Reproductive parameters of female Varroa destructor and the impact of mating in worker brood of Apis mellifera

Alattal, Y., AlGhamdi, A., Single, A., Javed Ansari, M, Alkathiri, H. (2017) Fertility and reproductive rate of Varroa mite, Varroa destructor, in native and exotic honeybee, Apis mellifera L., colonies under Saudi Arabia conditions., Saudi Journal of Biological Sciences 24: 992-995, https://doi.org/10.1016/j.sjbs.2016.12.018

Alberti, G., Hänel, H. (1986) Fine structure of the genital system in the bee parasite, Varroa jacobsoni (Gamasida: Dermanyssina) with remarks on spermiogenesis, spermatozoa and capacitation. Exp. Appl. Acarol. 2, 63-104, https://doi.org/10.1007/BF01193355

Anderson, D. L., Trueman, J. W. H. (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. App. Acarol., 24(3), 165-189, https://doi.org/10.1023/A:1006456720416

Baldini, F., Gabrieli, P., South, A., Valim, C., Mancini, F., & Catteruccia, F. (2013) The interaction between a sexually transferred steroid hormone and a female protein regulates oogenesis in the malaria mosquito Anopheles gambiae. PLoS Biol, 11(10), e1001695, https://doi.org/10.1371/journal.pbio.1001695

Bruce, W.A., Chiesa, F., Marchetti, S., Griffiths, D.A. (1988) Laboratory feeding of Varroa jacobsoni Oudemans on natural and artificial diets (Acari: Varroidae). Apidologie 19 (2):209-218

De Ruijter, A. (1987) Reproduction of Varroa jacobsoni during successive brood cycles of the honeybee. Apidologie, 18 (4), 321-326

Dietemann, V., Nazzi, F., Martin, S.J., Anderson, D.L., Locke, B., Delaplane, K.S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., Ellis, J.D. (2013) Standard methods for Varroa research. J. Apicult. Res. 52(1). https://doi.org/10.3896/IBRA.1.52.1.09

Donzé, G., Guerin, P.M. (1994) Behavioral attributes and parental care of Varroa mites parasitizing honeybee brood. Behav. Ecol. Sociobiol. 34: 305–319

Donzé, G., Herrmann, M., Bachofen, B., Guerin, P.M. (1996) Effect of mating frequency and brood cell infestation rate on the reproductive success of the honeybee parasite Varroa jacobsoni. Ecol. Entomol. 21, 17-26, https://doi.org/10.1111/j.1365-2311.1996.tb00261.x

Frey, E., Odemer, R., Blum, T., Rosenkranz, P. (2013) Activation and interruption of the reproduction of Varroa destructor is triggered by host signals (Apis mellifera). J. Invertebr. Pathol. 113(1), 56-62, https://doi.org/10.1016/j.jip.2013.01.007

Fries I., Rosenkranz P. (1996) Number of reproductive cycles of Varroa jacobsoni in honey-bee (Apis mellifera) colonies. Exp. Appl. Acarol. 20(2): 103-112, https://doi.org/10.1007/BF00051156

Fries, I., Lindström, A., Rosenkranz, P., Frey, E., Odemer, R., Schroeder, A., de Miranda, J.R., Yanez, O., Paxton, R.J. (2011) The principal parasites and pathogenes of honeybees, Bees in Europe and Sustainable Honey Production, ISBN: 978-1-61209-336-9

Fuchs, S. (1994) Non-reproducing Varroa jacobsoni Oud. in honey bee worker cells—status of mites or effect of brood cells? Exp. Appl. Acarol., 18(5), 309-317, https://doi.org/10.1007/BF00132320

Garrido, C., Rosenkranz, P. (2003) The reproductive program of female Varroa destuctor mites is triggered by its host, Apis mellifera. Exp. Appl. Acarol., 31: 269-273, https://doi.org/10.1023/B:APPA.0000010386.10686.9f

Garrido, C., Rosenkranz, P. (2004) Volatiles of the honey bee larva initiate oogenesis in the parasitic mite Varroa destructor. Chemoecology 14: 193-197, https://doi.org/10.1007/s00049-004-0278-0

Garrido, C., Rosenkranz, P., Paxton, R., & Gonçalves, L. (2003) Temporal changes in Varroa destructor fertility and haplotype in Brazil. Apidologie 34(6), 535-541, https://doi.org/10.1051/apido:2003041

Genersch, E., Von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., Berg, S., Ritter, W., Mühlen, W., Gisder, S., Meixner, M., Liebig, G., 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, https://doi.org/10.1051/apido/2010014

Gunzman, L. I., Phokasem, P., Khongphinitbunjong, K., Frake, A. M., Chantawannakul, P. (2018) Successful reproduction of unmated Tropilaelaps mercedesae and its implication on mite population growth in Apis mellifera colonies. J. Invertebr. Pathol.153, 35-37, https://doi.org/10.1016/j.jip.2018.02.010

Harris, J. W., Harbo, J. R. (1999) Low sperm counts and reduced fecundity of mites in colonies of honey bees (Hymenoptera: Apidae) resistant to Varroa jacobsoni (Mesostigmata: Varroidae). J. Econ. Entomol. 92: 83-90, https://doi.org/10.1093/jee/92.1.83

Häußermann, C. K., Ziegelmann, B., Bergmann, P., Rosenkranz, P. (2015) Male mites (Varroa destructor) perceive the female sex pheromone with the sensory pit organ on the front leg tarsi. Apidologie 46(6), 771-778, https://doi.org/10.1007/s13592-015-0367-9

Häußermann, C. K., Ziegelmann, B., Rosenkranz, P. (2016) Spermatozoa capacitation in female Varroa destructor. Exp. Appl. Acarol., 69(4), 371-387, https://doi.org/10.1007/s10493-016-0051-4

Häußermann, C. K., Ziegelmann, B., Rosenkranz, P. (2018) Spermatozoa production in male Varroa destructor and its impact on reproduction in worker brood of Apis mellifera. Exp. Appl. Acarol., 74(1), 43-53, https://doi.org/10.1007/s10493-018-0216-4

Houck, M.A., OConnor, B.M. (1991) Ecological and evolutionary significance of phoresy in the Astigmata. Annu. Rev. Entomol. 36: 611-36, https://doi.org/10.1146/annurev.en.36.010191.003143

Human, H., Brodschneider, R., Dietemann, V., Dively, G., Ellis, J. D., Forsgren, E., Fries, I., Hatjina, F., Hu, F., Jaffé, R., Bruun Jensen, A., Köhler, A., Magyar, J.P., Özkýrým, A., Prik, C., Rose, R., Strauss, U., Tanner, G., Tarpy, D., van der Steen, J., Vaudo, A., Vesnæs, F., Wilde, J., Williams, G., Zheng, H. (2013) Miscellaneous standard methods for Apis mellifera research. J. Apicult. Res., 52(4), 1-53, https://doi.org/10.3896/IBRA.1.52.4.10

Jagersbacher-Baumann, J., Ebermann, E. (2012) Methods for rearing scutacarid mites (Acari, Heterostigmatina) and the influence of laboratory cultures on morphometric variables. Exp. Appl. Acarol., https://doi.org/10.1007/s10493-012-9621-2

Jones, L.D., Davies, C.R., Steele, G.M., Nuttall, P.A. (1988) The rearing and maintenance of ixodid and argasid ticks in the laboratory. Anim. Tech. 39 (2):99-106

Kirrane, M.J., De Guzman, L., Rinderer, T.E., Frake, A.M., Wagnitz, J., Whelan, P.M. (2011) Asynchronous development of honey bee host and Varroa destructor (Mesostigmata: Varroidae) influences reproductive potential of mites. Jour. Econ. Entom., Volume 104, Issue 4, p. 1146-1152, https://doi.org/10.1603/EC11035

Kiszewski, A.E., Matuschka, F-R., Spielmann, A. (2001) Mating strategies and spermiogenesis in ixodid ticks. Annu. Rev. Entomol. 46:167-82, https://doi.org/10.1146/annurev.ento.46.1.167

Locke, B., Fries, I. (2011) Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie, 42(4), 533-542, https://doi.org/10.1007/s13592-011-0029-5

Martin, S.J. (1994) Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Exp. Appl. Acarol. 18, 87-100, https://doi.org/10.1007/BF00055033

Martin, S.J. (1995) Ontogenesis of the mite Varroa jacobsoni Oud. in drone brood of the honeybee Apis mellifera L. under natural conditions. Exp. Appl. Acarol. 19, 199–210, https://doi.org/10.1007/BF00130823

Martin, S.J., Kemp, D. (1997) Average number of reproductive cycles performed by Varroa jacobsoni in honey bee (Apis mellifera) colonies. J. Apicult. Res. 36:113-123, https://doi.org/10.1080/00218839.1997.11100937

Martin, S., Holland, K., Murray, M. (1997) Non-reproduction in the honeybee mite Varroa jacobsoni. Exp. Appl. Acarol. 21(8), 539-549, https://doi.org/10.1023/A:1018492231639

McCulloch, J. B., Owen, J. P. (2012) Arrhenotoky and oedipal mating in the northern fowl mite (Ornithonyssus sylviarum) (Acari: Gamasida: Macronyssidae), Parasites & Vectors 5:281, https://doi.org/10.1186/1756-3305-5-281

Mondet, F., Rau, A., Klopp, C., Rohmer, M., Severac, D., Le Conte, Y., Alaux, C. (2018) Transcriptome profiling of the honeybee parasite Varroa destructor provides new biological insights into the mite adult life cycle. BMC Genomics 19: 328, https://doi.org/10.1186/s12864-018-4668-z

Nazzi, F., Milani, N. (1994) A technique for reproduction of Varroa jacobsoni Oud under laboratory conditions. Apidologie 25:579-584, https://doi.org/10.1051/apido:19940608

Oliver, J.H. (1971) Parthenogenesis in mites and ticks (Arachnida: Acari). Am. Zoologist, 11:283-299, https://doi.org/10.1093/icb/11.2.283

Ramsey, S., Gulbronson, C.J., Mowery, J., Ochoa, R., vanEngelsdrop, D., Bauchan, G. (2019a) A multi-microscopy approach to discover the feeding site and host tissue consumed by Varroa destructor on host honey bees. Proceedings of Microscopy & Microanalysis, Volume 24, pp. 1258-1259, https://doi.org/10.1017/S1431927618006773

Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., Lim, D., Joklik, J., Cicero, J.M., Ellis, J.D., Hawthorne, D., vanEngelsdorp, D. (2019b) Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116(5), 1792-1801, https://doi.org/10.1073/pnas.1818371116

Rosenkranz, P. (1999) Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America. Apidologie 30, 159-172, https://doi.org/10.1051/apido:19990206

Rosenkranz, P., Engels, W. (1994) Infertility of Varroa jacobsoni females after invasion into Apis mellifera worker brood as a tolerance factor against varroatosis. Apidologie 25, 402-402, https://doi.org/10.1051/apido:19940407

Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010) Biology and control of Varroa destructor. J. Invertrebr. Pathol. 103, 96-119, https://doi.org/10.1016/j.jip.2009.07.016

Sabelis, M. W., & Nagelkerke, C. J. (1988) Evolution of pseudo-arrhenotoky. Experimental and Applied Acarology, 4(3), 301-318, https://doi.org/10.1007/BF01196192

Tabart, J., Colin, M-E., Carayon, J-L., Tene, N., Payre, B., Vetillard, A. (2013) Artificial feeding of Varroa destructor through a chitosan membrane: a tool for studying the host-microparasite relationship. Exp. Appl. Acarol. 61: 107-118, https://doi.org/10.1007/s10493-013-9675-9

Tuan, S.-J., Lin, Y.-H., Yang, C.-M., Atlihan, R., Saska, P., Chi, H. (2016) Survival and reproductive strategies in two-spotted spider mites: Demographic analysis of arrhenotokous parthenogenesis of Tetranychus urticae (Acari: Tetranychidae), J. Econ. Entomol., 1-8, https://doi.org/10.1093/jee/tov386

Weller, S. (2008): Populationsdynamik der parasitsichen Bienenmilbe Varroa destructor in vorselektierten Bienenvölkern (A. mellifera L.) unter besonderer Berücksichtigung der Reproduktion, Diplomarbeit der Landesanstalt für Bienenkunde, Universität Hohenheim, Stuttgart

Wendling, S., Guillet, B., Roy, L., Kreiter, S., Colin, M. E. (2014) Fertilization and fertility in the female of Varroa destructor, a key point for the parasite population dynamics. Apidologie, 45(6), 722-732, https://doi.org/10.1007/s13592-014-0291-4

Wolfner, M. F. (2009) Battle and ballet: molecular interactions between the sexes in Drosophila. J. Hered., 100(4), 399-410, https://doi.org/10.1093/jhered/esp013

Xie, X., Huang, Z.Y., Zeng, Z. (2016) Why do Varroa mites prefer nurse bees? Scientific Reports, https://doi.org/10.1038/srep28228

Xu, G., Wu, H., Huan, Z., Mo, G., Wan, M. (2001) Study on the reproductive characteristics of rice tarsonemid mite, Steneotarsonmus spinki Smiley (Acari: Tarsonemidae) Sys. Appl. Acarol. 6, 45-49, https://doi.org/10.11158/saa.6.1.7

Ziegelmann, B., Rosenkranz, P. (2014) Mating disruption of the honeybee mite Varroa destructor under laboratory and field conditions. Chemoecology. doi:https://doi.org/10.1007/s00049-014-0155, https://doi.org/10.1007/s00049-014-0155-4

Ziegelmann, B., Lindenmayer, A., Steidle, J., Rosenkranz, P. (2013a) The mating behavior of Varroa destructor is triggered by a female sex pheromone. Apidologie 44, 314-323, https://doi.org/10.1007/s13592-012-0182-5

Ziegelmann, B., Tolasch, T., Steidle, J.L.M., Rosenkranz, P. (2013b) The mating behavior of Varroa destructor is triggered by a female sex pheromone. Part 2: Identification and dose-dependent effects of components of the Varroa sex pheromone. Apidologie 44, 481-490, https://doi.org/10.1007/s13592-013-0198-5