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The Chemical Basis for Nestmate Recognition and Mate Discrimination in Social Insects

  • Brian H. Smith
  • Michael D. Breed

Abstract

In this chapter we discuss the chemical basis for nestmate recognition in social insects. Animals that live in family groups are often able to discriminate family members from non-family members. For example, humans and other mammals can use a variety of cues—visual, auditory, and perhaps olfactory—to learn the identities of family members. Birds, on the other hand, rely primarily on auditory cues (Beecher, 1988). While any phenotypic trait that is associated with group membership could be utilized in nestmate recognition, studies of social insects have shown that they depend solely on olfactory cues to discriminate family members from other conspecifics.

Keywords

Social Insect Cuticular Hydrocarbon Floral Scent Macrocyclic Lactone Nestmate Recognition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Ayasse, M., Engels, W., Hefetz, A., Lübke, G., and Franke, W. (1990) Ontogenetic patterns in amounts and proportions of Dufour’s gland volatile secretions in virgin and nesting queens of Lasioglossum malachurum (Hymenoptera: Halictidae). Z. Naturforsch. 45c: 709–714.Google Scholar
  2. Ayasse, M., Engels, W., Hefetz, A., Tengö, J., Lübke, G., and Franke, W. (1993) Ontogenetic patterns of volatiles identified in Dufour’s gland extracts from queens and workers of the primitively eusocial halictine bee, Lasioglossum malachurum (Hymenoptera: Halictidae). Insectes Soc. 40: 41–58.CrossRefGoogle Scholar
  3. Barrows, E. M. (1975a) Individually distinctive odors in an invertebrate. Behav. Biol. 15: 57–64.PubMedCrossRefGoogle Scholar
  4. Barrows, E. M. (1975b) Mating behavior in halictine bees (Hymenoptera: Halictidae): III. Copulatory behavior and olfactory communication. Insectes Soc. 22: 307–331.CrossRefGoogle Scholar
  5. Barrows, E. M., Bell, W. J., and Michener, C. D. (1975) Individual odor differences and their social functions in insects. Proc. Nat. Acad. Sci. USA 72: 2824–2828.PubMedCrossRefGoogle Scholar
  6. Bateson, P. P. G. (1983) Optimal outbreeding. In: Mate Choice (Bateson, P.P.G., ed.). pp 367–377. Cambridge U. Press, Cambridge. U.K.Google Scholar
  7. Beecher, M. D. (1988) Kin recognition in birds. Behav. Genet. 18: 465–482.PubMedCrossRefGoogle Scholar
  8. Bekoff, M. (1981) Mammalian sibling interactions. Genes, facilitative environments, and the coefficient of familiarity. In: Parental Care In Mammals (Gubernick, D. J., and Klopfer, P. H.eds.). pp. 307–346. Plenum, New York.CrossRefGoogle Scholar
  9. Bell, W.J. (1974) Recognition of resident and non-resident individuals in intraspecific nest defense of a primitively eusocial halictine bee. J. Comp. Physiol. 93: 195–202.CrossRefGoogle Scholar
  10. Bell, W. J., and Hawkins, W. A. (1974) Patterns of intraspecific agonisitc interactions involved in nest defense of a primitively eusocial halictine bee. J. Comp. Physiol. 93: 183–193.CrossRefGoogle Scholar
  11. Bennett, B. (1989) Nestmate recognition systems in a monogynous-polygynous species pair of ants. Parts I and II. Sociobiol. 16: 121–147.Google Scholar
  12. Bergström, G. and Tengö, J. (1979) C24, C22, C20, and C18 macrocyclic lactones in halictid bees. Acta Chem. Scand. B33: 390.CrossRefGoogle Scholar
  13. Blaustein, A. R. (1983) Kin recognition mechanisms: Phenotype matching or recognition alleles. Am. Nat. 121: 749–754.CrossRefGoogle Scholar
  14. Blum, M. S. and Fales, H. M. (1988) Eclectic chemisociality of the honeybee: A wealth of behaviors, pheromones, and exocrine glands. J. Chem. Ecol. 14: 2099–2107.CrossRefGoogle Scholar
  15. Blum, M. S., Fales, H. M., Jones, T. H., Rinderer, T. E. and Tucker, K. W. (1983) Caste-specific esters derived from the queen honey bee sting apparatus. Comp. Biochem. Physiol. 75B:237–238.Google Scholar
  16. Bonavita-Cougourdan, A., Clement, J-L., and Lange, C. (1989) The role of cuticular hydrocarbons in recognition of larvae by workers of the ant Camponotus vagus: Changes in the chemical signature in response to social environment. Sociobiol. 16: 49–74.Google Scholar
  17. Bowden, R.M. and Breed, M.D. (in press) The effects of floral extracts and oils on nestmate recognition in the honey bee. J. Insect Behav. Google Scholar
  18. Breed, M. D. (1981) Individual recognition and learning of queen odors by worker honeybees (Apis mellifera). Proc. Natl. Acad. Sci. USA 78: 2635–2637.PubMedCrossRefGoogle Scholar
  19. Breed, M. D. (1983) Nestmate recognition in honey bees. Anim. Behav. 31: 86–91.CrossRefGoogle Scholar
  20. Breed, M. D. (1987) Multiple inputs in the nestmate discrimination system of the honey bee. In: The Chemistry and Biology of Social Insects (Eder, J., and Rembold, H., eds). pp. 461–462. Verlag J. Peperny: Munich, Germany.Google Scholar
  21. Breed, M. D. (1993) Odour detection in bees. Nature 362: 120.CrossRefGoogle Scholar
  22. Breed, M. D. and Bennett, B. (1987) Kin recognition in highly eusocial insects. In: Kin Recognition In Animals (Fletcher, D.J.C. and Michener, C.D., eds.). pp. 243–285. John Wiley, Chichester, U.K.Google Scholar
  23. Breed, M.D., Garry, M.F., Pearce, A.N., Hibbard, B.E., Bjostad, L.B., and Page, R.E. (in press) The role of wax comb in honey bee nestmate recognition: Genetic effects on comb discrimination, acquisition of comb cues by bees, and passage of cues among individuals. Anim. Behav. Google Scholar
  24. Breed, M.D., Hibbard, B.E., Bjostad, L.B., and Page, R.E. (in press) Genetic component of variation in comb wax hydrocarbons produced by honey bees. J. Chem. Ecol. Google Scholar
  25. Breed, M. D. and G. Julian. (1992) Honey bee nestmate recognition: Simple rules do not apply. Nature. 357: 685–686.CrossRefGoogle Scholar
  26. Breed, M. D., Smith, T. A., and Torres, A. (1992a) Guard honey bees: role in nestmate recognition and replacement. Annals Entomol. Soc. Am. 85: 633–637.Google Scholar
  27. Breed, M. D., Butler, L., and Stiller, T. M. (1985) Kin recognition by worker honey bees in genetically mixed groups. Proc. Natl. Acad. Sci. USA 82: 3058–3061.PubMedCrossRefGoogle Scholar
  28. Breed, M. D., Fewell, J. H. and Williams, K. R. (1988a) Comb wax mediates the acquisition of nest-mate recognition cues in honey bees. Proc. Natl. Acad. Sci. USA 85: 8766–8769.PubMedCrossRefGoogle Scholar
  29. Breed, M. D. and Stiller, T. M. (1992) Honey bee, Apis mellifera, nestmate discrimination: hydrocarbon effects and the evolutionary implications of comb choice. Anim. Behav. 43: 875–883.CrossRefGoogle Scholar
  30. Breed, M. D., Stiller, T. M., and Moor, M. J., (1988b) The ontogeny of kin discrimination cues in the honey bee, Apis mellifera. Behav. Genet. 18: 439–448.CrossRefGoogle Scholar
  31. Breed, M. D., Stiller, T. M., Blum, M. S., and Page, R. E., Jr. (1992b) Honey bee nestmate recognition: effects of queen fecal pheromones. J. Chem. Ecol. 18: 1633–1640.CrossRefGoogle Scholar
  32. Brothers, D. J., and Michener, C. D. (1974) Interactions in colonies of primitively social bees, III. Ethometry of division of labor in Lasioglossum zephyrum. J. Comp. Physiol. 90: 129–168.CrossRefGoogle Scholar
  33. Buckle, G. R., and Greenberg, L. (1981) Nestmate recognition in sweat bees (Lasioglos-sum zephyrum): Does an individual recognize its own odour or only odours of its nestmates? Anim. Behav. 29: 802–809.CrossRefGoogle Scholar
  34. Butts, D. P., Camann, M. A., and Espelie, K. E. (1993) Discriminant analysis of cuticular hydrocarbons of the baldfaced hornet, Dolichovespula maculata. Sociobiol. 21: 193–201.Google Scholar
  35. Cane, J. H. (1981) Dufour’s gland secretion in the cell linings of bees (Hymenoptera: Apoidea). J. Chem. Ecol. 7: 403–410.CrossRefGoogle Scholar
  36. Carlin, N. F. and Hölldobler, B. (1986) The kin recognition system of carpenter ants (Camponotus spp.) I. Hierarchical cues in small colonies. Behav. Ecol. Sociobiol. 19: 123–134.CrossRefGoogle Scholar
  37. Carlson, D. A. and Bolton, A. B.. (1984) Identification of Africanized and European honey bees using extracted hydrocarbons. Bull. Entomol. Soc. Am. 30: 32–35.Google Scholar
  38. Clement, J-L., Bonavita-Cougourdan, A. and Lange, C. (1987) Nestmate recognition and cuticular hydrocarbons in Camponotus vagus. In: The Chemistry and Biology of Social Insects (Eder, J. and Rembold, H., eds.). pp. 473–474. Verlag J. Peperny, Munich, Germany.Google Scholar
  39. Collins, A. M. and Blum, M. S. (1983) Alarm responses caused by newly identified compounds derived from the honey bee sting. J. Chem. Ecol. 9: 57–65.CrossRefGoogle Scholar
  40. Crewe, R. M. (1982) Compositional variability, the key to the social signals produced by honey bee mandibular glands. In: The Biology of Social Insects (Breed, M.D., Michener, C.D. and Evans, H.E., eds.). pp. 318–322. Westview Press, Boulder, Colorado.Google Scholar
  41. Crosland, M. W. J. (1989) Kin recognition in the ant Rhytidoponera confusa. II. Gestalt odour. Anim. Behav. 37: 920–926.CrossRefGoogle Scholar
  42. Crozier R. H., Smith B. H., and Crozier Y. C. (1987) Relatedness and population structure of the primitively eusocial bee Lasioglossum zephyrum in Kansas. Evolution 41: 902–910.CrossRefGoogle Scholar
  43. Dawkins, R. 1982. The extended phenotype. Freeman: Oxford.Google Scholar
  44. de Lello, E. 1971) Adexnal glands of the sting apparatus of bees: Anatomy and histology. II. (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 44: 14–20.Google Scholar
  45. Espelie, K. E., and Hermann, H. R. (1990) Surface lipids of the social wasp Polistes annularis (L.) and its nest and nest pedicel. J. Chem. Ecol. 16: 1841–1852.CrossRefGoogle Scholar
  46. Espelie, K. E., Butz, V. M., and Dietz, A. (1990a) Decyl-decanoate—A major component of the tergite glands of honeybee queens. J. Apic. Res. 29: 15–19.Google Scholar
  47. Espelie, K. E., Wenzel, J. W. and Chang, G. (1990b) Surface lipids of social wasp Polistes metricus Say and its nest and nest pedicel and their relation to nestmate recognition. J. Chem. Ecol. 16: 2229–2241.CrossRefGoogle Scholar
  48. Ferguson, I. D., Gamboa, G. J. and Jones, J. K. (1987) Discrimination between natal and non-natal nests by the social wasps Dolichovespula maculata and Polistes fuscatus. J. Kansas Entomol. Soc. 60: 65–69.Google Scholar
  49. Foster, R. and Gamboa, G. (1989) Nest entrance marking with colony specific odors by the bumble bee Bombus occidentalis. Ethology 81: 273–278.CrossRefGoogle Scholar
  50. Francis, B. R., Blanton, W. E., Littlefield, J. L. and Nunamaker, R. A. (1989) Hydrocarbons of the cuticle and hemolymph of the adult honey bee. Ann. Entomol. Soc. Am. 82: 486–494.Google Scholar
  51. Franks, N. R., Blum, M., Smith, R.-K. and Allies, A. B. (1990) Behavior and chemical disguise of cuckoo ant Leptothorax kutteri in relation to its host Leptothorax acervorum.. J. Chem. Ecol. 16: 1431–1444.CrossRefGoogle Scholar
  52. Free, J. B. (1959) The effect of moving colonies of honeybees to new sites on their subsequent foraging behaviour. J. Agr. Sci. 53: 1–9.CrossRefGoogle Scholar
  53. Frumhoff, P. C. and Schneider, S. (1987) The social consequence of honeybee polyandry: kinship influences worker interactions within colonies. Anim. Behav. 35: 255–262.CrossRefGoogle Scholar
  54. Gamboa, G. J., Foster, R. L. and Richards, K. W. (1987) Intraspecific nest and brood recognition by queens of the bumble bee, Bombus occidentalis. Can. J. Zool. 65: 2893–2897.CrossRefGoogle Scholar
  55. Gamboa, G. J., Reeve, H. K. and Pfennig, D. W. (1986a) The evolution and ontogeny of nestmate recognition in social wasps. Ann. Rev. Entomol. 31: 431–454.CrossRefGoogle Scholar
  56. Gamboa, G. J., Reeve, H. K., Ferguson, I. and Wacker, T. L. (1986b) Nestmate recognition in social wasps: the origin and acquisition of recognition odours. Anim. Behav. 34: 685–695.CrossRefGoogle Scholar
  57. Getz, W. M. (1991) The honey bee as a model kin recognition system. In: Kin Recognition (Hepper, P. G., ed.). pp. 358–412. Cambridge University Press, Cambridge, U.K.Google Scholar
  58. Getz, W. M. (1993) Odour detection in bees. Nature 362: 119–120.CrossRefGoogle Scholar
  59. Getz, W.M., and Page, R.E. (1991) Chemosensory kin-communication systems and kin recognition in honey bees. Ethology 87: 298–315.CrossRefGoogle Scholar
  60. Getz, W. M. and Smith, K. B. (1986) Honeybee kin recognition: learning self and nestmate phenotypes. Anim. Behav. 34: 1617–1626.CrossRefGoogle Scholar
  61. Getz, W. M. and Smith, K. B. (1987) Olfactory sensitivity and discrimination of mixtures in the honey bee, Apis mellifera. J. Comp. Physiol. A. 160:239–245.CrossRefGoogle Scholar
  62. Getz, W. M., Brückner, D. and Parisian, T. R. (1982) Kin structure and the swarming behavior of the honeybee, Apis mellifera. Behav. Ecol. Sociobiol. 10: 265–270.CrossRefGoogle Scholar
  63. Getz, W. M., Brückner, D. and Smith, K. B. (1989) The ontogeny of cuticular chemosensory cues in worker honey bees Apis mellifera. Apidologie 20: 105–113.CrossRefGoogle Scholar
  64. Getz, W. M. and Page, R. E. (1991) Chemosensory kin-communication systems and kin recognition in honey bees. Ethology 87: 298–315.CrossRefGoogle Scholar
  65. Greenberg, L. (1979) Genetic component of bee odor in kin recognition. Science 206: 1095–1097.PubMedCrossRefGoogle Scholar
  66. Hamilton, W. D. (1964) The genetical evolution of social behaviour. Parts I and II. J. Theor Biol. 7: 1–16.PubMedCrossRefGoogle Scholar
  67. Hefetz, A., Bergström, G., and Tengö, J. (1986) Species, individual, and kin specific blends in Dufour’s gland secretions of halictine bees—Chemical evidence. J. Chem. Ecol. 12: 197–208.CrossRefGoogle Scholar
  68. Hefetz, A., Blum, M. S., Eickwort, G. C., and Wheeler, J. W. (1978) Chemistry of the Dufour’s gland secretion of halictine bees. Comp. Biochem. Physiol. 61B: 129–132.Google Scholar
  69. Hefetz, A., Fales, H. M., and Batra, S. W. T. (1979) Natural polyesters: Dufour’s gland macrocyclic lactones form brood cell laminesters in Colletes bees. Science 204: 415–417.PubMedCrossRefGoogle Scholar
  70. Hepburn, H. R. (1986) Honey Bees and Wax. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
  71. Hepper, P. G. (1991) Kin Recognition. Cambridge University Press, Cambridge, U.K.CrossRefGoogle Scholar
  72. Hölldobler, B. and Michener, C. D. (1980) Mechanisms of identification and discrimination in social Hymenoptera. In: Evolution of Social Behavior: Hypotheses and Empirical Tests. (Markl, H., ed.). pp. 35–58. Verlag Chemie, Weinheim, Germany.Google Scholar
  73. Isigrini, M., Lenoir, A. and Jaisson, P. (1985) Preimaginal learning as a basis of colony-brood recognition in the ant, Cataglyphis cursor. Proc. Natl. Acad. Sci. USA. 82: 8545–8547.CrossRefGoogle Scholar
  74. Kaitala, V., Smith, B.H., and Getz, W.M. (1990) Nesting strategies of primitively eusocial bees: A model of nest usurpation during the solitary state of the nesting cycle. J. Theor. Biol. 144: 445–471.CrossRefGoogle Scholar
  75. Kalmus, H. and Ribbands, C. R. (1952) The origin of odors by which honey bees distinguish their companions. Proc. Royal Soc. (B) 140: 50–59.CrossRefGoogle Scholar
  76. Knudsen, J. T., Tollsten, L. and Bergström, L. G. (1993) Floral scents—A checklist of volatile compounds isolated by head-space techniques. Phytochem. 33: 253–280.CrossRefGoogle Scholar
  77. Kukuk, P. F., Breed, M. D., Sobti, A., and Bell, W. J. (1977) The contributions of kinship and conditioning to nest recognition and colony member recognition in a primitively eusocial bee, Lasioglossum zephyrum. Behav. Ecol. Sociobiol. 2: 319–327.CrossRefGoogle Scholar
  78. Michener, C. D. (1974) The Social Behavior of the Bees. Harvard University Press, Cambridge, MA.Google Scholar
  79. Michener, C. D. (1978) The parasitic groups of the Halictidae (Hymenoptera, Apoidea). University Kansas Sci. Bull. 51: 291–339.Google Scholar
  80. Michener, C. D. and Smith, B. H. (1987) Kin recognition in primitively social insects. In: Kin recognition in animals (Fletcher, D.J.C. and Michener, C.D., eds.). pp. 209–242. John Wiley, Chichester, U.K.Google Scholar
  81. Morel, L. and Vander Meer, R. K. (1987) Nestmate recognition in Camponotus floridianus: Behavioral and chemical evidence for the role of age and social experience. In: Chemistry and Biology of Social Insects (Eder, J. and Rembold, H., eds.). pp. 471–472. Verlag J. Peperny, Munich, Germany.Google Scholar
  82. Moritz, R. F. A. and Crewe, R. M. (1988) Chemical signals of queens in kin recognition of honeybees, Apis mellifera L. J. Comp. Physiol. A 164: 83–89.CrossRefGoogle Scholar
  83. Moritz, R. F. A. and South wick, E. E. (1987) Metabolic test of volatile odor labels as kin recognition cues in honey bees (Apis mellifera). J. exp. Zool. 243: 503–507.CrossRefGoogle Scholar
  84. Moure, J. S., C. M. F. and Hurd, P. D. (1987) An Annotated Catalog of the Halictid Bees of the Western Hemisphere (Hymenoptera; Halictidae). Smithsonian Inst. Press, Washington, D.C.Google Scholar
  85. Noonan, K. C. (1986) Recognition of queen larvae by worker honey bees (Apis mellifera L.). Ethology 73: 295–306.CrossRefGoogle Scholar
  86. Obin, M. S. (1986) Nestmate recognition cues in laboratory and field colonies of Solenopsis invicta Buren: effect of environment and the role of cuticular hydrocarbons. J. Chem. Ecol. 12: 1965–1975.CrossRefGoogle Scholar
  87. Packer, L. (1991) The evolution of social behavior and nest architecture in sweat bees of the subgenus Evylaeus (Hymenoptera: Halictidae): a phylogenetic approach. Behav. Ecol. Sociobiol. 29: 153–160.CrossRefGoogle Scholar
  88. Page, R. E. and Erickson, E. (1986) Kin recognition and virgin queen acceptance by worker honey bees (Apis mellifera L.). Anim. Behav. 34: 1061–1069.CrossRefGoogle Scholar
  89. Page, R. E. Jr., Metealf, R. A., Metealf, R. L., Erickson, E. H. Jr. and Lampman, R. L. (1991) Extractable hydrocarbons and kin recognition in the honey bee. J. Chem. Ecol. 17: 745–756.CrossRefGoogle Scholar
  90. Pfennig, D. W., Gamboa, G. J., Reeve, H. K., Shellman-Reeve, J. and Ferguson, I. D. (1983) The mechanism of nestmate discrimination in social wasps (Polistes, Hymenoptera, Vespidae). Behav. Ecol. Sociobiol. 13: 299–305.CrossRefGoogle Scholar
  91. Plateaux-Quénu, C. (1959) Un nouveau type de société d’insectes: Halictus marginatus Brullé (Hymenoptera, Apoidea). Ann. Biol. 35: 325–444.Google Scholar
  92. Ratnieks, F.L.W. (1991) The evolution of genetic odorcue diversity in social Hymenoptera. Am. Nat. 137: 202–226.CrossRefGoogle Scholar
  93. Reeve, H. K. (1989) The evolution of conspecific acceptance thresholds. Am. Nat. 133: 407–435.CrossRefGoogle Scholar
  94. Singer, T. L. and Espelie, K. E. (1992) Social wasps use nest paper hydrocarbons for nestmate recognition. Anim. Behav. 44: 63–68.CrossRefGoogle Scholar
  95. Singer, T. L., Camann, M. A., and Espelie, K. E. (1992a) Discriminant analysis of cuticular hydrocarbons of social wasp Polistes exclamans Viereck and surface hydrocarbons of its nest paper and pedicel. J. Chem. Ecol. 18: 785–797.CrossRefGoogle Scholar
  96. Singer, T. L., Espelie, K. E., and Himmelsbach, D. S. (1992b) Ultrastructural and chemical examination of paper and pedicel from laboratory and field nests of the social wasp Polistes metricus Say. J. Chem. Ecol. 18: 77–86.CrossRefGoogle Scholar
  97. Smith, B. H. (1983) Recognition of female kin by male bees through olfactory signals. Proc. Natl. Acad. Sci. USA 80: 4551–4553.PubMedCrossRefGoogle Scholar
  98. Smith, B. H. (1987) Effects of genealogical relationship and colony age on the dominance hierarchy of the primitively eusocial bee Lasioglossum zephyrum (Hymenoptera: Halictidae). Anim. Behav. 35: 211–217.CrossRefGoogle Scholar
  99. Smith, B. H. (1992) Merging mechanism and adaptation: an ethological approach to learning and generalization. In: Insect Learning: Ecological and Evolutionary Perspectives (Papaj, D.R. and Lewis, A.C., eds.). pp. 126–158. Chapman and Hall, New York, N.Y.Google Scholar
  100. Smith B. H., and Ayasse M. (1987) Kin-based male mating preferences in two species of halictine bees (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 20: 313–318.CrossRefGoogle Scholar
  101. Smith, B. H., and Weller, C. (1989) Social competition among gynes in halictine bees: the influence of bee size and pheromones on behavior. J. Insect Behav. 2: 397–411.CrossRefGoogle Scholar
  102. Smith, B. H., and Wenzel, J. W. (1988) Pheromonal covariation and kinship in social bee Lasioglossum zephyrum (Hymenoptera: Halictidae). J. Chem. Ecol. 14: 87–94.CrossRefGoogle Scholar
  103. Smith, B. H., Carlson, R. G., and Frasier, J. (1985) Identification and bioassay of macrocyclic lactone sex pheromone of the halictine bee Lasioglossum zephyrum. J. Chem. Ecol. 11: 1447–1456.CrossRefGoogle Scholar
  104. Tulloch, A. P. (1980) Beeswax—composition and analysis. Bee World 61: 47–62.Google Scholar
  105. Vander Meer, R. K., Saliwanchik, D. and Lavine, B. (1989) Temporal changes in colony cuticular hydrocarbon patterns of Solenopsis invicta: Implications for nestmate recognition. J. Chem. Ecol. 15: 2115–2125.CrossRefGoogle Scholar
  106. Wcislo, W. T. (1987) The role of learning in the mating biology of a sweat bee Lasioglossum zephyrum (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 20: 179–185.CrossRefGoogle Scholar
  107. Wcislo, W. T. (1993) Attraction and learning in mate-finding by solitary bees, Lasioglossum (Dialictus) figuersi Wcislo and Nomia triangulifera Vachal (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 31: 139–148.CrossRefGoogle Scholar
  108. Westrich, P. (1989) Die Wildbienen Baden-Württembergs; Spezieller Teil. Verlag Eugen Ulmer, Stuttgart, Germany.Google Scholar
  109. Yanega, D. (1988) Social plasticity and early-diapausing females in a primitively eusocial bee. Proc. Natl. Acad. Sci. USA. 85: 4374–4377.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1995

Authors and Affiliations

  • Brian H. Smith
    • 1
  • Michael D. Breed
    • 2
  1. 1.Department of EntomologyOhio State UniversityUSA
  2. 2.Department of Environmental, Population, and Organismic BiologyUniversity of ColoradoUSA

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