Parasites, parasitoids, and hive products that are potentially deleterious to wild and commercially raised bumble bees (Bombus spp.) in North America
DOI:
https://doi.org/10.26786/1920-7603(2023)710Keywords:
bombus, bumble bee, symbionts, parasites, pathogensAbstract
Bumble bees are important pollinators for a great diversity of wild and cultivated plants, and in many parts of the world certain species have been found to be in decline, gone locally extinct, or even globally extinct. A large number of symbionts live on, in, or with these social bees. We give an overview of what is known about bumble bee ecto-symbionts and parasitoids. We provide information on assessment of risks posed by select bumble bee symbionts and methods for their detection, quantification, and control. In addition, we assess honey bee hive products such as pollen and wax that are used in commercial bumble bee production, and highlight key risks and knowledge gaps. Knowledge of these potential threats to native pollinators is important and they need to be managed in the context of national and international commercial trade in bumble bees to prevent pest introduction and pathogen spillover that can threaten native bees.
References
Abdalla FC, Sampaio G, Pedrosa M, Sipriano TP, Domingues CEC, Silva-Zacarin ECM, de Camargo DA (2014) Larval development of Physocephala (Diptera, Conopidae) in the bumble bee Bombus morio (Hymenoptera, Apidae). Revista Brasileira de Entomologia 58. https://doi.org/10.1590/S0085-56262014000400003
Adler LS, Michaud KM, Ellner SP, McArt SH, Stevenson PC, Irwin RE (2018) Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees. Ecology 99: 2535-2545. https://doi.org/10.1002/ecy.2503.
Alford DV (1968) The biology and immature stages of Syntretus splendidus (Marshall) (Hymenoptera: Braconidae, Euphorinae), a parasite of adult bumblebees. Transactions of the Royal Entomological Society of London 120: 375-393. https://doi.org/10.1111/j.1365-2311.1968.tb00343.x.
Álvarez Hidalgo E, Hernandez-Flores JL, Andrade Moreno VD, Ramos López M, Romero Gómez S, Vázquez Cruz MA, Torres Ruíz A, Alvarado Osuna C, Jones GH, Arvizu Hernández I, Estrada Martínez A, Campos-Guillén J (2020) Gamma irradiation effects on the microbial content in commercial bee pollen used for bumblebee mass rearing. Radiation Physics and Chemistry 168: 108511. https://doi.org/10.1016/j.radphyschem.2019.108511.
Ambrose JT, Stanghellini MS, Hopkins DI (2000) A scientific note on the threat of small hive beetles (Aethina tumida Murray) to bumble bee (Bombus spp.) colonies in the United States. Apidologie 31: 455-456. https://doi.org/10.1051/apido:2000136
An J-D, Guo Z-B, Li J-L, Luo Q-H, Wu J (2007) Morphological characters and bionomics of Plodia interpunctella, a pest in Bombus lucorum colonies breeding in captivity. Chinese Bulletin of Entomology 44: 698-702.
Arismendi N, Bruna A, Zapata N, Vargas M (2016) Molecular detection of the tracheal mite Locustacarus buchneri in native and non-native bumble bees in Chile. Insectes Sociaux 63: 629-633. https://doi.org/10.1007/s00040-016-0502-2.
Bailey L, Ball BV (1991) Honey Bee Pathology. 2nd edn. Academic Press.
Bortolotti L, Pošćić F, Bogo G (2020) Comparison of different pollen substitutes for the feeding of laboratory reared bumble bee (Bombus terrestris) colonies. Journal of Apicultural Science 64: 91-104. https://doi.org/10.2478/jas-2020-0013.
Bousquet Y (1989) A review of the North American genera of cryptophaginae (Coleoptera Cryptophagidae). Coleopterists Bulletin 43: 1-17.
Brown BV (1993) Taxonomy and preliminary phylogeny of the parasitic genus Apocephalus, subgenus Mesophora (Diptera: Phoridae). Systematic Entomology 18: 191-230. https://doi.org/10.1111/j.1365-3113.1993.tb00662.x.
Camras S (1996) New information on the New World Physocephala (Diptera: Conopidae. Entomological News 107: 104-112.
Camras S, Hurd PD, Jr. (1957) The Conopid flies of California (Diptera). Bulletin of the California Insect Survey 6: 19-50.
Carvell C, Rothery P, Pywell RF, Heard MS (2008) Effects of resource availability and social parasite invasion on field colonies of Bombus terrestris. Ecological Entomology 33: 321-327. https://doi.org/10.1111/j.1365-2311.2007.00961.x.
Chauzat M-P, Faucon J-P, Martel A-C, Lachaize J, Cougoule N, Aubert M (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. Journal of Economic Entomology 99: 253-262. https://doi.org/10.1093/jee/99.2.253.
Chavarria G (1994) Phoresy on a neotropical bumblebee (Hymenoptera: Apidae) by Antherophagus (Coleoptera: Cryptophagidae). Psyche 101: 084604. https://doi.org/10.1155/1994/84604.
Chen Y, Evans J, Feldlaufer M (2006) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology 92: 152-159. https://doi.org/10.1016/j.jip.2006.03.010.
Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: Pathogen spillover from commercial to wild populations. Biological Conservation 129: 461-467. https://doi.org/10.1016/j.biocon.2005.11.013
Core A, Runckel C, Ivers J, Quock C, Siapno T, DeNault S, Brown B, DeRisi J, Smith CD, Hafernik J (2012) A new threat to honey bees, the parasitic phorid fly Apocephalus borealis. PLOS ONE 7: e29639. https://doi.org/10.1371/journal.pone.0029639.
Coupland JB, Barker GM (2004) Natural enemies of terrestrial molluscs: Diptera as predators and parasitoids of terrestrial gastropods, with emphasis on Phoridae, Calliphoridae, Sarcophagidae, Muscidae, and Fanniidae (ed. by GM Barker) CABI Publishing, Wallingford, U.K., pp. 85-158.
Cuthbertson AGS, Wakefield ME, Powell ME, Marris G, Anderson H, Budge GE, Mathers JJ, Blackburn LF, Brown MA (2013) The small hive beetle Aethina tumida: A review of its biology and control measures. Current Zoology 59: 644-653. https://doi.org/10.1093/czoolo/59.5.644.
Dahlem GA, Downes J, William L (1996) Revision of the genus Boettcheria in America North of Mexico (Diptera: Sarcophagidae). Insecta Mundi 10.
Dahms E (1984a) Revision of the genus Melittobia (Chalcidoidea: Eulophidae) with the description of seven new species. Memoirs of the Queensland Museum 21: 271-336.
Dahms EC (1984b) A review of the biology of species in the the genus Melittobia (Hymenoptera: Eulophidae) with interpretations and additions using observations on Melittobia australica. Memoirs of the Queensland Museum 21: 337-360.
de Wael L, de Greef M, Laere O (1993) Melittobia acasta and Bombacarus buchneri, dangerous parasites in the in vitro rearing of bumble bees. Apiacta 28: 93-101.
de Wael L, de Greef M, van Laere O (1995) Biology and control of Melittobia acasta. Bee World 76: 72-76. https://doi.org/10.1080/0005772X.1995.11099244.
Delfinado MD, Baker EW (1976) Notes on Hypopi (Acarina) associated with bees and wasps (Hymenoptera). Journal of the New York Entomological Society 84: 76-90.
Eickwort GC (1990) Associations of mites with social insects. Annual Review of Entomology 35: 469-488. https://doi.org/10.1146/annurev.en.35.010190.002345.
Eyer M, Chen YP, Schäfer MO, Pettis J, Neumann P (2009) Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie 40: 419-428. https://doi.org/10.1051/apido:2008051.
Figueroa LL, Sadd BM, Tripodi AD, Strange JP, Colla SR, Duennes MA, Evans EC, Lehmann DM, Moylett H, Richardson L, Smith JW, Smith TA, Spevak EM, Inouye DW (2023) Endosymbionts that threaten commercially raised and wild bumble bees (Bombus spp.). Journal of Pollination Ecology 33(2): 14-36. https://doi.org/10.26786/1920-7603(2023)713
Flores JM, Spivak M, Gutiérrez I (2005) Spores of Ascosphaera apis contained in wax foundation can infect honeybee brood. Veterinary Microbiology 108: 141-144. https://doi.org/10.1016/j.vetmic.2005.03.005.
Freeman BA (1966) Notes on Conopid flies, including insect host, plant and phoretic relationships (Diptera: Conopidae). Journal of the Kansas Entomological Society 39: 123-131.
Fries I (1988) Comb replacement and Nosema disease (Nosema apis Z.) in honey bee colonies. Apidologie 19: 343-354. https://doi.org/10.1051/apido:19880402
Frison TH (1917) Notes on Bombidae, and on the life History of Bombus auricomus Robt. Annals of the Entomological Society of America 10: 277-286. https://doi.org/10.1093/aesa/10.3.277.
Frison TH (1921) Antherophagus ochraceus Mels. in the nests of bumblebees. The American Naturalist 55: 188-192. https://doi.org/10.1086/279807
Frison TH (1926) Contribution to the knowledge of the interrelations of the bumblebees of Illinois with their animate environment. Annals of the Entomological Society of America 19: 203-235. https://doi.org/10.1093/aesa/19.2.203.
Gabritschevsky E (1926) Convergence of coloration between American pilose flies and bumblebees (Bombus). The Biological Bulletin 51: 269-286. https://doi.org/10.2307/1536943.
Gekière A, Habay J, Michez D (2022) Monitoring of parasites in bumblebee colonies developed from controlled nesting of wild queens (Hymenoptera: Apidae: Bombus). OSMIA: 45-54.
Gibson JF, Slatosky AD, Malfi RL, Roulston TH, Davis SE (2016) Eclosion of Physocephala tibialis (Say) (Diptera: Conpidae) from a Bombus (Apidae: Hymenoptera) host: A video record. Journal of the Entomological Society of Ontario 145: 51-60.
Gilliam M, Taber S, Lorenz BJ, Prest DB (1988) Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. Journal of Invertebrate Pathology 52: 314-325. https://doi.org/10.1016/0022-2011(88)90141-3.
Goka K, Okabe K, Yoneda M, Niwa S (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites. Molecular Ecology 10: 2095-2099. https://doi.org/10.1046/j.0962-1083.2001.01323.x
Goldblatt JW, Fell RD (1984) Parasites and parasitization rates in bumble bee queens, Bombus spp. (Hymenoptera: Apidae), in southwestern Virginia. Environmental Entomology 13: 1661-1665. https://doi.org/10.1093/ee/13.6.1661.
Goldblatt JW, Fell RD (1987) Adult longevity of workers of the bumble bees Bombus fervidus (F.) and Bombus pennsylvanicus (DeGeer) (Hymenoptera: Apidae). Canadian Journal of Zoology 65: 2349-2353. https://doi.org/10.1139/z87-354
González JM, Matthews RW (2005) An annotated bibliography of Melittobia (Hymenoptera: Eulophidae). Carribean Journal of Science, Special Publication 8: 1-41.
González JM, Teran JB, Matthews RW (2004) Review of the biology of Melittobia acasta (Walker)(Hymenoptera: Eulophidae) and additions on development and sex ratio of the species. Carribean Journal of Science 40: 52-61.
Goulson D (2009) Bumblebees: Behaviour, Ecology, and Conservation. 2nd edn. Oxford University Press, Oxford.
Goulson D, Hughes WOH, Derwent LC, Stout JC (2002) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130: 267-273. https://doi.org/10.1007/s004420100803
Graystock P, Goulson D, Hughes WOH (2015) Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proceedings of the Royal Society B: Biological Sciences 282: 20151371. https://doi.org/10.1098/rspb.2015.1371.
Graystock P, Jones JC, Pamminger T, Parkinson JF, Norman V, Blane EJ, Rothstein L, Wäckers F, Goulson D, Hughes WOH (2016) Hygienic food to reduce pathogen risk to bumblebees. Journal of Invertebrate Pathology 136: 68-73. https://doi.org/10.1016/j.jip.2016.03.007.
Haas SM, Cardinal S, Beaulieu F, Forrest JRK (2019) Mite-y bees: bumble bees (Bombus spp., Hymenoptera: Apidae) host a relatively homogeneous mite (Acari) community, shaped by bee species identity but not by geographic proximity. Ecological Entomology 44: 333-346. https://doi.org/10.1111/een.12706.
Haydak MH, Dietz A (1965) Influence of the diet on the development and brood rearing of honeybees, Vol. 20: XV Beekeeping Congress (ed., Bucharest.
Higes M, Martín-Hernández R, Garrido-Bailón E, García-Palencia P, Meana A (2008) Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology 97: 76-78. https://doi.org/10.1016/j.jip.2007.06.002.
Hobbs GA (1967) Ecology of species of Bombus (Hymenoptera: Apidae) in southern Alberta. VI. Subgenus Pyrobombus. The Canadian Entomologist 99: 1271-1292. https://doi.org/10.4039/Ent991271-12.
Hobbs GA, Nummi WO, Virostek JF (1962) Managing colonies of bumble bees (Hymenoptera: Apidae) for pollination purposes. The Canadian Entomologist 94: 1121-1132. https://doi.org/10.4039/Ent941121-11.
Hoffmann D, Pettis JS, Neumann P (2008) Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens). Insectes Sociaux 55: 153-162. https://doi.org/10.1007/s00040-008-0982-9.
Houck MA, ed. (1993) Mites: Ecological and Evolutionary Analyses of Life-History Patterns. Springer New York, NY.
Hunter PE, Husband RW (1973) Pneumolaelaps (Acarina: Laelapidae) mites from North America and Greenland. The Florida Entomologist 56: 77-91. https://doi.org/10.2307/3493231.
Husband RW, Brown TM (1976) Insects associated with Michigan bumblebees (Bombus spp.). The Great Lakes Entomologist 9: 57-62.
Husband RW, Sinha RN (1970) A revision of the genus Locustacarus with a key to genera of the family Podapolipidae (Acarina). Annals of the Entomological Society of America 63: 1152-1162. https://doi.org/10.1093/aesa/63.4.1152.
Jagersbacher-Baumann J (2015) Traditional and geometric morphometric analyses reveal homogeneity in European Scutacarus acarorum Goeze, 1780 populations (Acari: Scutacaridae: Heterostigmatina). Journal of Natural History 49: 1173-1190. https://doi.org/10.1080/00222933.2014.974705.
Jagersbacher-Baumann J, Ebermann E (2013) Methods for rearing scutacarid mites (Acari, Heterostigmatina) and the influence of laboratory cultures on morphometric variables. Experimental and Applied Acarology 59: 447-462. https://doi.org/10.1007/s10493-012-9621-2.
Kissinger CN, Cameron SA, Thorp RW, White B, Solter LF (2011) Survey of bumble bee (Bombus) pathogens and parasites in Illinois and selected areas of northern California and southern Oregon. Journal of Invertebrate Pathology 107: 220-224. https://doi.org/10.1016/j.jip.2011.04.008.
Klimov P, O'Connor B, Ochoa R, G. B, Scher J (2016) Bee Mite ID: Bee-associated Mite Genera of the World, Vol. 2023: USDA and University of Michigan, http://idtools.org/id/mites/beemites/index.php.
Klimov PB, Oconnor BM, Ochoa R, Bauchan GR, Scher J (2017) Bee Mite ID - an online resource on identification of mites associated with bees of the World. Journal of the Acarological Society of Japan 26: 25-29. https://doi.org/10.2300/acari.26.25
Koch J, Strange J, Williams P (2012) Bumble bees of the western United States. USDA USFS and Pollinator Partnership.
Koch JBU, McCabe LM, Love BG, Cox-Foster D (2021) Genetic and usurpation data support high incidence of bumble bee nest invasion by socially parasitic bumble bee, Bombus insularis. Journal of Insect Science 21. https://doi.org/10.1093/jisesa/ieab063.
Kwon YJ, Amin MR, Inn NSL (2012a) Morphological features, development and reproduction of Melittobia acasta on Bombus terrestris. Entomological Research 42: 73-78. https://doi.org/10.1111/j.1748-5967.2011.00360.x.
Kwon YJ, Amin MR, Inn NSL (2012b) Parasitism and oviposition of Melittobia acasta on Bombus terrestris: Impact of larval overwintering and host status on pupation and adult emergence. Entomological Research 42: 94-98. https://doi.org/10.1111/j.1748-5967.2011.00361.x.
Kwon YJ, Saeed S, Duchateau MJ (2003) Control of Plodia interpunctella (Lepidoptera: Pyralidae), a pest in Bombus terrestris (Hymenoptera: Apidae) colonies. The Canadian Entomologist 135: 893-902. https://doi.org/10.4039/n03-013.
LaSalle J (1994) North American genera of Tetrastichinae (Hymenoptera: Eulophidae). Journal of Natural History 28: 109-236. https://doi.org/10.1080/00222939400770091.
Macfarlane RP (1975) The nematode Sphaerularia bombi (Sphaerulariidae) and the Mite Locustacurus buchneri (Podapolipidae) in bumble bee queens Bombus spp. (Apidae) in New Zealand. New Zealand Entomologist 6: 79-79. https://doi.org/10.1080/00779962.1975.9723109.
Macfarlane RP, Lipa JJ, Liu HJ (1995) Bumble bee pathogens and internal enemies. Bee World 76: 130-148. https://doi.org/10.1080/0005772X.1995.11099259
MacFarlane RP, Pengelley DH (1977) Brachicoma spp. (Sarcophagidae) and Melittobia chalybdii (Eulophidae) as parasites of the brood of Bombus spp. (Apidae) in southern Ontario. Proceedings of the Entomological Society of Ontario 108: 31-35.
MacFarlane RP, Pengelly DH (1974) Conopidae and Sarcophagidae as parasites of adult Bombinae in Ontario. Proceedings of the Entomological Society of Ontario 105: 55-59.
Malfi RL, Davis SE, Roulston TaH (2014) Parasitoid fly induces manipulative grave-digging behaviour differentially across its bumblebee hosts. Animal Behaviour 92: 213-220. http://dx.doi.org/10.1016/j.anbehav.2014.04.005.
Malfi RL, Roulston TaH (2014) Patterns of parasite infection in bumble bees (Bombus spp.) of Northern Virginia. Ecological Entomology 39: 17-29. https://doi.org/10.1111/een.12069.
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. Ecological Monographs 88: 653-671. https://doi.org/10.1002/ecm.1327.
Martin S, Carruthers J, Williams P, Drijfhout F (2010) Host specific social parasites (Psithyrus) indicate chemical recognition system in bumblebees. Journal of Chemical Ecology 36: 855-863. https://doi.org/10.1007/s10886-010-9805-3.
Matthews RW, González JM, Matthews JR, Deyrup LD (2009) Biology of the parasitoid Melittobia (Hymenoptera: Eulophidae). Annual Review of Entomology 54: 251-266. https://doi.org/10.1146/annurev.ento.54.110807.090440 .
Mattila HR, Otis GW (2006) Influence of pollen diet in spring on development of honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology 99: 604-613. https://doi.org/10.1093/jee/99.3.604.
McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (1981) Manual of Nearctic Diptera, Vol. 1: Biosystematics Research Institute, Research Branch, Agriculture Canada, Ottawa, Ontario, p. 674.
McCorquodale DB, Beresford RG, Francis JM, Thomson CE, Bartlett CM (1998) Prevalence of Sphaerularia bombi (Nematoda: Tylenchida: Spaerulariidae) in bumble bee queens (Hymenoptera: Apidae) on Cape Breton Island, Nova Scotia, Canada. The Canadian Entomologist 130: 877-882. https://doi.org/10.4039/Ent130877-6.
Meeus I, Brown MJF, De Graaf DC, Smagghe G (2011) Effects of invasive parasites on bumble bee declines. Conservation Biology 25: 662-671. https://doi.org/10.1111/j.1523-1739.2011.01707.x.
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. Journal of Invertebrate Pathology 121: 64-69. https://doi.org/10.1016/j.jip.2014.06.011.
Milum VG (1940) Larval pests common to nests of bumblebees and combs of the honeybee. Journal of Economic Entomology 33: 81-83. https://doi.org/10.1093/jee/33.1.81.
Milum VG (1953) Vitula edmandsii as a pest of honeybee combs. Journal of Economic Entomology 46: 710-711. https://doi.org/10.1093/jee/46.4.710.
Mitchell TB (1962) Bees of the Eastern United States. The North Carolina Agricultural Experiment Station, Raleigh, NC.
Mohandass S, Arthur FH, Zhu KY, Throne JE (2007) Biology and management of Plodia interpunctella (Lepidoptera: Pyralidae) in stored products. Journal of Stored Products Research 43: 302-311. https://doi.org/10.1016/j.jspr.2006.08.002.
Monfared AR, Azhari S, Gilasian E (2013) Volucella bombylans (Syrphidae, Diptera) recorded from a colony of Bombus mesomelas (Apidae, Hymenoptera) in Iran. Linzer Biologische Beiträge 45: 829-836.
Müller CB, Schmid-Hempel P (1993) Exploitation of cold temperature as defence against parasitoids in bumblebees. Nature 363: 65-67. https://doi.org/10.1038/363065a0
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLOS ONE 5: e9754. https://doi.org/10.1371/journal.pone.0009754.
Mullins JL, Strange JP, Tripodi AD (2019) Why are queens broodless? Failed nest initiation not linked to parasites, mating status, or ovary development in two bumble bee species of Pyrobombus (Hymenoptera: Apidae: Bombus). Journal of Economic Entomology 113: 575-581. https://doi.org/10.1093/jee/toz330.
Naughton J, Tiedeken EJ, Garvey M, Stout JC, Rowan NJ (2017) Pulsed light inactivation of the bumble bee trypanosome parasite Crithidia bombi. Journal of Apicultural Research 56: 144-154. https://doi.org/10.1080/00218839.2017.1289668.
Neumann P, Elzen PJ (2004) The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): Gaps in our knowledge of an invasive species. Apidologie 35: 229-247. https://doi.org/10.1051/apido:2004010
Neumann P, Evans JD, Pettis JS, Pirk CWW, Schäfer MO, Tanner G, Ellis JD (2013) Standard methods for small hive beetle research. Journal of Apicultural Research 52: 1-32. https://doi.org/10.3896/IBRA.1.52.4.19.
Nørgaard Holm S, Skou JP (1972) Studies on trapping, nesting, and rearing of some Magachile species (Hymenoptera, Megachilidae) and on their parasites in Denmark. Insect Systematics & Evolution 3: 169-180. https://doi.org/10.1163/187631272X00274.
O'Connor BM (1992) Ontogeny and systematics of the genus Cerophagus (Acari: Gaudiellidae), mites associated with bumblebees. The Great Lakes Entomologist 25.
Oertel E (1963) Greater wax moth develops on bumble bee cells. Journal of Economic Entomology 56: 543-544. https://doi.org/10.1093/jee/56.4.543
Otterstatter MC, Gegear RJ, Colla SR, Thomson JD (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behavioral Ecology and Sociobiology 58: 383-389. https://doi.org/10.1007/s00265-005-0945-3
Otterstatter MC, Whidden TL (2004) Patterns of parasitism by tracheal mites (Locustacarus buchneri) in natural bumble bee populations. Apidologie 35: 351-357. https://doi.org/10.1051/apido:2004024
Otterstatter MC, Whidden TL, Owen RE (2002) Contrasting frequencies of parasitism and host mortality among phorid and conopid parasitoids of bumble-bees. Ecological Entomology 27: 229-237. https://doi.org/10.1046/j.1365-2311.2002.00403.x
Parks R (2016) An observation of the beetle Antherophagus (Coleoptera: Cryptophagidae) Interacting with Bombus appositus Cresson (Hymenoptera: Apidae). Entomological News 126: 213-215, 213. https://doi.org/10.3157/021.126.0307
Parsons CT (1948) A classification of North American Conopidae. Annals of the Entomological Society of America 41: 223-246. https://doi.org/10.1093/aesa/41.2.223.
Pereira KdS, Meeus I, Smagghe G (2019) Honey bee-collected pollen is a potential source of Ascosphaera apis infection in managed bumble bees. Scientific Reports 9: 4241. https://doi.org/10.1038/s41598-019-40804-2.
Peterson BV (1987) Phoridae, Vol. 2: Manual of Nearctic Diptera (ed. by JF McAlpine, BV Peterson, GE Shewell, HJ Teskey, JR Vockeroth & DM Wood) Biosystematics Research Centre, Research Branch, Agriculture Canada, Ottawa, pp. 689-712.
Plath OE (1922) Notes on Psithyrus, with records of two new American hosts. The Biological Bulletin 43: 23-44. https://doi.org/10.2307/1536689.
Plischuk S, Meeus I, Smagghe G, Lange CE (2011) Apicystis bombi (Apicomplexa: Neogregarinorida) parasitizing Apis mellifera and Bombus terrestris (Hymenoptera: Apidae) in Argentina. Environmental Microbiology Reports 3: 565-568. https://doi.org/10.1111/j.1758-2229.2011.00261.x.
Richards KW (1984) Food preference, growth, and development of larvae of the driedfruit moth, Vitula edmandsae serratilineella, Ragonot (Lepidoptera: Pyralidae). Journal of the Kansas Entomological Society 57: 28-33.
Richards LA, Richards KW (1976) Parasitid mites associated with bumblebees in Alberta, Canada (Acarina: Parasitidae; Hymenoptera: Apidae). 2. Biology. University of Kansas Science Bulletin 51: 1-18.
Royce LA, Krantz GW (1989) Observations on pollen processing by Pneumolaelaps longanalis (Acari: Laelapidae), a mite associate of bumblebees. Experimental & Applied Acarology 7: 161-165. https://doi.org/10.1007/BF01270436.
Rożej E, Witaliński W, Szentgyörgyi H, Wantuch M, Moroń D, Woyciechowski M (2012) Mite species inhabiting commercial bumblebee (Bombus terrestris) nests in Polish greenhouses. Experimental and Applied Acarology 56: 271-282. https://doi.org/10.1007/s10493-012-9510-8.
Ryckman RE (1953) Notes on the ecology of Bombus sonorus in Orange County, California and new parasite records. Pan-Pacific Entomologist 29: 144-146.
Sarro E, Tripodi A, Woodard SH (2022) Bumble bee (Bombus vosnesenskii) queen nest searching occurs independent of ovary developmental status. Integrative Organismal Biology 4. https://doi.org/10.1093/iob/obac007.
Sattler K (1988) The correct name of the North American dried fruit moth in Europe (Lepidoptera: Pyralidae). Insect Systematics & Evolution 19: 455-458. https://doi.org/10.1163/187631289X00564.
Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88: 147-158. https://doi.org/10.1007/s001140100222
Schmid-Hempel P, Durrer S (1991) Parasites, floral resources and reproduction in natural populations of bumblebees. Oikos 62: 342-350. https://doi.org/10.2307/3545499
Schmid-Hempel P, Müller C, Schmid-Hempel R, Shykoff JA (1990) Frequency and ecological correlates of parasitism by conopid flies (Conopidae, Diptera) in populations of bumblebees. Insectes Sociaux 37: 14-30. https://doi.org/10.1007/BF02223812.
Schmid-Hempel P, Schmid-Hempel R (1990) Endoparasitic larvae of conopid flies alter pollination behavior of bumblebees. Naturwissenschaften 77: 450-452. https://doi.org/10.1007/BF01135951
Schmid-Hempel P, Stauffer H-P (1998) Parasites and flower choice of bumblebees. Animal Behaviour 55: 819-825. https://doi.org/10.1006/anbe.1997.0661
Schmid-Hempel R, Schmid-Hempel P (1989) Superparasitism and larval competition in conopid flies (Dipt., Conopidae), parasitizing bumblebees (Hym., Apidae). Mitteilungen der schweizerischen entomologischen Gesellschaft 62: 279-289.
Schmid-Hempel R, Schmid-Hempel P (1991) Endoparasitic flies, pollen-collection by bumblebees and a potential host-parasite conflict. Oecologia 87: 227-232. https://doi.org/10.1007/BF00325260
Scholtens B, Solis MA (2015) Annotated check list of the Pyraloidea (Lepidoptera) of America North of Mexico. ZooKeys 535. https://doi.org/10.3897/zookeys.535.6086.
Shewell GE (1989) Sarcophagidae, Vol. 2: Manual of Nearctic Diptera (ed. by JF McAlpine, BV Peterson, HJ Teskey, JR Vockeroth & DM Wood) Agriculture Canada. Research Branch.
Shimanuki H, Knox DA (2000) Diagnosis of Honey Bee Diseases, Vol. AH-690: U. S. Department of Agriculture, pp. 1-61.
Simone-Finstrom M, Aronstein K, Goblirsch M, Rinkevich F, de Guzman L (2018) Gamma irradiation inactivates honey bee fungal, microsporidian, and viral pathogens and parasites. Journal of Invertebrate Pathology 153: 57-64. https://doi.org/10.1016/j.jip.2018.02.011.
Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, vanEngelsdorp D, Lipkin WI, dePamphilis CW, Toth AL, Cox-Foster DL (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: e14357. https://doi.org/10.1371/journal.pone.0014357
Smith KGV (1969) Diptera: Conopidae. Royal Entomological Society of London, London.
Smith KGV, Peterson B (1987) Conopidae, Vol. 2: Manual of Nearctic Diptera (ed. by JF McAlpine, BJ Peterson, GE Shewell, HJ Teskey, JR Vockeroth & D Woods) Research Branch, Agriculture Canada, Ottawa, pp. 759-756.
Solis MA (2006) Key to selected Pyraloidea (Lepidoptera) larvae intercepted at US ports of entry: Revision of Pyraloidea in “Keys to some frequently intercepted Lepidopterous larvae.”: USDA Systematic Entomology Laboratory, pp. 1-58.
Solis MA (2007) Phylogenetic studies and modern classification of the Pyraloidea (Lepidoptera). Revista Colombiana de Entomología 33: 1-8. https://doi.org/10.25100/socolen.v33i1.9306
Solis MA, Metz MA (2008) Aphomia Hübner and Paralipsa Butler species (Lepidoptera: Pyralidae: Galleriinae) known to occur in the United States and Canada. Proceedings of the Entomological Society of Washington 110: 592-601.
Spiewok S, Neumann P (2006) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida). Ecological Entomology 31: 623-628. https://doi.org/10.1111/j.1365-2311.2006.00827.x.
Stegmaier CE (1972) Notes on some Sarcophagidae (Diptera) reared from snails (Mollusca) in Florida. The Florida Entomologist 55: 237-242. https://doi.org/10.2307/3493372.
Stone A (1965) A catalog of the Diptera of America north of Mexico: by U.S. Department of Agriculture), 1696 pp., USDA Publications.
Strange JP, Baur A, Koch JB (2014) A scientific note on Bombus (Psithyrus) insularis invasions of bumblebee nests and honeybee hives in the western USA. Apidologie 45: 554-556. https://doi.org/10.1007/s13592-014-0271-8.
Strange JP, Colla SR, Duennes MA, Evans EC, Figueroa LL, Lehmann DM, Moylett H, Richardson L, Sadd BM, Smith JW, Smith TA, Spevak EM, Tripodi AD, Inouye DW (2023) An evidence-based rationale for a North American commercial bumble bee clean stock certification program Journal of Pollination Ecology. 33(1): 1-13. https://doi.org/10.26786/1920-7603(2023)721
Thorp RW, Horning DS, Jr., Dunning LL (1983) Bumble bees and cuckoo bumble bees of California. Bulletin of the California Insect Survey 23: 1-79.
Townsend LH (1935) The mature larva and puparium of Brachycoma sarcophagina (Townsend) (Diptera: Metopiidae). Proceedings of the Entomological Society of Washington 38: 92-98.
Velthuis HHW, 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. https://doi.org/10.1051/apido:2006019
Wharton RA, Marsh PM, Sharky MJ, eds. (1997) Manual of the New World Genera of the Family Braconidae (Hymenoptera). International Society of Hymenopterists, Washington, D.C.
Wheeler WM (1919) The phoresy of Antherophagus. Psyche 26: 093829. https://doi.org/10.1155/1919/93829.
Whitfield JB, Cameron SA (1993) Comparative notes on Hymenopteran parasitoids in bumble bee and honey-bee colonies (Hymenoptera, Apidae) reared adjacently. Entomological News 104: 240-248.
Williams J (1997) Insects: Lepidoptera (Moths): Honey Bee Pets, Predators and Diseases (ed. by RA Morse & K Flottum) Peacock Press, pp. 105-127.
Williams P, H. (2008) Do the parasitic Psithyrus resemble their host bumblebees in colour pattern? Apidologie 39: 637-649. https://doi.org/10.1051/apido:2008048
Williams P, Thorp R, Richardson L, Colla S (2014) Bumble bees of North America: An Identification Guide. Princeton University Press, Princeton, NJ.
Wu JY, Anelli CM, Sheppard WS (2011) Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLOS ONE 6: e14720. https://doi.org/10.1371/journal.pone.0014720.
Yoneda M, Furuta H, Kanbe Y, Tsuchida K, Okabe K, Goka K (2008a) Reproduction and transmission within a colony of bumblebee tracheal mite Locustacarus buchneri (Acari: Podapolipidae) in Bombus terrestris (Hymenoptera: Apidae). Applied Entomology and Zoology 43: 391-395. https://doi.org/10.1303/aez.2008.391.
Yoneda M, Furuta H, Tsuchida K, Okabe K, Goka K (2008b) Commercial colonies of Bombus terrestris (Hymenoptera: Apidae) are reservoirs of the tracheal mite Locustacarus buchneri (Acari: Podapolipidae). Applied Entomology and Zoology 43: 73-76. https://doi.org/10.1303/aez.2008.73.
Yook H-S, Lim S-I, Byun M-W (1998) Changes in microbiological and physicochemical properties of Bee pollen by application of gamma irradiation and ozone treatment. Journal of Food Protection 61: 217-220. https://doi.org/10.4315/0362-028x-61.2.217.
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Copyright (c) 2023 Elaine C. Evans, James P. Strange, Ben M. Sadd, Amber D. Tripodi, Laura L. Figueroa, Laurie Davies Adams, Sheila R. Colla, Michelle A. Duennes, David M. Lehmann, Heather Moylett, Leif Richardson, James W. Smith, Tamara A. Smith, Edward M. Spevak, David W. Inouye
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