Advertisement

Apidologie

, Volume 50, Issue 5, pp 689–703 | Cite as

Methods for rearing ground-nesting bees under laboratory conditions

  • Ryan J. LeonardEmail author
  • Alexandra N. Harmon-Threatt
Review article

Abstract

Ground-nesting bees are largely undervalued, both in terms of their use as model species for behavioural studies, and in terms of their agricultural benefit as pollinators in crop systems. But, why? One potential barrier limiting their use as model species may be our understanding of how to effectively establish and maintain ground-nesting bees in the laboratory. Here we review how artificial nests are used to study ground-nesting bees and provide guidelines for building, starting and maintaining artificial nests. Ultimately, appropriate design and maintenance of artificial nests will allow researchers to explore a suite of interesting questions related to this important group of pollinating insects, from natural history to the origins of eusociality and the effects of environmental contaminants.

Keywords

ground-nesting bee artificial nest rearing Lasioglossum 

Notes

Acknowledgements

The authors thank Jim Cane, Katja Hogendoorn, T’ai Roulston and Quinn McFrederick for advice regarding ground-nesting bee rearing and maintenance. The authors also thank Caitlyn Drayton-Taylor, Nick Anderson, Katie Barie, Scott Clem, Jon Tetlie, Anna Grommes and Benjamin Chiavini for feedback during manuscript preparation.

Authors contribution

RJL and A.N.T-H conceived and wrote review. All authors read and approved the final manuscript.

Funding information

Ryan J. Leonard is funded USAD NIFA 2018-67013-27537.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13592_2019_679_MOESM1_ESM.docx (22 kb)
ESM 1. (DOCX 21 kb)

References

  1. Andrade-Silva, A., and F. Nascimento. (2012).Multifemale nests and social behavior in Euglossa melanotricha (Hymenoptera, Apidae, Euglossini). J. Hymenopt. Res. 26:1–16.CrossRefGoogle Scholar
  2. Barrows, E. M. (1975). Mating behavior in halictine bees (Hymenoptera: Halictidae): III. Copulatory behavior and olfactory communication. Insect. Soc. 22(3):307–331.CrossRefGoogle Scholar
  3. Barrows, E. M. (1976). Mating behavior in halictine bees (Hymenoptera: Halictidae): II. Micro-territorial and patrolling behaviour in male male of Lasioglossum rohweriInsect. Soc. 40(4):377–389.Google Scholar
  4. Barrows, E. M., W. J. Bell, and C. D. Michener. (1975). Individual odor differences and their social functions in insects. PNAS 72(7):2824–2828.PubMedCrossRefGoogle Scholar
  5. Batra, S. W. T. (1964). Behaviour of the social bee, Lasioglossum zephyrum, within the nest (Hymenoptera: Halictidae). Insect. Soc. 11:159–186.CrossRefGoogle Scholar
  6. Batra, S. W. T. (1968). Behavior of some social and solitary halictine bees within their nests: a comparative study (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 41(1):120–133.Google Scholar
  7. Batra, S. W. T. (1970). Behavior of the alkali bee, Nomia melanderi, within the nest (Hymenoptera: Halictidae). Ann. Entomol. Soc. Am. 63(2):400–406.CrossRefGoogle Scholar
  8. Batra, S. W. T. (1984). Solitary bees. SA 250(2):120–127.Google Scholar
  9. Bell, W. J. (1973). Factors controlling initiation of vitellogenesis in a primitively social bee, Lasioglossum zephyrum (Hymenoptera: Halictidae). Insect. Soc. 20(3):253–260.CrossRefGoogle Scholar
  10. Bell, W. J., M. D. Breed, K. W. Richards, and C. D. Michener. (1974). Social, stimulatory and motivational factors involved in intraspecific nest defense of a primitively eusocial halictine bee. J. Comp. Physiol. 93(3):173–181.CrossRefGoogle Scholar
  11. Bell, M. C., R. N. Spooner-hart, and A. M. Haigh. (2006). Pollination of greenhouse tomatoes by the Australian bluebanded bee Amegilla (Zonamegilla) holmesi (Hymenoptera: Apidae). J. Econ. Entomol. 99(2):437–442.PubMedCrossRefGoogle Scholar
  12. Boff, S., C. A. Saito, and I. A. Santos. (2017). Multiple aggressions among nestmates lead to weak dominance hampering primitively eusocial behaviour in an orchid bee. Sociobiology 64(2):202–211.CrossRefGoogle Scholar
  13. Bohart, G. E. (1955). Time relationships in the nest construction and life cycle of the alkali bee. Ann. Entomol. Soc. Am. 48(5):403–406.CrossRefGoogle Scholar
  14. Bosch, J., and W. Kemp. (2005). Alfalfa leafcutting bee population dynamics, flower availability, and pollination rates in two Oregon alfalfa fields. J. Econ. Entomol. 98(4):1077–1086.PubMedCrossRefGoogle Scholar
  15. Brand, N., and M. Chapuisat. (2012). Born to be bee, fed to be worker? The caste system of a primitively eusocial insect. Front. Zool. 9(1):35.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Breed, M. D., and G. J. Gamboa. (1977). Behavioral control of workers by queens in primitively eusocial bees. Science 195(4279):694–696.PubMedCrossRefGoogle Scholar
  17. Breed, M. D., J. M. Silverman, and W. J. Bell. (1978). Agonistic behavior, social interactions, and behavioral specialization in a primitively eusocial bee. Insect. Soc. 25(4):351–364.CrossRefGoogle Scholar
  18. Brothers, D. J., and C. D. Michener. (1974). Interactions in colonies of primitively social bees. J. Comp. Physiol. 90(2):129–168.CrossRefGoogle Scholar
  19. Buckle, G. R. (1982). Queen-worker behavior and nesmate interactions in young colonies of Lasioglossum zephyrum. Insect. Soc. 29(2):125–137.CrossRefGoogle Scholar
  20. Buckle, G. R. (1984). A second look at queen-forager interactions in the primitively eusocial halictid, Lasioglossum zephyrum. J. Kansas Entomol. Soc. 57(1):1–6.Google Scholar
  21. Buckle, G. R., and L. Greenberg. (1981). Nestmate recognition in sweat bees (Lasioglossum zephyrum): does an individual recognize its own odour or only odours of its nestmates? Anim. Behav. 29(3):802–809.CrossRefGoogle Scholar
  22. Bushmann, S. L., F. A. Drummond, L. A. Beers, and E. Groden. (2012). Wild bumblebee (Bombus) diversity and Nosema (Microsporidia: Nosematidae) infection levels associated with lowbush blueberry (Vaccinium angustifolium) production and commercial bumblebee pollinators. Psyche (Camb Mass) 2012: 429398.Google Scholar
  23. Cameron, S., J. Whitfield, C. Hulslander, W. Cresko, S. Isenberg, and R. King. (1996). Nesting biology and foraging patterns of the solitary bee Melissodes rustica (Hymenoptera: Apidae) in northwest Arkansas. J. Kansas Entomol. Soc. 69(4):260–273.Google Scholar
  24. Cane, J. H. (1991). Soils of ground-nesting bees (Hymenoptera, Apoidea) - texture, moisture, cell depth and climate. J. Kansas Entomol. Soc. 64(4):406–413.Google Scholar
  25. Cane, J. H. (1997). Ground-nesting bees: the neglected pollinator resource for agriculture. Acta Hortic. 437:309–324.CrossRefGoogle Scholar
  26. Cane, J. H. (2008). A native ground-nesting bee (Nomia melanderi) sustainably managed to pollinate alfalfa across an intensively agricultural landscape. Apidologie 39:315–323.CrossRefGoogle Scholar
  27. Cane, J. H. (2015). Landscaping pebbles attract nesting by the native ground-nesting bee Halictus rubicundus (Hymenoptera: Halictidae). Apidologie 46:728–734.CrossRefGoogle Scholar
  28. Cane, J. H., and J. L. Neff. (2011). Predicted fates of ground-nesting bees in soil heated by wildfire: Thermal tolerances of life stages and a survey of nesting depths. Biol. Conserv. 144(11):2631–2636.CrossRefGoogle Scholar
  29. Dalmazzo, M., and A. Roig-Alsina. (2012). Nest structure and notes on the social behavior of Augochlora amphitrite (Schrottky) (Hymenoptera, Halictidae). J. Hymenopt. Res. 26:17–29.CrossRefGoogle Scholar
  30. Dalmazzo, M., and A. Roig-Alsina. (2015). Social biology of Augochlora (Augochlora) phoemonoe (Hymenoptera, Halictidae) reared in laboratory nests. Insect. Soc. 62(3):315–323.CrossRefGoogle Scholar
  31. Danforth, B. N. (1991a). Female foraging and intranest behaviour of a communal bee, Perdita portalis (Hymeoptera, Andrenidae). Ann. Entomol. Soc. Am. 84(5):537–548.CrossRefGoogle Scholar
  32. Danforth, B. N. (1991b). The morphology and behavior of dimorphic males in Perdita portalis (Hymenoptera : Andrenidae). Behav. Ecol. Sociobiol. 29(4):235–247.CrossRefGoogle Scholar
  33. Davison, P., and J. Field. (2018a). Limited social plasticity in the socially polymorphic sweat bee Lasioglossum calceatum. Behav. Ecol. Sociobiol. 72(3):56.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Davison, P. J., and J. Field. (2018b). Environmental barriers to sociality in an obligate eusocial sweat bee. Insect. Soc. 65(4):549–559.CrossRefGoogle Scholar
  35. Donovan, B. J., B. G. Howlett, and M. K. Walker. (2010). Relocation and establishment of nesting populations of the native bee Leioproctus huakiwi Donovan (Hymenoptera: Colletidae). N. Z. Entomol. 33(1):109–113.CrossRefGoogle Scholar
  36. European Food Safety Authority. (2013). Guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J., 3295.Google Scholar
  37. Forrest, J. R. K., and J. D. Thomson. (2011). An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol. Monogr. 81(3):469–491.CrossRefGoogle Scholar
  38. Fortel, L., M. Henry, L. Guilbaud, H. Mouret, and B. E. Vaissière. (2016). Use of human-made nesting structures by wild bees in an urban environment. J. Insect Conserv. 20(2):239–253.CrossRefGoogle Scholar
  39. Fründ, J., S. L. Zieger, and T. Tscharntke. (2013). Response diversity of wild bees to overwintering temperatures. Oecologia 173(4):1639–1648.PubMedCrossRefPubMedCentralGoogle Scholar
  40. Graham, J. R., Willcox, E., & Ellis, J. D. (2015). The potential management of a ground-nesting, solitary bee: Anthophora abrupta (Hymenoptera: Apidae). Fla. Entomol. 98(2):528–536.CrossRefGoogle Scholar
  41. Greenberg, L. (1982a). Persistent habituation to female odor by male sweat bees, (Lasioglossum zephyrum) (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 55(3): 525–531.Google Scholar
  42. Greenberg, L. (1982b). Year-round culturing and productivity of a sweat bee, Lasioglossum zephyrum (Hymenoptera, Halictidae). J. Kansas Entomol. Soc. 55(1):13–22.Google Scholar
  43. Greenberg, L., and G. R. Buckle. (1981). Inhibition of worker mating by queens in a sweat bee, Lasioglossum zephyrum. Insect. Soc. 28(4):347–352.CrossRefGoogle Scholar
  44. Grundel, R., R. P. Jean, K. J. Frohnapple, G. A. Glowacki, P. E. Scott, and N. B. Pavlovic. (2010). Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient. Ecol. Appl. 20(6):1678–1692.PubMedCrossRefGoogle Scholar
  45. Hartman, C. G. (1943). A glass-tube method for oberving the home life of solitary bees and wasps. Sch. Sci. Math. 43(8):709–711.CrossRefGoogle Scholar
  46. Hogendoorn, K., C. L. Gross, M. Sedgley, and M. A. Keller. (2006). Increased tomato yield through pollination by native Australian Amegilla chlorocyanea (Hymenoptera: Anthophoridae). J. Econ. Entomol. 99(3):828–833.PubMedCrossRefGoogle Scholar
  47. Holbrook, C. T., R. M. Clark, R. Jeanson, S. M. Bertram, P. F. Kukuk, and J. H. Fewell. (2009). Emergence and consequences of division of labor in associations of normally solitary sweat bees. Ethology 115(4):301–310.CrossRefGoogle Scholar
  48. Holbrook, C. T., P. F. Kukuk, and J. H. Fewell. (2013). Increased group size promotes task specialization in a normally solitary halictine bee. Behaviour 150(12):1449–1466.CrossRefGoogle Scholar
  49. Jeanson, R., P. F. Kukuk, and J. H. Fewell. (2005). Emergence of division of labour in halictine bees: contributions of social interactions and behavioural variance. Anim. Behav. 70(5):1183–1193.CrossRefGoogle Scholar
  50. Jeanson, R., R. M. Clark, C. T. Holbrook, S. M. Bertram, J. H. Fewell, and P. F. Kukuk. (2008). Division of labour and socially induced changes in response thresholds in associations of solitary halictine bees. Anim. Behav. 76(3):593–602.CrossRefGoogle Scholar
  51. Johansen, C., D. Mayer, H. Homan, and J. Capizz. (1976). Alkali bees: their biology and management for alfalfa seed production in the Pacific Northwest. Publication, Pacific Northwest Cooperative Extension Service No. PNW.Google Scholar
  52. Kamm, D. R. (1974). Effects of temperature, day length, and number of adults on the sizes of cells and offspring in a primitively social bee (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 47(1):8–18.Google Scholar
  53. Kapheim, K. M., and M. M. Johnson. (2017). Juvenile hormone, but not nutrition or social cues, affects reproductive maturation in solitary alkali bees (Nomia melanderi). J. Exp. Biol. 220(20):3794–3801.PubMedCrossRefGoogle Scholar
  54. Kearns, C. A., and D. M. Oliveras. (2009). Environmental factors affecting bee diversity in urban and remote grassland plots in Boulder, ColoradoJ. Insect Conserv. 13(6):655–665.CrossRefGoogle Scholar
  55. Kim, J., N. Williams, and C. Kremen. (2006). Effects of cultivation and proximity to natural habitat on ground-nesting native bees in California sunflower fields. J. Kansas Entomol. Soc. 79(4):309–320.CrossRefGoogle Scholar
  56. Kopit, A. M., and T. L. Pitts-Singer. (2018). Routes of Pesticide Exposure in Solitary, Cavity-Nesting Bees. Environ. Entomol. 47(3):499–510.CrossRefGoogle Scholar
  57. Kratschmer, S., B. Pachinger, M. Schwantzer, D. Paredes, M. Guernion, F. Burel, A. Nicolai, P. Strauss, T. Bauer, and M. Kriechbaum. (2018). Tillage intensity or landscape features: what matters most for wild bee diversity in vineyards? Agric. Ecosyst. Environ. 266:142–152.CrossRefGoogle Scholar
  58. Krattinger, K. (1975). Genetic mobility in Typha. Aquat. Bot. 1:57–70.CrossRefGoogle Scholar
  59. Kritsky, G. (2010). The quest for the perfect hive: a history of innovation in bee culture. Oxford University Press.Google Scholar
  60. Kukuk, P. F., and R. H. Crozier. (1990). Trophallaxis in a communal halictine bee Lasioglossum (Chilalictus) erythrurum. PNAS 87(14):5402–5404.PubMedCrossRefGoogle Scholar
  61. Kukuk, P. F., and P. C. Decelles. (1986). Behavioral evidence for population structure in Lasioglossum (Dialictus) zephyrum female dispersion patterns. Behav. Ecol. Sociobiol. 19(4):233–239.CrossRefGoogle Scholar
  62. Kukuk, P. F., and B. May. (1991). Colony dynamics in a primitavely eusocial Halictine bee Lasioglossum (Dialictus) zephyrum (Hymenoptera, Halictidae). Insect. Soc. 38(2):171–189.CrossRefGoogle Scholar
  63. Kukuk, P. F., and M. Schwarz. (1987). Intranest behavior of the communal sweat bee Lasioglossum (Chilalictus) erythrurum (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 60(1):58–64.Google Scholar
  64. Kukuk, P. F., M. D. Breed, S. Anita, and W. J. Bell. (1977). The contributions of kinship and conditioning to nest recognition and colony member recognition in a primitively eusocial bee, Lasioglossum zephyrum (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 2(3):319–327.CrossRefGoogle Scholar
  65. Kumar, S. (1975). Relations among Bee Size, Cell Size, and Caste, in Lasioglossum zephyrum (Hymenoptera, Halictidae). J. Kansas Entomol. Soc. 48(3):374–380.Google Scholar
  66. Linsley, E. G., J. W. MacSwain, and R. F. Smith. (1952). Outline for ecological life histories of solitary and semi-social bees. Ecology 33(4):558–567.CrossRefGoogle Scholar
  67. MacIvor, J. S. (2017). Cavity-nest boxes for solitary bees: a century of design and research. Apidologie 48(3):311–327.CrossRefGoogle Scholar
  68. MacIvor, J. S., and L. Packer. (2015). ‘Bee hotels’ as tools for native pollinator conservation: a premature verdict? PLoS One 10(3):e0122126.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Malyshev, S. (1925). The nesting habits of Anthophora Latr. Trudy leningrObshch. Estest 55:137–183.Google Scholar
  70. Marinho, D., J. Andrade, R. O. Araujo, and F. Vivallo. (2018). A new technique in the excavation of ground-nest bee burrows (Hymenoptera: Apoidea). Rev. Bras. Entomol. 62(1):1–4.CrossRefGoogle Scholar
  71. Martins, R. P., S. T. M. Guerra, and M. S. Barbeitos. (2001). Variability in egg-to-adult development time in the bee Ptilothrix plumata and its parasitoids. Ecol. Entomol. 26:609–616.CrossRefGoogle Scholar
  72. Martins, C. F., M. P. Peixoto, and C. M. L. Aguiar. (2014). Plastic nesting behavior of Centris (Centris) flavifrons (Hymenoptera: Apidae: Centridini) in an urban area. Apidologie 45(2):156–171.CrossRefGoogle Scholar
  73. McFrederick, Q. S., and D. R. Taylor. (2013). Evolutionary history of nematodes associated with sweat bees. Mol. Phylogenet. Evol. 66(3):847–856.PubMedCrossRefGoogle Scholar
  74. Michener, C. D. (1966). The bionomics of a primitively social bee, Lasioglossum versatum (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 39(2):193–217.Google Scholar
  75. Michener, C. D. (1974). The social behavior of the bees: a comparative study. Harvard University Press.Google Scholar
  76. Michener, C. D. (2000). The bees of the world. JHU press.Google Scholar
  77. Michener, C. D., and D. J. Brothers. (1971). A simplified observation nest for burrowing bees. J. Kansas Entomol. Soc. 44(2):236–239.Google Scholar
  78. Michener, C. D., and D. J. Brothers. (1974). Were workers of eusocial Hymenoptera initially altruistic or oppressed? PNAS 71(3):671–674.PubMedCrossRefGoogle Scholar
  79. Michener, C. D., E. A. Cross, H. V. Daly, C. W. Rettenmeyer, and A. Wille. (1955). Additional techniques for studying the behavior of wild bees. Insect. Soc. 2(3):237–246.CrossRefGoogle Scholar
  80. Michener, C. D., D. J. Brothers, and D. R. Kamm. (1971). Interactions in colonies of primitively social bees: II, some queen-worker relations in Lasioglossum zephyrum. J. Kansas Entomol. Soc. 44(2):276–279.Google Scholar
  81. Moroń, D., I. M. Grześ, P. Skórka, H. Szentgyörgyi, R. Laskowski, S. G. Potts, and M. Woyciechowski. (2012). Abundance and diversity of wild bees along gradients of heavy metal pollution. J. Appl. Ecol. 49(1):118–125.CrossRefGoogle Scholar
  82. Mueller, U. G., and B. Wolf-Mueller. (1993). A method for estimating the age of bees: Age-dependent wing wear and coloration in the Wool-Carder bee Anthidium manicatum (hymenoptera: Megachilidae). J. Insect Behav. 6(4):529–537.CrossRefGoogle Scholar
  83. Norden, B.B. (1984). Nesting biology of Anthophora abrupta (Hymenoptera: Anthophoridae). J. Kansas Entomol. Soc. 57(2):243–262.Google Scholar
  84. Parker, F. D., and H. W. Potter. (1974). Methods of transferring and establishing Alkali bees. Environ. Entomol. 3(5):739–743.CrossRefGoogle Scholar
  85. Paxton, R. J., M. Ayasse, J. Field, and A. Soro. (2002). Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites. Mol. Ecol. 11(11):2405–2416.PubMedCrossRefGoogle Scholar
  86. Plateaux-Quénu, C. (1992). Comparative biological data in two closely related eusocial species: Evylaeus calceatus (Scop.) and Evylaeus albipes (F.) (Hym., Halictinae). Insect. Soc. 39(4):351–364.CrossRefGoogle Scholar
  87. Plateaux-Quénu, C., L. Plateaux, and L. Packer. (2000). Population-typical behaviours are retained when eusocial and non-eusocial forms of Evylaeus albipes (F.) (Hymenoptera, Halictidae) are reared simultaneously in the laboratory. Insect. Soc. 47(3):263–270.CrossRefGoogle Scholar
  88. Polidori, C., and L. Borruso. (2012). Socially peaceful: foragers of the eusocial bee Lasioglossum malachurum are not aggressive against non-nestmates in circle-tube arenas. Acta Ethol. 15(1):15–23.CrossRefGoogle Scholar
  89. Potts, S., and P. Willmer. (1997). Abiotic and biotic factors influencing nest-site selection by Halictus rubicundus, a ground-nesting halictine bee. Ecol. Entomol. 22(3):319–328.CrossRefGoogle Scholar
  90. Praz, C. J., A. Müller, and S. Dorn. (2008). Host recognition in a pollen-specialist bee: evidence for a genetic basis. Apidologie 39(5):547–557.CrossRefGoogle Scholar
  91. Roulston, T. H., and J. H. Cane. (2000). Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222(1–4):187–209.CrossRefGoogle Scholar
  92. Roulston, T. H., and J. H. Cane. (2002). The effect of pollen protein concentration on body size in the sweat bee Lasioglossum zephyrum (Hymenoptera : Apiformes). Evol. Ecol. 16(1):49–65.CrossRefGoogle Scholar
  93. Rozen, J. G. (2016). Nesting biology of the solitary bee Epicharis albofasciata (Apoidea: Apidae: Centridini). Am. Mus. Novit. 3869:1–8.CrossRefGoogle Scholar
  94. Ruddle, N., C. Elston, O. Klein, A. Hamberger, and H. Thompson. (2018). Effects of exposure to winter oilseed rape grown from thiamethoxam-treated seed on the red mason bee Osmia bicornis. Environ. Toxicol. Chem. 37(4):1071–1083.PubMedCrossRefGoogle Scholar
  95. Schäffler, I., and S. Dötterl. (2011). A day in the life of an oil bee: phenology, nesting, and foraging behavior. Apidologie 42(3):409–424.CrossRefGoogle Scholar
  96. Schmidt, J. O., S. L. Buchmann, and M. Glaiim. (1989). The nutritional value of Typha latifolia pollen for bees. J. Apic. Res. 28(3):155–165.CrossRefGoogle Scholar
  97. Shebl, M. A., R. M. Al Aser, and A. Ibrahim. (2016). Nesting biology and seasonality of long-horned bee Eucera nigrilabris Lepeletier (Hymenoptera: Apidae). Sociobiology 63(4):1031–1037.CrossRefGoogle Scholar
  98. Sick, M., M. Ayasse, J. Tengö, W. Engels, G. Lübke, and W. Francke. (1994). Host-parasite relationships in six species of Sphecodes bees and their halictid hosts: Nest intrusion, intranidal behavior, and Dufour's gland volatiles (Hymenoptera: Halictidae). J. Insect Behav. 7(1):101–117.CrossRefGoogle Scholar
  99. Simpson, B. (1983). Evolution and diversity of floral rewards. Handbook of experimental pollination biology. 142–159.Google Scholar
  100. Smith, B. H. (1987). Effects of genealogical relationship and colony age on the dominance hierarchy in the primitively eusocial bee Lasioglossum zephyrum. Anim. Behav. 35(1):211–217.CrossRefGoogle Scholar
  101. Staab, M., G. Pufal, T. Tscharntke, and A. M. Klein. (2018). Trap nests for bees and wasps to analyse trophic interactions in changing environments—A systematic overview and user guide. Methods Ecol. Evol. 9(11):2226–2239.CrossRefGoogle Scholar
  102. Stephen, W. P. (1960a). Artificial bee beds for the propagation of the Alkali bee, Nomia melander. J. Econ. Entomol. 53(6):1025–1030.CrossRefGoogle Scholar
  103. Stephen, W. P. (1960b). Studies in the alkali bee (Nomia melanderi Ckll.) II. Preliminary investigations on the effect of soluble salts on alkali bee nesting sites. Agricultural Experiment Station, Oregon State College, Corvallis, Oregon.Google Scholar
  104. Stephen, W. P. (1965). Effects of soil moisture on survival of prepupae of the alkali bee. J. Econ. Entomol. 58(3):472–474.CrossRefGoogle Scholar
  105. Stockhammer, K. A. (1966). Nesting habits and life cycle of a sweat bee, Augochlora pura (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 39(2):157–192.Google Scholar
  106. Strohm, E., and A. Bordon-Hauser. (2003). Advantages and disadvantages of large colony size in a halictid bee: the queen's perspective. Behav. Ecol. 14(4):546–553.CrossRefGoogle Scholar
  107. Ullmann, K. S., M. H. Meisner, and N. M. Williams. (2016). Impact of tillage on the crop pollinating, ground-nesting bee, Peponapis pruinosa in CaliforniaAgric. Ecosyst. Environ. 232:240–246.CrossRefGoogle Scholar
  108. Vinchesi, A. C., and D. B. Walsh. (2014). Quadrat method for assessing the population abundance of a commercially managed native soil-nesting bee, Nomia melanderi (Hymenoptera: Halictidae), in proximity to alfalfa seed production in the Western United States. J. Econ. Entomol. 107(4):1695–1699.PubMedCrossRefGoogle Scholar
  109. Wcislo, W. T. (1992). Attraction and learning in mate-finding by solitary bees, Lasioglossum (Dialictus) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 31(2):139–148.CrossRefGoogle Scholar
  110. Yanega, D. (1990). Philopatry and nest founding in a primitively social bee, Halictus rubicundus. Behav. Ecol. Sociobiol. 27(1):37–42.CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of Illinois Urbana-ChampaignUrbanaUSA

Personalised recommendations