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Natural Strategies for the Control Of Natural strategies for the control of Paenibacillus larvae, the causative agent of American foulbrood in honey bees: a review Rosa Maria Alonso-Salces, Noelia Melina Cugnata, Elisa Guaspari, Maria Celeste Pellegrini, Inés Aubone, Fiorella Giselle de Piano, Karina Antunez, Sandra Rosa Fuselli To cite this version: Rosa Maria Alonso-Salces, Noelia Melina Cugnata, Elisa Guaspari, Maria Celeste Pellegrini, Inés Aubone, et al.. Natural strategies for the control of Paenibacillus larvae, the causative agent of American foulbrood in honey bees: a review. Apidologie, Springer Verlag, 2017, 48 (3), pp.387-400. 10.1007/s13592-016-0483-1. hal-01676926 HAL Id: hal-01676926 https://hal.archives-ouvertes.fr/hal-01676926 Submitted on 6 Jan 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2017) 48:387–400 Review article * INRA, DIB and Springer-Verlag France, 2016 DOI: 10.1007/s13592-016-0483-1 Natural strategies for the control of Paenibacillus larvae , the causative agent of American foulbrood in honey bees: a review 1,3 1,3 1,3 Rosa Maria ALONSO-SALCES , Noelia Melina CUGNATA , Elisa GUASPARI , 1,2 1 3,4 Maria Celeste PELLEGRINI , Inés AUBONE , Fiorella Giselle DE PIANO , 5 1,2 Karina ANTUNEZ , Sandra Rosa FUSELLI 1Grupo de Investigación Microbiología Aplicada, Centro de Investigación en Abejas Sociales, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Dean Funes, B7602AYL, 3350, Mar del Plata, Argentina 2Comisión de Investigaciones Científicas, La Plata, Argentina 3Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina 4Cátedra de Apicultura, Departamento de Producción Animal, Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina 5Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay Received 16 May 2016 – Revised 8 October 2016 – Accepted 16 November 2016 Abstract – American foulbrood (AFB) is a severe bacterial disease that affects larvae of honey bees (Apis mellifera ). The causative agent of AFB is the spore-forming bacteria Paenibacillus larvae. The use of antibiotics for the control of AFB has led to the appearance of resistant bacterial strains and residues in beehive products. Nowadays, antibiotics are legally banned in several countries, and the affected colonies have to be destroyed by burning the hives. Therefore, the development of alternative methods for the control and prevention of AFB is necessary. In this context, different natural strategies based on the application of essential oils, plant extracts, propolis, royal jelly, nonconventional natural molecules, bacteria, and bacteriocines, have been studied in vitro and in vivo for the prevention and control of P. larv ae .The experimental data achieved from these studies are reviewed and discussed in the present review, which intend to be a starting point for future research in the field. Paenibacillus larvae / American foulbrood / Apis mellifera / natural products 1. INTRODUCTION 2010). AFB only kills infected honey bee larvae; however, it eventually leads to the collapse of the American foulbrood (AFB) is the most severe entire colony when left untreated. AFB is consid- bacterial disease that affects honey bees, having a ered to be very contagious; therefore, it is a noti- nearly cosmopolitan distribution (Genersch fiable disease in most countries (Djukic et al. 2014). AFB’s causative agent is Paenibacillus larvae , which is a flagellated gram-positive bac- Electronic supplementary material The online version of terium, whose main characteristic is the formation this article (doi:10.1007/s13592-016-0483-1) contains of highly resistant endospores. This pathogen af- supplementary material, which is available to authorized fects the breeding during the larval or pupal stages users. (Genersch et al. 2006); its spores being the infec- Corresponding author: S. Fuselli, tious form. Honey bee larvae are more susceptible [email protected] to infection during the first 36 h after egg hatching Manuscript editor: David Tarpy (Ashiralieva and Genersch 2006), indeed only ten 388 R. Alonso-Salces et al. spores are required to make a larva of less than and prevention is forbidden in several coun- 24 h old ill (Bamrick 1967). However, at later tries, and the affected colonies have to be larval developmental stages, spore doses needed destroyed by burning the hives (Mutinelli to successfully infect a larva are too high to occur 2003). This action represents a drastic solution under natural conditions (Genersch et al. 2005). with a high cost for beekeepers, and further- The infection takes place by the ingestion of the more, it cannot be used as a preventive method spores with the food provided by adult worker to combat AFB (Kochansky et al. 2001). In bees (nurses) to the larvae (Hansen and this context, the development of alternative Brodsgaard 1999). Spores germinate in the larval and effective methods for the control and pre- midgut and massively proliferate for several days. vention of AFB disease is crucial. These At a later stage, P. l arv ae reaches the peritrophic methods should consider the evidence of bacterial-resistant phenomenon and comply matrix, penetrates into the epidermal cells, pro- with strict EU policies as well as with current ducing septicemia, and finally causing the death trends of green consumerism (Lewis and of the larva. In the last instance, the corpses are Ausubel 2006). In the present review, the re- digested by vegetative bacterial cells and convert- search studies focused on the development of ed to dried scales containing millions of P. l arv ae natural strategies for the control and preven- spores (Hansen and Brodsgaard 1999;Cornman tion of AFB carried out so far are summarized, et al. 2013; Djukic et al. 2014). The most conspic- including the use of essential oils, plant ex- uous symptoms in colonies suffering from clinical tracts, propolis, royal jelly, nonconventional AFB disease are irregular brood capping, showing natural molecules, bacteria, and bacteriocines capped and uncapped cells scattered irregularly for the aimed purpose. across the brood frames; dark, sunken, and often B ^ punctured caps emitting a foul odor; brown 2. NATURAL PRODUCTS FOR glue residues of the dead larvae forming a charac- THE PREVENTION AND CONTROL teristic ropey thread when it is pulled out with a OF AMERICAN FOULBROOD wooden stick or a match; and a hard scale of larval residues at the bottom of the cell. Traditional AFB 2.1. Essential oils diagnosis is based on the observation of these clinical symptoms in the beehive and on the mi- Essential oils (EOs) are natural volatile and crobial cultivation of material from infected colo- complex products obtained as secondary metabo- nies (De Graaf et al. 2006). lites of aromatic plants, having different biological TheresistanceofP. l arvae endospores is a effects (anticancer, anti-inflammatory, insect re- main issue in the control and prevention of pellent, antimicrobial, antiviral, and antioxidant). AFB because these endospores can survive Since EOs affect many targets at the same time, no for more than 35 years in honey and/or on cases of resistance or adaptation have been detect- the beekeeping material and resist high tem- ed (Adorjan and Buchbauer 2010). Several EOs peraturesaswellastheactionofthemost have been evaluated for the in vitro and in vivo commonly used disinfectants (Bamrick 1967). control of P. l arv ae ,aswellastheiracuteoral Most treatments are based on the use of broad toxicity to Apis mellifera (Tables I, II,andIII in spectrum antibiotics, which, in most cases, the Electronic supplementary material). have been used continuously and excessively. Indeed, different antibiotics, such as sulfathia- 2.1.1. In vitro assays to control P. larvae zole and oxytetracycline hydrochloride (OTC), are able to inhibit the growth of P. larvae , but EOs from Achyrocline satureioides , Carum its use and abuse for decades led to the ap- carvi , Cinamomum sp., Cinnamomum pearance of resistant strains and residues that zeylanicum , Citrus paradise , Cuminum contaminate beehive products. For these rea- cyminum , Cymbopogon citratus , Eucalyptus sons, the use of antibiotics for AFB treatment cinerea , Melaleuca alternifolia , Mentha Control of American foulbrood in honey bees 389 piperita , Minthostachys verticillata , Origanum (Gende et al. 2010b). EOs from Artemisia majorana , Origanum vulgare , Polygonum absinthium , Artemisia annua , Lepechinia flori- bistorta , Salvia officinalis and Salvia sclarea , bunda , C. paradisi , Cymbopogon nardus , Mela- Syzygium aromaticum , Tagetes minuta , Thymus leuca viridiflora , C. zeylanicum , Rosmarinus vulgaris , Verbena , Pimenta dioica (L.) Merr., officinalis , Carapa guianensis , Copaifera Litsea cubeba Pers., Trachyspermum ammi L., officinalis , M. alternifolia , Mentha aff. arvensis , Mentha arvensis L., Mentha spicata L., Illicium Mentha aff. rotundifolia , P. dioica (L.) Merr., verum Hook.f, Myristica fragrans Gronov.,
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