Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México

Biological Invasions

Volumn 17, Issue 7, 2015, Pages 2043-2053

  Sachman Ruiz, Bernardo ^a,b   Narváez Padilla, Verónica ^c   Reynaud, Enrique ^d  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^b INSTITUTO NACIONAL DE INVESTIGACIONES FORESTALES   (Mexico)

^c UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^d INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Bumble bee diagnosis; Colony collapse disorder; Emerging infectious diseases; Pathogen spillover

Indexed keywords

BEE; COLONY; COLONY STRUCTURE; COMMERCIAL SPECIES; COMMERCIALIZATION; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; INVASIVE SPECIES; NATIVE SPECIES; POLLINATION; POLLINATOR; POPULATION DECLINE; RELATIVE ABUNDANCE; SELECTION; WILD POPULATION;

MEXICO [NORTH AMERICA];

APIS MELLIFERA; BOMBUS (GENUS); BOMBUS IMPATIENS; CHRONIC BEE PARALYSIS VIRUS; DEFORMED WING VIRUS; LOCUSTACARUS BUCHNERI; NOSEMA BOMBI;

EID: 84930376528     PISSN: 13873547     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10530-015-0859-6     Document Type: Article

References (52)

1. Al-Abbadi AA, Hassawi DS, Abu-Mallouh SA, Al-mazra MS (2010) Novel detection of Israel acute paralysis virus and Kashmir bee virus from honeybees Apis mellifera L. (Hymenoptera: Apidae) of Jordan using reverse transcriptase PCR technique. Appl Entomol Zool 45:183–190
2. Arbetman MP, Meeus I, Morales CL, Aizen M, Smagghe G (2012) Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol Invasions 15:489–494
3. Bailey L, Gibbs AJ, Woods RD (1963) Two viruses from adult honey bees (Apies mellifera L.). Virology 21:390–395
4. Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Topolska G, Ritter W, Pechhacker H, Nowotny N (2007) Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Appl Environ Microbiol 73:3605–3611
5. Blanchard P, Schurr F, Celle O, Cougoule N, Drajnudel P, Thiéry R, Faucon JP, Ribière M (2008) First detection of Israeli acute paralysis virus (IAPV) in France, a dicistrovirus affecting honeybees (Apis mellifera). J Invertebr Pathol 99:348–350
6. Brown MJF (2011) The trouble with bumblebees. Nature 469:169–170
7. Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427
8. 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
9. Cameron SA, Lozier JD, Strange JP, Koch JP, Cordes N, Solter LF (2010) Patterns of widespread decline in North American bumble bees. PNAS 108:662–667
10. Celle O, Blanchard P, Olivier V, Schurr F, Cougoule N, Faucon JP, Ribière M (2008) Detection of Chronic bee paralysis virus (CBPV) genome and its replicative RNA form in various hosts and possible ways of spread. Virus Res 133:280–284
11. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467
12. 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 (80-) 318:283–287
13. De Miranda JR, Drebot M, Tyler S, Shen M, Cameron CE, Stoltz DB, Camazine SM (2004) Complete nucleotide sequence of Kashmir bee virus and comparison with acute bee paralysis virus. J Gen Virol 85:2263–2270
14. Duennes MA, Lozier JD, Hines HM, Cameron SA (2012a) Geographical patterns of genetic divergence in the widespread Mesoamerican bumble bee Bombus ephippiatus (Hymenoptera: Apidae). Mol Phylogenet Evol 64:219–231
15. Duennes MA, Lozier JD, Hines HM, Cameron SA (2012b) Molecular phylogenetics and evolution geographical patterns of genetic divergence in the widespread Mesoamerican bumble bee Bombus ephippiatus (Hymenoptera: Apidae). Mol Phylogenet Evol 64:219–231
16. Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366
17. Gallai N, Salles J-M, Settele J, Vaissiére BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821
18. Gillespie S (2010) Factors affecting parasite prevalence among wild bumblebees. Ecol Entomol 35:737–747
19. Goka K (2010a) Introduction to the Special Feature for Ecological Risk Assessment of Introduced Bumblebees: status of the European bumblebee, Bombus terrestris, in Japan as a beneficial pollinator and an invasive alien species. Appl Entomol Zool 45:1–6
20. Goka K (2010b) Biosecurity measures to prevent the incursion of invasive alien species into Japan and to mitigate their impact The Invasive Alien Species Act in Japan. Rev Sci Tech Off Int Epiz 29:299–310
21. Goka K, Okabe K, Yoneda M, Niwa S (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites. Mol Ecol 10:2095–2099
22. Govan VA, Leat N, Allsopp M, Davison S (2000) Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology 277:457–463
23. Graystock P, Yates K, Evison SEF, et al (2013) The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J Appl Ecol 1207–1215
24. Graystock P, Goulson D, Hughes W. (2014) The relationship between managed bees and the prevalence of parasites in bumblebees. PeerJ 2:e522. doi:10.7717/peerj.522
25. Kearns CA, Thomson JD (2001) The natural history of bumblebees: a sourcebook for investigation. University Press of Colorado, Colorado
26. Kissinger CN, Cameron SA, Thorp RW, White B, Solter L, Hill G (2011) Survey of bumble bee (Bombus) pathogens and parasites in Illinois and selected areas of northern California and southern Oregon. J Invertebr Pathol 107:220–224
27. Kondo NI, Yamanaka D, Kanbe Y, Kawate YK, Yoneda M, Tsuchida K, Goka K (2009) Reproductive disturbance of Japanese bumblebees by the introduced European bumblebee Bombus terrestris. Naturwissenschaften 96:467–475
28. Kukielka D, Sánchez-Vizcaíno JM (2010) First detection of Israeli Acute Paralysis Virus (IAPV) in Spanish honeybees. Spanish J Agric Res 8:308–311
29. Lanzi G, De Miranda JR, Boniotti MB, Cameron C, Lavazza A, Capucci L, Camazine SM, Rossi C (2006) Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.). J Virol 80:4998–5009
30. Maharramov J, Meeus I, Maebe K et al (2013) Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS ONE 8:6–13
31. Maori E, Lavi S, Mozes-Koch R et al (2007) Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination. J Gen Virol 88:3428–3438
32. Meeus I, de Graaf DC, Jans K, Smagghe G (2010a) Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109:107–115
33. Meeus I, Smagghe G, Siede R, Jans K, de Graaf GC (2010b) Multiplex RT-PCR with broad-range primers and an exogenous internal amplification control for the detection of honeybee viruses in bumblebees. J Invertebr Pathol 105:200–203
34. Meeus I, Brown MJF, De Graaf DC, Smagghe G (2011) Effects of invasive parasites on bumble bee declines. Conserv Biol 25:662–671
35. Morkeski A, Averil lAL (2010) Wild bee status and evidence for pathogen spillover with honey bees. Am Bee J 150(11):1049–1052
36. 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 159:269–276
37. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
38. Otterstatter MC, Thomson JD (2008) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators ? PLoS ONE 3:1–9
39. Pitts-Singer T, James R (2008) Do weather conditions correlate with findings in failed, provision-filled nest cells of Megachile rotundata (Hymenoptera: Megachilidae) in western North America? J Econ Entomolo 101:674–685
40. Plischuk S, Lange CE (2009) Invasive Bombus terrestris (Hymenoptera: Apidae) parasitized by a flagellate (Euglenozoa: Kinetoplastea) and a neogregarine (Apicomplexa: Neogregarinorida). J Invertebr Pathol 102:263–265
41. Rutrecht ST, Brown MJF (2008) The life-history impact and implications of multiple parasites for bumble bee queens. Int J Parasitol 38:799–808
42. Shipp JL, Whitfield GH, Papadopolus AP (1994) Effectiveness of the bumble bee, Bombus impatiens Cr. (Hymenoptera: Apidae), as a pollinator of green house sweet pepper. Sci Hortic (Amsterdam) 57:29–39
43. Singh R, Levitt AL, Rajotte EG et al (2010) RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5:1–16
44. Stubbs CS, Drummond FA (2001) Bombus impatiens (Hymenoptera: Apidae): an alternative to Apis mellifera (Hymenoptera: Apidae) for lowbush blueberry pollination. J Econ Entomol 94:609–616
45. Tay WT, O’Mahony EM, Paxton RJ (2005) Complete rRNA gene sequences reveal that the microsporidium Nosema bombi infects diverse bumblebee (Bombus spp.) hosts and contains multiple polymorphic sites. J Eukaryot Microbiol 52:505–513
46. Velthius HW, Van Doorn A (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37:421–451
47. Watanabe ME (2006) Colony collapse disorder: many suspects, no smoking gun. Bioscience 58:384–388
48. Whitehorn PR, Tinsley MC, Brown MJF, 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(3):149–157
49. Whittington RJ, Winston ML (2004) Comparison and examination of Bombus occidentalis and Bombus impatiens (Hymenoptera: Apidae) in tomato greenhouses. J Econ Entomolo 97:1384–1389
50. Yoneda MY, Uruta HF, Suchida KT, Kabe KO, Oka KG (2008) Commercial colonies of Bombus terrestris (Hymenopter: Apidae) are reservoirs of the tracheal mite Locustacarus buchneri (Acari: Podapolipidae). Appl Entomol Zool 43:73–76
51. Yue C, Genersch E (2005) RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 86:3419–3424
52. Yukl SA, Boritz E, Busch M et al (2013) Challenges in detecting HIV persistence during potentially curative interventions: a study of the Berlin patient. PLoS Pathog 9:1–13