Genetic diversity and prevalence of Varroa destructor, Nosema apis, and N. ceranae in managed honey bee (Apis mellifera) colonies in the Caribbean island of Dominica, West Indies

References

• Aizen, M. A., & Harder, L. D. (2009). The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology, 19(11), 915–918. doi:10.1016/j.cub.2009.03.071
   PubMed Web of Science ®Google Scholar
• Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A., & Omholt, S. W. (2004). Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering? Journal of Economic Entomology, 97(3), 741–747. doi: 10.1093/jee/97.3.741
   PubMed Web of Science ®Google Scholar
• Anderson, D. L., & Giacon, H. (1992). Reduced pollen collection by honey bee (Hymenoptera, Apidae) colonies infected with Nosema apis and sacbrood virus. Journal of Economic Entomology, 85, 47–51. doi:10.1093/jee/85.1.47
   Web of Science ®Google Scholar
• Aronstein, K., & Douglas, A. (2012). Lessons learned by the managed pollinator CAP: Impacts of varroa parasitism on honey bee health. American Bee Journal, 152, 790–798.
   Google Scholar
• Bailey, L. (1981). Honey bee pathology (124 pp.).London, UK: Academic Press.
   Google Scholar
• Bailey, L., & Ball, B. V. (1991). Honey bee pathology (2nd ed., 208 pp.).London, UK: Academic Press.
   Google Scholar
• Boecking, O., & Genersch, E. (2008). Varroosis – the ongoing crisis in beekeeping. Journal für Verbraucherschutz und Lebensmittelsicherheit, 3, 221–228. doi: 10.1007/s00003-008-0331-y
   Web of Science ®Google Scholar
• Bravo, J., Carbonell, V., Valdebenito, J. T., Figueroa, C., Valdovinos, C. E., Martín-Hernández, R., …, Delporte, C. (2014). Identification of Nosema ceranae in the Valparaíso District, Chile. Archivos de Medicina Veterinaria, 46, 487–491. doi: 10.4067/S0301-732X2014000300021
   Google Scholar
• Breed, M. D., Guzmán-Novoa, E., & Hunt, G. J. (2004). Defensive behavior of honey bees: Organization, genetics, and comparisons with other bees. Annual Review of Entomology, 49, 271–298. doi: 10.1146/annurev.ento.49.061802.123155
   PubMed Web of Science ®Google Scholar
• Calderón, R. A., Sánchez, L. A., Yañez, O., & Fallas, N. (2008) Presence of Nosema ceranae in Africanized honey bee colonies in Costa Rica. Journal of Apicultural Research, 47(4), 328–329.doi: 10.1080/00218839.2008.11101485
   Web of Science ®Google Scholar
• Cantwell, G. E. (1970). Standard methods for counting Nosema spores. American Bee Journal, 110(6), 22–223.
   Google Scholar
• Chen, Y., Evans, J. D., Smith, I. B., & Pettis, J. S. (2008). Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology, 97, 186–188. doi: 10.1016/j.jip.2007.07.010
   PubMed Web of Science ®Google Scholar
• Chen, Y., Pettis, J. S., Evans, J. D., Kramer, M., & Feldlaufer, M. F. (2004). Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor. Apidologie, 35, 441–448. doi: 10.1051/apido:2004031
   Web of Science ®Google Scholar
• Clarke, K. E., Rinderer, T. E., Franck, P. P., Quezada-Euán, J. G., & Oldroyd, B. (2002). The Africanization of honeybees (Apis mellifera L.) of the Yucatan: A study of a massive hybridization event across time. Evolution, 56(7), 1462–1474.
   PubMed Web of Science ®Google Scholar
• Cox, B. (1994). AHB in Puerto Rico. American Bee Journal, 134(10), 668–669.
   Google Scholar
• Crane, E. E. (1999). The world history of beekeeping and honey hunting (682 pp.). Cardiff, UK: International Bee Research Association.
   Google Scholar
• Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D., Locke, B., Delaplane, K. S., …, Ellis, J. D. (2013). Standard methods for varroa research. In V. Dietemann, J. D. Ellis & P. Neumann (Eds), The COLOSS BEEBOOK, Volume II: standard methods for Apis mellifera pest and pathogen research. Journal of Apicultural Research, 52(1),doi: 10.3896/IBRA.1.52.1.09
   PubMed Web of Science ®Google Scholar
• Duay, P., De Jong, D., & Engels, W. (2003). Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie, 34, 61–65. doi: 10.1051/apido:2002052
   Web of Science ®Google Scholar
• Forsgren, E., & Fries, I. (2013). Temporal study of Nosema spp. in a cold climate. Environmental Microbiology Reports, 5, 78–82. doi: 10.1111/j.1758-2229.2012.00386.x
   PubMed Web of Science ®Google Scholar
• Fries, I. (1997). Protozoa. In R. A. Morse & K. Flottum (Eds.). Honey bee pests, predators and diseases (pp. 59–76). Medina, OH: A I Root Company.
   Google Scholar
• Fries, I. (1993). Nosema apis – A parasite in the honey bee colony. Bee World, 74(1), 5–19.doi: 10.1080/0005772X.1993.11099149
   Web of Science ®Google Scholar
• Fries, I., Feng, F., Da Silva, A., Slemenda, B., & Pieniakzek, J. (1996). Nosema ceranae n. sp. (Microspora, Nosematidae). Morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis ceranae (Hymenoptera, Apidae). European Journal of Protistology, 32, 356–365. doi:10.1016/S0932-4739(96)80059-9
   Web of Science ®Google Scholar
• Fries, I., Imdorf, A., & Rosenkranz, P. (2006). Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie, 37, 564–570. doi:10.1051/apido:2006031
   Web of Science ®Google Scholar
• Galindo-Cardona, A., Acevedo-Gonzalez, J. P., Rivera-Merchand, B., & Tugrul, G. (2013). Genetic structure of the gentle Africanized honey bee population (gAHB) in Puerto Rico. BMC Genetics, 14, 65. doi:10.1186/1471-2156-14-65
   PubMed Web of Science ®Google Scholar
• Gallai, N., Salles, J.-M., Settele, J., & Vaissière, B. E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Entomology, 68, 810–821. doi:10.1016/j.ecolecon.2008.06.014
   Web of Science ®Google Scholar
• Garedew, A., Schmolz, E., & Lamprecht, I. (2004). The energy and nutritional demand of the parasitic life of the mite Varroa destructor. Apidologie, 35, 419–430. doi:10.1051/apido:2004032
   Web of Science ®Google Scholar
• Garnery, L., Cornuet, J. M., & Solignac, M. (1992). Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Molecular Ecology, 1(3), 145–154. doi:10.1111/j.1365-294X.1992.tb00170.x
   PubMed Web of Science ®Google Scholar
• Garnery L., Franck, P., Baudry, E., Vautrin, D., Cornuet, J.-M., & Solignac, M. (1998). Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica) I. Mitochondrial DNA. Genetics Selection Evolution, 30 (Suppl), S31–S47. doi:10.1186/1297-9686-30-S1-S31
   Google Scholar
• Garnery, L., Solignac, M., Celebrano, G., & Cornuet, J. M. (1993). A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia, 49(11), 1016–1021. doi:10.1007/BF02125651
   Google Scholar
• Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology, 87, 87–97. doi:10.1007/s00253-010-2573-8
   PubMed Web of Science ®Google Scholar
• Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., …, Rosenkranz, P. (2010). The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41, 332–352. doi:10.1051/apido/2010014
   Web of Science ®Google Scholar
• Giacobino, A., Molineri, A., Cagnolo, N. B., Merke, J., Orellano, E., Bertozzi, E., …, Signorini, M. (2015). Risk factors associated with failures of varroa treatments in honey bee colonies without broodless period. Apidologie, 46 (5), 573–582. doi:10.1007/s13592-015-0347-0
   Web of Science ®Google Scholar
• Giersch, T., Berg, T., Galea, F., & Hornitzky, M. (2009). Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie, 40, 117–123. doi:10.1051/apido/2008065
   Web of Science ®Google Scholar
• Gisder, S., Hedtke, K., Möckel, N., Frielitz, M.-C., Linde, A., & Genersch, E. (2010). Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Applied Environmental Microbiology, 76, 3032–3038. doi:10.1128/AEM.03097-09
   PubMed Web of Science ®Google Scholar
• Guzmán-Novoa, E., Eccles, L., Calvete, Y., Mcgowan, J., Kelly, P. G., & Correa Benitez, A. (2010). Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie, 41, 443–450. doi: 10.1051/apido/2009076
   Web of Science ®Google Scholar
• Hassanein, M. H. (1953). The influence of Nosema apis on the larval honey bee. Annals of Applied Biology, 38, 844–846.
   Web of Science ®Google Scholar
• Higes, M., Martin, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honey bees in Europe. Journal of Invertebrate Pathology, 92, 93–95. doi:10.1016/j.jip.2006.02.005
   PubMed Web of Science ®Google Scholar
• Higes, M., Martin-Hernandez, R., Botias, C., Garrido-Bailon, E., Gonzalez-Porto, A. V., Nozal, M. J. D., …, Meana, A. (2008). How natural infection by Nosema ceranae causes honey bee colony collapse. Environmental Microbiology, 10, 2659–2669. doi:10.1111/j.1462-2920.2008.01687.x
   PubMed Web of Science ®Google Scholar
• Higes, M., Martin-Hernandez, R., Garrido-Bailon, E., Botias, C., & Meana, A. (2009). The presence of Nosema ceranae (Microsporidia) in North African honey bees (Apis mellifera intermissa). Journal of Apicultural Research, 48(3), 217–219.doi: 10.3896/IBRA.1.48.3.12
   Web of Science ®Google Scholar
• Horn, T. (2006). Bees in America: How the honey bee shaped a nation (352 pp.). Lexington, KY: University Press of Kentucky.
   Google Scholar
• Invernizzi, C., Abud, C., Tomasco, I. H., Harriet, J., Ramallo, G., Campa, J., …, Mendoza, Y. (2009). Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay . Journal of Invertebrate Pathology, 101, 150–153. doi: 10.1016/j.jip.2009.03.006
   PubMed Web of Science ®Google Scholar
• Kerr, W. E. (1967). The history of the introduction of African bees to Brazil. South African Bee Journal, 39, 3–5.
   Google Scholar
• Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., …, Paxton, R.J. (2007). Wide-spread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96, 1–10. doi:10.1016/j.jip.2007.02.014
   PubMed Web of Science ®Google Scholar
• Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunnigham, S. A., Kremen, C., Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B Biological Sciences, 274, 303–313. doi:10.1098/rspb.2006.3721
   PubMed Web of Science ®Google Scholar
• Korpela, S., Aarhus, A., Fries, I., & Hansen, H. (1992). Varroa jacobsoni Oud. in cold climates: Population growth, winter mortality and influence on the survival of honey bee colonies. Journal of Apicultural Research, 31(3–4), 157–164.doi: 10.1080/00218839.1992.11101278
   Web of Science ®Google Scholar
• Macedo, P. A., Wu, J., & Ellis, M. D. (2002). Using inert dusts to detect and assess varroa infestations in honey bee colonies. Journal of Apicultural Research, 41(1–2), 3–7.doi: 10.1080/00218839.2002.11101062
   Web of Science ®Google Scholar
• Malone, L. A., Giacon, H. A., & Newton, M. R. (1995). Comparison of the responses of some New Zealand and Australian honey bees (Apis mellifera L) to Nosema apis Z. Apidologie, 26, 495–502. doi:10.1051/apido:19950606
   Web of Science ®Google Scholar
• Matheson, A. (1993). World bee health report. Bee World, 74, 176–212. doi:10.1080/0005772X.1993.11099183
   Web of Science ®Google Scholar
• Martin-Hernandez, R., Botias, C., Bailon, E. G., Martinez-Salvador, A., Prieto, L., Meana, A., & Higes, M. (2012). Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environmental Microbiology, 14, 2127–2138. doi:10.1111/j.1462-2920.2011.02645.x
   PubMed Web of Science ®Google Scholar
• Martin-Hernandez, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailon, E., & Higes, M. (2007). The outcome of the colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73, 6331–6338. doi:10.1128/AEM.00270-07
   PubMed Web of Science ®Google Scholar
• Medici, S. K., Sarlo, E. G., Porrini, M. P., Braunstein, M., & Eguaras, M. J. (2012). Genetic variation and widespread dispersal of Nosema ceranae in Apis mellifera apiaries from Argentina. Parasitology Research, 110, 859–864. doi:10.1007/s00436-011-2566-2
   PubMed Web of Science ®Google Scholar
• Meixner, M. D., Francis, R. M., Gajda, A., Kryger, P., Andonov, S., Uzunov, A., et al. (2014). Occurrence of parasites and pathogens in honey bee colonies used in a European genotype-environment interactions experiment. Journal of Apicultural Research, 53(2), 215–229.doi: 10.3896/IBRA.1.53.2.04
   Web of Science ®Google Scholar
• Mondet, F., de Miranda, J. R., Kretzschmar, A., Le Conte, Y., & Mercer, A. R. (2014). On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathogens, 10(8), e1004323. doi:10.1371/journal.ppat.1004323
   PubMed Web of Science ®Google Scholar
• Mulholland, G., Traver, B., Johnson, N., & Fell, R. (2012). Individual variability of Nosema ceranae infections in Apis mellifera colonies. Insects, 3(4), 1143–1155. doi:10.3390/insects3041143
   PubMedGoogle Scholar
• Pacini, A., Mira, A., Molineri, A., Giacobino, A., Bulacio Cagnolo, N., Aignasse, A., …, Signorini, M. (2016). Distribution and prevalence of Nosema apis and N. ceranae in temperate and subtropical eco-regions of Argentina. Journal of Invertebrate Pathology, 141, 34–37. doi:10.1016/j.jip.2016.11.002
   PubMed Web of Science ®Google Scholar
• Paxton, R., Klee, J., Korpela, 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. doi:10.1051/apido:2007037
   Web of Science ®Google Scholar
• Rangel, J., Baum, K., Rubink, W. L., Coulson, R. N., Johnston, J. S., & Traver, B. E. (2015). Prevalence of Nosema species in a feral honey bee population: A 20-year survey. Apidologie, 47, 561–571. doi:10.1007/s13592-015-0401-y
   Web of Science ®Google Scholar
• Rangel, J., Traver, B. E., Stevens, G., Howe, M., & Fell, R. D. (2013). Survey for Nosema spp. in Belize apiaries. Journal of Apicultural Research, 52(2), 62–66.doi: 10.3896/IBRA.1.52.2.12
   Web of Science ®Google Scholar
• Rinderer, T. E., & Sylvester, H. A. (1978). Variation in response to Nosema apis, longevity, and hoarding behavior in a free-mating population of the honey bee. Annals of the Entomological Society of America, 71, 372–374. doi:10.1093/aesa/71.3.372
   Web of Science ®Google Scholar
• Rivera-Marchand, B. (2006). Africanized Bees in Puerto Rico (100 pp.). PhD thesis. University of Puerto Rico, Río Piedras.
   Google Scholar
• Rivera-Marchand, B., Keularts, J., Oskay, D., & Giray, T. (2008). Coexistence of feral Africanized and European honey bees (Hymenoptera: Apoidea: Apidae) on St. Croix Island. Caribbean Journal of Science, 44(2), 264–266. doi:10.18475/cjos.v44i2.a18
   Web of Science ®Google Scholar
• Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, 96–119. doi:10.1016/j.jip.2009.07.016
   PubMed Web of Science ®Google Scholar
• Sanford, M. T. (1996). What of the Africanized honey bee? APIS, 14(9), 1.
   Google Scholar
• Schneider, S. S., DeGrandi-Hoffman, G., & Smith, D. R. (2004). The African honey bee: Factors contributing to a successful invasion. Annual Review of Entomology, 49, 351–376. doi:10.1146/annurev.ento.49.061802.123359
   PubMed Web of Science ®Google Scholar
• Sheppard, W. S. (1989). A history of the introduction of honey bee races into the United States. American Bee Journal, 129, 617–619.
   Google Scholar
• Smith, K. M., Loh, E. H., Rostal, M. K., Zambrana-Torrelio, C. M., Mendiola, L., & Daszak, P. (2013). Pathogens, pests, and economics: drivers of honey bee colony declines and losses. Ecohealth, 10(4), 434–445. doi:10.1007/s10393-013-0870-2
   PubMed Web of Science ®Google Scholar
• Teixeira, E. W., Dos Santos, L. G., Sattler, A., Message, D., Alves, M. L., Martins, M. F., …, Francoy, T.M. (2013). Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology, 114, 250–254. doi:10.1016/j.jip.2013.09.002
   PubMed Web of Science ®Google Scholar
• Traver, B. E., & Fell R.D. (2011). Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology, 107(1), 43–49. doi:10.1016/j.jip.2011.02.003
   PubMed Web of Science ®Google Scholar
• Traynor, K. S., Rennich, K., Forsgren, E., Rose, R., Pettis, J., Kunker, G., …, vanEngelsdorp, D. (2016). Multiyear survey targeting disease incidence in US honey bees. Apidologie, 47, 325–347. doi:10.1007/s13592-016-0431-0
   Web of Science ®Google Scholar
• Vetharaniam, I. (2012). Predicting reproduction rate of Varroa. Ecological Modelling, 224, 11–17. doi:10.1016/j.ecolmodel.2011.10.016
   Web of Science ®Google Scholar
• Wang, D. I., & Moeller, F. E. (1970). The division of labor and queen attendance behaviour of Nosema-infected worker honey bees. Journal of Economic Entomology, 63, 1539–1541. doi:10.1093/jee/63.5.1539
   Web of Science ®Google Scholar
• Wannarka, M. (2016). Honey bee plants in Grenada, eastern Caribbean. Peace Corps Manual. Retrieved June 2, 2017, from http://teca.fao.org/resource/honey-bee-plants-grenada-eastern-caribbean.
   Google Scholar
• Whitfield, C. W., Behura, S. K., Berlocher, S. H., Clark, A. G., Johnston, J. S., Sheppard, W. S., …, Tsutsui, N.D. (2007). Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science, 314, 642–645. doi:10.1126/science.1132772
   Web of Science ®Google Scholar
• Wilkinson, D., & Smith, G. C. (2002). A model of the mite parasite, Varroa destructor, on honeybees (Apis mellifera) to investigate parameters important to mite population growth. Ecological Modelling, 148, 263–275. doi:10.1016/S0304-3800(01)00440-9
   Web of Science ®Google Scholar
• Williams, G., Shafer, R. E. L., Rogers, D., & Shutler, D. (2008). First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. Journal of Invertebrate Pathology, 97(2), 189–192.
   PubMed Web of Science ®Google Scholar