1932

Abstract

Evidence for global bee population declines has catalyzed a rapidly evolving area of research that aims to identify the causal factors and to effectively assess the status of pollinator populations. The term pollinator health emerged through efforts to understand causes of bee decline and colony losses, but it lacks a formal definition. In this review, we propose a definition for pollinator health and synthesize the available literature on the application of standardized biomarkers to assess health at the individual, colony, and population levels. We focus on biomarkers in honey bees, a model species, but extrapolate the potential application of these approaches to monitor the health status of wild bee populations. Biomarker-guided health measures can inform beekeeper management decisions, wild bee conservation efforts, and environmental policies. We conclude by addressing challenges to pollinator health from a One Health perspective that emphasizes the interplay between environmental quality and human, animal, and bee health.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-020518-115045
2020-02-15
2024-06-17
Loading full text...

Full text loading...

/deliver/fulltext/animal/8/1/annurev-animal-020518-115045.html?itemId=/content/journals/10.1146/annurev-animal-020518-115045&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ollerton J, Winfree R, Tarrant S 2011. How many flowering plants are pollinated by animals?. Oikos 120:321–26
    [Google Scholar]
  2. 2. 
    Aizen MA, Harder LD. 2009. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19:915–18
    [Google Scholar]
  3. 3. 
    Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C et al. 2010. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–52
    [Google Scholar]
  4. 4. 
    Kulhanek K, Steinhauer N, Rennich K, Caron DM, Sagili RR et al. 2017. A national survey of managed honey bee 2015–2016 annual colony losses in the USA. J. Apic. Res. 56:328–40
    [Google Scholar]
  5. 5. 
    Mathiasson ME, Rehan SM. 2019. Status changes in the wild bees of north‐eastern North America over 125 years revealed through museum specimens. Insect Conserv. Divers. 12:278–88
    [Google Scholar]
  6. 6. 
    Liere H, Jha S, Philpott SM 2017. Intersection between biodiversity conservation, agroecology, and ecosystem services. Agroecol. Sustain. Food Syst. 41:723–60Review highlights the close relationship between agricultural management practices, biodiversity, landscape composition, and their potential effects on pollination services.
    [Google Scholar]
  7. 7. 
    Goulson D, Nicholls E, Botias C, Rotheray EL 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957
    [Google Scholar]
  8. 8. 
    Hillyard TN. 1965. Facts about beekeeping in England. Bee World 46:77–85
    [Google Scholar]
  9. 9. 
    Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P 2012. Predictive markers of honey bee colony collapse. PLOS ONE 7:e32151
    [Google Scholar]
  10. 10. 
    Kielmanowicz MG, Inberg A, Lerner IM, Golani Y, Brown N et al. 2015. Prospective large-scale field study generates predictive model identifying major contributors to colony losses. PLOS Pathog 11:e1004816
    [Google Scholar]
  11. 11. 
    Smart M, Pettis J, Rice N, Browning Z, Spivak M 2016. Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use. PLOS ONE 11:e0152685First study connecting effects of agricultural intensity to colony performance and individual bee health.
    [Google Scholar]
  12. 12. 
    Amdam GV, Hartfelder K, Norberg K, Hagen A, Omholt SW 2004. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering?. J. Econ. Entomol. 97:741–47
    [Google Scholar]
  13. 13. 
    Locke B. 2016. Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 47:467–82
    [Google Scholar]
  14. 14. 
    Meixner MD, Kryger P, Costa C 2015. Effects of genotype, environment, and their interactions on honey bee health in Europe. Curr. Opin. Insect Sci. 10:177–84
    [Google Scholar]
  15. 15. 
    Wood TJ, Gibbs J, Graham KK, Isaacs R 2019. Narrow pollen diets are associated with declining Midwestern bumble bee species. Ecology 100:e02697
    [Google Scholar]
  16. 16. 
    Bortz WM. 2005. Biological basis of determinants of health. Am. J. Public Health 95:389–92
    [Google Scholar]
  17. 17. 
    Winfree R, Reilly JR, Bartomeus I, Cariveau DP, Williams NM, Gibbs J 2018. Species turnover promotes the importance of bee diversity for crop pollination at regional scales. Science 359:791–93This study demonstrates the importance of beta-diversity to maximize pollination services at regional scales.
    [Google Scholar]
  18. 18. 
    Ptolemy AS, Rifai N. 2010. What is a biomarker? Research investments and lack of clinical integration necessitate a review of biomarker terminology and validation schema. Scand. J. Clin. Lab. Investig. 70:6–14
    [Google Scholar]
  19. 19. 
    Kindig D, Stoddart G. 2003. What is population health?. Am. J. Public Health 93:380–83
    [Google Scholar]
  20. 20. 
    Wu-Smart J, Spivak M. 2016. Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Sci. Rep. 6:32108
    [Google Scholar]
  21. 21. 
    Wu-Smart J, Spivak M. 2018. Effects of neonicotinoid imidacloprid exposure on bumble bee (Hymenoptera: Apidae) queen survival and nest initiation. Environ. Entomol. 47:55–62
    [Google Scholar]
  22. 22. 
    Lee KV, Goblirsch M, McDermott E, Tarpy DR, Spivak M 2019. Is the brood pattern within a honey bee colony a reliable indicator of queen quality?. Insects 10:12Highlights the complexity of colony phenotype and shows that laying pattern is often misconstrued as only a queen problem.
    [Google Scholar]
  23. 23. 
    Fine JD, Shpigler HY, Ray AM, Beach NJ, Sankey AL et al. 2018. Quantifying the effects of pollen nutrition on honey bee queen egg laying with a new laboratory system. PLOS ONE 13:9e0203444 https://doi.org/10.1371/journal.pone.0203444
    [Crossref] [Google Scholar]
  24. 24. 
    Delaney DA, Keller JJ, Caren JR, Tarpy DR 2011. The physical, insemination, and reproductive quality of honey bee queens (Apis mellifera L.). Apidologie 42:1–13
    [Google Scholar]
  25. 25. 
    Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV 2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. PNAS 103:962–67
    [Google Scholar]
  26. 26. 
    Brodschneider R, Crailsheim K. 2010. Nutrition and health in honey bees. Apidologie 41:278–94
    [Google Scholar]
  27. 27. 
    Bowen-Walker PL, Gunn A. 2001. The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomol. Exp. Appl. 101:207–17
    [Google Scholar]
  28. 28. 
    Roulston TH, Cane JH. 2000. The effect of diet breadth and nesting ecology on body size variation in bees (Apiformes). J. Kans. Entomol. Soc. 73:129–42
    [Google Scholar]
  29. 29. 
    Renauld M, Hutchinson A, Loeb G, Poveda K, Connelly H 2016. Landscape simplification constrains adult size in a native ground-nesting bee. PLOS ONE 11:e0150946Empirical study that reports significantly smaller body size of individuals in more intensified agricultural areas.
    [Google Scholar]
  30. 30. 
    Youngsteadt E, Appler RH, López-Uribe MM, Tarpy DR, Frank SD 2015. Urbanization increases pathogen pressure on feral and managed honey bees. PLOS ONE 10:e0142031
    [Google Scholar]
  31. 31. 
    Alaux C, Soubeyrand S, Prado A, Peruzzi M, Maisonnasse A et al. 2018. Measuring biological age to assess colony demographics in honeybees. PLOS ONE 13:e0209192
    [Google Scholar]
  32. 32. 
    Wang J. 2014. Marker-based estimates of relatedness and inbreeding coefficients: an assessment of current methods. J. Evol. Biol. 27:518–30
    [Google Scholar]
  33. 33. 
    Jha S, Kremen C. 2013. Resource diversity and landscape-level homogeneity drive native bee foraging. PNAS 110:555–58
    [Google Scholar]
  34. 34. 
    Scriven JJ, Woodall LC, Goulson D 2013. Nondestructive DNA sampling from bumblebee faeces. Mol. Ecol. Resourc. 13:225–29
    [Google Scholar]
  35. 35. 
    Roulston TH, Goodell K. 2011. The role of resources and risks in regulating wild bee populations. Annu. Rev. Entomol. 56:293–312Comprehensive review of the different factors regulating population size in wild bees.
    [Google Scholar]
  36. 36. 
    Scofield HN, Mattila HR. 2015. Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLOS ONE 10:e0121731
    [Google Scholar]
  37. 37. 
    Goulson D, Peat J, Stout JC, Tucker J, Darvill B et al. 2002. Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?. Anim. Behav. 64:123–30
    [Google Scholar]
  38. 38. 
    Greenleaf SS, Williams NM, Winfree R, Kremen C 2007. Bee foraging ranges and their relationship to body size. Oecologia 153:589–96
    [Google Scholar]
  39. 39. 
    de Guzman L, Frake A, Simone-Finstrom M 2017. Comparative flight activities and pathogen load of two stocks of honey bees reared in gamma-irradiated combs. Insects 8:127
    [Google Scholar]
  40. 40. 
    Goblirsch M, Huang ZY, Spivak M 2013. Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae infection. PLOS ONE 8:e58165
    [Google Scholar]
  41. 41. 
    Natsopoulou ME, McMahon DP, Paxton RJ 2016. Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee. Behav. Ecol. Sociobiol. 70:1019–31
    [Google Scholar]
  42. 42. 
    Perry CJ, Søvik E, Myerscough MR, Barron AB 2015. Rapid behavioral maturation accelerates failure of stressed honey bee colonies. PNAS 112:3427–32
    [Google Scholar]
  43. 43. 
    Rueppell O, Bachelier C, Fondrk MK, Page RE Jr 2007. Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42:1020–32
    [Google Scholar]
  44. 44. 
    Terman A, Brunk UT. 2006. Oxidative stress, accumulation of biological “garbage,” and aging. Antioxid. Redox Signal. 8:197–204
    [Google Scholar]
  45. 45. 
    Anderson KE, Ricigliano VA, Mott BM, Copeland DC, Floyd AS, Maes P 2018. The queen's gut refines with age: longevity phenotypes in a social insect model. Microbiome 6:108
    [Google Scholar]
  46. 46. 
    Seehuus SC, Krekling T, Amdam GV 2006. Cellular senescence in honey bee brain is largely independent of chronological age. Exp. Gerontol. 41:1117–25
    [Google Scholar]
  47. 47. 
    Carvalho SM, Belzunces LP, Carvalho GA, Brunet J-L, Badiou-Beneteau A 2013. Enzymatic biomarkers as tools to assess environmental quality: a case study of exposure of the honeybee Apis mellifera to insecticides. Environ. Toxicol. Chem. 32:2117–24
    [Google Scholar]
  48. 48. 
    Simone-Finstrom M, Li-Byarlay H, Huang MH, Strand MK, Rueppell O, Tarpy DR 2016. Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Sci. Rep. 6:32023
    [Google Scholar]
  49. 49. 
    Margotta JW, Roberts SP, Elekonich MM 2018. Effects of flight activity and age on oxidative damage in the honey bee, Apis mellifera. J. Exp. Biol. 221: jeb183228
    [Google Scholar]
  50. 50. 
    Williams JB, Roberts SP, Elekonich MM 2008. Age and natural metabolically-intensive behavior affect oxidative stress and antioxidant mechanisms. Exp. Gerontol. 43:538–49
    [Google Scholar]
  51. 51. 
    Li-Byarlay H, Huang MH, Simone-Finstrom M, Strand MK, Tarpy DR, Rueppell O 2016. Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage. Exp. Gerontol. 83:15–21
    [Google Scholar]
  52. 52. 
    Schmid-Hempel P. 2005. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50:529–51
    [Google Scholar]
  53. 53. 
    Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL et al. 2006. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol 15:645–56
    [Google Scholar]
  54. 54. 
    López-Uribe MM, Fitzgerald A, Simone-Finstrom M 2017. Inducible versus constitutive social immunity: examining effects of colony infection on glucose oxidase and defensin-1 production in honeybees. R. Soc. Open Sci. 4:170224
    [Google Scholar]
  55. 55. 
    Alaux C, Ducloz F, Crauser D, Le Conte Y 2010. Diet effects on honeybee immunocompetence. Biol. Lett. 6:562–65
    [Google Scholar]
  56. 56. 
    Ricigliano VA, Mott BM, Maes PW, Floyd AS, Fitz W et al. 2019. Honey bee colony performance and health are enhanced by apiary proximity to US Conservation Reserve Program (CRP) lands. Sci. Rep. 9:4894Highlights the potential of colony-level molecular biomarkers to assess the effects of landscape conservation efforts.
    [Google Scholar]
  57. 57. 
    Evison SEF, Fazio G, Chappell P, Foley K, Jensen AB, Hughes WOH 2016. Innate expression of antimicrobial peptides does not explain genotypic diversity in resistance to fungal brood parasites in the honey bee. Apidologie 47:206–15
    [Google Scholar]
  58. 58. 
    Simone-Finstrom M, Walz M, Tarpy DR 2016. Genetic diversity confers colony-level benefits due to individual immunity. Biol. Lett. 12:20151007
    [Google Scholar]
  59. 59. 
    Decanini LI, Collins AM, Evans JD 2007. Variation and heritability in immune gene expression by diseased honeybees. J. Hered. 98:195–201
    [Google Scholar]
  60. 60. 
    Nazzi F, Pennacchio F. 2018. Honey bee antiviral immune barriers as affected by multiple stress factors: a novel paradigm to interpret colony health decline and collapse. Viruses 10:159
    [Google Scholar]
  61. 61. 
    Di Prisco G, Annoscia D, Margiotta M, Ferrara R, Varricchio P et al. 2016. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. PNAS 113:3203–8
    [Google Scholar]
  62. 62. 
    Schmid MR, Brockmann A, Pirk CWW, Stanley DW, Tautz J 2008. Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J. Insect Physiol. 54:439–44
    [Google Scholar]
  63. 63. 
    López-Uribe MM, Appler RH, Youngsteadt E, Dunn RR, Frank SD, Tarpy DR 2017. Higher immunocompetence is associated with higher genetic diversity in feral honey bee colonies (Apis mellifera). Conserv. Genet. 18:659–66
    [Google Scholar]
  64. 64. 
    Alaux C, Allier F, Decourtye A, Odoux J-F, Tamic T et al. 2017. A “landscape physiology” approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats. Sci. Rep. 7:40568
    [Google Scholar]
  65. 65. 
    Alaux C, Dantec C, Parrinello H, Le Conte Y 2011. Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and Varroa-parasitized bees. BMC Genom 12:496
    [Google Scholar]
  66. 66. 
    Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A et al. 2013. Influence of pollen nutrition on honey bee health: Do pollen quality and diversity matter?. PLOS ONE 8:e72016
    [Google Scholar]
  67. 67. 
    Pokhrel V, DeLisi NA, Danka RG, Walker TW, Ottea JA, Healy KB 2018. Effects of truck-mounted, ultra low volume mosquito adulticides on honey bees (Apis mellifera) in a suburban field setting. PLOS ONE 13:e0193535
    [Google Scholar]
  68. 68. 
    Berenbaum MR, Johnson RM. 2015. Xenobiotic detoxification pathways in honey bees. Curr. Opin. Insect Sci. 10:51–58
    [Google Scholar]
  69. 69. 
    Manjon C, Troczka BJ, Zaworra M, Beadle K, Randall E et al. 2018. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr. Biol. 28:1137–43.e5
    [Google Scholar]
  70. 70. 
    Mao W, Schuler MA, Berenbaum MR 2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). PNAS 108:12657–62
    [Google Scholar]
  71. 71. 
    Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34
    [Google Scholar]
  72. 72. 
    Kwong WK, Medina LA, Koch H, Sing K-W, Soh EJY et al. 2017. Dynamic microbiome evolution in social bees. Sci. Adv. 3:e1600513
    [Google Scholar]
  73. 73. 
    Lee FJ, Rusch DB, Stewart FJ, Mattila HR, Newton ILG 2015. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ. Microbiol. 17:796–815
    [Google Scholar]
  74. 74. 
    Ricigliano VA, Fitz W, Copeland DC, Mott BM, Maes P et al. 2017. The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism. Arch. Insect Biochem. Physiol. 96:e21406
    [Google Scholar]
  75. 75. 
    Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA 2017. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. PNAS 114:4775–80
    [Google Scholar]
  76. 76. 
    Rubanov A, Russell KA, Rothman JA, Nieh JC, McFrederick QS 2019. Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure. Sci. Rep. 9:3820
    [Google Scholar]
  77. 77. 
    Schwarz RS, Moran NA, Evans JD 2016. Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. PNAS 113:9345–50
    [Google Scholar]
  78. 78. 
    Kwong WK, Mancenido AL, Moran NA 2017. Immune system stimulation by the native gut microbiota of honey bees. R. Soc. Open Sci. 4:170003
    [Google Scholar]
  79. 79. 
    Anderson KE, Ricigliano VA. 2017. Honey bee gut dysbiosis: a novel context of disease ecology. Curr. Opin. Insect Sci. 22:125–32
    [Google Scholar]
  80. 80. 
    Mockler BK, Kwong WK, Moran NA, Koch H 2018. Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl. Environ. Microbiol. 84:e02335
    [Google Scholar]
  81. 81. 
    Koch H, Schmid-Hempel P. 2012. Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system. Ecol. Lett. 15:1095–103
    [Google Scholar]
  82. 82. 
    Powell E, Ratnayeke N, Moran NA 2016. Strain diversity and host specificity in a specialized gut symbiont of honeybees and bumblebees. Mol. Ecol. 25:4461–71
    [Google Scholar]
  83. 83. 
    Ellegaard KM, Engel P. 2019. Genomic diversity landscape of the honey bee gut microbiota. Nat. Commun. 10:446
    [Google Scholar]
  84. 84. 
    Jones JC, Fruciano C, Hildebrand F, Al Toufalilia H, Balfour NJ et al. 2018. Gut microbiota composition is associated with environmental landscape in honey bees. Ecol. Evol. 8:441–51
    [Google Scholar]
  85. 85. 
    Rothman JA, Andrikopoulos C, Cox-Foster D, McFrederick QS 2019. Floral and foliar source affect the bee nest microbial community. Microb. Ecol. 78:506–16
    [Google Scholar]
  86. 86. 
    Francis RM, Nielsen SL, Kryger P 2013. Varroa-virus interaction in collapsing honey bee colonies. PLOS ONE 8:e57540
    [Google Scholar]
  87. 87. 
    Martin S. 1998. A population model for the ectoparasitic mite Varroa jacobsoni in honey bee (Apis mellifera) colonies. Ecol. Model. 109:267–81
    [Google Scholar]
  88. 88. 
    Danka RG, Harris JW, Dodds GE 2016. Selection of VSH-derived “Pol-line” honey bees and evaluation of their Varroa-resistance characteristics. Apidologie 47:483–90
    [Google Scholar]
  89. 89. 
    de Guzman L, Rinderer TE, Frake AM 2007. Growth of Varroa destructor (Acari: Varroidae) populations in Russian honey bee (Hymenoptera: Apidae) colonies. Ann. Entomol. Soc. Am. 100:187–95
    [Google Scholar]
  90. 90. 
    Harbo JR, Harris JW. 2005. Suppressed mite reproduction explained by the behaviour of adult bees. J. Apic. Res. 44:21–23
    [Google Scholar]
  91. 91. 
    Kirrane MJ, de Guzman LI, Holloway B, Frake AM, Rinderer TE, Whelan PM 2015. Phenotypic and genetic analyses of the Varroa sensitive hygienic trait in Russian honey bee (Hymenoptera: Apidae) colonies. PLOS ONE 10:e0116672
    [Google Scholar]
  92. 92. 
    Dietemann V, Nazzi F, Martin SJ, Anderson DL, Locke B et al. 2013. Standard methods for Varroa research. J. Apic. Res. 52:1–54
    [Google Scholar]
  93. 93. 
    Lee KV, Moon RD, Burkness EC, Hutchison WD, Spivak M 2010. Practical sampling plans for Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae) colonies and apiaries. J. Econ. Entomol. 103:1039–50
    [Google Scholar]
  94. 94. 
    DeGrandi-Hoffman G, Ahumada F, Danka R, Chambers M, DeJong EW, Hidalgo G 2017. Population growth of Varroa destructor (Acari: Varroidae) in colonies of Russian and unselected honey bee (Hymenoptera: Apidae) stocks as related to numbers of foragers with mites. J. Econ. Entomol. 110:809–15
    [Google Scholar]
  95. 95. 
    Delaplane KS, van der Steen J, Guzman-Novoa E 2013. Standard methods for estimating strength parameters of Apis mellifera colonies. J. Apic. Res. 52:1–12
    [Google Scholar]
  96. 96. 
    Goulson D, Hughes W, Derwent L, Stout J 2002. Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–73
    [Google Scholar]
  97. 97. 
    Vaudo AD, Farrell LM, Patch HM, Grozinger CM, Tooker JF 2018. Consistent pollen nutritional intake drives bumble bee (Bombus impatiens) colony growth and reproduction across different habitats. Ecol. Evol. 8:5765–76Study linking specific nutritional requirements to bumble bee colony health.
    [Google Scholar]
  98. 98. 
    Mattila HR, Seeley TD. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–64
    [Google Scholar]
  99. 99. 
    Meikle WG, Corby-Harris V, Carroll MJ, Weiss M, Snyder LA et al. 2019. Exposure to sublethal concentrations of methoxyfenozide disrupts honey bee colony activity and thermoregulation. PLOS ONE 14:e0204635
    [Google Scholar]
  100. 100. 
    Meikle WG, Weiss M, Maes PW, Fitz W, Snyder LA et al. 2017. Internal hive temperature as a means of monitoring honey bee colony health in a migratory beekeeping operation before and during winter. Apidologie 48:666–80
    [Google Scholar]
  101. 101. 
    Huang SK, Csaki T, Doublet V, Dussaubat C, Evans JD et al. 2014. Evaluation of cage designs and feeding regimes for honey bee (Hymenoptera: Apidae) laboratory experiments. J. Econ. Entomol. 107:54–62
    [Google Scholar]
  102. 102. 
    Ricigliano VA, Mott BM, Floyd AS, Copeland DC, Carroll MJ, Anderson KE 2018. Honey bees overwintering in a southern climate: longitudinal effects of nutrition and queen age on colony-level molecular physiology and performance. Sci. Rep. 8:10475
    [Google Scholar]
  103. 103. 
    Salmela H, Stark T, Stucki D, Fuchs S, Freitak D et al. 2016. Ancient duplications have led to functional divergence of vitellogenin-like genes potentially involved in inflammation and oxidative stress in honey bees. Genome Biol. Evol. 8:495–506
    [Google Scholar]
  104. 104. 
    Barroso-Arévalo S, Vicente-Rubiano M, Puerta F, Molero F, Sánchez-Vizcaíno JM 2019. Immune related genes as markers for monitoring health status of honey bee colonies. BMC Vet. Res. 15:72
    [Google Scholar]
  105. 105. 
    Oldroyd BP, Fewell JH. 2007. Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol. 22:408–13
    [Google Scholar]
  106. 106. 
    Palmer KA, Oldroyd BP. 2003. Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90:265–68
    [Google Scholar]
  107. 107. 
    Tarpy DR. 2003. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. Lond. B Biol. Sci. 270:99–103
    [Google Scholar]
  108. 108. 
    Tarpy DR, vanEngelsdorp D, Pettis JS 2013. Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften 100:723–28
    [Google Scholar]
  109. 109. 
    Strassmann J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc 48:1–13
    [Google Scholar]
  110. 110. 
    Cremer S, Pull CD, Fürst MA 2018. Social immunity: emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63:105–23
    [Google Scholar]
  111. 111. 
    Simone-Finstrom M. 2017. Social immunity and the superorganism: behavioral defenses protecting honey bee colonies from pathogens and parasites. Bee World 94:21–29
    [Google Scholar]
  112. 112. 
    Wilson-Rich N, Spivak M, Fefferman NH, Starks PT 2009. Genetic, individual, and group facilitation of disease resistance in insect societies. Annu. Rev. Entomol. 54:405–23
    [Google Scholar]
  113. 113. 
    Meunier J. 2015. Social immunity and the evolution of group living in insects. Philos. Trans. R. Soc. B Biol. Sci. 370:20140102
    [Google Scholar]
  114. 114. 
    Momot JP, Rothenbuhler WC. 1971. Behaviour genetics of nest cleaning in honeybees. VI. Interactions of age and genotype of bees, and nectar flow. J. Apic. Res. 10:11–21
    [Google Scholar]
  115. 115. 
    Gerdts J, Dewar RL, Simone-Finstrom M, Edwards T, Angove M 2018. Hygienic behaviour selection via freeze-killed honey bee brood not associated with chalkbrood resistance in eastern Australia. PLOS ONE 13:e0203969
    [Google Scholar]
  116. 116. 
    Tsvetkov N, Samson-Robert O, Sood K, Patel HS, Malena DA et al. 2017. Chronic exposure to neo-nicotinoids reduces honey bee health near corn crops. Science 356:1395–97
    [Google Scholar]
  117. 117. 
    Mondet F, Alaux C, Severac D, Rohmer M, Mercer AR, Le Conte Y 2015. Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Sci. Rep. 5:10454
    [Google Scholar]
  118. 118. 
    Guarna MM, Hoover SE, Huxter E, Higo H, Moon K-M et al. 2017. Peptide biomarkers used for the selective breeding of a complex polygenic trait in honey bees. Sci. Rep. 7:8381
    [Google Scholar]
  119. 119. 
    Harpur BA, Guarna MM, Huxter E, Higo H, Moon K-M et al. 2019. Integrative genomics reveals the genetics and evolution of the honey bee's social immune system. Genome Biol. Evol. 11:937–48
    [Google Scholar]
  120. 120. 
    Page RE, Robinson GE, Fondrk MK, Nasr ME 1995. Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav. Ecol. Sociobiol. 36:387–96
    [Google Scholar]
  121. 121. 
    Gilioli G, Sperandio G, Hatjina F, Simonetto A 2019. Towards the development of an index for the holistic assessment of the health status of a honey bee colony. Ecol. Indic. 101:341–47
    [Google Scholar]
  122. 122. 
    Richard F-J, Aubert A, Grozinger CM 2008. Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 6:50
    [Google Scholar]
  123. 123. 
    Wagoner KM, Spivak M, Rueppell O 2018. Brood affects hygienic behavior in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 111:2520–30
    [Google Scholar]
  124. 124. 
    Simone-Finstrom M, Borba R, Wilson M, Spivak M 2017. Propolis counteracts some threats to honey bee health. Insects 8:46
    [Google Scholar]
  125. 125. 
    Spivak M, Goblirsch M, Simone-Finstrom M 2019. Social-medication in bees: the line between individual and social regulation. Curr. Opin. Insect Sci. 33:49–55
    [Google Scholar]
  126. 126. 
    Moreau SJM. 2013. “It stings a bit but it cleans well:. ” venoms of Hymenoptera and their antimicrobial potential. J. Insect Physiol. 59:186–204
    [Google Scholar]
  127. 127. 
    Bucekova M, Valachova I, Kohutova L, Prochazka E, Klaudiny J, Majtan J 2014. Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys. Die Naturwiss 101:661–70
    [Google Scholar]
  128. 128. 
    Jones B, Shipley E, Arnold KE 2018. Social immunity in honeybees—density dependence, diet, and body mass trade-offs. Ecol. Evol. 8:4852–59
    [Google Scholar]
  129. 129. 
    Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD et al. 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–87
    [Google Scholar]
  130. 130. 
    Evans JD, Schwarz RS. 2011. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 19:614–20
    [Google Scholar]
  131. 131. 
    Schwarz RS, Huang Q, Evans JD 2015. Hologenome theory and the honey bee pathosphere. Curr. Opin. Insect Sci. 10:1–7Review discusses honey bee microbial associates as an extension of the colony phenotype and host health.
    [Google Scholar]
  132. 132. 
    McMenamin AJ, Flenniken ML. 2018. Recently identified bee viruses and their impact on bee pollinators. Curr. Opin. Insect Sci. 26:120–29
    [Google Scholar]
  133. 133. 
    Schwarz RS, Teixeira EW, Tauber JP, Birke JM, Martins MF et al. 2014. Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. Microbiol. Open 3:341–55
    [Google Scholar]
  134. 134. 
    Glenny W, Cavigli I, Daughenbaugh KF, Radford R, Kegley SE, Flenniken ML 2017. Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PLOS ONE 12:e0182814
    [Google Scholar]
  135. 135. 
    Pirk CWW, de Miranda JR, Kramer M, Murray TE, Nazzi F et al. 2013. Statistical guidelines for Apis mellifera research. J. Apic. Res. 52:1–24
    [Google Scholar]
  136. 136. 
    Thaduri S, Stephan JG, de Miranda JR, Locke B 2019. Disentangling host-parasite-pathogen interactions in a Varroa-resistant honeybee population reveals virus tolerance as an independent, naturally adapted survival mechanism. Sci. Rep. 9:6221
    [Google Scholar]
  137. 137. 
    Jensen AB, Pedersen BV, Eilenberg J 2009. Differential susceptibility across honey bee colonies in larval chalkbrood resistance. Apidologie 40:524–34
    [Google Scholar]
  138. 138. 
    McFrederick QS, Thomas JM, Neff JL, Vuong HQ, Russell KA et al. 2017. Flowers and wild megachilid bees share microbes. Microb. Ecol. 73:188–200
    [Google Scholar]
  139. 139. 
    Forsgren E, Olofsson TC, Vásquez A, Fries I 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41:99–108
    [Google Scholar]
  140. 140. 
    Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E et al. 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLOS ONE 7:e33188
    [Google Scholar]
  141. 141. 
    Lebuhn G, Droege S, Connor EF, Gemmill-Herren B, Potts SG et al. 2013. Detecting insect pollinator declines on regional and global scales. Conserv. Biol. 27:113–20
    [Google Scholar]
  142. 142. 
    Batáry P, Báldi A, Kleijn D, Tscharntke T 2011. Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis. Proc. R. Soc. B Biol. Sci. 278:1894–902
    [Google Scholar]
  143. 143. 
    Whitehorn PR, Tinsley MC, Brown MJF, Darvill B, Goulson D 2011. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proc. R. Soc. B Biol. Sci. 278:1195–202
    [Google Scholar]
  144. 144. 
    Jaffé R, Pope N, Acosta AL, Alves DA, Arias MC et al. 2016. Beekeeping practices and geographic distance, not land use, drive gene flow across tropical bees. Mol. Ecol. 25:5345–58
    [Google Scholar]
  145. 145. 
    López‐Uribe MM, Jha S, Soro A 2019. A trait‐based approach to predict population genetic structure in bees. Mol. Ecol. 28:1919–29
    [Google Scholar]
  146. 146. 
    Lozier J. 2014. Revisiting comparisons of genetic diversity in stable and declining species: assessing genome‐wide polymorphism in North American bumble bees using RAD sequencing. Mol. Ecol. 23:788–801
    [Google Scholar]
  147. 147. 
    López-Uribe MM, Cane JH, Minckley RL, Danforth BN 2016. Crop domestication facilitated rapid geographical expansion of a specialist pollinator, the squash bee Peponapis pruinosa. Proc. R. Soc. B Biol. Sci 283:20160443
    [Google Scholar]
  148. 148. 
    Ogilvie JE, Forrest JRK. 2017. Interactions between bee foraging and floral resource phenology shape bee populations and communities. Curr. Opin. Insect Sci. 21:75–82
    [Google Scholar]
  149. 149. 
    Requier F, Odoux J-F, Tamic T, Moreau N, Henry M et al. 2015. Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol. Appl. 25:881–90
    [Google Scholar]
  150. 150. 
    Vaudo AD, Tooker JF, Grozinger CM, Patch HM 2015. Bee nutrition and floral resource restoration. Curr. Opin. Insect Sci. 10:133–41
    [Google Scholar]
  151. 151. 
    Whitehorn PR, O'Connor S, Wackers FL, Goulson D 2012. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351–52
    [Google Scholar]
  152. 152. 
    Gill RJ, Ramos-Rodriguez O, Raine NE 2012. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–8
    [Google Scholar]
  153. 153. 
    Meeus I, Pisman M, Smagghe G, Piot N 2018. Interaction effects of different drivers of wild bee decline and their influence on host-pathogen dynamics. Curr. Opin. Insect Sci. 26:136–41
    [Google Scholar]
  154. 154. 
    Tosi S, Nieh JC, Sgolastra F, Cabbri R, Medrzycki P 2017. Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. R. Soc. B Biol. Sci. 284:20171711Study provides mechanistic evidence that two major stressors, field-realistic nutritional deficiency and pesticide exposure, can synergistically interact.
    [Google Scholar]
  155. 155. 
    Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R et al. 2010. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLOS ONE 5:e9754
    [Google Scholar]
  156. 156. 
    Reeves AM, O'Neal ST, Fell RD, Brewster CC, Anderson TD 2018. In-hive acaricides alter biochemical and morphological indicators of honey bee nutrition, immunity, and development. J. Insect Sci. 18:8
    [Google Scholar]
  157. 157. 
    Mussen EC, Lopez JE, Peng CYS 2004. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environ. Entomol. 33:1151–54
    [Google Scholar]
  158. 158. 
    Raymann K, Bobay L-M, Moran NA 2018. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol. Ecol. 27:2057–66
    [Google Scholar]
  159. 159. 
    McArt SH, Urbanowicz C, McCoshum S, Irwin RE, Adler LS 2017. Landscape predictors of pathogen prevalence and range contractions in US bumblebees. Proc. R. Soc. B Biol. Sci. 284:20172181
    [Google Scholar]
  160. 160. 
    Dolezal AG, Toth AL. 2018. Feedbacks between nutrition and disease in honey bee health. Curr. Opin. Insect Sci. 26:114–19
    [Google Scholar]
  161. 161. 
    O'Neal ST, Anderson TD, Wu-Smart JY 2018. Interactions between pesticides and pathogen susceptibility in honey bees. Curr. Opin. Insect Sci. 26:57–62
    [Google Scholar]
  162. 162. 
    Gibbs EPJ. 2014. The evolution of One Health: a decade of progress and challenges for the future. Vet. Rec. 174:85–91
    [Google Scholar]
  163. 163. 
    Eilers EJ, Kremen C, Smith Greenleaf S, Garber AK, Klein A-M 2011. Contribution of pollinator-mediated crops to nutrients in the human food supply. PLOS ONE 6:e21363
    [Google Scholar]
  164. 164. 
    Smith MR, Singh GM, Mozaffarian D, Myers SS 2015. Effects of decreases of animal pollinators on human nutrition and global health: a modelling analysis. Lancet 386:1964–72
    [Google Scholar]
  165. 165. 
    Power AG. 2010. Ecosystem services and agriculture: tradeoffs and synergies. Philos. Trans. R. Soc. B Biol. Sci. 365:2959–71
    [Google Scholar]
  166. 166. 
    Klein A-M, Boreux V, Fornoff F, Mupepele A-C, Pufal G 2018. Relevance of wild and managed bees for human well-being. Curr. Opin. Insect Sci. 26:82–88Review of the evidence that bees contribute not only to food security via pollination but also to a wide range of benefits for human well-being, including medical resources and human spiritual practices.
    [Google Scholar]
  167. 167. 
    Cane JH, Sipes S. 2006. Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. Plant-Pollinator Interactions: From Specialization to Generalization NM Waser, J Ollerton 99–122 Chicago: Univ. Chicago Press
    [Google Scholar]
  168. 168. 
    Cane JH. 1991. Soils of ground-nesting bees (Hymenoptera: Apoidea): texture, moisture, cell depth and climate. J. Kans. Entomol. Soc. 64:406–13
    [Google Scholar]
  169. 169. 
    Harbo JR, Harris JW. 2009. Responses to Varroa by honey bees with different levels of Varroa Sensitive Hygiene. J. Apic. Res. 48:156–61
    [Google Scholar]
  170. 170. 
    de Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE et al. 2013. Standard methods for virus research in Apis mellifera. J. Apic. Res 52:1–56
    [Google Scholar]
  171. 171. 
    Evans JD, Schwarz RS, Chen YP, Budge G, Cornman RS et al. 2013. Standard methods for molecular research in Apis mellifera. J. Apic. Res 52:1–54
    [Google Scholar]
  172. 172. 
    Traver BE, Fell RD. 2011. Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. J. Invertebr. Pathol. 107:43–49
    [Google Scholar]
  173. 173. 
    Cavigli I, Daughenbaugh KF, Martin M, Lerch M, Banner K et al. 2016. Pathogen prevalence and abundance in honey bee colonies involved in almond pollination. Apidologie 47:251–66
    [Google Scholar]
  174. 174. 
    Schurr F, Cougoule N, Rivière MP, Ribière-Chabert M, Achour H et al. 2017. Trueness and precision of the real-time RT-PCR method for quantifying the chronic bee paralysis virus genome in bee homogenates evaluated by a comparative inter-laboratory study. J. Virol. Methods 248:217–25
    [Google Scholar]
  175. 175. 
    Fries I, Chauzat MP, Chen YP, Doublet V, Genersch E et al. 2013. Standard methods for Nosema research. J. Apic. Res. 52:1–28
    [Google Scholar]
  176. 176. 
    Sammataro D, de Guzman L, George S, Ochoa R, Otis G 2013. Standard methods for tracheal mite research. J. Apic. Res. 52:1–20
    [Google Scholar]
  177. 177. 
    Meikle WG, Holst N. 2015. Application of continuous monitoring of honeybee colonies. Apidologie 46:10–22
    [Google Scholar]
  178. 178. 
    Sagili RR, Pankiw T, Keyan ZS 2005. Effects of soybean trypsin inhibitor on hypopharyngeal gland protein content, total midgut protease activity and survival of the honey bee (Apis mellifera L.). J. Insect Physiol. 51:953–57
    [Google Scholar]
  179. 179. 
    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. 54:1392–99
    [Google Scholar]
  180. 180. 
    López-Uribe MM, Sconiers WB, Frank SD, Dunn RR, Tarpy DR 2016. Reduced cellular immune response in social insect lineages. Biol. Lett. 12:20150984
    [Google Scholar]
  181. 181. 
    Evans JD, Pettis JS. 2005. Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 59:2270–74
    [Google Scholar]
  182. 182. 
    Praet J, Parmentier A, Schmid‐Hempel R, Meeus I, Smagghe G, Vandamme P 2018. Large‐scale cultivation of the bumblebee gut microbiota reveals an underestimated bacterial species diversity capable of pathogen inhibition. Environ. Microbiol. 20:214–27
    [Google Scholar]
  183. 183. 
    Martinson VG, Moy J, Moran NA 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl. Environ. Microbiol. 78:2830–40
    [Google Scholar]
  184. 184. 
    McFrederick QS, Rehan SM. 2019. Wild bee pollen usage and microbial communities co-vary across landscapes. Microbial Ecol 77:513–22
    [Google Scholar]
  185. 185. 
    Guarna MM, Melathopoulos AP, Huxter E, Iovinella I, Parker R et al. 2015. A search for protein biomarkers links olfactory signal transduction to social immunity. BMC Genomics 16:63
    [Google Scholar]
/content/journals/10.1146/annurev-animal-020518-115045
Loading
/content/journals/10.1146/annurev-animal-020518-115045
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error