Insectes Sociaux

, Volume 66, Issue 1, pp 91–105 | Cite as

An improved method for testing invertebrate encapsulation response as shown in the honey bee

  • N. Wilson-Rich
  • R. E. Bonoan
  • E. Taylor
  • L. Lwanga
  • P. T. StarksEmail author
Research Article


In 1882, Metchnikoff documented the encapsulation response (ER) of the invertebrate immune system. Since then, researchers have used Metchnikoff’s method to quantify immune function—and examine its relationship with ecological and behavioral factors—across various insect taxa. While scientists continue to uncover information regarding invertebrate immunity, behavioral ecology, and ecological immunology, the basics of Metchnikoff’s method have remained unchanged. All but two previous studies investigating insect immunity have used sterile or PBS-coated inducers, although we know that the immune system recognizes specific pathogens. To account for the specificity of the immune system, we modified Metchnikoff’s method and coated nylon monofilaments with pathogen-associated molecular patterns (PAMPs). Using honey bees (Apis mellifera), we examined ER using implants coated with PAMPs (“PAMPlants”) found on known honey bee parasites and pathogens. Lipopolysaccharide (LPS), peptidoglycan (PGN), and β-1, 3-glucan (B13G) PAMPlants mimicked an infection with Gram-negative bacteria, Gram-positive bacteria, and fungi, respectively. Our PAMPlants induced stronger responses than the control implants in both singly- (one PBS-coated or PAMP-coated implant) and doubly- (internal control; one PBS-coated and one PAMP-coated implant) implanted animals. In doubly-implanted individuals, there was a significant increase in response to B13G and LPS when compared with internal controls. The PGN and BSA did not differ from the internal controls in the doubly implanted individuals. These methods provide an improvement when exploring responses to specific pathogens and exploring topics within the field of invertebrate ecological immunity. When applied to social systems, these methods can be used to examine the evolution of disease resistance in societies.


Disease resistance Innate immunity Insect societies Invertebrate immunity Sociality 



We are grateful for the helpful comments from Kelsey K. Graham, Stephanie Clarke, Rebecca Czaja. ET and LL were funded through NSF DBI 0649190 granted to PTS. We also thank two anonymous reviewers and the editor for their helpful comments and suggestions.

Supplementary material

40_2018_668_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 28 KB)
40_2018_668_MOESM2_ESM.docx (21 kb)
Supplementary material 2 (DOCX 20 KB)


  1. Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2004) Sexual advertisement and immune function in an arachnid species (Lycosidae). Behav Ecol 15:602–606. CrossRefGoogle Scholar
  2. Allander K, Schmid-Hempel P (2000) Immune defence reaction in bumble-bee workers after a previous challenge and parasitic coinfection. Funct Ecol 14:711–717. CrossRefGoogle Scholar
  3. Antunez K, Martin-Hernandez R, Prieto L, Meana A, Zunino P, Higes M (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Envrion Microbiol 11:2284–2290CrossRefGoogle Scholar
  4. Appler RH, Frank SD, Tarpy DR (2015) Within-colony variation in the immunocompetency of managed and feral honey bees (Apis mellifera L.) in different urban landscapes. Insects 6:912–925. PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ashida M, Brey P (1997) Recent advances in research on the insect phenoloxidase cascade. In: Brey P, Hultmark D (eds) Molecular mechanisms of immune responses in insects. Chapman and Hall, London, pp 135–172Google Scholar
  6. Baer B, Schmid-Hempel P (2011) Unexpected consequences of polyandry for parasitism and fitness in the bumble bee, Bombus terrestris. Evolution 55:1639–1643CrossRefGoogle Scholar
  7. Beck G, Habicht GS (1996) Immunity and the invertebrates. Sci Am 275:60–66PubMedCrossRefGoogle Scholar
  8. Beck MH, Strand MR (2007) A novel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc Natl Acad Sci USA 104:19267–19272PubMedCrossRefGoogle Scholar
  9. Boete C, Paul REL, Koella JC (2002) Reduced efficacy of the immune melanization response in mosquitoes infected by malaria parasites. Parasitology 125:93–98. PubMedCrossRefGoogle Scholar
  10. Brandt A, Gorenflo A, Siede R, Meixner M, Buchler R (2016) The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J Insect Physiol 86:40–47. PubMedCrossRefGoogle Scholar
  11. Calleri DV, Reid EM, Rosengaus RB, Vargo EL, Traniello JFA (2006) Inbreeding and disease resistance in a social insect: effects of heterozygosity on immnnocompetence in the termite Zootermopsis angusticollis. Proc R Soc B 273:2633–2640. PubMedCrossRefGoogle Scholar
  12. Calleri DV, Rosengaus RB, Traniello JFA (2007) Immunity and reproduction during colony foundation in the dampwood termite Zootermopsis angusticollis. Physiol Entomol 32:136–142. CrossRefGoogle Scholar
  13. Carton Y, David JR (1983) Reduction of fitness in Drosophila adults surviving parasitization by a cynipid wasp. Experientia 39:231–233CrossRefGoogle Scholar
  14. Chernyak L, Tauber AI (1988) The birth of immunology: Metchnikoff, the embryologist. Cell Immunol 117:218–233PubMedCrossRefGoogle Scholar
  15. Civantos E, Ahnesjo J, Forsman A (2005) Immune function, parasitization and extended phenotypes in colour polymorphic pygmy grasshoppers. Biol J Lin Soc 85:373–383. CrossRefGoogle Scholar
  16. Contreras-Garduno J, Canales-Lazcano J, Cordoba-Aguilar A (2006) Wing pigmentation, immune ability, fat reserves and territorial status in males of the rubyspot damselfly, Hetaerina americana. J Ethol 24:165–173. CrossRefGoogle Scholar
  17. Daukste J, Kivleniece I, Krama T, Rantala MJ, Krams I (2012) Senescence in immune priming and attractiveness in a beetle. J Evolut Biol 25:1298–1304. CrossRefGoogle Scholar
  18. de Souza DJ, van Vlaenderen J, Moret Y, Lenoir A (2008) Immune response affects ant trophallactic behaviour. J Insect Physiol 54:828–832. PubMedCrossRefGoogle Scholar
  19. Debecker S, Sommaruga R, Maes T, Stoks R (2015) Larval UV exposure impairs adult immune function through a trade-off with larval investment in cuticular melanin. Funct Ecol 29:1292–1299. CrossRefGoogle Scholar
  20. Di Lelio I et al (2014) Functional analysis of an immune gene of Spodoptera littoralis by RNAi. J Insect Physiol 64:90–97. PubMedCrossRefGoogle Scholar
  21. Doums C, Schmid-Hempel P (2000) Immunocompetence in workers of a social insect, Bombus terrestris L., in relation to foraging activity and parasitic infection. Can J Zool 78:1060–1066CrossRefGoogle Scholar
  22. Duong TM, McCauley SJ (2016) Predation risk increases immune response in a larval dragonfly (Leucorrhinia intacta). Ecology 97:1605–1610PubMedCrossRefGoogle Scholar
  23. Freitak D, Ots I, Vanatoa A, Horak P (2003) Immune response is energetically costly in white cabbage butterfly pupae. Proc R Soc B 270:S220–S222. PubMedCrossRefGoogle Scholar
  24. Gershman SN (2008) Sex-specific differences in immunological costs of multiple mating in Gryllus vocalis field crickets. Behav Ecol 19:810–815. CrossRefGoogle Scholar
  25. Gherlenda AN, Haigh AM, Moore BD, Johnson SN, Riegler M (2016) Climate change, nutrition and immunity: effects of elevated CO2 and temperature on the immune function of an insect herbivore. J Insect Physiol 85:57–64. PubMedCrossRefGoogle Scholar
  26. Gilbert R, Uetz GW (2016) Courtship and male ornaments as honest indicators of immune function. Anim Behav 117:97–103. CrossRefGoogle Scholar
  27. Glinski Z, Jaroz J (2001) Infection and immunity in the honey bee, Apis mellifera. Apiacta 36:12–20Google Scholar
  28. González M, Cost FG, Peretti AV (2015) Funnel-web construction and estimated immune costs in Aglaoctenus lagotis (Araneae: Lycosidae). J Arachnol 43:158–167CrossRefGoogle Scholar
  29. Gordon SM (2008) Elie Metchnikoff: father of natural immunity. J Eur Immunol 38:3257–3264CrossRefGoogle Scholar
  30. Gorman MJ, Cornel AJ, Collins FH, Paskewitz SM (1996) A shared genetic mechanism for melanotic encapsulation of CM-Sephadex beads and a malaria parasite, Plasmodium cynomolgi B, in the mosquito, Anopheles gambiae. Exp Parasitol 84:380–386PubMedCrossRefGoogle Scholar
  31. Haviola S, Kapari L, Ossipov V, Rantala MJ, Ruuhola T, Haukioja E (2007) Foliar phenolics are differently associated with Epirrita autumnata growth and immunocompetence. J Chem Ecol 33:1013–1023. PubMedCrossRefGoogle Scholar
  32. Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949CrossRefGoogle Scholar
  33. Hu QQ, Wei XH, Li YP, Wang JL, Liu XS (2017) Identification and characterization of a gene involved in the encapsulation response of Helicoverpa armigera haemocytes. Insect Mol Biol 26:752–762. PubMedCrossRefGoogle Scholar
  34. Kang Y, Blanco K, Davis T, Wang Y, DeGrandi-Hoffman G (2016) Disease dynamics of honeybees with Varroa destructor as parasite and virus vector. Math Biosci 275:71–92PubMedCrossRefGoogle Scholar
  35. Kangassalo K, Kosonen K, Pölkki M, Sorvari J, Krams I, Rantala MJ (2016) Immune challenge has a negative effect on cuticular darkness in the mealworm beetle, Tenebrio molitor. Annales Zoologici Fennici 53:255–262CrossRefGoogle Scholar
  36. Kapari L, Haukioja E, Rantala MJ, Ruuhola T (2006) Defoliating insect immune defense interacts with induced plant defense during a population outbreak. Ecology 87:291–296. PubMedCrossRefGoogle Scholar
  37. Kelly CD (2016) Effect of nutritional stress and sex on melanotic encapsulation rate in the sexually size dimorphic Cook Strait giant weta (Deinacrida rugosa). Can J Zool 94:787–792. CrossRefGoogle Scholar
  38. Kelly CD (2017) Sexually dimorphic effect of mating on the melanotic encapsulation response in the harem-defending Wellington tree weta, Hemideina crassidens (Orthoptera: Tettigonioidea: Anostostomatidae). Ethology 123:785–792. CrossRefGoogle Scholar
  39. Kelly CD, Jennions MD (2009) Sexually dimorphic immune response in the harem polygynous Wellington tree weta Hemideina crassidens. Physiol Entomol 34:177–179CrossRefGoogle Scholar
  40. Kirschman LJ, Quade AH, Zera AJ, Warne RW (2017) Immune function trade-offs in response to parasite threats. J Insect Physiol 98:199–204. PubMedCrossRefGoogle Scholar
  41. Kivleniece I, Krams I, Daukste J, Krama T, Rantala MJ (2010) Sexual attractiveness of immune-challenged male mealworm beetles suggests terminal investment in reproduction. Anim Behav 80:1015–1021. CrossRefGoogle Scholar
  42. Klemola N, Klemola T, Rantala MJ, Ruuhola T (2007) Natural host-plant quality affects immune defence of an insect herbivore. Entomologia Experimentalis Et Applicata 123:167–176. CrossRefGoogle Scholar
  43. Konig C, Schmid-Hempel P (1995) Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proc R Soc B 260:225–227. CrossRefGoogle Scholar
  44. Koskimaki J, Rantala MJ, Taskinen J, Tynkkynen K, Suhonen J (2004) Immunocompetence and resource holding potential in the damselfly, Calopteryx virgo L. Behav Ecol 15:169–173. CrossRefGoogle Scholar
  45. Kimbrell DA, Beutler B (2001) The evolution and genetics of innate immunity. Nat Rev Genet 2:256–267PubMedCrossRefGoogle Scholar
  46. Kraaijeveld AR, Limentani EC, Godfray HCJ (2001) Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc R Soc B Biol Sci 268:259–261CrossRefGoogle Scholar
  47. Krams I, Daukste J, Kivleniece I, Krama T, Rantala MJ (2013) Previous encapsulation response enhances within individual protection against fungal parasite in the mealworm beetle Tenebrio molitor. Insect Sci 20:771–777. PubMedCrossRefGoogle Scholar
  48. Krams I et al (2015a) Effects of food quality on trade-offs among growth, immunity and survival in the greater wax moth Galleria mellonella. Insect Sci 22:431–439. PubMedCrossRefGoogle Scholar
  49. Krams IA, Krama T, Trakimas G, Kaasik A, Rantala MJ, Škute A (2015b) Reproduction is costly in an infected aquatic insect. Ethol Ecol Evolut 29:74–84. CrossRefGoogle Scholar
  50. Krams I et al (2016) A dark cuticle allows higher investment in immunity, longevity and fecundity in a beetle upon a simulated parasite attack. Oecologia 182:99–109. PubMedCrossRefGoogle Scholar
  51. Krams IA et al (2017) Microbiome symbionts and diet diversity incur costs on the immune system of insect larvae. J Exp Biol 220:4204–4212. PubMedCrossRefGoogle Scholar
  52. Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc B 273:823–829. PubMedCrossRefGoogle Scholar
  53. Leonard C, Ratcliffe NA, Rowley AF (1985) The role of prophenoloxidase activation in non-self recognition and phagocytosis by insect blood cells. J Insect Physiol 31:789–799CrossRefGoogle Scholar
  54. Li W, Evans JD, Li J, Su S, Hamilton M, Chen Y (2017) Spore load and immune response of honey bees naturally infected by Nosema ceranae. Parasitol Res 116:3265–3274PubMedCrossRefGoogle Scholar
  55. Li LF, Xu ZW, Liu NY, Wu GX, Ren XM, Zhu JY (2018) Parasitism and venom of ectoparasitoid Scleroderma guani impairs host cellular immunity. Arch Insect Biochem Physiol 98
  56. Lopez-Uribe MM, Sconiers WB, Frank SD, Dunn RR, Tarpy DR (2016) Reduced cellular immune response in social insect lineages. Biol Lett 12:20150984 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Mariani F et al (2012) Parasitic interactions between Nosema spp. and Varroa destructor in Apis mellifera colonies. Zoo Trop 30:81–90Google Scholar
  58. Martin SJ (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38:1082–1093CrossRefGoogle Scholar
  59. Moreno-Garcia M, Cordoba-Aguilar A, Conde R, Lanz-Mendoza H (2013) Current immunity markers in insect ecological immunology: assumed trade-offs and methodological issues. B Entomol Res 103:127–139CrossRefGoogle Scholar
  60. Negri P, Quintana S, Maggi M, Szawarski N, Lamattina L, Eguaras M (2014) Apis mellifera hemocytes generate increased amounts of nitric oxide in response to wounding/encapsulation. Apidologie 45:610–617. CrossRefGoogle Scholar
  61. Nurnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
  62. Ochiai M, Ashida M (1988) Purification of a B1,3-glucan recognition protein in the prophenoloxidase activating system from hemolymph of the silkworm, Bombyx mori. J Biol Chem 263:12056–12062PubMedGoogle Scholar
  63. Paskewitz S, Riehle MA (1994) Response of plasmodium refractory and susceptible strains of Anopheles gambiae to inoculated sephadex beads. Dev Comp Immunol 18:369–375PubMedCrossRefGoogle Scholar
  64. Paxton RJ, 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 38:558–565CrossRefGoogle Scholar
  65. Pereira KD, Guedes NMP, Serrao JE, Zanuncio JC, Guedes RNC (2017) Superparasitism, immune response and optimum progeny yield in the gregarious parasitoid Palmistichus elaeisis. Pest Manag Sci 73:1101–1109. CrossRefGoogle Scholar
  66. Polkki M, Kangassalo K, Rantala MJ (2014) Effects of interaction between temperature conditions and copper exposure on immune defense and other life-history traits of the blow fly Protophormia terraenovae. Environ Sci Technol 48:8793–8799. PubMedCrossRefGoogle Scholar
  67. Pomfret JC, Knell RJ (2006) Immunity and the expression of a secondary sexual trait in a horned beetle. Behav Ecol 17:466–472. CrossRefGoogle Scholar
  68. Postel S, Kemmerling B (2009) Plant systems for recognition of pathogen-associated molecular patterns. Semin Cell Dev Biol 20:1025–1031PubMedCrossRefGoogle Scholar
  69. Prokkola J, Roff D, Karkkainen T, Krams I, Rantala MJ (2013) Genetic and phenotypic relationships between immune defense, melanism and life-history traits at different temperatures and sexes in Tenebrio molitor. Heredity 111:89–96. PubMedPubMedCentralCrossRefGoogle Scholar
  70. Pye AE (1974) Microbial activation of prophenoloxidase from immune insect larvae. Nature 251:610–613PubMedCrossRefGoogle Scholar
  71. Rantala MJ, Kortet R (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol J Linn Soc 79:503–510. CrossRefGoogle Scholar
  72. Rantala MJ, Kortet R (2004) Male dominance and immunocompetence in a field cricket. Behav Ecol 15:187–191. CrossRefGoogle Scholar
  73. Rantala MJ, Roff DA (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket Gryllus bimaculatus. Funct Ecol 19:323–330. CrossRefGoogle Scholar
  74. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc B 269:1681–1685. PubMedCrossRefGoogle Scholar
  75. Rantala MJ, Vainikka A, Kortet R (2003) The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle. Proc R Soc B 270:2257–2261. PubMedCrossRefGoogle Scholar
  76. Rantala MJ, Viitaniemi H, Roff DA (2011) Effects of inbreeding on potential and realized immune responses in Tenebrio molitor. Parasitology 138:906–912. PubMedCrossRefGoogle Scholar
  77. Raymann K, Moran NA (2018) The role of the gut microbiome in health and disease of adult honey bee workers. Curr Opin Insect Sci 26:97–104PubMedPubMedCentralCrossRefGoogle Scholar
  78. Robb T, Jamieson IG, Forbes MR (2003) Morphs and immunity of the alpine weta, Hemideina maora: influence of temperature, selection, and associations with density and cuticular melanism. Ecol Entomol 28:738–746CrossRefGoogle Scholar
  79. Ryder JJ, Siva-Jothy MT (2000) Male calling song provides a reliable signal of immune function in a cricket. Proc R Soc B 267:1171–1175. PubMedCrossRefGoogle Scholar
  80. Sadd BM, Siva-Jothy MT (2006) Self-harm caused by an insect’s innate immunity. Proc R Soc B 273:2571–2574. PubMedCrossRefGoogle Scholar
  81. Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol 45:519–548PubMedCrossRefGoogle Scholar
  82. Schmid-Hempel R, Schmid-Hempel P (1998) Colony performance and immunocompetence of a social insect, Bombus terrestris in poor and variable environments. Funct Ecol 12:22–30CrossRefGoogle Scholar
  83. Silva FWS, Elliot SL (2016) Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest. Ecol Evolut 6:3672–3683. CrossRefGoogle Scholar
  84. Siva-Jothy MT (2000) A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proc Roy Soc B Biol Sci 267:2523–2527. CrossRefGoogle Scholar
  85. Smilanich AM, Dyer LA, Gentry GL (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90:1434–1440. PubMedCrossRefGoogle Scholar
  86. Smith VJ (2016) Immunology of invertebrates: cellular. In: Delves P (ed) Encyclopedia of life science. Wiley, New YorkGoogle Scholar
  87. Sorvari J, Hakkarainen H, Rantala MJ (2008) Immune defense of ants is associated with changes in habitat characteristics. Environ Entomol 37:51–56.;2 PubMedCrossRefGoogle Scholar
  88. Sorvari J, Rantala LM, Rantala MJ, Hakkarainen H, Eeva T (2007) Heavy metal pollution disturbs immune response in wild ant populations. Environ Pollut 145:324–328. PubMedCrossRefGoogle Scholar
  89. Spivak M (1996) Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie 27:245–260CrossRefGoogle Scholar
  90. Spivak M, Reuter GS (2001) Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32:555–565CrossRefGoogle Scholar
  91. Srygley RB, Jaronski ST (2018) Protein deficiency lowers resistance of Mormon crickets to the pathogenic fungus Beauveria bassiana. J Insect Physiol 105:40–45. PubMedCrossRefGoogle Scholar
  92. Srygley RB, Lorch PD (2011) Weakness in the band: nutrient-mediated trade-offs between migration and immunity of Mormon crickets Anabrus simplex. Anim Behav 81:395–400. CrossRefGoogle Scholar
  93. Srygley RB, Lorch PD, Simpson SJ, Sword GA (2009) Immediate protein dietary effects on movement and the generalised immunocompetence of migrating Mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae). Ecol Entomol 34:663–668. CrossRefGoogle Scholar
  94. Starks PT, Blackie CA, Seeley TD (2000) Fever in honey bee colonies. Naturwissenschaften 87:229–231PubMedCrossRefGoogle Scholar
  95. Tauber AI (2003) Metchnikoff and the phagocytosis theory. Nat Rev Mol Cell Biol 4:897–901PubMedCrossRefGoogle Scholar
  96. Teng ZW, Xu G, Gan SY, Chen X, Fang Q, Ye GY (2016) Effects of the endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae) parasitism, venom, and calyx fluid on cellular and humoral immunity of its host Chilo suppressalis (Lepidoptera: Crambidae) larvae. J Insect Physiol 85:46–56. PubMedCrossRefGoogle Scholar
  97. Trudeau D, Washburn JO, Volkman LE (2001) Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. J Virol 75:996–1003PubMedPubMedCentralCrossRefGoogle Scholar
  98. Vainikka A, Rantala MJ, Seppala O, Suhonen J (2007) Do male mealworm beetles, Tenebrio molitor, sustain the honesty of pheromone signals under immune challenge? Acta Ethol 10:63–72. CrossRefGoogle Scholar
  99. Vainio L, Hakkarainen H, Rantala MJ, Sorvari J (2004) Individual variation in immune function in the ant Formica exsecta; effects of the nest body size sex. Evolut Ecol 18:75–84. CrossRefGoogle Scholar
  100. van Engelsdorp D, Meixner 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–S95CrossRefGoogle Scholar
  101. Vanikova S, Noskova A, Pristas P, Judova J, Javorsky P (2015) Heterotrophic bacteria associated with Varroa destructor mite. Apidologie 46:369–379CrossRefGoogle Scholar
  102. Wang P et al (2017) C-type lectin interacting with beta-integrin enhances hemocytic encapsulation in the cotton bollworm, Helicoverpa armigera. Insect Biochemistry Molecular Biology 86:29–40. PubMedCrossRefGoogle Scholar
  103. Washburn JO, Kirkpatrick BA, Volkman LE (1996) Insect protection against viruses. Nature 383:767–767CrossRefGoogle Scholar
  104. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  105. Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, CambridgeGoogle Scholar
  106. Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649CrossRefGoogle Scholar
  107. Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL (2002) Coping with crowds: density-dependent disease resistance in desert locusts. Proc Natl Acad Sci 99:5471–5475. PubMedCrossRefGoogle Scholar
  108. Wilson-Rich N, Starks PT (2010) The Polistes war: weak immune function in the invasive Polistes dominulus relative to the natie P. fuscatus. Insectes Soc 57:47–52CrossRefGoogle Scholar
  109. Wootton EC, Dyrynda EA, Ratcliffe NA (2006) Interaction between non-specific electrostatic forces and humoral factors in haemocyte attachment and encapsulation in the edible cockle Cerastoderma edule. J Exp Biol 209:1326–1335. PubMedCrossRefGoogle Scholar
  110. Wilson-Rich N, Dres ST, Starks PT (2008) The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). J Insect Physiol 54:1392–1399. PubMedCrossRefGoogle Scholar
  111. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423PubMedCrossRefGoogle Scholar
  112. Wilson-Rich N, Hester F, Pilowsky JA, Foo B, Tien T, Starks PT (2014) A test of the haploid susceptibility hypothesis using a species with naturally occurring variation in ploidy. Insectes Soc 61:163–169CrossRefGoogle Scholar
  113. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
  114. Wu M et al (2014) Inhibitory effect of gut bacteria from the Japanese honey bee, Apis cerana japonica, against Melissococcus plutonius, the causal agent of European foulbrood disease. J Insect Sci 14:1–13Google Scholar
  115. Yaroslavtseva ON, Dubovskiy IM, Khodyrev VP, Duisembekov BA, Kryukov VY, Glupov VV (2017) Immunological mechanisms of synergy between fungus Metarhizium robertsii and bacteria Bacillus thuringiensis ssp. morrisoni on Colorado potato beetle larvae. J Insect Physiol 96:14–20. PubMedCrossRefGoogle Scholar
  116. Zhong K, Liu ZC, Wang JL, Liu XS (2017) The entomopathogenic fungus Nomuraea rileyi impairs cellular immunity of its host Helicoverpa armigera. Arch Insect Biochem Physiol. PubMedCrossRefGoogle Scholar
  117. Zhuo XR et al (2018) 20-Hydroxyecdysone promotes release of GBP-binding protein from oenocytoids to suppress hemocytic encapsulation. Insect Biochem Mol Biol 92:53–64. PubMedCrossRefGoogle Scholar
  118. Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Curr Opin Plant Biol 8:353–360PubMedCrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Department of BiologyTufts UniversityMedfordUSA
  2. 2.Urban Beekeeping Laboratory and Bee Sanctuary, Inc., Best Bees CompanyBostonUSA

Personalised recommendations