Interactions between females of Protandrena evansi (Hymenoptera: Andrenidae), a communal nesting bee
Tolerant behaviour Communal species Hymenoptera Chile
Main Article Content
This paper reports the results of a behavioral study carried out at Farellones, Metropolitan Region, Chile, using females of Protandrena evansi. Tolerant and intolerant behaviors were observed in an experimental arena where pairs of females from the same nest (intra-nest interaction) or from different nest (inter-nest interaction) were placed. Neither tolerant nor intolerant behaviors were different between intra-nest and inter-nest females. In a second experiment the behavioral responses performed by females towards cuticular extracts from nestmate and from non-nestmate females were evaluated. Both bioassays showed that P. evansi females do not exhibit a discriminative behavioral pattern between nestmate and non-nestmate females. Additionally, tolerant behaviors were the most frequent in both experimental interactions (intra and inter-nest interactions). These results suggest that this species has a communal social structure.
FLORES-PRADO, L., CHIAPPA, E., & MANTE, M. (2012). Interactions between females of Protandrena evansi (Hymenoptera: Andrenidae), a communal nesting bee. Revista Colombiana De Entomología, 38(1), 118–123. https://doi.org/10.25100/socolen.v38i1.8968
ABRAMS, J.; EICKWORT, G. C. 1981. Nest switching and guarding by the communal sweat bee Aapostemon virescens (Hymenoptera: Halictidae). Insectes Sociaux 28: 105-116.
BEEKMAN, M.; WOSSLER, T.; MARTIN, S.; RATNIEKS, F. 2002. Parasitic Cape honeybee workers (Apis mellifera capensis) are not given differential treatment by African guards (A. m. scutellata). Insectes Sociaux 49: 216-220.
BOULAY. R.; LENOIR, A. 2001. Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah. Behaviour Process 55: 67-73.
BREED, M. D. 1983. Nestmate recognition in honeybees. Animal Behaviour 31: 86-91.
BREED, M. D. 1998. Recognition pheromones of the honeybee. The chemistry of nestmate recognition. BioScience 48: 463470.
BREED, M.; SILVERMAN, J.; BELL, W. 1979. Agonistic Behavior, Social Interactions, and Behavioral Specialization in a Primitively Eusocial Bee. Insectes Sociaux 25: 351-364.
BREED, M. D. FEWELL, J. H.; WILLIAMS, K. R. 1988. Comb wax mediates the acquisition of nestmate recognition cues in honeybees. Proceedings of the National. Academy of Sciences U.S.A. 85: 8766-8769.
BROTHERS, D. J.; MICHENER, C. D. 1974. Interactions in colonies of primitively social bees. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 90 (2): 129-168.
BUCKLE, G. R. 1982. Queen-Worker Behavior and Nesmate Interactions in Young Colonies of Lasioglossum zephyrum. Insectes Sociaux 29: 125-137.
CHIAPPA, E.; RUZ, L.; GARCÍA, V. 2005. Biología de machos de Protandrena evansi Ruz y Chiappa (Hymenoptera: Andrenidae) (Farellones, Región Metropolitana, Chile). Acta Entomológica Chilena 29: 15-22.
CHIAPPA, E.; CASTRO, R. 2006. Comportamiento de nidificación comunal y de abastecimiento de Protandena evansi Ruz y Chiappa (Hymenoptera: Andrenidae: Panurginae) en Farellones, Región Metropolitana, Chile. Acta Entomológica Chilena 31: 7-14.
CROZIER, R. H.; PAMILO, P. 1996. Evolution of social insect colonies. Oxford University Press. 306 p.
CUSTER, C. P. 1928. The bee that works in stone: Perdita opuntiae Cockerell. Psyche 35: 67-83.
DANFORTH, B. N. 1991. Female foraging and intranest behavior of a communal bee, Perdita portalis (Hymenoptera: Andrenidae). Annals of the Entomological Society of America 84: 537-548.
FIELD, J. 1992. Intraespecific parasitism as an alternative reproductive tactic in nest-building wasp and bees. Biological Reviews 67: 79-126.
FLORES-PRADO, L.; CHIAPPA, E.; NIEMEYER, H. M. 2008a.
Nesting biology, life cycle, and interactions between females of Manuelia postica, a solitary species of the Xylocopinae (Hymenoptera: Apidae). New Zealand Journal of Zoology 35: 93-102.
FLORES-PRADO, L.; AGUILERA, D.; NIEMEYER, H. M. 2008b. Nest-mate recognition in Manuelia postica (Apidae: Xylocopinae): an eusocial trait is present in a solitary bee. Proceedings of the Royal Society, B. 275: 285-291.
FLORES-PRADO, L.; NIEMEYER, H. M. 2010. Kin Recognition in the largely solitary bee, Manuelia postica (Apidae: Xylocopinae). Ethology 116: 466-471.
GETZ, W. M. 1991. The honeybee as model kin recognition system. pp. 358-412. In: Hepper, G. P. (Ed.). King recognition. Cambridge University Press. Cambridge. 457 p.
GRIXTI, J., ZAYED, A.; PACKER, L. 2004. Behavorial interactions among females of Acamptopoeum submetallicum (Spinola) and Nolanomelissa toroi Rozen (Hymemoptera: Andrenidae). Journal of Hymenoptera Research 13: 48-56.
HOFFMANN, A.; ARROYO, M.; LIBERONA, F.; MUÑOZ, M.; WATSON, J. 1998. Plantas altoandinas en la flora silvestre de Chile. Ediciones Fundación Claudio Gay, Santiago de Chile. 281 p.
HOGENDOORN, K.; LEYS, R. 1993. The superseded female’s dilemma: factors that influence guarding behaviour of the carpenter bee Xylocopa pubescens. Behavioral Ecology and Sociobiology 33: 371-381.
HÖLLDOBLER, B.; MICHENER, C. 1980. Mechanisms of identification and discrimination in social Hymenoptera. pp. 35-58. In: Markl, H. (Ed.). Evolution of social behavior: Hypotheses and empirical tests. Weinheim: Verlag Chemie.
HÖLLDOBLER, B.; WILSON, E. O. 1990. The Ants. Harvard University Press, Cambridge. 548 p.
HOWARD, R. W.; BLOMQUIST, G.J. 1982. Chemical ecology and biochemistry of insect hydrocarbons. Annual Review of Entomology 27: 149-172.
HOWARD, R. W.; BLOMQUIST, G.J. 2005. Ecological, behavioural and biochemical aspects of insect hydrocarbons. Annual Review of Entomology 50: 371-393.
INOUE, T.; ROUBIK, D. W.; SUKA, T. 1999. Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini). Insectes Sociaux 46: 208-218.
JAISSON, P. 1991. Kinship and fellowship in ants and social wasps, pp. 61-93. In: Hepper, G. P. (Ed.). King recognition. Cambridge University Press. Cambridge. 457 p.
KELLER, L. 1997. Indiscriminate altruism: unduly nice parents and siblings. Trends in Ecology and Evolution 12: 99-103.
KUKUK, P. 1980. Diurnal Activity of a Primitively Eusocial Bee, Lasioglossum zephyrum, within the Nest. Journal of the Kansas Entomological Society 53 (1): 149-156.
KUKUK, P. 1992. Social interactions and familiarity in a communal Halictine bee Lasioglossum (Chilalictus) hemichalceum. Ethology 91: 291: 300.
McCONNELL-GARNER J.; KUKUK, P. F. 1997. Behavioral Interactions of two solitary Halictine bees with comparisons among solitary, communal and eusocial species. Ethology 103: 19-32.
MASON, C. A. 1988. Division of labor and adult interactions in eusocial colonies of two allodapines bee species (Hymenoptera: Anthophoridae). Journal of the Kansas Entomological Society 61: 477-491.
MICHENER, C. D. 1963. Observations on bionomics of a colonial bee of the genus Perdita (Hymenoptera: Apoidea: Panurginae). Journal of the Kansas Entomological Society 36: 114-118.
MICHENER, C. D. 1969. Comparative social behavior of bees. Annual Review of Entomology 14: 299-342.
MICHENER, C. D. 1974. The social behavior of the bees. A comparative study. Harvard Univ. Press. Cambridge, M.A. 404 p.
MICHENER, C. D. 2007. The Bees of the world. Johns Hopkins University Press, Baltimore, Maryland. 953 p.
MUNSTER-SWENDSEN, M. 1968. On the biology of the solitary bee Panurgus bankasianus Kirby (Hymenoptera: Apidae), including some ecological aspects. Arsskrift Kongelige Veterinaer Og Landbohojskole 51: 215-241.
PABALAN, N.; DAVEY, G.; PACKER, L. 2000. Escalation of Aggressive Interactions During Staged Encounters in Halictus ligatus Say (Hymenoptera: Halictidae), with a Comparison of Circle Tube Behaviors with Others Halictine Species. Journal of Insect Behavior 13: 627-650.
PACKER. L. 1986. Multiple-foundress associations in a temperate population of Halictus ligatus (Hymenoptera; Halictidae). Canadian Journal of Zoology 64: 2325-2332.
PACKER, L. 2000. The Biology of Trincohalictus prognathus (Perez) (Hymenoptera: Halictidae: Halictini). Journal of Hymenoptera Research 9: 53-61.
PAXTON, R. J.; THORÉN, P. A.; TENGÖ, J.; ESTOUP, A.; PAMILIO, P. 1996. Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera: Andrenidae), using microsatellites. Molecular Ecology 5: 511-519.
PAXTON, R. J.; KUKUK, P. F.; TENGÖ, J. 1999. Effects of familiarity and nestmate number on social interactions in two communal bees, Andrena scotica and Panurgus calcaratus (Hymenoptera, Andrenidae). Insectes Sociaux 46: 109-118.
PEREIRA-MARTINS, S. R. 1991. Biología de Eulema nigrita. Atividades nidais. Papéis Avulsos de Zoología 37: 237-243.
PUSEY, A. E.; WOLF, M. 1996. Inbreeding avoidance in animals.Trends in Ecology and Evolution 11: 201-206.
ROZEN, J. 1966. Systematics of the larvae of North American panurgine bees (Hymenoptera: Apoidea). American Museum Novitates 2259: 1-22.
ROZEN, J. G. 1989. Life history studies of the “primitive” panurgine bees (Hymenoptera: Andrenidae: Panurginae). American Museum Novitates 2692: 1-27.
RUZ, L.; ROZEN, J., JR. 1993. South American Panurginae bees (Apoidea: Andrenidae: Panurginae), part I. Biology, mature larva, and description of a new genus and species. American Museum Novitates 3057: 1-12.
SIEGEL, S.; CASTELLAN, JR. N.J. 1988. Nonparametric statistics for the behavioral sciences, 2ª Ed. McGraw-Hill International Editions. 399 p.
SINGER, T. L. 1998. Roles of hydrocarbons in the recognition systems of insects. American Zoologist 38: 394-405.
SMITH, B.; WELLER, C. 1989. Social competition among gynes in Halictine bees: The influence of bee size and pheromones on behavior. Journal of Insect Behavior 2: 397-411.
SMITH, B. H.; BREED M. D. 1995. The Chemical Basis for Nestmate Recognition and Mate Discrimination in Social Insect, pp. 387-317. In: Carde, R. T.; Bell, W. J. (Eds.). Chemical Ecology of Insects 2, Chapman y Hall, New York. 433 p.
SOKAL, R. R.; ROHLF, F. J. 1995. Biometry. The principles and practice of statistics in biological research. 3ª Ed. W.H. Freeman and company, New York. 887 p.
TENGÖ, J. J.; ERICKSON, A. K.; BORG-KARLSON, B. H.; SMITH H. D. 1988. Mate-locating strategies and multimodal communication in male mating behavior of Panurgus bankasianus and P. calcaratus (Apoidea, Andrenidae). Journal of the Kansas Entomological Society 61: 388-395.
WCISLO, W.; DANFORTH, B. 1997. Secondarily solitary: the evolutionary loss of social behavior. Trends in Ecology and Evolution 12: 468-474.
BEEKMAN, M.; WOSSLER, T.; MARTIN, S.; RATNIEKS, F. 2002. Parasitic Cape honeybee workers (Apis mellifera capensis) are not given differential treatment by African guards (A. m. scutellata). Insectes Sociaux 49: 216-220.
BOULAY. R.; LENOIR, A. 2001. Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah. Behaviour Process 55: 67-73.
BREED, M. D. 1983. Nestmate recognition in honeybees. Animal Behaviour 31: 86-91.
BREED, M. D. 1998. Recognition pheromones of the honeybee. The chemistry of nestmate recognition. BioScience 48: 463470.
BREED, M.; SILVERMAN, J.; BELL, W. 1979. Agonistic Behavior, Social Interactions, and Behavioral Specialization in a Primitively Eusocial Bee. Insectes Sociaux 25: 351-364.
BREED, M. D. FEWELL, J. H.; WILLIAMS, K. R. 1988. Comb wax mediates the acquisition of nestmate recognition cues in honeybees. Proceedings of the National. Academy of Sciences U.S.A. 85: 8766-8769.
BROTHERS, D. J.; MICHENER, C. D. 1974. Interactions in colonies of primitively social bees. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 90 (2): 129-168.
BUCKLE, G. R. 1982. Queen-Worker Behavior and Nesmate Interactions in Young Colonies of Lasioglossum zephyrum. Insectes Sociaux 29: 125-137.
CHIAPPA, E.; RUZ, L.; GARCÍA, V. 2005. Biología de machos de Protandrena evansi Ruz y Chiappa (Hymenoptera: Andrenidae) (Farellones, Región Metropolitana, Chile). Acta Entomológica Chilena 29: 15-22.
CHIAPPA, E.; CASTRO, R. 2006. Comportamiento de nidificación comunal y de abastecimiento de Protandena evansi Ruz y Chiappa (Hymenoptera: Andrenidae: Panurginae) en Farellones, Región Metropolitana, Chile. Acta Entomológica Chilena 31: 7-14.
CROZIER, R. H.; PAMILO, P. 1996. Evolution of social insect colonies. Oxford University Press. 306 p.
CUSTER, C. P. 1928. The bee that works in stone: Perdita opuntiae Cockerell. Psyche 35: 67-83.
DANFORTH, B. N. 1991. Female foraging and intranest behavior of a communal bee, Perdita portalis (Hymenoptera: Andrenidae). Annals of the Entomological Society of America 84: 537-548.
FIELD, J. 1992. Intraespecific parasitism as an alternative reproductive tactic in nest-building wasp and bees. Biological Reviews 67: 79-126.
FLORES-PRADO, L.; CHIAPPA, E.; NIEMEYER, H. M. 2008a.
Nesting biology, life cycle, and interactions between females of Manuelia postica, a solitary species of the Xylocopinae (Hymenoptera: Apidae). New Zealand Journal of Zoology 35: 93-102.
FLORES-PRADO, L.; AGUILERA, D.; NIEMEYER, H. M. 2008b. Nest-mate recognition in Manuelia postica (Apidae: Xylocopinae): an eusocial trait is present in a solitary bee. Proceedings of the Royal Society, B. 275: 285-291.
FLORES-PRADO, L.; NIEMEYER, H. M. 2010. Kin Recognition in the largely solitary bee, Manuelia postica (Apidae: Xylocopinae). Ethology 116: 466-471.
GETZ, W. M. 1991. The honeybee as model kin recognition system. pp. 358-412. In: Hepper, G. P. (Ed.). King recognition. Cambridge University Press. Cambridge. 457 p.
GRIXTI, J., ZAYED, A.; PACKER, L. 2004. Behavorial interactions among females of Acamptopoeum submetallicum (Spinola) and Nolanomelissa toroi Rozen (Hymemoptera: Andrenidae). Journal of Hymenoptera Research 13: 48-56.
HOFFMANN, A.; ARROYO, M.; LIBERONA, F.; MUÑOZ, M.; WATSON, J. 1998. Plantas altoandinas en la flora silvestre de Chile. Ediciones Fundación Claudio Gay, Santiago de Chile. 281 p.
HOGENDOORN, K.; LEYS, R. 1993. The superseded female’s dilemma: factors that influence guarding behaviour of the carpenter bee Xylocopa pubescens. Behavioral Ecology and Sociobiology 33: 371-381.
HÖLLDOBLER, B.; MICHENER, C. 1980. Mechanisms of identification and discrimination in social Hymenoptera. pp. 35-58. In: Markl, H. (Ed.). Evolution of social behavior: Hypotheses and empirical tests. Weinheim: Verlag Chemie.
HÖLLDOBLER, B.; WILSON, E. O. 1990. The Ants. Harvard University Press, Cambridge. 548 p.
HOWARD, R. W.; BLOMQUIST, G.J. 1982. Chemical ecology and biochemistry of insect hydrocarbons. Annual Review of Entomology 27: 149-172.
HOWARD, R. W.; BLOMQUIST, G.J. 2005. Ecological, behavioural and biochemical aspects of insect hydrocarbons. Annual Review of Entomology 50: 371-393.
INOUE, T.; ROUBIK, D. W.; SUKA, T. 1999. Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini). Insectes Sociaux 46: 208-218.
JAISSON, P. 1991. Kinship and fellowship in ants and social wasps, pp. 61-93. In: Hepper, G. P. (Ed.). King recognition. Cambridge University Press. Cambridge. 457 p.
KELLER, L. 1997. Indiscriminate altruism: unduly nice parents and siblings. Trends in Ecology and Evolution 12: 99-103.
KUKUK, P. 1980. Diurnal Activity of a Primitively Eusocial Bee, Lasioglossum zephyrum, within the Nest. Journal of the Kansas Entomological Society 53 (1): 149-156.
KUKUK, P. 1992. Social interactions and familiarity in a communal Halictine bee Lasioglossum (Chilalictus) hemichalceum. Ethology 91: 291: 300.
McCONNELL-GARNER J.; KUKUK, P. F. 1997. Behavioral Interactions of two solitary Halictine bees with comparisons among solitary, communal and eusocial species. Ethology 103: 19-32.
MASON, C. A. 1988. Division of labor and adult interactions in eusocial colonies of two allodapines bee species (Hymenoptera: Anthophoridae). Journal of the Kansas Entomological Society 61: 477-491.
MICHENER, C. D. 1963. Observations on bionomics of a colonial bee of the genus Perdita (Hymenoptera: Apoidea: Panurginae). Journal of the Kansas Entomological Society 36: 114-118.
MICHENER, C. D. 1969. Comparative social behavior of bees. Annual Review of Entomology 14: 299-342.
MICHENER, C. D. 1974. The social behavior of the bees. A comparative study. Harvard Univ. Press. Cambridge, M.A. 404 p.
MICHENER, C. D. 2007. The Bees of the world. Johns Hopkins University Press, Baltimore, Maryland. 953 p.
MUNSTER-SWENDSEN, M. 1968. On the biology of the solitary bee Panurgus bankasianus Kirby (Hymenoptera: Apidae), including some ecological aspects. Arsskrift Kongelige Veterinaer Og Landbohojskole 51: 215-241.
PABALAN, N.; DAVEY, G.; PACKER, L. 2000. Escalation of Aggressive Interactions During Staged Encounters in Halictus ligatus Say (Hymenoptera: Halictidae), with a Comparison of Circle Tube Behaviors with Others Halictine Species. Journal of Insect Behavior 13: 627-650.
PACKER. L. 1986. Multiple-foundress associations in a temperate population of Halictus ligatus (Hymenoptera; Halictidae). Canadian Journal of Zoology 64: 2325-2332.
PACKER, L. 2000. The Biology of Trincohalictus prognathus (Perez) (Hymenoptera: Halictidae: Halictini). Journal of Hymenoptera Research 9: 53-61.
PAXTON, R. J.; THORÉN, P. A.; TENGÖ, J.; ESTOUP, A.; PAMILIO, P. 1996. Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera: Andrenidae), using microsatellites. Molecular Ecology 5: 511-519.
PAXTON, R. J.; KUKUK, P. F.; TENGÖ, J. 1999. Effects of familiarity and nestmate number on social interactions in two communal bees, Andrena scotica and Panurgus calcaratus (Hymenoptera, Andrenidae). Insectes Sociaux 46: 109-118.
PEREIRA-MARTINS, S. R. 1991. Biología de Eulema nigrita. Atividades nidais. Papéis Avulsos de Zoología 37: 237-243.
PUSEY, A. E.; WOLF, M. 1996. Inbreeding avoidance in animals.Trends in Ecology and Evolution 11: 201-206.
ROZEN, J. 1966. Systematics of the larvae of North American panurgine bees (Hymenoptera: Apoidea). American Museum Novitates 2259: 1-22.
ROZEN, J. G. 1989. Life history studies of the “primitive” panurgine bees (Hymenoptera: Andrenidae: Panurginae). American Museum Novitates 2692: 1-27.
RUZ, L.; ROZEN, J., JR. 1993. South American Panurginae bees (Apoidea: Andrenidae: Panurginae), part I. Biology, mature larva, and description of a new genus and species. American Museum Novitates 3057: 1-12.
SIEGEL, S.; CASTELLAN, JR. N.J. 1988. Nonparametric statistics for the behavioral sciences, 2ª Ed. McGraw-Hill International Editions. 399 p.
SINGER, T. L. 1998. Roles of hydrocarbons in the recognition systems of insects. American Zoologist 38: 394-405.
SMITH, B.; WELLER, C. 1989. Social competition among gynes in Halictine bees: The influence of bee size and pheromones on behavior. Journal of Insect Behavior 2: 397-411.
SMITH, B. H.; BREED M. D. 1995. The Chemical Basis for Nestmate Recognition and Mate Discrimination in Social Insect, pp. 387-317. In: Carde, R. T.; Bell, W. J. (Eds.). Chemical Ecology of Insects 2, Chapman y Hall, New York. 433 p.
SOKAL, R. R.; ROHLF, F. J. 1995. Biometry. The principles and practice of statistics in biological research. 3ª Ed. W.H. Freeman and company, New York. 887 p.
TENGÖ, J. J.; ERICKSON, A. K.; BORG-KARLSON, B. H.; SMITH H. D. 1988. Mate-locating strategies and multimodal communication in male mating behavior of Panurgus bankasianus and P. calcaratus (Apoidea, Andrenidae). Journal of the Kansas Entomological Society 61: 388-395.
WCISLO, W.; DANFORTH, B. 1997. Secondarily solitary: the evolutionary loss of social behavior. Trends in Ecology and Evolution 12: 468-474.
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