Artículo

Garrido, P.M.; Antúnez, K.; Martín, M.; Porrini, M.P.; Zunino, P.; Eguaras, M.J. "Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides" (2013) Journal of Insect Physiology. 59(1):113-119
La versión final de este artículo es de uso interno. El editor solo permite incluir en el repositorio el artículo en su versión post-print. Por favor, si usted la posee enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The mite Varroa destructor is an ectoparasite affecting honey bees worldwide. Synthetic acaricides have been among the principal tools available to beekeepers for its control, although several studies have shown its negative effects on honey bee physiology. Recent research suggests that those molecules strongly impact on immune signaling cascades and cellular immunity. In the present work, LC50 in six-day-old bees were determined for the following acaricides: tau-fluvalinate, flumethrin, amitraz and coumaphos. According to this obtained value, a group of individuals was treated with each acaricide and then processed for qPCR analysis. Transcript levels for genes encoding antimicrobial peptides and immune-related proteins were assessed. Flumethrin increased the expression of hymenoptaecin when comparing treated and control bees. Significant differences were recorded between coumaphos and flumethrin treatments, while the first one reduced the expression of hymenoptaecin and abaecin, the last one up-regulated their expressions. No significant statistically changes were recorded in the expression levels of vitellogenin, lysozyme or glucose dehydrogenase among bees treated with acaricides and control bees. This work constitutes the first report, under laboratory conditions, about induction of immune related genes in response to synthetic miticides. © 2012 Elsevier Ltd.

Registro:

Documento: Artículo
Título:Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides
Autor:Garrido, P.M.; Antúnez, K.; Martín, M.; Porrini, M.P.; Zunino, P.; Eguaras, M.J.
Filiación:Laboratorio de Artrópodos, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata - CONICET, Mar del Plata, Buenos Aires, Argentina
Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay
Centro de Investigaciones Biológicas, CEBB-MdP-INBA, Fundación para Investigaciones Biológicas Aplicadas (FIBA)-CONICET, Mar del Plata, Argentina
Idioma: Inglés
Palabras clave:Apis mellifera; Immune related genes; LC50; Synthetic acaricides; acaricide; insect protein; acaricide; apiculture; cytology; ectoparasite; enzyme activity; gene expression; honeybee; immunity; mite; molecular analysis; signaling; animal; article; bee; drug effect; gene expression; genetics; growth, development and aging; immunology; synthesis; Acaricides; Animals; Bees; Gene Expression; Insect Proteins; Acari; Apis mellifera; Apoidea; Varroa destructor
Año:2013
Volumen:59
Número:1
Página de inicio:113
Página de fin:119
DOI: http://dx.doi.org/10.1016/j.jinsphys.2012.10.019
Título revista:Journal of Insect Physiology
Título revista abreviado:J. Insect Physiol.
ISSN:00221910
CODEN:JIPHA
CAS:Acaricides; Insect Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00221910_v59_n1_p113_Garrido

Referencias:

  • Abbott, W., A method of computing the effectiveness of an insecticide (1925) Journal of Economic Entomology, 18, pp. 265-267
  • Alaux, C., Dantec, C., Parrinello, H., Le Conte, Y., Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa parasitized bees (2011) BioMed Central Genomics, 12, p. 496
  • Amdam, G.V., Omholt, S.W., The regulatory anatomy of honeybee lifespan (2002) Journal of Theoretical Biology, 216, pp. 209-228
  • Amdam, G.V., Omholt, W., The hive bee to forager transition in honeybee colonies: the double repressor hypothesis (2003) Journal of Theoretical Biology, 223, pp. 451-464
  • Amdam, G.V., Hartfelder, K., Norberg, K., Hagen, A., Omholt, S.W., Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering? (2004) Journal of Economic Entomology, 97 (3), pp. 741-747
  • Amdam, G.V., Simoes, Z.L.P., Hagen, A., Norberg, K., Schrøder, K., Mikkelsen, Ø., Kirkwood, T.B.L., Omholt, S.W., Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees (2004) Experimental Gerontology, 39, pp. 767-773
  • Antúnez, K., Martin-Hernandez, R., Prieto, L., Meana, A., Zunino, P., Higes, M., Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia) (2009) Environmental Microbiology, 11, pp. 2284-2290
  • Bandyopadhyay, R., Inhibition of acetylcholine esterase by permethrin and its reversion by acetylthiocholine (1982) Indian Journal of Experimental Biology, 20, pp. 488-491
  • Bendahou, N., Bounias, M., Fleche, C., Toxicity of cypermethrin and fenitrothion on the hemolymph carbohydrates, head acetylcholinesterase, and thoracic muscle Na+, K+-ATPase of emerging honeybees (Apis mellifera mellifera. L) (1999) Ecotoxicology and Environmental Safety, 44, pp. 139-146
  • Bevk, D., Kralj, J., Čokl, A., Coumaphos affects food transfer between workers of honeybee Apis mellifera (2012) Apidologie, 43, pp. 465-470
  • Boecking, O., Genersch, E., Varroosis - the ongoing crisis in bee keeping (2008) Journal für Verbraucherschutz und Lebensmittelsicherheit, 3, pp. 221-228
  • Bogdanov, S., Kilchenmann, V., Imdorf, A., Acaricide residues in beeswax and honey (1997) Apiacta, 32, pp. 72-80
  • Boncristiani, H., Underwood, R., Schwarz, R., Evans, J.D., Pettis, J., vanEngelsdorp, D., Direct effect of acaricides on pathogen loads and gene expression levels of honey bee Apis mellifera (2012) Journal of Insect Physiology, 58 (5), pp. 613-620
  • Burley, L.M., The effect of miticides on the reproductive physiology of honey bee (Apis mellifera L.) queens and drones (2007), Unpublished M.Sc Thesis, Virginia Polytechnic Institute and State University, Blacksburg, Virginia Tech, USACasteels, P., Ampe, C., Jacobs, F., Tempst, P., Functional and chemical of Hymenoptaecin, an antibacterial polypeptide that is infection-inducible in the honeybee (Apis mellifera) (1993) Journal of Biological Chemistry, 268, pp. 7044-7054
  • Chan, Q.W.T., Melathopoulos, A.P., Pernal, S.F., Foster, L.J., The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae (2009) BioMed Central Genomics, 10, p. 387
  • Chauzat, M.P., Faucon, J.P., Pesticide residues in beewax samples collected from honey bee colonies (Apis mellifera L.) in France (2007) Pest Management Science, 63, pp. 1100-1106
  • Claudianos, C., Ranson, H., Johnson, R.M., Biswas, S., Schuler, M.A., Berenbaum, M.R., Feyereisen, R., Oakeshott, J.G., A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee (2006) Insect Molecular Biology, 15 (5), pp. 615-636
  • Collins, A.M., Pettis, J.S., Wilbanks, R., Feldlaufer, M.F., Performance of honey bee (Apis mellifera) queens reared in beeswax cells impregnated with coumaphos (2004) Journal of Apicultural Research, 43 (3), pp. 128-134
  • Cox, R.L., Wilson, W.T., Effects of permethrin on the behavior of individually tagged honey bees, Apis mellifera L. (Hymenoptera, Apidae) (1984) Environmental Entomology, 13, pp. 375-378
  • Cox-Foster, D.L., Stehr, J.E., Induction and localization of FAD-glucose dehydrogenase (GLD) during encapsulation of abiotic implants in Manduca sexta larvae (1994) Journal of Insect Physiology, 40, pp. 235-249
  • Cox-Foster, D.L., Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran, N.A., Quan, P.L., Lipkin, W.I., A metagenomic survey of microbes in honey bee colony collapse disorder (2007) Science, 318, pp. 283-287
  • Cremonez, T.M., De Jong, D., Bitondi, M.M.G., Quantification of hemolymph proteins as a fast method for testing protein diets for honey bees (Hymenoptera: Apidae) (1998) Journal of Economic Entomology, 91, pp. 1284-1289
  • Currie, R.W., Fluvalinate queen tabs for use against Varroa jacobsoni Oud.: efficacy and impact on honey bee, Apis mellifera L., queen and colony performance (1999) American Bee Journal, 139 (11), pp. 871-876
  • Daffre, S., Klysten, P., Samakovlis, C., Hultmark, D., The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract (1994) Biochemical and Biophysical Research Communications, 194, pp. 152-162
  • Dainat, B., Evans, J.D., Chen, Y.P., Gauthier, L., Neumann, P., Predictive markers of honey bee colony collapse (2012) Public Library of Science (PLoS) ONE, 7 (2), pp. e32151
  • Danka, R.G., Rinderer, T.E., Hellmich, R.L., Collins, A.M., Comparative toxicities of 4 topically applied insecticides to Africanized and European honey-bees (Hymenoptera, Apidae) (1986) Journal of Economic Entomology, 79, pp. 18-21
  • Decker, H., Jaenicke, E., Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins (2004) Developmental and Comparative Immunology, 28, pp. 673-687
  • Duff, S.R., Furgala, B., Some effects of menthol and fluvalinate on mite-free honey bee (Apis mellifera L.) colonies (1992) American Bee Journal, 132 (7), pp. 476-477
  • Ellis, J.D., Delaplane, K.S., Hood, W.M., Efficacy of a bottom screen device, apistan, and apilife var, in controlling Varroa destructor (2001) American Bee Journal, 141 (11), pp. 813-816
  • Elzen, P.J., Westervelt, D., Detection of coumaphos resistance in Varroa destructor in Florida (2002) American Bee Journal, 142, pp. 291-292
  • Elzen, P.J., Baxter, J.R., Spivak, M., Wilson, W.T., Amitraz resistance in Varroa: new discovery in North America (1999) American Bee Journal, 139 (5), p. 362
  • Elzen, P.J., Baxter, J.R., Spivak, M., Wilson, W.T., Control of Varroa jacobsoni Oud. resistant to fluvalinate and amitraz using coumaphos (2000) Apidologie, 31, pp. 437-441
  • Evans, J.D., Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease (2006) Journal of Invertebrate Pathology, 93, pp. 135-139
  • Falchuk, K.H., The molecular basis for the role of zinc in developmental biology (1998) Molecular and Cellular Biochemistry, 188, pp. 41-48
  • Fell, R.D., Tignor, K., Miticide effects on the reproductive physiology of queens and drones (2001) American Bee Journal, 141 (12), pp. 888-889
  • Fries, I., Aarhus, A., Hansen, H., Korpela, S., Comparisons of diagnostic methods for detection of Varroa jacobsoni in honey bee (Apis mellifera) colonies at low infestation levels (1991) Experimental and Applied Acarology, 10, pp. 279-287
  • Gregorc, A., Ellis, J.D., Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides (2011) Pesticide Biochemistry and Physiology, 99, pp. 200-207
  • Haarmann, T., Spivak, M., Weaver, D., Weaver, B., Glenn, T., Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations (2002) Journal of Economic Entomology, 95 (1), pp. 28-35
  • Higes, M., García-Palencia, P., Martín-Hernández, R., Meana, A., Experimental infection of Apis mellifera honeybees with the Microsporidia Nosema ceranae (2007) Journal of Invertebrate Pathology, 94, pp. 211-217
  • Johnson, R.M., Pollock, H.S., Berenbaum, M.R., Synergistic interactions between in-hive miticides in Apis mellifera (2009) Journal of Economic Entomology, 102, pp. 474-479
  • Lavine, M.D., Strand, M.R., Insect hemocytes and their role in immunity (2002) Insect Biochemistry and Molecular Biology, 32, pp. 1295-1309
  • Lindberg, C., Melathopoulus, A., Winston, M., Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymenoptera: Apidae) parasite (2000) Journal of Economic Entomology, 93, pp. 89-198
  • Locke, B., Forsgren, E., Fries, I., de Miranda, J.R., Acaricide treatment affects viral dynamics control colonies via both host physiology and mite in Varroa destructor-infested honey bee (2012) Applied Environmental Microbiology, 78 (1), p. 227
  • Lodesani, M., Costa, C., Bigliardi, M., Colombo, R., Acaricide residues in bees wax and organic beekeeping (2003) Apiacta, 38, pp. 31-33
  • Loucif-Ayad, W., Aribi, N., Soltani, N., Evaluation of Secondary Effects of some Acaricides on Apis Mellifera Intermissa (Hymenoptera, Apidae): Acetylcholinesterase and Glutathione S-Transferase Activities (2008) European Journal of Scientific Research, 21 (4), pp. 642-649
  • Lovallo, N.C., Cox-Foster, D.L., Alteration in FADglucose dehydrogenase activity and hemocyte behaviour contribute to initial disruption of Manduca sexta immune response to Cotesia congregata parasitoids (1999) Journal of Insect Physiology, 45, pp. 1037-1048
  • Maggi, M., Ruffinengo, S., Damiani, N., Sardella, N., Eguaras, M.J., A first detection of Varroa destructor resistance to coumaphos in Argentina (2009) Experimental and Applied Acarology, 47 (4), pp. 317-320
  • Maggi, M.D., Ruffinengo, S.R., Negri, P., Eguaras, M.J., Resistance phenomena to amitraz from populations of the ectoparasitic mite Varroa destructor of Argentina (2010) Parasitology Research, 107, pp. 1189-1192
  • Maggi, M.D., Ruffinengo, S.R., Mendoza, Y., Ojeda, P., Ramallo, G., Floris, I., Eguaras, M.J., Susceptibility of Varroa destructor (Acari: Varroidae) to synthetic acaricides in Uruguay: Varroa mites' potential to develop acaricide resistance (2011) Parasitology Research, 108, pp. 815-821
  • Martel, A.C., Zeggane, S., Aurieres, C., Drajnudel, P., Faucon, J.P., Aubert, M., Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar or Asuntol 50 (2007) Apidologie, 38, pp. 534-544
  • Maver, L., Poklukar, J., Coumaphos and amitraz residues in Slovenian honey (2003) Apiacta, 38, pp. 54-57
  • Milani, N., The resistance of Varroa jacobsoni Oud to pyrethroids: a laboratory assay (1995) Apidologie, 26, pp. 415-429
  • Mocchegiani, E., Muzzioli, M., Gicconi, R., Zinc, metallothioneins, immune responses, survival and ageing (2000) Biogerontology, 1, pp. 133-143
  • Mullin, C.A., Frazier, M., Frazier, J.L., Ashcraft, S., Simonds, R., van Engelsdorp, D., Pettis, J.S., High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health (2010) Public Library of Science (PLoS) ONE, 5 (3), pp. e9754
  • Munch, D., Amdam, G.V., Wolschin, F., Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee (2008) Functional Ecology, 22, pp. 407-421
  • Nielsen, S.A., Brodsgaard, C.J., Hansen, H., Effects on detoxification enzymes in different life stages of honeybees (Apis mellifera L., Hymenoptera: Apidae) treated with a synthetic pyrethroid (flumethrin) (2000) Alternatives to Laboratory Animals: ATLA, 28, pp. 437-443
  • Orantes-Bermejo, F.J., Gómez-Pajuelo, A., Megías-Megías, M., Torres Fernández-Piñar, C., Pesticide residues in beeswax and beebread samples collected from honey bee colonies (Apis mellifera L.) in Spain. Possible implications for bee losses (2010) Journal of Apicultural Research, 49, pp. 243-250
  • Pareja, L., Colazzo, M., Pérez-Parada, A., Niell, S., Carrasco-Letelier, L., Besil, N., Cesio, M.V., Heinzen, H., Detection of pesticides in active and depopulated beehives in Uruguay (2011) International Journal of Environmental Research and Public Health, 8, pp. 3844-3858
  • Pettis, J.S., Wilson, W.T., Shimanuki, H., Teel, P.D., Fluvalinate treatment of queen and worker honeybees (Apis mellifera L.) and effects on subsequent mortality, queen acceptance and supersedure (1991) Apidologie, 22, pp. 1-7
  • Pettis, J.S., Collins, A.M., Wilbanks, R., Feldlaufer, M.F., Effects of coumaphos on queen rearing in the honey bee, Apis mellifera (2004) Apidologie, 35, pp. 605-610
  • Pfaffl, M., A new mathematical model for relative quantification in real time RT PCR (2001) Nucleic Acids Research, 29, pp. 2002-2007
  • Rinderer, T.E., De Guzman, L., Lancaster, V.A., Delatte, G.T., Stelzer, J.A., Varroa in the mating yard: the effects of Varroa jacobsoni and Apistan on drone honey bees (1999) American Bee Journal, 139, pp. 134-139
  • Rosenkranz, P., Aumeier, P., Ziegelmann, B., Biology and control of Varroa destructor (2010) Journal of Invertebrate Pathology, 103, pp. 96-119
  • Ruffinengo, S.R., Eguaras, M.J., Floris, I., Faverín, C., Bailac, P.N., Ponzi, M.I., LD50 and repellent effects of essential oils from Argentinian wild plant species on Varroa destructor (2005) Journal of Economic Entomology, 98, pp. 651-655
  • Seehuus, S.C., Norberg, K., Gimsa, U., Krekling, T., Amdam, G.V., Reproductive protein protects sterile honeybee workers from oxidative stress (2006) Proceedings of the National Academy of Science of the United States of America, 103, pp. 962-967
  • Skinner, J.A., Parkman, J.P., Studer, M.D., Evaluation of honey bee miticides, including temporal and thermal effects on formic acid gel vapours, in the central south eastern USA (2001) Journal of Apicultural Research, 40 (3-4), pp. 81-89
  • Sokol, R., The influence of a multimonth persistence of Fluwarol in a hive of a honey bee colony (1996) Medycyna Weterynaryjna, 52, pp. 718-720
  • Stoner, A., Wilson, W.T., Moffett, J.O., Effects of longterm feeding of low doses of fenvalerate or fluvalinate in sucrose syrup on honey bees Apis mellifera in standard-sized field colonies (1984) Journal of the Georgia Entomological Society, 19, pp. 490-498
  • Suwannapong, G., Yemor, T., Boonpakdee, C., Benbow, M.E., Nosema ceranae, a new parasite in Thai honeybees (2010) Journal of Invertebrate Pathology, 106, pp. 236-241
  • vanBuren, N.W.M., Marien, A.G.H., Oudejans, R.C.H.M., Velthuis, H.H.W., Perizin, an acaricide to combat the mite Varroa jacobsoni: its distribution in and influence on the honeybee Apis mellifera (1992) Physiological Entomology, 17, pp. 288-296
  • vanBuren, N.W.M., Marien, A.G.H., Velthuis, H.H.W., The role of trophallaxis in the distribution of Perizin in a honeybee colony with regard to the control of the Varroa mite (1992) Entomologia Experimentalis et Applicata, 65, pp. 157-164
  • Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes (2002) Genome Biology, 3 (7), p. 0034
  • Wallner, K., Varroacides and their residues in bee products (1999) Apidologie, 30, pp. 235-248
  • Wang, R.W., Liu, Z.Q., Dong, K., Elzen, P.J., Pettis, J., Huang, Z.Y., Association of novel mutations in a sodium channel gene with fluvalinate resistance in the mite, Varroa destructor (2002) Journal of Apicultural Research, 41, pp. 17-25
  • Westcott, L.C., Winston, M.L., Chemical acaricides in Apis mellifera L. (Hymenoptera: Apidae) colonies: do they cause non-lethal effects (1999) Canadian Entomology, 131, pp. 363-371
  • Wilson-Rich, N., Dres, S.T., Starks, P.T., The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera) (2008) Journal of Insect Physiology, 54, pp. 1392-1399
  • Wu, J., Anelli, C., Sheppard, W.S., Sub-Lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity (2011) Public Library of Science (PLoS) One, 6 (2), pp. e14720
  • Yang, X., Cox-Foster, D.L., Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification (2005) Proceedings of the National Academy of Sciences, 21, pp. 7470-7475
  • Yang, X., Cox-Foster, D., Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge (2007) Parasitology, 134, pp. 405-412

Citas:

---------- APA ----------
Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P. & Eguaras, M.J. (2013) . Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides. Journal of Insect Physiology, 59(1), 113-119.
http://dx.doi.org/10.1016/j.jinsphys.2012.10.019
---------- CHICAGO ----------
Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P., Eguaras, M.J. "Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides" . Journal of Insect Physiology 59, no. 1 (2013) : 113-119.
http://dx.doi.org/10.1016/j.jinsphys.2012.10.019
---------- MLA ----------
Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P., Eguaras, M.J. "Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides" . Journal of Insect Physiology, vol. 59, no. 1, 2013, pp. 113-119.
http://dx.doi.org/10.1016/j.jinsphys.2012.10.019
---------- VANCOUVER ----------
Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P., Eguaras, M.J. Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides. J. Insect Physiol. 2013;59(1):113-119.
http://dx.doi.org/10.1016/j.jinsphys.2012.10.019