honey bees. Vet. Microbiol. 145(1–2), 129–133, https://doi.org/10.1016/j.vetmic.2010.03.018.
Forsgren E., Locke B., Sircoulomb F., Schäfer M.O., 2018. Bacterial diseases in honeybees. Curr. Clin. Microbiol. Rep. 5(1), 18–25.
Forsgren E., Stevanovic J., Fries I., 2008. Variability in germination and in temperature and storage resistance among Paenibacillus larvae genotypes. Vet. Microbiol. 129(3–4), 342–349, https://doi.org/10.1016/j.vetmic.2007.12.001.
Fries I., Lindström A., Korpela S., 2006. Vertical transmission of American foulbrood (Paeni-bacillus larvae) in honey bees (Apis mellifera). Vet. Microbiol. 114, 269–274, https://doi.org/10.1016/j.vetmic.2005.11.068.
Fries I., Raina S., 2003. American foulbrood and African honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 96(6), 1641–1646, https://doi.org/10.1603/0022-0493-96.6.1641.
Fünfhaus A., Göbel J., Ebeling J., Knispel H., Garcia-Gonzalez E., Genersch E., 2018. Swarming motility and biofilm formation of Paenibacillus larvae, the etiological agent of American Foulbrood of honey bees (Apis mellifera). Sci. Rep. 8(1), 8840, https://doi.org/ 10.1038/s41598-018-27193-8.
Fuselli S.R., Rosa S.B.G. de la, Gende L.B., Eguaras M.J., Fritz R., 2006. Antimicrobial activity of some Argentinean wild plant essential oils against Paenibacillus larvae larvae, causal agent of American foulbrood (AFB). J. Apic. Res. 45(1), 2–7.
Gende L.B., Floris I., Fritz R., Eguaras M.J., 2008. Antimicrobial activity of cinnamon (Cin-namomum zeylanicum) essential oil and its main components against Paenibacillus larvae from Argentine. B. Insectol. 61(1), 1–4.
Genersch E., 2010. American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103, S10-S19, https://doi.org/10.1016/j.jip.2009.06.015.
Genersch E., Ashiralieva A., Fries I., 2005. Strain-and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honeybees. Appl. Environ. Microbiol. 71(11), 7551–7555, https://doi.org/10.1128/ AEM.71.11.7551-7555.2005.
Genersch E., Forsgren E., Pentikäinen J., Ashiralieva A., Rauch S., Kilwinski J., Fries I., 2006. Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int. J. Syst. Evol. Microbiol. 56, 501–511, https://doi.org/10.1099/ijs.0.63928-0.
Genersch E., Otten C., 2003. The use of repetitive element PCR fingerprinting (rep-PCR) for genetic subtyping of German field isolates of Paenibacillus larvae subsp. larvae. Apidologie 34(3), 195–206, https://doi.org/10.1051/apido:2003025.
Gilgert W., Vaughan M., 2011. The value of pollinators and pollinator habitat to rangelands: connections among pollinators, insects, plant communities, fish, and wildlife. Rangelands 33(3), 14–19.
Gliński Z., Kostro K., Luft-Deptula D., Zdanowska M., Zaremba E., 2006. Choroby pszczół. PWRiL, Warszawa, 130–137.
Gonzalez M.J., Marioli J.M., 2010. Antibacterial activity of water extracts and essential oils of various aromatic plants against Paenibacillus larvae, the causative agent of American Foulbrood. J. Invertebr. Pathol. 104(3), 209–213, https://doi.org/10.1016/j.jip.2010.04.005.
Gregorc A., Bowen I.D., 2000. Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline. Cell. Biol. Int. 24(5), 319–324, https://doi.org/10.1006/cbir.1999.0490.
Hadzimuratovic M., Nevjestic A., Rukavina L., Sabirovic M., 1986. Prevalence of bee and brood diseases in Bosnia and Hercegovina in the period 1980–1984. Vet. Glas. 40(7/8), 505–508.
Hansen H., Brødsgaard C.J., 1999. American foulbrood: a review of its biology, diagnosis and control. Bee World 80(1), 5–23, https://doi.org/10.1080/0005772X.1999.11099415.
Hayes Jr J., Underwood R.M., Pettis J., 2008. A survey of honey bee colony losses in the US, fall 2007 to spring 2008. PloS One 3(12), e4071, https://doi.org/10.1371/journal.pone.0004071.
Hornitzky M.A.Z., Clark S., 1991. Culture of Bacillus larvae from bulk honey samples for the detection of American foulbrood. J. Apic. Res. 30(1), 13–16, https://doi.org/10.1080 00218839.1991.11101228.
Hung, K.L.J., Kingston J.M., Albrecht M., Holway D.A., Kohn J.R., 2018. The worldwide im-portance of honey bees as pollinators in natural habitats. Proc. R. Soc. B 285(1870), 20172140, DOI: 10.1098/rspb.2017.2140.
https://www.cabi.org/isc/datasheet/109548#68454B2B-77E7-4AF4-8156-38F41C1C9EF5
Mahdi O.S., Fisher N.A., 2018. Sporulation and germination of Paenibacillus larvae cells. Curr. Protoc. Microbiol. 48(1), 9E–2.
Munawar M.S., Raja S., Waghchoure E.S., Barkat M., 2010. Controlling American foulbrood in honeybees by shook swarm method. Pakistan J. Agric. Res. 23(1–2), 53–58.
Murray K.D., Aronstein K.A., 2008. Transformation of the Gram-positive honey bee pathogen, Paenibacillus larvae, by electroporation. J. Microbiol. Methods, 75(2), 325–328, https://doi. org/10.1016/j.mimet.2008.07.007.
Näumann G., Mahrt E., Himmelreich A., Mohring A., Frerichs H., 2012. Traces of contamination-well preserved in honey: investigation of veterinary drugs and American foulbrood in honeys of global origin. J. Verbrauch. Lebensm. 7(1), 35–43, https://doi.org/10.1007/s00003-015-0995-z.
Owen R., 2017. Role of Human Action in the Spread of Honey Bee (Hymenoptera: Apidae) Path-ogens. J. Econ. Entomol. 110(3), 797–801, https://doi.org/10.1093/jee/tox075.
Peng C.Y.S., Mussen E., Fong A., Cheng P., Wong G., Montague M.A., 1996. Laboratory and Field Studies on the Effects of the Antibiotic Tylosin on Honey Bee Apis mellifera L. (Hy-menoptera: Apidae) Development and Prevention of American Foulbrood Disease. J. Invertebr. Pathol. 67(1), 65–71, https://doi.org/10.1006/jipa.1996.0010.
Schuch D.M.T., Tochetto L.G., Sattler A., 2003. Detection of Paenibacillus larvae subsp. larvae spores in Brazil. Pesq. Agropec. Bras. 38(3), 441–444, https://doi.org/10.1590/S0100- -204X2003000300015.
Semkiw P., 2017. Sektor pszczelarski w Polsce w 2017 roku. Instytut Ogrodnictwa, Zakład Pszczelnictwa w Puławach.
Skubida P., Semkiw P., 2011. Pszczelarstwo ekologiczne w Europie i na świecie. J. Res. Appl. Agricult. Eng. 56(4), 102–106.
Smith F.G., 1953. Beekeeping in the tropics. Bee World 34(12), 233–245.
Spivak M., Reuter G.S., 2001. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32(6), 555–565.
Teixeira É.W., Guimarães-Cestaro L., Alves M., Martins M.F., Luz C.F.P. da, Serrão J.E., 2017. Spores of Paenibacillus larvae, Ascosphaera apis, Nosema ceranae and Nosema apis in bee products supervised by the Brazilian Federal Inspection Service. Rev. Bras. Entomol., https://doi.org/10.1016/j.rbe.2018.04.001.
White G.F., 1907. The cause of American foulbrood (No. 94). US Government Printing Office.
Wilde J., 2013. Encyklopedia pszczelarska. PWRiL, Warszawa.
www.webofknowledge.com
Yoshiyama M., Kimura K., 2009. Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J. Invertebr. Pathol. 102(2), 91–96, https://doi.org/10.1016/j.jip.2009.07.005.
Al-Fattah M.A.A., El-Awady M., Gelan M.I., Barakat O.S., 2010. Microbiological and molecular diagnosis of American foulbrood in honeybee (Apis mellifera L.) colonies. Arab. J. Biotech. 13(1), 1–12.
Alippi A.M., 1995. Detection of Bacillus larvae spores in Argentinian honeys by using a semi-selective medium. Microbiología. Sem. 11, 343–350.
Alippi A.M., Reynaldi F.J., 2006. 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. J. Invertebr. Pathol. 91(3), 141–146, https://doi.org/ 10.1016/j.jip.2005. 12.002.
Alippi A.M., Ringuelet J.A., Cerimele E.L., Re M.S., Henning C.P., 1996. Antimicrobial activity of some essential oils against Paenibacillus larvae, the causal agent of American foulbrood disease. J. Herbs. Spices Med. Plants. 4(2), 9–16.
Antúnez K., Harriet J., Gende L., Maggi M., Eguaras M., Zunino P., 2008. Efficacy of natural propolis extract in the control of American Foulbrood. Vet. Microbiol. 131(3–4), 324–331, https://doi.org/10.1016/j.vetmic.2008.04.011.
Arredondo D., Castelli L., Porrini M.P., Garrido P.M., Eguaras M.J., Zunino P., Antúnez K., 2018. Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Benef. Microbes. 9(2), 279–290, https://doi. org/10. 3920/BM2017.0075.
Ash C., Priest F.G., Collins M.D., 1994. Paenibacillus gen. nov. Validation of the Publication of New Names and New Combinations Previously Effectively Published Outside the IJSB. Int. J. Syst. Bacteriol. 44, 852–853.
Bailey L., 1968. Honey bee pathology. Annu. Rev. Entomol. 13(1), 191–212.
Bíliková K., Wu G., Šimúth J., 2001. Isolation of a peptide fraction from honeybee royal jelly as a potential antifoulbrood factor. Apidologie 32(3), 275–283.
Brødsgaard C.J., Ritter W., Hansen H., 1998. Response of in vitro reared honey bee larvae to various doses of Paenibacillus larvae larvae spores. Apidologie 29(6), 569–578, https://doi.org/10.1051/apido:19980609.
Chantawannakul P., Dancer B.N., 2001. American foulbrood in honey bees. Bee World 82(4), 168–180.
Chorbiński P., 2004. Zwalczanie grzybicy otorbielakowej pszczoły miodnej. Życie Wet. 79(11), 613–615.
Crane E., 1990. Bees and beekeeping: science, practice and world resources. Heinemann Newnes, Oxford.
Cuthbertson A.G.S., Brown M.A., 2009. Issues affecting British honey bee biodiversity and the need for conservation of this important ecological component. Int. J. Environ. Sci. Technol. 6(4), 695–699, https://doi.org/10.1007/BF03326110.
De Rycke P.H., Joubert J.J., Hosseinian S.H., Jacobs F.J., 2002. The possible role of Varroa de-structor in the spreading of American foulbrood among apiaries. Exp. Appl. Acarol. 27(4), 313–318, https://doi.org/10.1023/A:1023392912999.
Djukic M., Brzuszkiewicz E., Fünfhaus A., Voss J., Gollnow K., Poppinga L., Daniel R., 2014. How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS One, 9(3), e90914, https://doi.org/10.1371/journal.pone.0090914.
Dsouza M., Taylor M.W., Turner S.J., Aislabie J., 2014. Genome-based comparative analyses of Antarctic and temperate species of Paenibacillus. PloS One, 9(10), e108009, https://doi.org/10.1371/journal.pone.0108009.
Engel P., Moran N.A., 2013. Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes 4(1), 60–65.
Evans J.D., Schwarz R.S., 2011. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol. 19(12), 614–620, https://doi.org/10.1016/j.tim.2011.09.003.
Flesar J., Havlik J., Kloucek P., Rada V., Titera D., Bednar M., Kokoska L., 2010. In vitro growth-inhibitory effect of plant-derived extracts and compounds against Paenibacillus larvae and their acute oral toxicity to adult honey bees. Vet. Microbiol. 145(1–2), 129–133, https://doi.org/10.1016/j.vetmic.2010.03.018.
Forsgren E., Locke B., Sircoulomb F., Schäfer M.O., 2018. Bacterial diseases in honeybees. Curr. Clin. Microbiol. Rep. 5(1), 18–25.
Forsgren E., Stevanovic J., Fries I., 2008. Variability in germination and in temperature and storage resistance among Paenibacillus larvae genotypes. Vet. Microbiol. 129(3–4), 342–349, https://doi.org/10.1016/j.vetmic.2007.12.001.
Fries I., Lindström A., Korpela S., 2006. Vertical transmission of American foulbrood (Paeni-bacillus larvae) in honey bees (Apis mellifera). Vet. Microbiol. 114, 269–274, https://doi.org/10.1016/j.vetmic.2005.11.068.
Fries I., Raina S., 2003. American foulbrood and African honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 96(6), 1641–1646, https://doi.org/10.1603/0022-0493-96.6.1641.
Fünfhaus A., Göbel J., Ebeling J., Knispel H., Garcia-Gonzalez E., Genersch E., 2018. Swarming motility and biofilm formation of Paenibacillus larvae, the etiological agent of American Foulbrood of honey bees (Apis mellifera). Sci. Rep. 8(1), 8840, https://doi.org/ 10.1038/s41598-018-27193-8.
Fuselli S.R., Rosa S.B.G. de la, Gende L.B., Eguaras M.J., Fritz R., 2006. Antimicrobial activity of some Argentinean wild plant essential oils against Paenibacillus larvae larvae, causal agent of American foulbrood (AFB). J. Apic. Res. 45(1), 2–7.
Gende L.B., Floris I., Fritz R., Eguaras M.J., 2008. Antimicrobial activity of cinnamon (Cin-namomum zeylanicum) essential oil and its main components against Paenibacillus larvae from Argentine. B. Insectol. 61(1), 1–4.
Genersch E., 2010. American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103, S10-S19, https://doi.org/10.1016/j.jip.2009.06.015.
Genersch E., Ashiralieva A., Fries I., 2005. Strain-and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honeybees. Appl. Environ. Microbiol. 71(11), 7551–7555, https://doi.org/10.1128/ AEM.71.11.7551-7555.2005.
Genersch E., Forsgren E., Pentikäinen J., Ashiralieva A., Rauch S., Kilwinski J., Fries I., 2006. Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int. J. Syst. Evol. Microbiol. 56, 501–511, https://doi.org/10.1099/ijs.0.63928-0.
Genersch E., Otten C., 2003. The use of repetitive element PCR fingerprinting (rep-PCR) for genetic subtyping of German field isolates of Paenibacillus larvae subsp. larvae. Apidologie 34(3), 195–206, https://doi.org/10.1051/apido:2003025.
Gilgert W., Vaughan M., 2011. The value of pollinators and pollinator habitat to rangelands: connections among pollinators, insects, plant communities, fish, and wildlife. Rangelands 33(3), 14–19.
Gliński Z., Kostro K., Luft-Deptula D., Zdanowska M., Zaremba E., 2006. Choroby pszczół. PWRiL, Warszawa, 130–137.
Gonzalez M.J., Marioli J.M., 2010. Antibacterial activity of water extracts and essential oils of various aromatic plants against Paenibacillus larvae, the causative agent of American Foulbrood. J. Invertebr. Pathol. 104(3), 209–213, https://doi.org/10.1016/j.jip.2010.04.005.
Gregorc A., Bowen I.D., 2000. Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline. Cell. Biol. Int. 24(5), 319–324, https://doi.org/10.1006/cbir.1999.0490.
Hadzimuratovic M., Nevjestic A., Rukavina L., Sabirovic M., 1986. Prevalence of bee and brood diseases in Bosnia and Hercegovina in the period 1980–1984. Vet. Glas. 40(7/8), 505–508.
Hansen H., Brødsgaard C.J., 1999. American foulbrood: a review of its biology, diagnosis and control. Bee World 80(1), 5–23, https://doi.org/10.1080/0005772X.1999.11099415.
Hayes Jr J., Underwood R.M., Pettis J., 2008. A survey of honey bee colony losses in the US, fall 2007 to spring 2008. PloS One 3(12), e4071, https://doi.org/10.1371/journal.pone.0004071.
Hornitzky M.A.Z., Clark S., 1991. Culture of Bacillus larvae from bulk honey samples for the detection of American foulbrood. J. Apic. Res. 30(1), 13–16, https://doi.org/10.1080 00218839.1991.11101228.
Hung, K.L.J., Kingston J.M., Albrecht M., Holway D.A., Kohn J.R., 2018. The worldwide im-portance of honey bees as pollinators in natural habitats. Proc. R. Soc. B 285(1870), 20172140, DOI: 10.1098/rspb.2017.2140.
https://www.cabi.org/isc/datasheet/109548#68454B2B-77E7-4AF4-8156-38F41C1C9EF5
Mahdi O.S., Fisher N.A., 2018. Sporulation and germination of Paenibacillus larvae cells. Curr. Protoc. Microbiol. 48(1), 9E–2.
Munawar M.S., Raja S., Waghchoure E.S., Barkat M., 2010. Controlling American foulbrood in honeybees by shook swarm method. Pakistan J. Agric. Res. 23(1–2), 53–58.
Murray K.D., Aronstein K.A., 2008. Transformation of the Gram-positive honey bee pathogen, Paenibacillus larvae, by electroporation. J. Microbiol. Methods, 75(2), 325–328, https://doi. org/10.1016/j.mimet.2008.07.007.
Näumann G., Mahrt E., Himmelreich A., Mohring A., Frerichs H., 2012. Traces of contamination-well preserved in honey: investigation of veterinary drugs and American foulbrood in honeys of global origin. J. Verbrauch. Lebensm. 7(1), 35–43, https://doi.org/10.1007/s00003-015-0995-z.
Owen R., 2017. Role of Human Action in the Spread of Honey Bee (Hymenoptera: Apidae) Path-ogens. J. Econ. Entomol. 110(3), 797–801, https://doi.org/10.1093/jee/tox075.
Peng C.Y.S., Mussen E., Fong A., Cheng P., Wong G., Montague M.A., 1996. Laboratory and Field Studies on the Effects of the Antibiotic Tylosin on Honey Bee Apis mellifera L. (Hy-menoptera: Apidae) Development and Prevention of American Foulbrood Disease. J. Invertebr. Pathol. 67(1), 65–71, https://doi.org/10.1006/jipa.1996.0010.
Schuch D.M.T., Tochetto L.G., Sattler A., 2003. Detection of Paenibacillus larvae subsp. larvae spores in Brazil. Pesq. Agropec. Bras. 38(3), 441–444, https://doi.org/10.1590/S0100- -204X2003000300015.
Semkiw P., 2017. Sektor pszczelarski w Polsce w 2017 roku. Instytut Ogrodnictwa, Zakład Pszczelnictwa w Puławach.
Skubida P., Semkiw P., 2011. Pszczelarstwo ekologiczne w Europie i na świecie. J. Res. Appl. Agricult. Eng. 56(4), 102–106.
Smith F.G., 1953. Beekeeping in the tropics. Bee World 34(12), 233–245.
Spivak M., Reuter G.S., 2001. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32(6), 555–565.
Teixeira É.W., Guimarães-Cestaro L., Alves M., Martins M.F., Luz C.F.P. da, Serrão J.E., 2017. Spores of Paenibacillus larvae, Ascosphaera apis, Nosema ceranae and Nosema apis in bee products supervised by the Brazilian Federal Inspection Service. Rev. Bras. Entomol., https://doi.org/10.1016/j.rbe.2018.04.001.
White G.F., 1907. The cause of American foulbrood (No. 94). US Government Printing Office.
Wilde J., 2013. Encyklopedia pszczelarska. PWRiL, Warszawa.
www.webofknowledge.com
Yoshiyama M., Kimura K., 2009. Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J. Invertebr. Pathol. 102(2), 91–96, https://doi.org/10.1016/j.jip.2009.07.005.
MICHAŁ SCHULZ
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie, ul. Akademicka 13, 20-950
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie, ul. Akademicka 13, 20-950
ALEKSANDRA ŁOŚ
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
PATRYCJA SKOWRONEK
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
ADAM STANISZEWSKI
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
BARTŁOMIEJ IWAŃSKI
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
ŁUKASZ WÓJCIK
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
ANETA STRACHECKA
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
Instytut Biologicznych Podstaw Produkcji Zwierzęcej, Wydział Biologii, Nauk o Zwierzętach i Biogospodarki, Uniwersytet Przyrodniczy w Lublinie
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