Arthropod-Plant Interactions

, Volume 10, Issue 1, pp 1–8 | Cite as

Shakers and head bangers: differences in sonication behavior between Australian Amegilla murrayensis (blue-banded bees) and North American Bombus impatiens (bumblebees)

  • Callin M. SwitzerEmail author
  • Katja Hogendoorn
  • Sridhar Ravi
  • Stacey A. Combes
Original Paper


Many bees collect pollen by grasping the anthers of a flower and vibrating their flight muscles at high frequencies—a behavior termed sonication, or buzz-pollination. Here we compare buzz-pollination on Solanum lycopersicum (cherry tomatoes) by two bees that fill similar niches on different continents—in Australia, Amegilla murrayensis (blue-banded bee), and in North America, Bombus impatiens (bumblebee). We collected audio recordings of buzz-pollination and quantified the frequency and length of buzzes, as well as the total time spent per flower. We found that A. murrayensis buzzes at significantly higher frequencies (~350 Hz) than B. impatiens (~240 Hz) and flaps its wings at higher frequencies during flight. There was no difference in the length of a single buzz, but A. murrayensis spent less time on each flower, as B. impatiens buzzed the flower several times before departing, whereas A. murrayensis typically buzzed the flower only once. High-speed videos of A. murrayensis during buzz-pollination revealed that its physical interaction with the flower differs markedly from the mechanism described for Bombus and other bees previously examined. Rather than grasping the anther cone with its mandibles and shaking, A. murrayensis taps the anther cone with its head at the high buzzing frequencies generated by its flight muscles. This unique behavior, combined with its higher buzzing frequency and reduced flower visit duration, suggests that A. murrayensis may be able to extract pollen more quickly than B. impatiens, and points to the need for further studies directly comparing the pollination effectiveness of these species.


Sonication Solanum Vibration Pollination Native bees 



The authors thank Christopher De Ieso and Remko Leijs for help in collecting data in the Adelaide Botanic Garden, as well as the staff of the Adelaide Botanic Garden, notably Carolyn Sawtell and Robert Hatcher, for allowing us to conduct research with their plants. We would also like to thank Robin Hopkins for helpful suggestions on the manuscript. This project was funded by a Putnam Expedition Grant to C.S. from the Harvard Museum of Comparative Zoology and by the National Science Foundation (CAREER IOS-1253677) to S.C.

Supplementary material

11829_2015_9407_MOESM1_ESM.docx (6.6 mb)
Supplementary material 1 (DOCX 6808 kb)
11829_2015_9407_MOESM2_ESM.mp4 (88.2 mb)
Online Resource 2 High-speed video of Amegilla murrayensis collecting pollen from a Solanum lycopersicum flower, demonstrating its unique “head-butting” behavior. (MP4 90313 kb)
11829_2015_9407_MOESM3_ESM.mp4 (27.3 mb)
Online Resource 3 High-speed video of Bombus impatiens collecting pollen from a Solanum lycopersicum flower, grasping the anthers with its mandibles. (MP4 27931 kb)
11829_2015_9407_MOESM4_ESM.mp4 (36.4 mb)
Online Resource 4 High-speed video of Lipotriches flavoviridis collecting pollen from a Dianella perfragrans flower, grasping the anthers with its mandibles. (MP4 37280 kb)


  1. Anderson GJ, Symon D (1988) Insect foragers on Solanum flowers in Australia. Ann Mo Bot Gard 75:842–852CrossRefGoogle Scholar
  2. Asada S, Ono M (1996) Crop pollination by Japanese bumblebees, Bombus spp. (Hymenoptera: Apidae): tomato foraging behavior and pollination efficiency. Appl Entomol Zool 31(4):581–586Google Scholar
  3. Bell M, Spooner-Hart R, Haigh A (2006) Pollination of greenhouse tomatoes by the Australian blue banded bee Amegilla (Zonamegilla) holmesi (Hymenoptera: Apidae). J Econ Entomol 99(2):437–442CrossRefPubMedGoogle Scholar
  4. Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. van Nostrand Reinhold Company Inc, New York, pp 73–113Google Scholar
  5. Buchmann SL, Hurley JP (1978) A biophysical model for buzz pollination in angiosperms. J Theor Biol 72(4):639–657CrossRefPubMedGoogle Scholar
  6. Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington, DCGoogle Scholar
  7. Burkart A, Lunau K, Schlindwein C (2011) Comparative bioacoustical studies on flight and buzzing of neotropical bees. J Pollinat Ecol 6(16):118–124Google Scholar
  8. Cane JH, Buchmann SL (1989) Novel pollen-harvesting behavior by the bee Protandrena mexicanorum (Hymenoptera: Andrenidae). J Insect Behav 2(3):431–436CrossRefGoogle Scholar
  9. Corbet SA, Huang SQ (2014) Buzz pollination in eight bumblebee-pollinated Pedicularis species: Does it involve vibration-induced triboelectric charging of pollen grains? Ann Bot 114(8):1665–1674PubMedCentralCrossRefPubMedGoogle Scholar
  10. Core Team R (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  11. De Luca PA, Vallejo-Marín M (2013) What’s the ‘buzz’about? The ecology and evolutionary significance of buzz-pollination. Curr Opin Plant Biol 16(4):429–435CrossRefPubMedGoogle Scholar
  12. De Luca PA, Bussiere LF, Souto-Vilaros D, Goulson D, Mason AC, Vallejo-Marín M (2013) Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers. Oecologia 172(3):805–816CrossRefPubMedGoogle Scholar
  13. Gegear RJ, Laverty TM (2001) The effect of variation among floral traits on the flower constancy of pollinators. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Animal behaviour and floral evolution. Cambridge University Press, Cambridge, pp 1–20CrossRefGoogle Scholar
  14. Harder LD (1990) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110–1125CrossRefGoogle Scholar
  15. Harder L, Barclay R (1994) The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon. Funct Ecol 8:509–517CrossRefGoogle Scholar
  16. Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133:323–344CrossRefGoogle Scholar
  17. Hogendoorn K, Steen Z, Schwarz MP (2000) Native Australian carpenter bees as a potential alternative to introducing bumble bees for tomato pollination in greenhouses. J Apic Res 39:67–74Google Scholar
  18. Hogendoorn K, Gross CL, Sedgley M, Keller MA (2006) Increased tomato yield through pollination by native Australian Amegilla chlorocyanea (Hymenoptera: Anthophoridae). J Econ Entomol 99(3):828–833CrossRefPubMedGoogle Scholar
  19. Javorek S, Mackenzie K, Vander Kloet S (2002) Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium). Ann Entomol Soc Am 95(3):345–351CrossRefGoogle Scholar
  20. Jesson LK, Barrett SC (2005) Experimental tests of the function of mirror-image flowers. Biol J Linn Soc 85(2):167–179CrossRefGoogle Scholar
  21. Josephson RK, Malamud JG, Stokes DR (2000) Asynchronous muscle: a primer. J Exp Biol 203(18):2713–2722PubMedGoogle Scholar
  22. King MJ (1993) Buzz foraging mechanism of bumble bees. J Apic Res 32:41–49Google Scholar
  23. King MJ, Buchmann SL (1996) Sonication dispensing of pollen from Solanum laciniatum flowers. Funct Ecol 10:449–456CrossRefGoogle Scholar
  24. King MJ, Buchmann SL (2003) Floral sonication by bees: mesosomal vibration by Bombus and Xylocopa, but not Apis (Hymenoptera: Apidae), ejects pollen from poricidal anthers. J Kans Entomol Soc 76:295–305Google Scholar
  25. King MJ, Buchmann SL, Spangler H (1996) Activity of asynchronous flight muscle from two bee families during sonication (buzzing). J Exp Biol 199(10):2317–2321PubMedGoogle Scholar
  26. MacKenzie K (1994) The foraging behavior of honey bees (Apis mellifera L) and bumble bees (Bombus spp) on cranberry (Vaccinium macrocarpon Ait). Apidologie 25:375–383CrossRefGoogle Scholar
  27. Michener CD (2000) The bees of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  28. Michener CD, Winston ML, Jander R (1978) Pollen manipulation and selected activities and structures in the family Apidae. Univ Kans Sci Bull 51:575–601CrossRefGoogle Scholar
  29. Morandin L, Laverty T, Kevan P (2001) Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses. J Econ Entomol 94(2):462–467CrossRefPubMedGoogle Scholar
  30. Neff JL, Simpson BB (1988) Vibratile pollen-harvesting by Megachile mendica Cresson (Hymenoptera, Megachilidae). J Kans Entomol Soc 61:242–244Google Scholar
  31. Roberts J, Cartar RV (2015) Shape of wing wear fails to affect load lifting in bumble bees with experimental wing wear. Can J Zool 93(7):531–537CrossRefGoogle Scholar
  32. Signal Developers (2013) Signal: signal processing. Accessed Oct 2015
  33. Sueur J, Aubin T, Simonis C (2008) Equipment review: seewave, a free modular tool for sound analysis and synthesis. Bioacoustics 18(2):213–226CrossRefGoogle Scholar
  34. Thorp RW, Estes JR (1975) Intrafloral behavior of bees on flowers of Cassia fasciculata. J Kans Entomol Soc 48:175–184Google Scholar
  35. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  36. Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507CrossRefGoogle Scholar
  37. Zimmerman M (1982) Optimal foraging: random movement by pollen collecting bumblebees. Oecologia 53(3):394–398CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.School of Agriculture, Food and WineThe University of AdelaideAdelaideAustralia
  3. 3.School of Aerospace, Mechanical, and Manufacturing EngineeringRMIT UniversityMelbourneAustralia
  4. 4.Department of Neurobiology, Physiology, and BehaviorUniversity of California, DavisDavisUSA

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