Risk factors associated with honey bee colony loss in apiaries in Galicia, NW Spain

Aranzazu Meana, Miguel Llorens-Picher, Amaia Euba, José L. Bernal, José Bernal, María García-Chao, Tierry Dagnac, Jose A. Castro-Hermida, Amelia V. Gonzalez-Porto, Mariano Higes, Raquel Martín-Hernández

Abstract


A cross-sectional study was carried out in Galicia, NW Spain, in order to estimate the magnitude of honey bee colony losses and to identify potential risk factors involved. A total of 99 samples from 99 apiaries were collected in spring using simple random sampling. According to international guidelines, the apiaries were classified as affected by colony loss or asymptomatic. Each sample consisted of worker bees, brood and comb-stored pollen. All worker bees and brood samples were analysed individually in order to detect the main honey bee pathogens. Moreover, the presence of residues of the most prevalent agrotoxic insecticides and acaricides was assessed in comb-stored pollen. The general characteristics of the apiaries and sanitary information regarding previous years was evaluated through questionnaires, while the vegetation surrounding the apiaries sampled was assessed by palynological analysis of comb-stored pollen. The colony loss prevalence was 53.5% (CI95%=43.2-63.9) and Nosema ceranae was found to be the only risk factor strongly associated with colony loss. The decision tree also pointed out the impact of the Varroa mite presence while variables such as apiary size, the incorrect application of Varroa mite treatments, and the presence of Acarapis woodi and Kashmir bee virus (KBV) were identified as possible co-factors.


Keywords


colony collapse; Apis mellifera; Nosema ceranae; Varroa destructor; imidacloprid; fipronil; comb-stored pollen

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References


AFSA, 2008. Weakening, collapse and mortality of bee colonies. Chiron J & Hattenberger AM (eds), 218 pp. Agence Française de Sécurité Sanitaire des Aliments

Arnaiz A, 2008. La peor cosecha de miel gallega. http://www.elcorreogallego.es/galicia/ecg/peor-cosecha-miel-gallega/idEdicion-2008-09-05/idNoticia-339628/ [13 March 2016].

Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, Falcaro C, Gallina A, Mutinelli F, 2010. Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol 105: 335-340. https://doi.org/10.1016/j.jip.2010.08.004

Ball BV, 1989. Varroa jacobsoni as a virus vector. In: Present status of varroatosis in Europe and progress in varroa mite control; Cavalloro R (Ed), pp: 241-244. Office for Official Publications of the European Communities, Luxemburg.

Bekele AZ, Mor SK, Phelps NB, Goyal SM, Armién AG, 2015. A case report of Nosema ceranae infection in honey bees in Minnesota, USA. Vet Quat 35 (1): 48-50. https://doi.org/10.1080/01652176.2014.981766

Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Nowotny N, 2006. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microbiol 72: 2414-2420. https://doi.org/10.1128/AEM.72.4.2414-2420.2006

Bernal J, Garrido-Bailón E, Del Nozal MJ, González-Porto AV, Martín-Hernández R, Diego JC Jiménez JJ, Bernal JL, Higes M, 2010. Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J Econ Entomol 103 (6): 1964-1971. https://doi.org/10.1603/EC10235

Betti M, Wahl L, Zamir M, 2014. Effects of infection on honey bee population dynamics: A model. PLoS One 9 (10): e110237. https://doi.org/10.1371/journal.pone.0110237

Blanchard P, Schurr F, Celle O, Cougoule N, Drajnudel P, Thiéry T, Faucon JP, Ribière M, 2008. First detection of Israeli acute paralysis virus (IAPV) in France, a dicistrovirus affecting honeybees (Apis mellifera). J Invertebr Pathol 99: 348-350. https://doi.org/10.1016/j.jip.2008.07.006

Botías C, Martín-Hernández R, Días J, García-Palencia P, Matabuena M, Juarranz A, Barrios L, Meana A, Nanetti A, Higes M, 2012. The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environ Microbiol 14 (4): 845-859. https://doi.org/10.1111/j.1462-2920.2011.02647.x

Brodschneider R, Crailsheim K, 2010. Nutrition and health in honey bees. Apidologie 41: 278-294. https://doi.org/10.1051/apido/2010012

Brooks WM (Ed), 1979. Induced epizootics: Protozoa. Workshop Proceedings Future Strategies in Pest Management Systems; Allen GE, Ignoffo C, Jaques R (eds), pp: 37-42. Gainesville FL, USA.

Cavigli I, Daughenbaugh KF, Martin M, Lerch M, Banner K, Garcia E, Brutscher LM, Flenniken ML, 2016. Pathogen prevalence and abundance in honey bee colonies involved in almond pollination. Apidologie 47: 251-266. https://doi.org/10.1007/s13592-015-0395-5

Cepero A, Ravoet J, Gómez-Moracho T, Bernal JL, Nozal MJ, Bartolomé C, Maside X, Meana A, González-Porto AV, deGraaf DC et al., 2014. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res Notes 7: 649. https://doi.org/10.1186/1756-0500-7-649

Chantawannakul P, Ward L, Boonham N, Brown M, 2006. A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in varroa mites collected from a Thai honeybee (Apis mellifera) apiary. J Invertebr Pathol 91: 69-73. https://doi.org/10.1016/j.jip.2005.11.001

Chen YP, Pettis JS, Collins A, Feldlaufer F, 2006. Prevalence and transmission of honeybee viruses. Appl Environ Microbiol 72: 606-611. https://doi.org/10.1128/AEM.72.1.606-611.2006

Chen YP, Siede R, 2007. Honey bee viruses. Adv Virus Res 70: 33-80. https://doi.org/10.1016/S0065-3527(07)70002-7

Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Brise T, Horning M, Geiser DM, et al., 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287. https://doi.org/10.1126/science.1146498

Dively GP, Embrey MS, Kamel A, Hawthorne DJ, Pettis JS, 2015. Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10 (3): e0118748. https://doi.org/10.1371/journal.pone.0118748

Dussaubat C, Sagastume S, Gómez-Moracho T, Botías C, García-Palencia P, Martín-Hernández R, Le Conte Y, Higes M, 2013. Comparative study of Nosema ceranae (Microsporidia) isolates from two different geographic origins. Vet Microbiol 162 (2-4): 670-678. https://doi.org/10.1016/j.vetmic.2012.09.012

Erdtman G, 1969. An introduction to the study of pollen grains and spores. Munksgaard, Copenhagen. 486 pp.

Faegri K, Iversen J, 1989. Textbook of pollen analysis. Blackwell Sci Publ, IV Ed. Munksgaard, Copenhagen.

FAO, 2008. Rapid assessment of pollinators' status: A contribution to the international initiative for the conservation and sustainable use of pollinators. Food and Agriculture Organization of the United Nations. http://www.fao.org/uploads/media/raps_2.pdf [13 March 2016].

Fenoy S, Rueda C, Higes M, Martín-Hernandez R, del Aguila C, 2009. High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl Environ Microbiol 75 (1): 6886-6889. https://doi.org/10.1128/AEM.01025-09

Fries I, 2010. Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103, Suppl 1: S73-79. https://doi.org/10.1016/j.jip.2009.06.017

García-Chao M, Agruña MJ, Sakkas V, Llompart M, Dagnac T, 2009.Validation of an off line spe lc-ms/ms method for the determination of systemic insecticide residues in honey and pollen samples collected in apiaries from Spain. Proc 4th Int Symp on Recent Advances in Food Analysis, Prague (Czech Republic), November 7-9.

Garrido-Bailón E, Martín-Hernández R, Botías C, Meana A, Prieto L, Higes M, 2009. New diagnostic method of Acarapis woodi a parasite of Apis mellifera L. by PCR-RFLPs. Prevalence of acarapisosis in Spain. Proc 41st Congress Apimondia, Montpellier (France).

Garrido-Bailón E, Martín-Hernández R, Meana A, Higes M, 2010a. Prevalence of Paenibacillus larvae, Melissococcus plutonius and Ascosphaera apis in Spain. Proc 4th Eur Conf of Apidologie (EURBEE). Meral Kence, (Turkey), 122 pp.

Garrido-Bailón E, Martín-Hernández R, Bernal J, Bernal JL, Martínez-Salvador A, Barrios L, Meana A, Higes M, 2010b. The detection of Israeli Acute Paralysis virus (IAPV), fipronil and imidacloprid in professional apiaries are not related with massive honey bee colony loss in Spain. Span J Agric Res 8 (3): 658-661. https://doi.org/10.5424/sjar/2010083-1262

González-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyorgyi H, Woyciechowski M, Vila M, 2013. Combined effects of global change pressures on animal mediated pollination. Trends Ecol Evol 28 (9): 524-530. https://doi.org/10.1016/j.tree.2013.05.008

Halm MP, Rortais A, Arnold G, Tasei JN, Rault S, 2006. New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). Environ Sci Technol 40: 2448-2454. https://doi.org/10.1021/es051392i

Higes M, Martin-Hernández R, Meana A, 2006. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92: 93-95. https://doi.org/10.1016/j.jip.2006.02.005

Higes M, Martín-Hernández R, Botías C, Garrido-Bailón E, González-Porto AV, Barrios L, del Nozal M, Bernal JL, Jiménez JJ, García P, Meana A, 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10: 2659-2669. https://doi.org/10.1111/j.1462-2920.2008.01687.x

Higes M, Martín-Hernández R, Garrido-Bailón E, González-Porto AV, García-Palencia P, Meana A, del Nozal MJ, Mayo R, Bernal JL, 2009. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Rep 1: 110-113. https://doi.org/10.1111/j.1758-2229.2009.00014.x

Higes M, Martín-Hernández R, Martínez-Salvador A, Garrido-Bailón E, González-Porto AV, Meana A, Bernal JL, del Nozal MJ, Bernal J, 2010a. A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ Microbiol Rep 2(2): 243-250. https://doi.org/10.1111/j.1758-2229.2009.00099.x

Higes M, Martín-Hernández R, Meana A, 2010b. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41: 375-392. https://doi.org/10.1051/apido/2010019

Higes M, Meana A, Bartolomé C, Botías C, Martín-Hernández R, 2013. Nosema ceranae (microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5: 17-29. https://doi.org/10.1111/1758-2229.12024

Huang Q, Kryger P, Le Conte Y, Moritz RF, 2012. Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J Invertebr Pathol 109(3): 297-302. https://doi.org/10.1016/j.jip.2012.01.004

Johnson RM, Ellis MD, Mullin CA, Frazier M, 2010. Pesticides and honey bee toxicity-USA. Apidologie 41: 312-331. https://doi.org/10.1051/apido/2010018

Le Conte Y, Navajas M, 2008. Climate change: impact on honey bee populations and diseases. Sci Techn Rev of the Office International des Epizooties 27: 499-510.

Lecocq A, Jensen AB, Kryger P, Nieh JC, 2016. Parasite infection accelerates age polyethism in young honey bees. Sci Rep 6: 22042. https://doi.org/10.1038/srep22042

Martín-Hernández R, Meana A, Prieto L, Martínez-Salvador A, Garrido-Bailon E, Higes M, 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73: 6331-6338. https://doi.org/10.1128/AEM.00270-07

Martín-Hernández R, Botías C, Bailón EG, Martínez-Salvador A, Prieto L, Meana A, Higes M, 2012. Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ Microbiol 14 (8): 2127-2138. https://doi.org/10.1111/j.1462-2920.2011.02645.x

McMullan JB, Brown MJ, 2009. A qualitative model of mortality in honey bee (Apis mellifera) colonies infested with tracheal mites (Acarapis woodi). Exp Appl Acarol 47 (3): 225-234. https://doi.org/10.1007/s10493-008-9213-3

Meeus I, de Graaf DC, Jans K, Smagghe G, 2010. Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109 (1): 107-115.

Moritz RFA, Erler S, 2016. Lost colonies found in a data mine: Global honey trade but not pests or pesticides as major cause of regional honeybee colony declines. Agric Ecosys Environ 216: 44-50. https://doi.org/10.1016/j.agee.2015.09.027

Mumford R, Barker I, Walsh K, Boonham N, 2000. The reliable detection of Potato mop-top and Tobacco rattle viruses directly from potato tubers, using a multiplex TaqMan® assay. Phytopathology 90: 1-6. https://doi.org/10.1094/PHYTO.2000.90.5.448

Nanetti A, Rodriguez-Garcia, C, Meana A, Martin-Hernandez R, Higes M, 2015. Effect of oxalic acid on Nosema ceranae infection. Res Vet Sci 102: 167-172. https://doi.org/10.1016/j.rvsc.2015.08.003

Naug D, 2009. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv 142: 2369-2372. https://doi.org/10.1016/j.biocon.2009.04.007

Nguyen BKC, Saegerman C, Pirad J, Mignon J, Widart B, Thirionet FJ, Verheggen D, Berkvens E, Haubruge E, 2009. Does imidacloprid seed-treated maize have an impact on honey bee mortality? J Econ Entomol 102: 616-623. https://doi.org/10.1603/029.102.0220

Ravoet J, Maharramov J, Meeus I, De Smet L, Wenseleers T, Smagghe G, de Graaf DC, 2013. Comprehensive Bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PloS One 8: e72443. https://doi.org/10.1371/journal.pone.0072443

Rosenkranz P, Aumeier P, Ziegelmann B, 2010. Biology and control of Varroa destructor. J Invert Pathol 103: S96-S119. https://doi.org/10.1016/j.jip.2009.07.016

Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, Andino R, DeRisi JL, 2011. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 6: e20656. https://doi.org/10.1371/journal.pone.0020656

Sánchez-Collado JG, Higes M, Barrio L, Martin-Hernandez R, 2014. Flow cytometry analysis of Nosema species to assess spore viability and longevity. Parasitol Res 113 (5): 1695-701. https://doi.org/10.1007/s00436-014-3814-z

Smirle MJ, Winston ML, Woodward KL, 1984. Development of a sensitive bioassay for evaluating sublethal pesticide effects on the honey bee (Hymenoptera: Apidae). J Econ Entomol 77: 63-67. https://doi.org/10.1093/jee/77.1.63

Staveley JP, Law SA, Fairbrother A, Menzie CA, 2014. A causal analysis of observed declines in managed honey bees (Apis mellifera). Hum Ecol Risk Assess 20: 566-591. https://doi.org/10.1080/10807039.2013.831263

Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F, Colin ME, Bergoin M, 2004. Prevalence and Seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 70: 7185-7191. https://doi.org/10.1128/AEM.70.12.7185-7191.2004

Thompson HM, Maus CH, 2007. The relevance of sublethal effects in honey bee testing for pesticide risk assessment. Pest Manag Sci 63: 1058-1061. https://doi.org/10.1002/ps.1458

Valdés B, Díez MJ, Fernández I, 1987. Atlas polínico de Andalucía Occidental. Instituto de Desarrollo Regional de la Universidad de Sevilla y Excma. Diputación de Cádiz, Sevilla.

Van der Zee R, Gómez-Moracho T, Pisa L, Sagastume S, García-Palencia P, Maside X, Bartolomé C, Martín-Hernández R, Higes M, 2014. Virulence and polar tube protein genetic diversity of Nosema ceranae (Microsporidia) field isolates from Northern and Southern Europe in honeybees (Apis mellifera iberiensis). Environ Microbiol Rep 6 (4): 401-413. https://doi.org/10.1111/1758-2229.12133

VanEngelsdorp D, Meixer MD, 2010. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 103: s80-s95. https://doi.org/10.1016/j.jip.2009.06.011

Villa JD, Bourgeois L, Danka RG, 2013. Negative evidence for effects of genetic origin of bees on Nosema ceranae, positive evidence for effects of Nosema ceranae on bees. Apidologie 44: 511-518. https://doi.org/10.1007/s13592-013-0201-1

Wolf S, McMahon DP, Lim KS, Pull CD, Clark SJ, Paxton RJ, Osborne JL, 2014. So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees. PloS One 9 (8): e103989. https://doi.org/10.1371/journal.pone.0103989

Yang X, Cox-Foster DL, 2005. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Nat Acad Sci USA 102 (21): 7470-7475. https://doi.org/10.1073/pnas.0501860102




DOI: 10.5424/sjar/2017151-9652