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In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia)

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Abstract

This study evaluated the activity of plant extracts on Nosema ceranae development and their toxicity on the infected host Apis mellifera. Newly emerged bees were fed ad libitum with enriched syrups after individual infection. Diets consisted of ethanolic extracts obtained from Artemisia absinthium, Allium sativum, Laurus nobilis, and Ilex paraguariensis diluted in syrup at 1% and 10% concentrations. Examination of individual midgut homogenates on day 19 post-infection indicated that 1% concentration of L. nobilis extract significantly inhibited N. ceranae development. Absinth extract, previously reported as effective against Nosema apis, did not diminish the number of N. ceranae spores throughout the experiment. Ten percent concentrations showed high toxicity on infected bees, but also a significant activity diminishing parasitosis development in short periods. Syrups with the addition of extracts were consumed avidly as the control, even more in some cases. The present study constitutes the first report of antiparasitic activity in vivo of plant extracts against the Microsporidian N. ceranae and postulate natural substances as an alternative for antiparasitic treatment.

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References

  • Adamczyk, S., Lázaro, R., Pérez-Arquillué, C., Conchello, P., Herrera, A. (2005) Evaluation of residues of essential oil components in honey after different anti-Varroa treatments. J Agric Food Chem. 53,10085–10090. doi:10.1021/jf051813f

    Google Scholar 

  • Adler, L.S. (2000) The ecological significance of toxic nectar. Oikos 91, 409–420

    Article  Google Scholar 

  • Ahameethunisa, A.R., Hopper, W. (2010) Antibacterial activity of Artemisia nilagirica leaf extracts against clinical and phytopathogenic bacteria. BMC Comp Altern Med 10, 6. http://www.biomedcentral.com/1472-6882/10/6

    Article  Google Scholar 

  • Ankri, S., Mirelman, D. (1999) Antimicrobial properties of allicin from garlic. Microbes Infect 2(2), 125–9 doi:10.1016/S1286-4579(99)80003-3

    Google Scholar 

  • Ankri, S., Miron, T., Rabinkov, A., Wilchek, M., Mirelman, D. (1997) Allicin from garlic strongly inhibits cysteine proteinases and cytopathic effects of Entamoeba histolytica. Antimicrob. Agents Chemother. 10, 2286–2288

    Google Scholar 

  • Berbehenn, R.V., Martin, M.M. (1994) Tannin sensitivity in larvae of Malacosoma disstria (Lepidoptera): roles of the pertitrophic envelope and midgut oxidation. J. Chem. Ecol. 20, 1985–2001

    Article  Google Scholar 

  • Block, E. (1992) The organosulfur chemistry of the genus Allium -Implication for the organic chemistry of sulfur. Angew. Chem. Int. 31, 1135–1178

    Article  Google Scholar 

  • Cantwell, G.E. (1970) Standard methods for counting nosema spores. Am. Bee Jj. 110, 220–223

    Google Scholar 

  • Costa, C., Lodesani, M., Maistrello, L. (2010) Effect of thymol and resveratrol administered with candy or syrup on the development of Nosema ceranae and on the longevity of honeybees (Apis mellifera L.) in laboratory conditions. Apidologie 41, 141–150

    Article  Google Scholar 

  • Damiani, N. (2010) Control del parásito Varroa destructor (Acari: Varroidae) en colmenas de Apis mellifera (Hymenoptera: Apidae). Doctoral thesis. School of Exact and Naturals Science. National University of Mar del Plata. Argentina (in Spanish)

  • Ertürk, O. (2006) Antibacterial and antifungal activity of ethanolic extracts from eleven spice plants. Sect. Cell. Mol. Biol. 61, 275–278

    Google Scholar 

  • Fries, I. (2010) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr. Pathol. 103, 73–79

    Article  Google Scholar 

  • Gende, L.B. (2009) Principales componentes de aceites esenciales relacionados con actividad antimicrobiana frente a Paenibacillus larvae. Doctoral thesis. School of Pharmacy and Biochemistry. University of Buenos Aires. Argentina (in Spanish).

  • Gende, L.B., Principal, J., Maggi, M.D., Palacios, S.M., Fritz, R., Eguaras, M.J. (2008) Extracto de Melia azedarach y aceites esenciales de Cinnamomun zeylanicum, Mentha piperita y Lavandula officinalis como control de Paenibacillus larvae. Zoot. Trop. 26, 151–156

    Google Scholar 

  • He, X.G. (2000) On-line identification of phytochemical constituents in botanical extracts by combined high-performance liquid chromatographic–diode array detection–mass spectrometric techniques. J. Chromatogr. 880, 203–232

    Article  CAS  Google Scholar 

  • Higes, M., García-palencia, P., Martín-Hernández, R., Meana, A. (2007) Experimental infection of Apis mellifera with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 94, 211–217

    Article  PubMed  Google Scholar 

  • Keeling, P.J., Fast, N.M. (2002) Microsporidia: Biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 56, 93–116

    Article  PubMed  CAS  Google Scholar 

  • Lawson, L.D. (1993) Bioactive organosulfur compound of garlic and garlic products: role in reducing blood lipids. In: Kinghorn, A.D., Balandrin, M.F. (eds.) Human medicinal agents from plants, pp. 306–330. American Chemical Society, Washington

    Chapter  Google Scholar 

  • Lawson, L.D., Block, E. (1997) Comments on garlic chemistry stability of s-(2-propenyl) 2 propene-1- sulfinothioate (allicin) in blood solvents and stimulated physiological fluids. J. Agric. Food. Chem. 45, 542

    Article  CAS  Google Scholar 

  • Leiro, J., Cano, E., Ubeira, F.M., Orallo, F., Sanmartìn, M.L. (2004) In vitro effects of resveratrol on the viability and infectivity of the Microsporidian Encephalitozoon cuniculi. Antimicrob. Agents Ch. 48, 2497–2501

    Article  CAS  Google Scholar 

  • Maistrello, L., Lodesani, M., Costa, C., Leonardi, F., Marani, G., Caldon, M., Mutinelli, F., Granato, A. (2008) Screening of natural compounds for the control of nosema disease in honey bees (Apis mellifera). Apidologie 39, 436–444

    Article  Google Scholar 

  • Martín-Hernández, R., Meana, A., Prieto, L., Martínez, S.A., Garrido-Bailón, E., Higes, M. (2007) Outcome of Colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 73, 6331–6338

    Article  PubMed  Google Scholar 

  • Mayack, C., Naug, D. (2009) Energetic stress in the honey bee Apis mellifera from Nosema ceranae infection. J. Invertebr. Pathol. 100(3), 185–188

    Article  PubMed  Google Scholar 

  • Mirelman, D., Monheit, D., Varon, S. (1987) Inhibition of growth of Entamoeba histolytica by Allicin, the active principle of garlic extract (Allium sativum). J. Infect. Dis. 156, 243–244

    Article  PubMed  CAS  Google Scholar 

  • Nanasombat, S., Lohasupthawee, P. (2005) Antibacterial activity of crude ethanolic extracts and essential oils of spices against salmonellae and other enterobacteria. Sci. Tech. J. 5, 462–469

    Google Scholar 

  • Nejad, B.S., Deokule, S.S. (2009) Anti-dermatophytic activity of Drynaria quercifolia (L.). Jundishapur. J. Microbiol. 2, 25–30

    Google Scholar 

  • Ong, E.S. (2004) Extraction methods and chemical standardization of botanicals and herbal preparations. J. Chromatogr. 812, 23–33

    CAS  Google Scholar 

  • Paxton, R.J., Klee, J., Korpelab, S., Fries, I. (2007) Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38, 558–565

    Article  Google Scholar 

  • Pohorecka, K. (2004a) Effect of standardized plant herb extracts on general condition of the honeybee (Apis mellifera l.). Bull. Vet. Inst. Pulawy. 48, 415–419

    Google Scholar 

  • Pohorecka, K. (2004b) Laboratory studies on the effect of standardized Artemisia absinthium L. extract on Nosema apis infection in the worker Apis mellifera. J. Apic. Sci. 48, 131–136

    Google Scholar 

  • Porrini, M.P., Audisio, M.C., Sabaté, D.C., Ibarguren, C., Medici, S.K., Sarlo, E.G., Garrido, P.M., Eguaras, M.J. (2010) Effect of bacterial metabolites on microsporidian Nosema ceranae and on its host Apis mellifera. Parasitol. Res. 107, 381–388

    Article  PubMed  Google Scholar 

  • Porrini, M.P., Sarlo, E.G., Medici, S.K., Garrido, P.M., Porrini, D.P., Eguaras, M.J. (2011) Nosema ceranae development in Apis mellifera: Influence of diet and infective inoculum. J. Apic. Res. 50(1), 35–41

    Article  Google Scholar 

  • Rinderer, T.E. (1976) Honey bees: individual feeding of large numbers of adult workers. J. Econ. Entomol. 69, 489–491

    Google Scholar 

  • Rodríguez Vaquero, M.J., Tomassini Serravalle, L.R., Manca de Nadra, M.C., Strasser de Saad, A.M. (2009) Antioxidant capacity and antibacterial activity of phenolic compounds from argentinean herbs infusions. Food Control. 21, 799–785

    Google Scholar 

  • Soylu, E.M., Tok, F.M., Soylu, S., Kaya, A.D., Evrendilek, G.A. (2005) Antifungal activities of essential oils on post harvest disease agent Penicillium digitatum. Pak. J. Biol. Sci. 8, 25–29

    Article  Google Scholar 

  • Tariq, K.A., Chishti, M.Z., Ahmada, F., Shawl, A.S. (2009) Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes. Vet. Parasitol. 160, 83–88

    Article  PubMed  CAS  Google Scholar 

  • Williams, G.R., Sampson, M.A., Shutler, D., Rogers, R. (2008) Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? J. Invertebr. Pathol. 99, 342–344

    Article  PubMed  CAS  Google Scholar 

  • Yoshida, M., Fuchigami, M., Nagao, T., Okabe, H., Matsunaga, K., Takata, J., Karube, Y., Tsuchihashi, R., Kinjo, J., Mihashi, K., Fujioka, T. (2005) Antiproliferative constituents from Umbelliferae plants VII. Active triterpenes and rosmarinic acid from Centella asiatica. Biol. Pharmacol. Bull. 28, 173–175

    Article  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank CONICET, UNMdP. This research was supported by ANPCyT (FONCyT), project PICT 890/06, to M.E. We thank the support provided by the 426 Animal Production Department, EEA INTA, Balcarce, the Fares Taie Laboratories Food Division and the contribution made by Enrique Tkacik.

Evaluation in vivo de l'activité anti-parasitaire d'extraits de plantes sur Nosema ceranae (Microsporidia)

Apis mellifera / Nosema ceranae / extrait de plante / traitement anti-parasitaire

Eine in vivo Methode zur Beurteilung der antiparasitischen Wirkung von Pflanzenextrakten gegen Nosema ceranae (Microsporidia)

Apis mellifera / Nosema ceranae / Pflanzenextrakt / antiparasitische Behandlung

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Authors and Affiliations

  1. Arthropods Laboratory, School of Exact and Natural Sciences, National University of Mar del Plata, Funes, 3350 (7600), Mar del Plata, Argentina

    Martín Pablo Porrini, Natalia Jorgelina Fernández, Paula Melisa Garrido, Liesel Brenda Gende, Sandra Karina Medici & Martín Javier Eguaras

  2. Agencia Nacional de Promoción Científica y Técnológica, Buenos Aires, Argentina

    Martín Pablo Porrini

  3. Consejo Nacional de Investigaciónes Científicas y Técnicas, Buenos Aires, Argentina

    Natalia Jorgelina Fernández, Paula Melisa Garrido, Liesel Brenda Gende, Sandra Karina Medici & Martín Javier Eguaras

Authors
  1. Martín Pablo Porrini
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  2. Natalia Jorgelina Fernández
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  3. Paula Melisa Garrido
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  4. Liesel Brenda Gende
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  5. Sandra Karina Medici
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  6. Martín Javier Eguaras
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Correspondence to Martín Pablo Porrini.

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Manuscript editor: David Tarpy

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Porrini, M.P., Fernández, N.J., Garrido, P.M. et al. In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia). Apidologie 42, 700–707 (2011). https://doi.org/10.1007/s13592-011-0076-y

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  • DOI: https://doi.org/10.1007/s13592-011-0076-y

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