Naturwissenschaften

, Volume 96, Issue 2, pp 195–200

Hesitation behaviour of hoverflies Sphaerophoria spp. to avoid ambush by crab spiders

Original Paper

Abstract

Pollinators possess several antipredator adaptations that minimise predation risk during foraging. In addition to morphological adaptations, hoverflies might have behavioural antipredator adaptations. We conducted three field experiments to investigate whether the “hesitation behaviour” of hoverflies Sphaerophoria spp., moving backwards and forwards in front of a flower, is effective in avoiding ambush predators on flowers. First, we compared the behaviour of different flower visitors, including several bees and other hoverflies, with Sphaerophoria spp. behaviour. Only Sphaerophoria spp. exhibited the hesitation behaviour in front of flowers. The flight behaviour was observed more frequently before landing on flowers than on leaves. Second, we investigated rejection by Sphaerophoria spp. to artificially placed corpses of the crab spider Thomisus labefactus. The rejection rate of flowers with a crab spider placed on or under it was significantly higher than that of non-treated flowers. Moreover, the presence of a spider on the flower decreased the number of hesitation displays, compared with non-treated flowers. Finally, to determine whether hesitation behaviour could be a consequence of floral assessment, we investigated hoverfly rejection of previously foraged flowers. Sphaerophoria spp. did not reject flowers that had been visited by the same individual or conspecifics within 3 min. We suggest that hesitation behaviour may be adaptive, enabling assessment of predation risk and hence avoiding ambush predators on flowers.

Keywords

Antipredator strategy Behavioural adaptation Floral assessment Predation risk Syrphidae 

References

  1. Ambrose JT (1990) Birds. In: Morse RA, Nowogrodzki R (eds) Honeybee pests, predators, and diseases. Cornell University Press, Ithaca, pp 156–176Google Scholar
  2. Asahina S, Ishihara T, Yasumatsu K (1965) Iconographia insectorum Japonicorum colore naturali edita volumen III. Hokuryu-kan, TokyoGoogle Scholar
  3. Caron DW (1990) Other insects. In: Morse RA, Nowogrodzki R (eds) Honeybee pests, predators, and diseases. Cornell University Press, Ithaca, pp 156–176Google Scholar
  4. Chittka L (2001) Camouflage of predatory crab spiders on flowers and the colour perception of bees (Aranida: Thomisidae/Hymenoptera: Apidae). Entomol Gener 25:181–187Google Scholar
  5. De Jong D (1990) Insects: Hymenoptera (ants, wasps, and bees). In: Morse RA, Nowogrodzki R (eds) Honeybee pests, predators, and diseases. Cornell University Press, Ithaca, pp 135–155Google Scholar
  6. Dukas R (1998) Evolutionary ecology of learning. In: Dukas R (ed) Cognitive ecology. University of Chicago Press, Chicago, pp 129–274Google Scholar
  7. Dukas R (2001a) Effects of perceived danger on flower choice by bees. Ecol Lett 4:327–333CrossRefGoogle Scholar
  8. Dukas R (2001b) Effects of predation risk on pollinators and plants. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, New York, pp 214–236Google Scholar
  9. Dukas R (2005) Bumble bee predators reduce pollinator density and plant fitness. Ecology 86:1401–1406CrossRefGoogle Scholar
  10. Dukas R, Morse DH (2003) Crab spiders affect flower visitation by bees. Oikos 101:157–163CrossRefGoogle Scholar
  11. Dukas R, Morse DH (2005) Crab spiders show mixed effects on flower visiting bees and no effect on plant fitness. Ecoscience 12:244–247CrossRefGoogle Scholar
  12. Evans HE, Eberhard JW (1970) The wasps. University of Michigan Press, Ann ArborGoogle Scholar
  13. Golding YC, Edmunds M (2000) Behavioural mimicry of honeybees (Apis mellifera) by droneflies (Diptera: Syrphidae: Eristalis spp.). Proc R Soc Lond B 267:903–909CrossRefGoogle Scholar
  14. Golding YC, Ennos AR, Edmunds M (2001) Similarity in flight behaviour between the honeybee Apis mellifera (Hymenoptera: Apidae) and its presumed mimic, the dronefly Eristalis tenax (Diptera: Syrphidae). J Exp Biol 204:139–145PubMedGoogle Scholar
  15. Golding YC, Edmunds M, Ennos AR (2005) Flight behaviour during foraging of the social wasp Vespula vulgaris (Hymenoptera: Vaspidae) and four mimetic hoverflies (Diptera: Syrphidae) Sericomyia silentis, Myathropa florea, Helophilus sp. and Syrphus sp. J Exp Biol 208:4523–4527PubMedCrossRefGoogle Scholar
  16. Goulson D, Wright NP (1998) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav Ecol 9:213–219CrossRefGoogle Scholar
  17. Goulson D, Chapman JW, Hughes WOH (2001) Discrimination of unrewarding flowers by different bee species; direct detection of rewards and use of repellent scent marks. J Ins Behav 14:669–678CrossRefGoogle Scholar
  18. Greco CF, Kevan PG (1995) Patch choice in the anthophilous ambush predator Phymata americana: improvement by switching hunting sites as part of the initial choice. Can J Zool 73:1912–1917CrossRefGoogle Scholar
  19. Heiling AM, Herberstein ME, Chittka L (2003) Crab-spiders manipulate flower signals. Nature 421:334PubMedCrossRefGoogle Scholar
  20. Howarth B, Clee C, Edmunds M (2000) The mimicry between British Syrphidae (Diptera) and aculeate Hymenoptera. Br J Ent Nat Hist 13:1–39Google Scholar
  21. Howarth B, Edmunds M, Gilbert F (2004) Does the abundance of hoverfly (Syrphidae) mimics depend on the numbers of their hymenopteran models? Evolution 58:367–375PubMedGoogle Scholar
  22. Lunau K, Hofmann N, Valentin S (2005) Response of the hoverfly species Eristalis tenax towards floral dot guides with colour transition from red to yellow. Entomol Gener 27:249–256Google Scholar
  23. Minckley RL, Roulston TH (2006) Incidental mutualisms and pollen specialization among bees. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions from specialization to generalization. University of Chicago Press, Chicago, pp 69–98Google Scholar
  24. Miyashita K (1999) Life history of Thomisus labefactus Karsch (Araneae: Thomisidae). Acta Arachnol 48:143–149CrossRefGoogle Scholar
  25. Morse DH (1979) Prey capture by the crab spider Misumena calycina calycina (Araneae: Thomisidae). Oecologia 39:309–319CrossRefGoogle Scholar
  26. Morse DH (1986) Predation risk to insects foraging at flowers. Oikos 46:223–228CrossRefGoogle Scholar
  27. Pianka ER (1974) Evolutionary ecology. Harper and Row, New YorkGoogle Scholar
  28. Proctor M, Yao P, Lack A (1996) The natural history of pollination. Timber, PortlandGoogle Scholar
  29. Reader T, Higginson AD, Barnard CJ, Gilbert FS (2006) The effects of predation risk from crab spiders on bee foraging behavior. Behav Ecol 17:933–939CrossRefGoogle Scholar
  30. Robertson IC, Maguire DK (2005) Crab spiders deter insect visitations to slickspot peppergrass flowers. Oikos 109:577–582CrossRefGoogle Scholar
  31. Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220CrossRefGoogle Scholar
  32. Saleh N, Ohashi K, Thomson JT, Chittka L (2006) Facultative use of repellent scent mark in foraging bumblebees: complex vs. simple flowers. Anim Behav 71:847–854CrossRefGoogle Scholar
  33. Stout JC, Goulson D (2002) The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behav Ecol Sociobiol 52:239–246CrossRefGoogle Scholar
  34. Sutherland JP, Sullivan MS, Poppy GM (1999) The influence of floral character on the foraging behaviour of the hoverfly, Episyrphus balteatus. Entomol Exp Appl 93:157–164CrossRefGoogle Scholar
  35. Théry M, Casas J (2002) Predator and prey views of spider camouflage. Nature 415:133PubMedCrossRefGoogle Scholar
  36. Yokoi T, Goulson D, Fujisaki K (2007) The use of heterospecific scent marks by the sweat bee Halictus aerarius. Naturwissenschaften 94:1021–1024PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Laboratory of Insect Ecology, Graduate School of AgricultureKyoto UniversityKyotoJapan

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