1932

Abstract

Bumble bees () are unusually important pollinators, with approximately 260 wild species native to all biogeographic regions except sub-Saharan Africa, Australia, and New Zealand. As they are vitally important in natural ecosystems and to agricultural food production globally, the increase in reports of declining distribution and abundance over the past decade has led to an explosion of interest in bumble bee population decline. We summarize data on the threat status of wild bumble bee species across biogeographic regions, underscoring regions lacking assessment data. Focusing on data-rich studies, we also synthesize recent research on potential causes of population declines. There is evidence that habitat loss, changing climate, pathogen transmission, invasion of nonnative species, and pesticides, operating individually and in combination, negatively impact bumble bee health, and that effects may depend on species and locality. We distinguish between correlational and causal results, underscoring the importance of expanding experimental research beyond the study of two commercially available species to identify causal factors affecting the diversity of wild species.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-011118-111847
2020-01-07
2024-10-04
Loading full text...

Full text loading...

/deliver/fulltext/ento/65/1/annurev-ento-011118-111847.html?itemId=/content/journals/10.1146/annurev-ento-011118-111847&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ahrne K, Bengtsson J, Elmqvist T 2009. Bumble bees (Bombus spp) along a gradient of increasing urbanization. PLOS ONE 4:e5574
    [Google Scholar]
  2. 2. 
    Aizen MA, Smith-Ramírez C, Morales CL, Vieli L, Sáez A et al. 2019. Coordinated species importation policies are needed to reduce serious invasions globally: the case of alien bumblebees in South America. J. Appl. Ecol. 56:100–6
    [Google Scholar]
  3. 3. 
    Aldridge G, Inouye DW, Forrest JR, Barr WA, Miller-Rushing AJ 2011. Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J. Ecol. 99:905–13
    [Google Scholar]
  4. 4. 
    An J-D, Huang J-X, Shao Y-Q, Zhang S-W, Wang B et al. 2014. The bumblebees of north China (Apidae, Bombus Latreille). Zootaxa 3830:1–89
    [Google Scholar]
  5. 5. 
    Arbetman MP, Gleiser G, Morales CL, Williams PH, Aizen MA 2017. Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence. Proc. R. Soc. B 284:20170204
    [Google Scholar]
  6. 6. 
    Bailey L, Gibbs J. 1964. Acute infection of bees with paralysis virus. J. Insect Pathol. 6:395–407
    [Google Scholar]
  7. 7. 
    Baron GL, Raine NE, Brown MJ 2017. General and species-specific impacts of a neonicotinoid insecticide on the ovary development and feeding of wild bumblebee queens. Proc. R. Soc. B 284:20170123
    [Google Scholar]
  8. 8. 
    Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL et al. 2013. Historical changes in northeastern US bee pollinators related to shared ecological traits. PNAS 110:4656–60
    [Google Scholar]
  9. 9. 
    Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S et al. 2011. Climate-associated phenological advances in bee pollinators and bee-pollinated plants. PNAS 108:20645–49
    [Google Scholar]
  10. 10. 
    Becher MA, Twiston-Davies G, Penny TD, Goulson D, Rotheray EL, Osborne JL 2018. Bumble-BEEHAVE: a systems model for exploring multifactorial causes of bumblebee decline at individual, colony, population and community level. J. Appl. Ecol. 55:2790–801
    [Google Scholar]
  11. 11. 
    Biella P, Bogliani G, Cornalba M, Manino A, Neumayer J et al. 2017. Distribution patterns of the cold adapted bumblebee Bombus alpinus in the Alps and hints of an uphill shift (Insecta: Hymenoptera: Apidae). J. Insect Conserv. 21:357–66
    [Google Scholar]
  12. 12. 
    Blackmore LM, Goulson D. 2014. Evaluating the effectiveness of wildflower seed mixes for boosting floral diversity and bumblebee and hoverfly abundance in urban areas. Insect Conserv. Divers. 7:480–84
    [Google Scholar]
  13. 13. 
    Bommarco R, Lundin O, Smith HG, Rundlöf M 2012. Drastic historic shifts in bumble-bee community composition in Sweden. Proc. R. Soc. B 279:309–15
    [Google Scholar]
  14. 14. 
    Bonmatin J-M, Giorio C, Girolami V, Goulson D, Kreutzweiser DP et al. 2015. Environmental fate and exposure; neonicotinoids and fipronil. Environ. Sci. Pollut. Res. 22:35–67
    [Google Scholar]
  15. 15. 
    Brown MJF, Schmid-Hempel R, Schmid-Hempel P 2003. Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. J. Anim. Ecol. 72:994–1002
    [Google Scholar]
  16. 16. 
    Brown MJF. 2017. Microsporidia: an emerging threat to bumblebees?. Trends Parasitol 33:754–62
    [Google Scholar]
  17. 17. 
    Brown MJF, Loosli R, Schmid-Hempel P 2000. Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–27
    [Google Scholar]
  18. 18. 
    Brunner FS, Schmid-Hempel P, Barribeau SM 2014. Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris. Proc. R. Soc. B 281:20140128
    [Google Scholar]
  19. 19. 
    Butler D. 2018. EU expected to vote on pesticide ban after major scientific review. Nature 555:150–51
    [Google Scholar]
  20. 20. 
    Cameron SA, Lim HC, Lozier JD, Duennes MA, Thorp R 2016. Test of the invasive pathogen hypothesis of bumble bee decline in North America. PNAS 113:4386–91
    [Google Scholar]
  21. 21. 
    Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N et al. 2011. Patterns of widespread decline in North American bumble bees. PNAS 108:662–67
    [Google Scholar]
  22. 22. 
    Carvell C, Bourke AFG, Dreier S, Freeman SN, Hulmes S et al. 2017. Bumblebee family lineage survival is enhanced in high-quality landscapes. Nature 543:547–49
    [Google Scholar]
  23. 23. 
    Carvell C, Bourke AFG, Osborne JL, Heard MS 2015. Effects of an agri-environment scheme on bumblebee reproduction at local and landscape scales. Basic Appl. Ecol. 16:519–30
    [Google Scholar]
  24. 24. 
    Charman TG, Sears J, Green RE, Bourke AFG 2010. Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus). Mol. Ecol. 19:2661–74
    [Google Scholar]
  25. 25. 
    Colla SR, Gadallah F, Richardson L, Wagner DL, Gall LF 2012. Assessing declines of North American bumble bees (Bombus spp) using museum specimens. Biodivers. Conserv. 21:3585–95
    [Google Scholar]
  26. 26. 
    Colla SR, Otterstatter MC, Gegear RJ, Thomson JD 2006. Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol. Conserv. 129:461–67
    [Google Scholar]
  27. 27. 
    Colla SR, Packer L. 2008. Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodivers. Conserv. 17:1379–91
    [Google Scholar]
  28. 28. 
    Connop S, Hill T, Steer J, Shaw P 2010. The role of dietary breadth in national bumblebee (Bombus) declines: simple correlation?. Biol. Conserv. 143:2739–46
    [Google Scholar]
  29. 29. 
    Conroy TJ, Palmer-Young EC, Irwin RE, Adler LS 2016. Food limitation affects parasite load and survival of Bombus impatiens (Hymenoptera: Apidae) infected with Crithidia (Trypanosomatida: Trypanosomatidae). Environ. Entomol. 45:1212–19
    [Google Scholar]
  30. 30. 
    Cordes N, Huang WF, Strange JP, Cameron SA, Griswold TL et al. 2012. Interspecific geographic distribution and variation of the pathogens Nosema bombi and Crithidia species in United States bumble bee populations. J. Invertebr. Pathol. 109:209–16
    [Google Scholar]
  31. 31. 
    Craddock HA, Huang D, Turner PC, Quiros-Alcala L, Payne-Sturges DC 2019. Trends in neonicotinoid pesticide residues in food and water in the United States, 1999–2015. Environ. Health 18:7
    [Google Scholar]
  32. 32. 
    Cresswell JE, Robert F-XL, Florance H, Smirnoff N 2014. Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Manag. Sci. 70:332–37
    [Google Scholar]
  33. 33. 
    Czerwinski MA, Sadd BM. 2017. Detrimental interactions of neonicotinoid pesticide exposure and bumblebee immunity. J. Exp. Zool. A 327:273–83
    [Google Scholar]
  34. 34. 
    Dance C, Botías C, Goulson D 2017. The combined effects of a monotonous diet and exposure to thiamethoxam on the performance of bumblebee micro-colonies. Ecotoxicol. Environ. Saf. 139:194–201
    [Google Scholar]
  35. 35. 
    Darvill B, Ellis JS, Lye GC, Goulson D 2006. Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol. Ecol. 15:601–11
    [Google Scholar]
  36. 36. 
    Darvill B, O'Connor S, Lye GC, Waters J, Lepais O, Goulson D 2010. Cryptic differences in dispersal lead to differential sensitivity to habitat fragmentation in two bumblebee species. Mol. Ecol. 19:53–63
    [Google Scholar]
  37. 37. 
    Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E et al. 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. PNAS 110:18466–71
    [Google Scholar]
  38. 38. 
    Diekötter T, Walther-Hellwig K, Conradi M, Suter M, Frankl R 2006. Effects of landscape elements on the distribution of the rare bumblebee species Bombus muscorum in an agricultural landscape. Biodivers. Conserv. 15:57–68
    [Google Scholar]
  39. 39. 
    Doublet V, Labarussias M, de Miranda JR, Moritz RF, Paxton RJ 2015. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 17:969–83
    [Google Scholar]
  40. 40. 
    Douglas MR, Rohr JR, Tooker JF 2015. Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield. J. Appl. Ecol. 52:250–60
    [Google Scholar]
  41. 41. 
    Douglas MR, Tooker JF. 2015. Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. field crops. Environ. Sci. Technol. 49:5088–97
    [Google Scholar]
  42. 42. 
    Ellis C, Park KJ, Whitehorn P, David A, Goulson D 2017. The neonicotinoid insecticide thiacloprid impacts upon bumblebee colony development under field conditions. Environ. Sci. Technol. 51:1727–32
    [Google Scholar]
  43. 43. 
    Ellis JS, Knight ME, Darvill B, Goulson D 2006. Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Mol. Ecol. 15:4375–86
    [Google Scholar]
  44. 44. 
    Eur. Food Saf. Auth 2015. Peer review of the pesticide risk assessment for bees for the active substance imidacloprid considering all uses other than seed treatments and granules. EFSA J 13:4211
    [Google Scholar]
  45. 45. 
    Fauser A, Sandrock C, Neumann P, Sadd B 2017. Neonicotinoids override a parasite exposure impact on hibernation success of a key bumblebee pollinator. Ecol. Entomol. 42:306–14
    [Google Scholar]
  46. 46. 
    Fauser-Misslin A, Sadd B, Neumann P, Sandrock C 2014. Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. J. Appl. Ecol. 51:450–59
    [Google Scholar]
  47. 47. 
    Fed. Reg 2019. Product cancellation order for certain pesticide registrations News release, May 20. https://www.federalregister.gov/documents/2019/05/20/2019-10447/product-cancellation-order-for-certain-pesticide-registrations
    [Google Scholar]
  48. 48. 
    Fitter AH, Fitter RSR. 2002. Rapid changes in flowering time in British plants. Science 296:1689–91
    [Google Scholar]
  49. 49. 
    Flanders RV, Wehling WF, Craghead AL 2003. Laws and regulations on the import, movement and release of bees in the United States. For Nonnative Crops: Whence Pollinators of the Future? K Strickler, JH Cane 99–111 Lanham, MD: Entomol. Soc. Am.
    [Google Scholar]
  50. 50. 
    Fries I. 2010. Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 103:S73–79
    [Google Scholar]
  51. 51. 
    Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MFJ 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–66
    [Google Scholar]
  52. 52. 
    Gamboa V, Ravoet J, Brunain M, Smagghe G, Meeus I et al. 2015. Bee pathogens found in Bombus atratus from Colombia: a case study. J. Invertebr. Pathol. 129:36–39
    [Google Scholar]
  53. 53. 
    Gegear RJ, Otterstatter MC, Thomson JD 2006. Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc. R. Soc. B 273:1073–78
    [Google Scholar]
  54. 54. 
    Gill RJ, Raine NE. 2014. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Funct. Ecol. 28:1459–71
    [Google Scholar]
  55. 55. 
    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]
  56. 56. 
    Gillespie SD, Adler SL. 2013. Indirect effects on mutualisms: parasitism of bumble bees and pollination service to plants. Ecology 94:454–64
    [Google Scholar]
  57. 57. 
    Glaum P, Simao MC, Vaidya C, Fitch G, Iulinao B 2017. Big city Bombus: using natural history and land-use history to find significant environmental drivers in bumble-bee declines in urban development. R. Soc. Open Sci. 4:170156
    [Google Scholar]
  58. 58. 
    Godfray HCJ, Blacquiere T, Field LM, Hails RS, Potts SG et al. 2015. A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. B 282:20151821
    [Google Scholar]
  59. 59. 
    Goulson D, Lepais O, O'Connor S, Osborne JL, Sanderson RA et al. 2010. Effects of land use at a landscape scale on bumblebee nest density and survival. J. Appl. Ecol. 47:1207–15
    [Google Scholar]
  60. 60. 
    Goulson D, Nicholls E, Botías C, Rotheray EL 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957
    [Google Scholar]
  61. 61. 
    Gradish AE, van der Steen J, Scott-Dupree CD, Cabrera AR, Cutler GC et al. 2019. Comparison of pesticide exposure in honey bees (Hymenoptera: Apidae) and bumble bees (Hymenoptera: Apidae): implications for risk assessments. Environ. Entomol. 48:12–21
    [Google Scholar]
  62. 62. 
    Graystock P, Blane EJ, McFrederick QS, Goulson D, Hughes WOH 2016. Do managed bees drive parasite spread and emergence in wild bees?. Int. J. Parasitol. Parasites Wildl. 5:64–75
    [Google Scholar]
  63. 63. 
    Graystock P, Goulson D, Hughes WO 2015. Parasites in bloom: Flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc. R. Soc. B 282:20151371
    [Google Scholar]
  64. 64. 
    Graystock P, Meeus I, Smagghe G, Goulson D, Hughes WO 2016. The effects of single and mixed infections of Apicystis bombi and deformed wing virus in Bombus terrestris. Parasitology 143:358–65
    [Google Scholar]
  65. 65. 
    Graystock P, Yates K, Darvill B, Goulson D, Hughes WO 2013. Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J. Invertebr. Pathol. 114:114–19
    [Google Scholar]
  66. 66. 
    Graystock P, Yates K, Evison SE, Darvill B, Goulson D, Hughes WO 2013. The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J. Appl. Ecol. 50:1207–15
    [Google Scholar]
  67. 67. 
    Grixti JC, Wong LT, Cameron SA, Favret C 2009. Decline of bumble bees (Bombus) in the North American Midwest. Biol. Conserv. 142:75–84
    [Google Scholar]
  68. 68. 
    Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N et al. 2017. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLOS ONE 12:e0185809
    [Google Scholar]
  69. 69. 
    Hass AL, Brachmann L, Batáry P, Clough Y, Behling H, Tscharntke T 2019. Maize-dominated landscapes reduce bumblebee colony growth through pollen diversity loss. J. Appl. Ecol. 56:294–304
    [Google Scholar]
  70. 70. 
    Hatfield R, Jepsen S, Thorp R, Richardson L, Colla S 2016. The IUCN Red List of Threatened Species: North America Rep., Int. Union Conserv. Nat Gland, Switz:.
    [Google Scholar]
  71. 71. 
    Hatfield RG, LeBuhn G. 2007. Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane meadows. Biol. Conserv. 139:150–58
    [Google Scholar]
  72. 72. 
    Health Canada 2019. Health Canada releases final pollinator re-evaluation decisions for neonicotinoid pesticides News release, April 11. https://www.canada.ca/en/health-canada/news/2019/04/some-cancellations-and-new-restrictions-to-protect-bees-and-other-pollinators.html
    [Google Scholar]
  73. 73. 
    Herrera JM, Ploquin EF, Rasmont P, Obeso JR 2018. Climatic niche breadth determines the response of bumblebees (Bombus spp) to climate warming in mountain areas of the Northern Iberian Peninsula. J. Insect Conserv. 22:771–79
    [Google Scholar]
  74. 74. 
    Hines HM, Hendrix SD. 2005. Bumble bee (Hymenoptera: Apidae) diversity and abundance in tallgrass prairie patches: effects of local and landscape floral resources. Environ. Entomol. 34:1477–84
    [Google Scholar]
  75. 75. 
    Inoue MN, Yokoyama J, Washitani I 2008. Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L) (Hymenoptera: Apidae). J. Insect Conserv. 12:135–46
    [Google Scholar]
  76. 76. 
    Int. Union Conserv. Nat 2012. IUCN Red List Categories and Criteria: Version 3.1 Gland, Switz.: Int. Union Conserv. Nat. , 2nd ed.. https://portals.iucn.org/library/sites/library/files/documents/RL-2001-001-2nd.pdf
    [Google Scholar]
  77. 77. 
    Jackson JM, Pimsler ML, Oyen KJ, Koch-Uhuad JB, Herndon JD et al. 2018. Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude. Mol. Ecol. 27:2926–42
    [Google Scholar]
  78. 78. 
    Jacobson MM, Tucker EM, Mathiasson M, Rehan SM 2019. Decline of bumble bees in northeastern North America, with special focus on Bombus terricola. Biol. Conserv 217:437–45
    [Google Scholar]
  79. 79. 
    Jha S. 2015. Contemporary human-altered landscapes and oceanic barriers reduce bumble bee gene flow. Mol. Ecol. 24:993–1006
    [Google Scholar]
  80. 80. 
    Kelly AE, Goulden ML. 2008. Rapid shifts in plant distribution with recent climate change. PNAS 105:11823–26
    [Google Scholar]
  81. 81. 
    Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM 2009. Parasite spillback: a neglected concept in invasion ecology?. Ecology 90:2047–56
    [Google Scholar]
  82. 82. 
    Kent CF, Dey A, Patel H, Tsvetkov N, Tiwari T et al. 2018. Conservation genomics of the declining North American bumblebee Bombus terricola reveals inbreeding and selection on immune genes. Front. Genet. 9:316
    [Google Scholar]
  83. 83. 
    Kerr JT, Pindar A, Galpern P, Packer L, Potts SG et al. 2015. Climate change impacts on bumblebees converge across continents. Science 349:177–80
    [Google Scholar]
  84. 84. 
    Kevan PG. 2008. Bombus franklini The IUCN Red List of Threatened Species 2008, e.T135295A4070259 Gland, Switz.: Int. Union Conserv. Nat https://www.iucnredlist.org/species/135295/4070259
    [Google Scholar]
  85. 85. 
    Kleijn D, Raemakers I. 2008. A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89:1811–23
    [Google Scholar]
  86. 86. 
    Koch H, Brown MJ, Stevenson PC 2017. The role of disease in bee foraging ecology. Curr. Opin. Insect Sci. 21:60–67
    [Google Scholar]
  87. 87. 
    Koch J, Lozier J, Ikerd H, Griswold T, Cordes N et al. 2015. USBombus, a database of contemporary survey data for North American bumble bees (Hymenoptera, Apidae, Bombus) distributed in the United States. Biodivers. Data J. 3:e6833
    [Google Scholar]
  88. 88. 
    Koch JB, Strange JP. 2012. The status of Bombus occidentalis and B. moderatus in Alaska with special focus on Nosema bombi incidence. Northwest Sci 86:212–21
    [Google Scholar]
  89. 89. 
    Koh I, Lonsdorf EV, Williams NM, Brittain C, Isaacs R et al. 2016. Modeling the status, trends, and impacts of wild bee abundance in the United States. PNAS 113:140–45
    [Google Scholar]
  90. 90. 
    Laycock I, Cotterell KC, O'Shea-Wheller TA, Cresswell JE 2014. Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. Ecotoxicol. Environ. Saf. 100:153–58
    [Google Scholar]
  91. 91. 
    Le Féon V, Schermann-Legionnet A, Delettre Y, Aviron S, Billeter R et al. 2010. Intensification of agriculture, landscape composition and wild bee communities: a large scale study in four European countries. Agric. Ecosyst. Environ. 137:143–50
    [Google Scholar]
  92. 92. 
    Lelej A, Proshchalykin M, Loktionov V, Antropov A, Astafurova Y, Zaytseva LA 2017. Annotated Catalogue of the Insects of Russian Far East Vladivostok, Russ: Dalnauka
    [Google Scholar]
  93. 93. 
    Leza M, Watrous KM, Bratu J, Woodard SH 2018. Effects of neonicotinoid insecticide exposure and monofloral diet on nest-founding bumblebee queens. Proc. R. Soc. B 285:20180761
    [Google Scholar]
  94. 94. 
    Li J, Chen W, Wu J, Peng W, An J et al. 2012. Diversity of Nosema associated with bumblebees (Bombus spp) from China. Int. J. Parasitol. 42:49–61
    [Google Scholar]
  95. 95. 
    Logan A, Ruiz-González MX, Brown MJF 2005. The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology 130:637–42
    [Google Scholar]
  96. 96. 
    Looney C, Strange JP, Freeman M, Jennings D 2019. The expanding Pacific Northwest range of Bombus impatiens Cresson and its establishment in Washington State. Biol. Invasions 21:1879–85
    [Google Scholar]
  97. 97. 
    Lozier JD, Cameron SA. 2009. Comparative genetic analyses of historical and contemporary collections highlight contrasting demographic histories for the bumble bees Bombus pensylvanicus and B. impatiens in Illinois. Mol. Ecol. 18:962–1083
    [Google Scholar]
  98. 98. 
    Maebe K, Meeus I, Maharramov J, Grootaert P, Michez D et al. 2013. Microsatellite analysis in museum samples reveals inbreeding before the regression of Bombus veteranus. Apidologie 44:188–97
    [Google Scholar]
  99. 99. 
    Maharramov J, Meeus I, Maebe K, Arbetman M, Morales C et al. 2013. Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLOS ONE 8:e81475
    [Google Scholar]
  100. 100. 
    Malfi RL, Walter JA, Roulston TAH, Stuligross C, McIntosh S, Bauer L 2018. The influence of conopid flies on bumble bee colony productivity under different food resource conditions. Ecol. Monogr. 88:653–71
    [Google Scholar]
  101. 101. 
    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]
  102. 102. 
    Manley R, Boots M, Wilfert L 2017. Condition-dependent virulence of slow bee paralysis virus in Bombus terrestris: Are the impacts of honeybee viruses in wild pollinators underestimated?. Oecologia 184:305–15
    [Google Scholar]
  103. 103. 
    Martinet B, Lecocq T, Smet J, Rasmont P 2015. A protocol to assess insect resistance to heat waves, applied to bumblebees (Bombus Latreille, 1802). PLOS ONE 10:e0118591
    [Google Scholar]
  104. 104. 
    Martinet B, Rasmont P, Cederberg B, Evrard D, Ødegaard F et al. 2015. Forward to the north: Two Euro-Mediterranean bumblebee species now cross the Arctic Circle. Ann. Soc. Entomol. France 51:303–9
    [Google Scholar]
  105. 105. 
    Martins AC, Melo GA. 2010. Has the bumblebee Bombus bellicosus gone extinct in the northern portion of its distribution range in Brazil?. J. Insect Conserv. 14:207–10
    [Google Scholar]
  106. 106. 
    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 284:20172181
    [Google Scholar]
  107. 107. 
    McFrederick QS, LeBuhn G. 2006. Are urban parks refuges for bumble bees Bombus spp (Hymenoptera: Apidae)?. Biol. Conserv. 129:372–82
    [Google Scholar]
  108. 108. 
    McMahon DP, Fürst MA, Caspar J, Theodorou P, Brown MJ, Paxton RJ 2015. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J. Anim. Ecol. 84:615–24
    [Google Scholar]
  109. 109. 
    Meeus I, de Miranda JR, de Graaf DC, Wäckers F, Smagghe G 2014. Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success. J. Invertebr. Pathol. 121:64–69
    [Google Scholar]
  110. 110. 
    Mideo N, Alizon S, Day T 2008. Linking within-and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23:511–17
    [Google Scholar]
  111. 111. 
    Miller-Struttmann NE, Geib JC, Franklin JD, Kevan PG, Holdo RM et al. 2015. Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349:1541–44
    [Google Scholar]
  112. 112. 
    Moerman R, Vanderplanck M, Fournier D, Jacquemart AL, Michez D 2017. Pollen nutrients better explain bumblebee colony development than pollen diversity. Insect Conserv. Divers. 10:171–79
    [Google Scholar]
  113. 113. 
    Moffat C, Buckland ST, Samson AJ, McArthur R, Pino VC et al. 2016. Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees. Sci. Rep. 6:24764
    [Google Scholar]
  114. 114. 
    Moffat C, Pacheco JG, Sharp S, Samson AJ, Bollan KA et al. 2015. Chronic exposure to neonicotinoids increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris). FASEB J 29:2112–19
    [Google Scholar]
  115. 115. 
    Morales C, Montalva J, Arbetman M, Aizen MA, Smith-Ramírez C et al. 2016. Bombus dahlbomii. In The IUCN Red List of Threatened Species 2016 Gland, Switz.: Int. Union Conserv. Nat. https://www.iucnredlist.org/species/21215142/100240441
    [Google Scholar]
  116. 116. 
    Morales CL, Arbetman MP, Cameron SA, Aizen MA 2013. Rapid ecological replacement of a native bumble bee by invasive species. Front. Ecol. Environ. 11:529–34
    [Google Scholar]
  117. 117. 
    Morens DM, Folkers GK, Fauci AS 2004. The challenge of emerging and re-emerging infectious diseases. Nature 430:242–49
    [Google Scholar]
  118. 118. 
    Murray TE, Coffey MF, Kehoe E, Horgan FG 2013. Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biol. Conserv. 159:269–76
    [Google Scholar]
  119. 119. 
    Naeem M, Yuan X, Huang J, An J 2018. Habitat suitability for the invasion of Bombus terrestris in East Asian countries: a case study of spatial overlap with local Chinese bumblebees. Sci. Rep. 8:11035
    [Google Scholar]
  120. 120. 
    Niu J, Meeus I, Smagghe G 2016. Differential expression pattern of Vago in bumblebee (Bombus terrestris), induced by virulent and avirulent virus infections. Sci. Rep. 6:34200
    [Google Scholar]
  121. 121. 
    O'Connor S, Park KJ, Goulson D 2012. Humans versus dogs; a comparison of methods for the detection of bumble bee nests. J. Apic. Res. 51:204–11
    [Google Scholar]
  122. 122. 
    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]
  123. 123. 
    Ollerton J. 2017. Pollinator diversity: distribution, ecological function, and conservation. Annu. Rev. Ecol. Evol. Syst. 48:353–76
    [Google Scholar]
  124. 124. 
    Ollerton J, Erenler H, Edwards M, Crockett R 2014. Pollinator declines: extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346:1360–62
    [Google Scholar]
  125. 125. 
    Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME et al. 2008. Bumblebee flight distances in relation to the forage landscape. J. Anim. Ecol. 77:406–15
    [Google Scholar]
  126. 126. 
    Otterstatter MC, Thomson JD. 2006. Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology 133:749–61
    [Google Scholar]
  127. 127. 
    Otti O, Schmid-Hempel P. 2007. Nosema bombi: a pollinator parasite with detrimental fitness effects. J. Invertebr. Pathol. 96:118–24
    [Google Scholar]
  128. 128. 
    Otti O, Schmid-Hempel P. 2008. A field experiment on the effect of Nosema bombi in colonies of the bumblebee Bombus terrestris. Ecol. Entomol 33:577–82
    [Google Scholar]
  129. 129. 
    Owen RE, Otterstatter MC, Cartar RV, Farmer A, Colla SR, O'Toole N 2012. Significant expansion of the distribution of the bumble bee Bombus moderatus (Hymenoptera: Apidae) in Alberta over 20 years. Can. J. Zool. 90:133–38
    [Google Scholar]
  130. 130. 
    Oyen KJ, Giri S, Dillon ME 2016. Altitudinal variation in bumble bee (Bombus) critical thermal limits. J. Thermal Biol. 59:52–57
    [Google Scholar]
  131. 131. 
    Palmier KM, Sheffield CS. 2019. First records of the Common Eastern Bumble Bee, Bombus impatiens Cresson (Hymenoptera: Apidae, Apinae, Bombini) from the prairies ecozone in Canada. Biodivers. Data J. 7:e30953
    [Google Scholar]
  132. 132. 
    Pascall DJ, Tinsley MC, Obbard DJ, Wilfert L 2019. Host evolutionary history predicts virus prevalence across bumblebee species. bioRxiv 498717. https://doi.org/10.1101/498717
    [Crossref]
  133. 133. 
    Peng W, Li J, Boncristiani H, Strange JP, Hamilton M, Chen Y 2011. Host range expansion of honey bee black queen cell virus in the bumble bee, Bombus huntii. Apidologie 42:650–58
    [Google Scholar]
  134. 134. 
    Piot N, Meeus I, Kleijn D, Scheper J, Linders T, Smagghe G 2019. Establishment of wildflower fields in poor quality landscapes enhances micro-parasite prevalence in wild bumble bees. Oecologia 189:149–58
    [Google Scholar]
  135. 135. 
    Plischuk S, Sanscrainte ND, Becnel JJ, Estep AS, Lange CE 2015. Tubulinosema pampeana spn. (Microsporidia, Tubulinosematidae), a pathogen of the South American bumble bee Bombus atratus. J. Invertebr. Pathol 126:31–42
    [Google Scholar]
  136. 136. 
    Ploquin EF, Herrera JM, Obeso JR 2013. Bumblebee community homogenization after uphill shifts in montane areas of northern Spain. Oecologia 173:1649–60
    [Google Scholar]
  137. 137. 
    Pope NS, Jha S. 2018. Seasonal food scarcity prompts long-distance foraging by a wild social bee. Am. Nat. 191:45–57
    [Google Scholar]
  138. 138. 
    Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE 2010. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25:345–53
    [Google Scholar]
  139. 139. 
    Potts SG, Imperatriz-Fonseca VL, Ngo HT, Biesmeijer JC, Breeze TD et al. 2016. IPBES: summary for policymakers of the assessment report of the Intergovernmental Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production Rep., Intergov. Panel Biodivers. Ecosyst. Serv., U.N. Environ. Progr Bonn, Ger: https://www.ipbes.net/system/tdf/spm_deliverable_3a_pollination_20170222.pdf?file=1&type=node&id=15248
    [Google Scholar]
  140. 140. 
    Pradervand JN, Pellissier L, Randin CF, Guisan A 2014. Functional homogenization of bumblebee communities in alpine landscapes under projected climate change. Clim. Change Responses 1:1
    [Google Scholar]
  141. 141. 
    Pyke GH, Thomson JD, Inouye DW, Miller TJ 2016. Effects of climate change on phenologies and distributions of bumble bees and the plants they visit. Ecosphere 7:e01267
    [Google Scholar]
  142. 142. 
    Rao S, Strange JP. 2012. Bumble bee (Hymenoptera: Apidae) foraging distance and colony density associated with a late-season mass flowering crop. Environ. Entomol. 41:905–15
    [Google Scholar]
  143. 143. 
    Rasmont P, Franzen M, Lecocq T, Harpke A, Roberts SPM et al. 2015. Climatic risk and distribution atlas of European bumblebees. BioRisk 10:1–236
    [Google Scholar]
  144. 144. 
    Rasmont P, Iserbyt S. 2014. Atlas of the European Bees: Genus Bombus Reading, UK: STEP Proj. , 3rd ed.. http://www.atlashymenoptera.net/page.asp?ID=169
    [Google Scholar]
  145. 145. 
    Rasmont P, Iserbyt S. 2012. The bumblebees scarcity syndrome: Are heat waves leading to local extinctions of bumblebees (Hymenoptera: Apidae: Bombus)?. Ann. Soc. Entomol. France 48:275–80
    [Google Scholar]
  146. 146. 
    Redhead JW, Dreier S, Bourke AFG, Heard MS, Jordan WC et al. 2016. Effects of habitat composition and landscape structure on worker foraging distances of five bumble bee species. Ecol. Appl. 26:726–39
    [Google Scholar]
  147. 147. 
    Ruiz-González MX, Bryden J, Moret Y, Reber-Funk C, Schmid-Hempel P, Brown MJ 2012. Dynamic transmission, host quality, and population structure in a multihost parasite of bumblebees. Evolution 66:3053–66
    [Google Scholar]
  148. 148. 
    Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederstrom V et al. 2015. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80
    [Google Scholar]
  149. 149. 
    Rutrecht ST, Brown MJ. 2008. The life-history impact and implications of multiple parasites for bumble bee queens. Int. J. Parasitol. 38:799–808
    [Google Scholar]
  150. 150. 
    Sachman-Ruiz B, Narváez-Padilla V, Reynaud E 2015. Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México. Biol. Invasions 17:2043–53
    [Google Scholar]
  151. 151. 
    Sadd BM, Barribeau SM. 2013. Heterogeneity in infection outcome: lessons from a bumblebee-trypanosome system. Parasite Immunol 35:339–49
    [Google Scholar]
  152. 152. 
    Sadd BM, Barribeau SM, Bloch G, de Graaf DC, Dearden P et al. 2015. The genomes of two key bumblebee species with primitive eusocial organization. Genome Biol 16:76
    [Google Scholar]
  153. 153. 
    Sanchez-Bayo F, Goka K. 2014. Pesticide residues and bees—a risk assessment. PLOS ONE 9:e94482
    [Google Scholar]
  154. 154. 
    Sanchez-Bayo F, Wyckhuys KAG. 2019. Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232:8–27
    [Google Scholar]
  155. 155. 
    Schmid-Hempel R, Eckhardt M, Goulson D, Heinzmann D, Lange C et al. 2014. The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol. 83:823–37
    [Google Scholar]
  156. 156. 
    Schmid-Hempel R, Schmid-Hempel P. 1998. Colony performance and immunocompetence of a social insect, Bombus terrestris, in poor and variable environments. Funct. Ecol. 12:22–30
    [Google Scholar]
  157. 157. 
    Scholer J, Krischik V. 2014. Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of Bombus impatiens. PLOS ONE 9:e91573
    [Google Scholar]
  158. 158. 
    Schoonvaere K, Smagghe G, Francis F, de-Graaf DC 2018. Study of the metatranscriptome of eight social and solitary wild bee species reveals novel viruses and bee parasites. Front. Microbiol. 9:177
    [Google Scholar]
  159. 159. 
    Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE et al. 2010. Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol. Rev. 85:777–95
    [Google Scholar]
  160. 160. 
    Sgolastra F, Medrzycki P, Bortolotti L, Renzi MT, Tosi S et al. 2017. Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Manag. Sci. 73:1236–43
    [Google Scholar]
  161. 161. 
    Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M et al. 2015. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. 22:5–34
    [Google Scholar]
  162. 162. 
    Siviter H, Brown MJF, Leadbeater E 2018. Sulfoxaflor exposure reduces bumblebee reproductive success. Nature 561:109–12
    [Google Scholar]
  163. 163. 
    Stanley DA, Garratt MPD, Wickens JB, Wickens VJ, Potts SG, Raine NE 2015. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528:548–50
    [Google Scholar]
  164. 164. 
    Stanley DA, Raine NE. 2016. Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants. Funct. Ecol. 30:1132–39
    [Google Scholar]
  165. 165. 
    Stanley DA, Smith KE, Raine NE 2015. Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Sci. Rep. 5:16508
    [Google Scholar]
  166. 166. 
    Sutherland WJ, Barnard P, Broad S, Clout M, Connor B et al. 2017. A 2017 Horizon scan of emerging issues for global conservation and biological diversity. Trends Ecol. Evol. 32:31–40
    [Google Scholar]
  167. 167. 
    Tooker JF, Douglas MR, Krupke CH 2017. Neonicotinoid seed treatments: limitations and compatibility with integrated pest management. Agric. Environ. Lett. 2:170026
    [Google Scholar]
  168. 168. 
    Torres-Ruiz A, Jones RW. 2012. Comparison of the efficiency of the bumble bees Bombus impatiens and Bombus ephippiatus (Hymenoptera: Apidae) as pollinators of tomato in greenhouses. J. Econ. Entomol. 105:1871–77
    [Google Scholar]
  169. 169. 
    van der Sluijs JP, Amaral-Rogers V, Belzunces LP, Bijleveld van Lexmond MFIJ, Bonmatin JM et al. 2015. Conclusions of the worldwide integrated assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning. Environ. Sci. Pollut. Res. 22:148–54
    [Google Scholar]
  170. 170. 
    van Der Steen JJ. 2008. Infection and transmission of Nosema bombi in Bombus terrestris colonies and its effect on hibernation, mating and colony founding. Apidologie 39:273–82
    [Google Scholar]
  171. 171. 
    Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM 2016. Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. PNAS 113:E4035–42
    [Google Scholar]
  172. 172. 
    Vaudo AD, Tooker JF, Grozinger CM, Patch HM 2015. Bee nutrition and floral resource restoration. Curr. Opin. Insect Sci. 10:113–41
    [Google Scholar]
  173. 173. 
    Vereecken NJ. 2017. A phylogenetic approach to conservation prioritization for Europe's bumblebees (Hymenoptera: Apidae: Bombus). Biol. Conserv. 206:21–30
    [Google Scholar]
  174. 174. 
    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]
  175. 175. 
    Whitehorn PR, Tinsley MC, Brown MJ, Goulson D 2013. Investigating the impact of deploying commercial Bombus terrestris for crop pollination on pathogen dynamics in wild bumble bees. J. Apic. Res. 52:149–57
    [Google Scholar]
  176. 176. 
    Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R et al. 2016. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351:594–97
    [Google Scholar]
  177. 177. 
    Williams PH. 1982. The distribution and decline of British bumble bees (Bombus Latr). J. Apic. Res. 21:236–45
    [Google Scholar]
  178. 178. 
    Williams PH. 1986. Environmental change and the distributions of British bumble bees (Bombus Latr). Bee World 67:50–61
    [Google Scholar]
  179. 179. 
    Williams PH. 2005. Does specialization explain rarity and decline among British bumblebees? A response to Goulson et al. Biol. Conserv. 122:33–43
    [Google Scholar]
  180. 180. 
    Williams PH, Araújo MB, Rasmont P 2007. Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth?. Biol. Conserv. 138:493–505
    [Google Scholar]
  181. 181. 
    Williams PH, Huang J-X, An J-D 2017. Bear wasps of the middle kingdom: a decade of discovering China's bumblebees. Antenna 41:21–24
    [Google Scholar]
  182. 182. 
    Williams PH, Jepsen S. 2018. Bumblebee Specialist Group report 2018 Rep., Bumblebee Spec. Group, Int. Union Conserv. Nat Gland, Switz: https://bumblebeespecialistgroup.org/wp-content/uploads/2019/03/BBSG-Annual-Report-2018.pdf
    [Google Scholar]
  183. 183. 
    Williams PH, Osborne JL. 2009. Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–87
    [Google Scholar]
  184. 184. 
    Winfree R, Bartomeus I, Cariveau DP 2011. Native pollinators in anthropogenic habitats. Annu. Rev. Ecol. Evol. Syst. 42:1–22
    [Google Scholar]
  185. 185. 
    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 359:791–93
    [Google Scholar]
  186. 186. 
    Wintermantel D, Locke B, Andersson GKS, Semberg E, Forsgren E et al. 2018. Field-level clothianidin exposure affects bumblebees but generally not their pathogens. Nat. Commun. 9:5446
    [Google Scholar]
  187. 187. 
    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]
  188. 188. 
    Wood TJ, Goulson D. 2017. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ. Sci. Pollut. Res. 24:17285–325
    [Google Scholar]
  189. 189. 
    Wood TJ, Holland JM, Hughes WO, Goulson D 2015. Targeted agri-environment schemes significantly improve the population size of common farmland bumblebee species. Mol. Ecol. 24:1668–80
    [Google Scholar]
  190. 190. 
    Xie Z, Williams PH, Tang Y 2008. The effect of grazing on bumblebees in the high rangelands of the east Tibetan Plateau of Sichuan. J. Insect Conserv. 12:695–703
    [Google Scholar]
/content/journals/10.1146/annurev-ento-011118-111847
Loading
/content/journals/10.1146/annurev-ento-011118-111847
Loading

Data & Media loading...

Supplementary Data

  • 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