Olfaction as a Target for Control of Honeybee Parasite Mite Varroa destructor

  • Victoria SorokerEmail author
  • Nitin Kumar Singh
  • Nurit Eliash
  • Erika Plettner


The mite Varroa destructor Anderson & Trueman (Acari: Varroidae) is a major global threat to the European honeybee Apis mellifera. The mite is an obligatory ectoparasite. It feeds on the hemolymph of bees and also serves as an active vector for pathogenic viruses, which have become more abundant and virulent since the invasion of the mite. The Varroa life cycle is tightly linked to that of a honeybee. The cycle can be generally divided into two main phases: a reproductive phase, in which the female Varroa parasitizes bee pupae and reproduce within sealed brood cells, and a phoretic phase, in which it parasitizes adult bees. Between these phases Varroa mites can wander on comb surfaces. Hive volatiles, mainly from adult bees and brood, play a crucial role in the parasite’s life cycle, by guiding host finding, selection and regulating its reproduction suggesting that the mite’s olfaction may be an important target for new specific control agents. This concept was proven with some synthetic volatile compounds. Inhibition of host sensing leads to incorrect Varroa host selection or reduction in mite’s ability to reach a host. Although the mode of action of these compounds is not yet clear, this approach seems promising towards an integrated and sustainable control over this major apicultural pest.



The authors gratefully acknowledge funding from the Natural Sciences and Engineering Research Council (NSERC) of Canada (Discovery grants # 477793-2015, 222923-2010 and Strategic Project grant # 396484-10 to EP) and from Chief Scientist of the Israeli Ministry of Agriculture grant #131-1815 and Israel Science Foundation Grant (No. 1652/14) to VS, and to Dan Eliash for the drawing of Fig. 6.1 and the illustration for Box 6.1.


  1. Akhtar Y, Isman MB, Paduraru PM, Nagabandi S, Nair R, Plettner E (2007) Screening of dialkoxybenzenes and disubstituted cyclopentene derivatives against the cabbage looper, Trichoplusia ni, for the discovery of new feeding and oviposition deterrents. J Agric Food Chem 55:10323–10330CrossRefPubMedGoogle Scholar
  2. Akhtar Y, Yu Y, Isman MB, Plettner E (2010) Dialkoxybenzene and dialkoxyallylbenzene feeding and oviposition deterrents against the cabbage looper, Trichoplusia ni: potential insect behavior control agents. J Agric Food Chem 58:4983–4991CrossRefPubMedGoogle Scholar
  3. Alaux C, Le Conte Y, Adams HA, Rodriguez-Zas S, Grozinger CM, Sinha S, Robinson GE (2009) Regulation of brain gene expression in honey bees by brood pheromone. Genes Brain Behav 8:309–319CrossRefPubMedGoogle Scholar
  4. Allan S (2010) Chemical ecology of tick-host interactions. In: Takken W, Knols B (eds) Ecology and control of vector-borne disease, Volume 2 Olfaction in vector-host interactions. Wageningen Academic Publishers, Wageningen, pp 327–348Google Scholar
  5. Axtell R, Foelix R, Coons L, Roshdy M (1971) Sensory receptors in ticks and mites. In: Proceedings of the 3rd International Congress Acarology held Prague (Czechoslovakia), August 31–September 6, pp 35–40Google Scholar
  6. Beaurepaire AL, Truong TA, Fajardo AC, Dinh TQ, Cervancia C, Moritz RFA (2015) Host specificity in the honeybee parasitic mite, Varroa spp. in Apis mellifera and Apis cerana. PLoS One 10:e0135103CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bjostad L (2000) Electrophysiological methods. In: Millar J, Haynes K (eds) Methods in chemical ecology, chemical methods. Kluwer Academic Publishers, Boston/Dordrecht/London, pp 339–369Google Scholar
  8. Boot WJ (1994) Methyl palmitate does not elicit invasion of honeybee brood cells by Varroa mites. Exp Appl Acarol 18:587–592CrossRefGoogle Scholar
  9. Boot WJ, Calis JNM, Beetsma J (1993) Invasion of Varroa jacobsons into honey bee brood cells: a matter of chance or choice? J Apic Res 32:167–174CrossRefGoogle Scholar
  10. Breed MD, Guzmán-Novoa E, Hunt GJ (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271–298CrossRefPubMedGoogle Scholar
  11. Cabrera Cordon AR, Shirk PD, Duehl AJ, Teal PEA (2013) Variable induction of vitellogenin genes in the varroa mite, Varroa destructor (Anderson & Trueman), by the honeybee, Apis mellifera L, host and its environment. Insect Mol Biol 22:88–103CrossRefPubMedGoogle Scholar
  12. Calderone NW, Lin S (2001) Behavioural responses of Varroa destructor (Acari: Varroidae) to extracts of larvae, cocoons and brood food of worker and drone honey bees, Apis mellifera (Hymenoptera: Apidae). Physiol Entomol 26:341–350CrossRefGoogle Scholar
  13. Carneiro FE, Torres RR, Strapazzon R, Ramírez SA, Guerra CV Jr, Kolling DF, Moretto G (2007) Changes in the reproductive ability of the mite Varroa destructor (Anderson e Trueman) in africanized honey bees (Apis mellifera L.) (Hymenoptera: Apidae) colonies in southern Brazil. Neotrop Entomol 36:949–952CrossRefPubMedGoogle Scholar
  14. Castillo C, Chen H, Graves C, Maisonnasse A, Le Conte Y, Plettner E (2012) Biosynthesis of ethyl oleate, a primer pheromone, in the honey bee (Apis mellifera L.). Insect Biochem Mol Biol 42:404–416CrossRefPubMedGoogle Scholar
  15. Cervo R, Bruschini C, Cappa F, Meconcelli S, Pieraccini G, Pradella D, Turillazi S (2014) High Varroa mite abundance influences chemical profiles of worker bees and mite-host preferences. J Exp Biol 217:2998–3001CrossRefPubMedGoogle Scholar
  16. Chipman AD et al (2014) The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. PLoS Biol 12:e1002005CrossRefPubMedPubMedCentralGoogle Scholar
  17. Corrêa-Marques MH, Medina LM, Martin SJ, De Jong D (2003) Comparing data on the reproduction of Varroa destructor. Genet Mol Res Genet Mol Res Genet Mol Res 2:1–6PubMedGoogle Scholar
  18. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6:e1001064CrossRefPubMedPubMedCentralGoogle Scholar
  19. Currie RW, Gatien P (2006) Timing acaricide treatments to prevent Varroa destructor (Acari: Varroidae) from causing economic damage to honey bee colonies. Can Entomol 138:238–252CrossRefGoogle Scholar
  20. De Bruyne M, Guerin PM (1998) Contact chemostimuli in the mating behaviour of the cattle tick, Boophilus microplus. Arch Insect Biochem Physiol 39:65–80CrossRefPubMedGoogle Scholar
  21. De Miranda J, Chen Y, Ribiere M, Gauthier L (2011) Varroa and viruses. In: Carreck N (ed) Varroa, still a problem in the 21st century? The International Bee Research Association, Cardiff, pp 11–32Google Scholar
  22. Del Piccolo F, Nazzi F, Della Vedova G, Milani N (2010) Selection of Apis mellifera workers by the parasitic mite Varroa destructor using host cuticular hydrocarbons. Parasitology 137:967–973CrossRefPubMedGoogle Scholar
  23. Dillier F, Fluri P, Guerin PM (2001) Die Varroamilbe riecht mit den Beinen. Schweiz Bienen-Ztg 124:28–31Google Scholar
  24. Dillier F, Fluri P, Imdorf A (2006) Review of the orientation behaviour in the bee parasitic mite Varroa destructor: sensory equipment and cell invasion behavior. Rev Suisse Zool 113:857–877CrossRefGoogle Scholar
  25. Dong X, Kashio M, Peng G et al (2016) Isoform-specific modulation of the chemical sensitivity of conserved TRPA1 channel in the major honeybee ectoparasitic mite, Tropilaelaps mercedesae. Open Biol 6:387–417CrossRefGoogle Scholar
  26. Donzé G, Herrmann M, Bachofen B, Guerin PM (1994) Effect of mating frequency and brood cell infestation rate on the reproductive success of the honeybee parasite Varroa jacobsoni. Ecol Entomol 21:17–26CrossRefGoogle Scholar
  27. Donzé G, Schnyder-Candrian S, Bogdanov S, Gurein P, Kilchenman V, Diehl P Monachon F (1998) Aliphatic alcohols and aldehydes of the honey bee cocoon induce arrestment behavior in Varroa destructor (Acari: Mesostigmata), an Ectoparasite of Apis mellifera. Arch Insect Biochem Physiol 37:129–145CrossRefGoogle Scholar
  28. Eliash N, Singh NK, Kamer Y, Pinenelli GR, Plettner P (2014) Can we disrupt the sensing of honey bees by the bee parasite Varroa destructor? PLoS One 9:e106889CrossRefPubMedPubMedCentralGoogle Scholar
  29. Eliash N, Singh NK, Thangarajan S, Soroker V (2017) Chemosensing of honeybee parasite, Varroa destructor: transcriptomic analysis. Sci Rep 7:13091CrossRefPubMedPubMedCentralGoogle Scholar
  30. Eliash N, Thangarajan S, Sela N, Goldenberg I, Zaidman I, Kamer Y, Rafaeli A, Soroker V (2019) Varroa chemosensory proteins: some are conserved across Arthropoda but others are arachnid specific. Insect Mol Biol. (in press) DOI: 10.1111/imb.12553Google Scholar
  31. Endris J, Baker R (1993) Action potentials recorded from the foreleg of Varroa jacobsoni after olfactory stimulation. Apidologie 24:488–489Google Scholar
  32. 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 113:56–62CrossRefPubMedGoogle Scholar
  33. Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97CrossRefPubMedGoogle Scholar
  34. Gomez-Diaz C, Bargeton B, Abuin L, Bukar N, Reina JH, Bartoi T, Graf M, Ong H, Ulbrich MH, Masson JF, Benton R (2016) A CD36 ectodomain mediates insect pheromone detection via a putative tunnelling mechanism. Nat Commun 7:11866CrossRefPubMedPubMedCentralGoogle Scholar
  35. Goodwin RM, Taylor MA, Mcbrydie HM, Cox HM (2006) Drift of Varroa destructor-infested worker honey bees to neighbouring colonies. J Apic Res 45:155–156CrossRefGoogle Scholar
  36. Gulia-Nuss M et al (2016) Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun 7:10507CrossRefPubMedPubMedCentralGoogle Scholar
  37. Guzmán-Novoa E, Eccles L, Calvete Y, McGowan J, Kelly PG, Correa-Benítez A (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario. Can Apidologie 41:443–450CrossRefGoogle Scholar
  38. Häußermann CK, 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 46:771–778CrossRefGoogle Scholar
  39. Hebets EA, Chapman RF (2000) Electrophysiological studies of olfaction in the whip spider Phrynus parvulus (Arachnida, Amblypygi). J Insect Physiol 46:1441–1448CrossRefPubMedGoogle Scholar
  40. Hoppe H, Ritter W (1988) The influence of the nasanov gland pheromone on the recognition of house bees and foragers by Varroa jacobsoni. Apidologie 19:165–172CrossRefGoogle Scholar
  41. Hoy MA, Waterhouse RM, Wu K, Estep AS, Ioannidis P, Palmer WJ, Pomerantz AF, Simão FA, Thomas J, Jiggins FM, Murphy TD, Pritham EJ, Robertson HM, Zdobnov M, Gibbs RA, Richards S (2016) Genome sequencing of the phytoseiid predatory mite Metaseiulus occidentalis reveals completely atomised Hox genes and super-dynamic intron evolution. Genome Biol Evol 8:1762–1775CrossRefPubMedPubMedCentralGoogle Scholar
  42. Iovinella I, Ban L, Song L, Pelosi P, Dani FR (2016) Proteomic analysis of castor bean tick Ixodes ricinus: a focus on chemosensory organs. Insect Biochem Mol Biol 78:58–68CrossRefPubMedGoogle Scholar
  43. Iovinella I, McAfee A, Mastrobuoni G, Kempa S, Foster LJ, Pelosi P, Dani FR (2018) Proteomic analysis of chemosensory organs in the honey bee parasite Varroa destructor: a comprehensive examination of the potential carriers for semiochemicals. J Proteome 181:131–141CrossRefGoogle Scholar
  44. Ishida Y, Tsuchiya W, Fujii T, Fujimoto Z, Miyazawa M, Ishibashi J, Matsuyama S, Ishikawa Y, Yamazaki T (2014) Niemann-Pick type C2 protein mediating chemical communication in the worker ant. Proc Natl Acad Sci U S A 111:3847–3852CrossRefPubMedPubMedCentralGoogle Scholar
  45. Keeling CI, Slessor KN, Higo HA, Winston ML (2003) New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc Natl Acad Sci U S A 100:4486–4491CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kraus B (1990) Effects of honey-bee alarm pheromone compounds on the behaviour of Varroa jacobsoni. Apidologie 21:127–134CrossRefGoogle Scholar
  47. Kraus B (1994) Factors influencing host choice of the honey bee parasite Varroa jacobsoni Oud. Exp Appl Acarol 18:435–443CrossRefGoogle Scholar
  48. Le Conte Y, Arnold G, Trouiller J, Masson C (1989) Attraction of the parasitic mite Varroa to the drone larvae of honey bees by simple aliphatic esters. Science 245:638–639CrossRefPubMedGoogle Scholar
  49. Le Conte Y, Trouiller J, Masson C, Chappe B (1990) Identification of a brood pheromone in honeybees. Naturwissenschaften 77:334–336CrossRefGoogle Scholar
  50. Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391CrossRefPubMedGoogle Scholar
  51. Leoncini I, Le Conte Y, Costagliola G, Plettner E, Toth AL, Wang M, Huang Z, Bécard JM, Crauser D, Slessor KN, Robinson GE (2004) Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proc Natl Acad Sci U S A 101:17559–17564CrossRefPubMedPubMedCentralGoogle Scholar
  52. Liu T, Peng YS (1990) Palpal tarsal sensilla of the female mite, Varroa jacobsoni Oud. Can Entomol 122:295–300CrossRefGoogle Scholar
  53. Locke B (2015) Inheritance of reduced Varroa mite reproductive success in reciprocal crosses of mite-resistant and mite-susceptible honey bees (Apis mellifera). Apidologie 47:583–588CrossRefGoogle Scholar
  54. Martin SJ (1994) Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Exp Appl Acarol 18:87–100CrossRefGoogle Scholar
  55. Martin S, Holland K, Murray M (1997) Non-reproduction in the honeybee mite Varroa jacobsoni. Exp Appl Acarol 21:539–549CrossRefGoogle Scholar
  56. Milani N, Nannelli R (1988) The tarsal sense organ in Varroa jacobsoni Oud.: SEM observations. In: Proceedings of the a meeting of the EC-Experts’ Group, Udine, Italy. pp 71–82Google Scholar
  57. Milani N, Della Vedova G, Nazzi F (2004) (Z)-8-Heptadecene reduces the reproduction of in brood cells. Apidologie 35:265–273CrossRefGoogle Scholar
  58. Missbach C, Dweck H, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, Grosse-Wilde E (2014) Evolution of insect olfactory receptors. Elife 3:e02115CrossRefPubMedPubMedCentralGoogle Scholar
  59. Nazzi F, Milani N (1996) The presence of inhibitors of the reproduction of Varroa jacobsoni Oud. (Gamasida: Varroidae) in infested cells. Exp Appl Acarol 20:617–623CrossRefGoogle Scholar
  60. Nazzi F, Le Conte Y (2016) Ecology of Varroa destructor, the major ectoparasite of the Western honey bee, Apis mellifera. Annu Rev Entomol 61:417–432CrossRefPubMedGoogle Scholar
  61. Nazzi F, Milani N, Della Vedova G (2002) (Z)-8-Heptadecene from infested cells reduces the reproduction of Varroa destructor under laboratory conditions. J Chem Ecol 28:2181–2190CrossRefPubMedGoogle Scholar
  62. Nazzi F, Milani N, Della Vedova G (2004) A semiochemical from larval food influences the entrance of Varroa destructor into brood cells. Apidologie 35:403–410CrossRefGoogle Scholar
  63. Nazzi F, Bortolomeazzi R, Della Vedova G, Del Piccolo F, Annoscia D, Milani N (2009) Octanoic acid confers to royal jelly varroa-repellent properties. Naturwissenschaften 96:309–314CrossRefPubMedGoogle Scholar
  64. Ngoc PCT, Greenhalgh R, Dermauw W, Rombauts S, Bajda S, Zhurov V, Grbić M, Van de Peer Y, Van Leeuwen T, Rouzé P, Clark RM (2016) Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist Chelicerate herbivore. Genome Biol Evol 8:3323–3339CrossRefPubMedPubMedCentralGoogle Scholar
  65. Papachristoforou A, Kagiava A, Papaefthimiou C, Termentzi A, Fokialakis N, Skaltsounis AL, Watkins M, Arnold G, Theophilidis G (2012) The bite of the honeybee: 2-Heptanone secreted from honeybee mandibles during a bite acts as a local anaesthetic in insects and mammals. PLoS One 7:e47432CrossRefPubMedPubMedCentralGoogle Scholar
  66. Pelosi P, Iovinella I, Felicioli A, Dani FR (2014) Soluble proteins of chemical communication: an overview across arthropods. Front Physiol 5:320CrossRefPubMedPubMedCentralGoogle Scholar
  67. Peñalva-Arana DC, Lynch M, Robertson HM (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors. BMC Evol Biol 9:79CrossRefPubMedPubMedCentralGoogle Scholar
  68. Peng G, Kashio M, Morimoto T, Li T, Zhu J, Tominaga M, Kadowaki T (2015) Plant-derived tick repellents activate the honey bee ectoparasitic mite TRPA1. Cell Rep 12:190–202CrossRefPubMedGoogle Scholar
  69. Pernal SF, Baird DS, Birmingham AL, Higo HA, Slessor KN, Winston ML (2005) Semiochemicals influencing the host-finding behaviour of Varroa destructor. Exp Appl Acarol 37:1–26CrossRefPubMedGoogle Scholar
  70. Pickett JA, Williams IH, Martin AP, Smith MC (1980) Nasonov pheromone of the honey bee, Apis mellifera L. (Hymenoptera: Apidae). J Chem Ecol 6(2):425–434CrossRefGoogle Scholar
  71. Pinnelli GR, Singh NK, Soroker V, Plettner E (2016) Synthesis of enantiopure alicyclic ethers and their activity on the chemosensory organ of the ectoparasite of honey bees, Varroa destructor. J Agric Food Chem 64:8653–8658CrossRefPubMedGoogle Scholar
  72. Plettner E, Gries R (2010) Agonists and antagonists of antennal responses of gypsy moth (Lymantria dispar) to the pheromone (+)-disparlure and other odorants. J Agric Food Chem 58:3708–3719CrossRefPubMedGoogle Scholar
  73. Plettner E, Eliash N, Singh NK, Pinnelli GR, Soroker V (2017) The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents. Apidologie 48:78–92CrossRefGoogle Scholar
  74. Rehm SM, Ritter W (1989) Sequence of the sexes in the offspring of Varroa jacobsoni and the resulting consequences for the calculation of the developmental period. Apidologie 20:339–343CrossRefGoogle Scholar
  75. Renthal R, Manghnani L, Bernal S, Qu Y, Griffith WP, Lohmeyer K, Guerrero FD, Borges LMF, Pérez de León A (2017) The chemosensory appendage proteome of Amblyomma americanum (Acari: Ixodidae) reveals putative odorant-binding and other chemoreception-related proteins. Insect Sci 24:730–742CrossRefPubMedGoogle Scholar
  76. Rickli M (1992) Palmitic acid released from honeybee worker larvae attracts the parasitic mite Varroa jacobsoni on servosphere. Naturwissenschaften 79:320–322CrossRefGoogle Scholar
  77. Rickli M, Diehl PA, Guerin PM (1994) Cuticle alkanes of honeybee larvae mediate arrestment of bee parasite Varroa jacobsoni. J Chem Ecol 20:2437–2453CrossRefPubMedGoogle Scholar
  78. Rosenkranz P, Garrido C (2004) Volatiles of the honey bee larva initiate oogenesis in the parasitic mite Varroa destructor. Chemoecology 14:193–197CrossRefGoogle Scholar
  79. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119CrossRefPubMedGoogle Scholar
  80. Sammataro D, Avitabile A (2011) The beekeeper’s handbook, 4th edn. Cornell University Press, IthacaGoogle Scholar
  81. Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol 45:519–548CrossRefPubMedGoogle Scholar
  82. Singh NK, Eliash N, Kamer Y, Zaidman I, Plettner E, Soroker V (2014) The effect of DEET on chemosensing of the honey bee and its parasite Varroa destructor. Apidologie 46:380–391CrossRefGoogle Scholar
  83. Singh NK, Eliash N, Pinnelli GR, Plettner E, Soroker V (2015) Specific disruption of Varroa chemosensing. Congr Int Actual Apícola, Poebla, Mexico. pp 73–77Google Scholar
  84. Singh NK, Eliash N, Stein I, Kamer Y, Zaidman I, Rafaeli A, Soroker V (2016) Identification and gene-silencing of a putative odorant receptor transcription factor in Varroa destructor: possible role in olfaction. Insect Mol Biol 25:181–190CrossRefPubMedGoogle Scholar
  85. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745CrossRefPubMedGoogle Scholar
  86. Tichy H, Barth F (1992) Fine structure of olfactory sensilla in myriapods and arachnids. Microsc Res Tech 391:372–391CrossRefGoogle Scholar
  87. Trouiller J, Milani N (1999) Stimulation of Varroa jacobsoni Oud. oviposition with semiochemicals from honeybee brood. Apidologie 30:3–12CrossRefGoogle Scholar
  88. Trouiller J, Arnold G, Chappe B, Le Conte Y, Masson C (1992) Semiochemical basis of infestation of honey bee brood by Varroa jacobsoni. J Chem Ecol 18:2041–2053CrossRefPubMedGoogle Scholar
  89. Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490CrossRefPubMedPubMedCentralGoogle Scholar
  90. Vizueta J, Frías-López C, Macías-Hernández N, Arnedo MA, Sánchez-Gracia A, Rozas J (2017) Evolution of chemosensory gene families in arthropods: insight from the first inclusive comparative transcriptome analysis across spider appendages. Genome Biol Evol 9:178–196PubMedGoogle Scholar
  91. Vogt RG, Miller NE, Litvack R, Fandino RA, Sparks J, Staples J, Friedman R, Dickens JC (2009) The insect SNMP gene family. Insect Biochem Mol Biol 39:448–456CrossRefPubMedGoogle Scholar
  92. Watson K, Stallins JA (2016) Honey bees and colony collapse disorder: a pluralistic reframing. Geogr Compass 10:222–236CrossRefGoogle Scholar
  93. Xie X, Huang ZY, Zeng Z (2016) Why do Varroa mites prefer nurse bees? Sci Rep 6:28228CrossRefPubMedPubMedCentralGoogle Scholar
  94. Xuan N, Guo X, Xie HY, Lou QN, Lu XB, Liu GX, Picimbon JF (2015) Increased expression of CSP and CYP genes in adult silkworm females exposed to avermectins. Insect Sci 22:203–219CrossRefPubMedGoogle Scholar
  95. Yoder J, Sammataro D (2003) Potential to control Varroa mites (Acari: Varroidae) using chemical ecology. Int J Acarol 29:139–143CrossRefGoogle Scholar
  96. Ziegelmann B, Tolasch T, Steidle JLM, Rosenkranz P (2013) 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 44:481–490CrossRefGoogle Scholar
  97. Zioni N, Soroker V, Chejanovsky N (2011) Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology 417:106–112CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Victoria Soroker
    • 1
    Email author
  • Nitin Kumar Singh
    • 1
  • Nurit Eliash
    • 1
    • 2
  • Erika Plettner
    • 3
  1. 1.Department of Entomology, Institute of Plant ProtectionAgricultural Research Organization, Volcani CenterBet DaganIsrael
  2. 2.Institute of Agroecology and Plant Health, Robert H. Smith Faculty of Agriculture, Food and EnvironmentHebrew University of JerusalemRehovotIsrael
  3. 3.Department of ChemistrySimon Fraser UniversityBurnabyCanada

Personalised recommendations