Skip to main content
SpringerLink
Log in

Recognition of scent marks in solitary bees to avoid previously visited flowers

  • Original Article
  • Published:
Ecological Research

Abstract

Knowing how floral visitors forage efficiently among flowers is important to understanding plant-pollinator interactions. When bees search for rewarding flowers, they use several visual cues to detect the available floral resources. In addition to these cues, bees can recognize scent marks, which are olfactory cues left on flowers foraged by previous visitors. This behavior is well known in social bees, such as honeybees and bumblebees. Although solitary bees do not need to give information about which flowers were foraged to conspecifics, several pieces of evidence have indicated the use of scent marks. However, it is unknown whether the behavior is widely used in many different bee species. We investigated whether four different solitary bees, Colletes patellatus (Colletidae), Andrena prostomias (Andrenidae), Osmia orientalis (Megachilidae), and Tetralonia mitsukurii (Apidae), can recognize flowers that have been foraged previously by visitors within 3 min. All four bees showed rejection responses to flowers foraged by conspecifics. However, our results showed that responses to foraged flowers varied among bee species. The tendency of A. prostomias and T. mitsukurii to reject the foraged flowers was pronounced, while in C. patellatus and O. orientalis it was weak. In both A. prostomias and T. mitsukurii, the rejection rate of flowers foraged by conspecifics decreased as the time lag after the last visit increased. Both bees visited the flowers from which pollen or nectar had been artificially removed. We suggest that A. prostomias and T. mitsukurii would recognize scent marks left by previous visitors, while the other two bees would not recognize them so strongly. It is likely that the decision to use scent marks is dependent either on the richness of resources or on the complexity of floral structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilar I, Sommeijer M (2001) The deposition of anal excretions by Melipona favosa foragers (Apidae: Meliponinae): behavioural observations concerning the location of food sources. Apidologie (Celle) 32:37–48. doi:10.1051/apido:2001109

    Article  Google Scholar 

  • Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). J Comp Physiol [A] 194:313–327. doi:10.1007/s00359-008-0321-7

    Article  Google Scholar 

  • Cameron SA (1981) Chemical signals in bumblebee foraging. Behav Ecol Sociobiol 9:257–260. doi:10.1007/BF00299880

    Article  Google Scholar 

  • Corbet SA, Kerslake CJ, Brown C, Morland NE (1984) Can bees select nectar-rich flowers in a patch? J Apic Res 23:234–242

    Google Scholar 

  • Dobson HEM, Bergström G (2000) The ecology and evolution of pollen odors. In: Dafni A, Hesse M, Pacini E (eds) Pollen and Pollination. Springer, Vienna, pp 63–88

    Google Scholar 

  • Eltz T (2006) Tracing pollinator footprints on natural flowers. J Chem Ecol 32:907–915. doi:10.1007/s10886-006-9055-6

    Article  PubMed  CAS  Google Scholar 

  • Frankie GW, Vinson SB (1977) Scent marking of passion flowers in Texas by females of Xylocopa virginica texana (Hymenoptera: Anthophoridae). J Kans Entomol Soc 50:613–625

    Google Scholar 

  • Free JB, Williams IH (1979) Communication by pheromones and other means in Apis florae colonies. J Apic Res 18:16–25

    Google Scholar 

  • Free JB, Williams IH (1983) Scent-marking of flowers by honeybees. J Apic Res 22:86–90

    Google Scholar 

  • Galen C, Kevan PG (1983) Bumblebee foraging and floral scent dimorphism: Bombus kirbyellus Curtis (Hymenoptera: Apidae) and Polemonium viscosum Nutt. (Polemoniaceae). Can J Zool 61:1207–1391

    Article  Google Scholar 

  • Gawleta N, Zimmermann Y, Eltz T (2005) Repellent foraging recognition across bee families. Apidologie (Celle) 36:325–330. doi:10.1051/apido:2005018

    Article  Google Scholar 

  • Gilbert F, Azmeh S, Barnard C, Behnke J, Collins SA, Hurst J et al (2001) Individually recognizable scent marks on flowers made by a solitary bee. Anim Behav 61:217–229. doi:10.1006/anbe.2000.1542

    Article  PubMed  Google Scholar 

  • Giurfa M (1993) The repellent scent-mark of the honeybee Apis mellifera ligustica and its role as a communication cue during foraging. Insectes Soc 40:59–67. doi:10.1007/BF01338832

    Article  Google Scholar 

  • Giurfa M, Núñez JA (1992) Honeybees mark with scent and reject recently visited flowers. Oecologia 89:113–117. doi:10.1007/BF00319022

    Article  Google Scholar 

  • Giurfa M, Núñez JA (1993a) Efficient floret inspection by honeybees in capitula of Carduud acanthoides. Ecol Entomol 18:116–122. doi:10.1111/j.1365-2311.1993.tb01192.x

    Article  Google Scholar 

  • Giurfa M, Núñez JA (1993b) Visual modulation of a scent-marking activity in the honeybee, Apis mellifera L. Naturwissenschaften 80:376–379. doi:10.1007/BF01138797

    Article  Google Scholar 

  • Giurfa NM, Núñez JA, Backhaus W (1994) Odour and colour information in the honeybee, Apis mellifera L. J Comp Physiol [A] 175:773–779. doi:10.1007/BF00191849

    Google Scholar 

  • Goulson D, Hawson SA, Stout JC (1998) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Anim Behav 55:199–206. doi:10.1006/anbe.1997.0570

    Article  PubMed  Google Scholar 

  • Goulson D, Stout JC, Langley J, Hughes WOH (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911. doi:10.1023/A:1026406330348

    Article  CAS  Google Scholar 

  • Goulson D, Chapman JW, Hughes WOH (2001) Discrimination of unrewarding flowers by bees: direct detection of rewards and use of repellent scent marks. J Insect Behav 14:669–677. doi:10.1023/A:1012231419067

    Article  Google Scholar 

  • Harder LD (1983) Flower handling efficiency of bumble bees: morphological aspects of probing time. Oecologia 57:274–280. doi:10.1007/BF00379591

    Article  Google Scholar 

  • Heinrich B (1979) Resource heterogeneity and patterns of movement in foraging bumblebees. Oecologia 40:235–245. doi:10.1007/BF00345321

    Article  Google Scholar 

  • Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth FG (2004) A stingless bee (Melipona seminigra) marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804

    Article  PubMed  CAS  Google Scholar 

  • Kadmon R, Shmida A, Selten R (1991) Within-plant foraging behavior of bees and its relationship to nectar distribution in Anchusa strigosa. Isr J Bot 40:283–294

    Google Scholar 

  • Kato M (1988) Bumblebee visits to Impatiens spp.: pattern and efficiency. Oecologia 76:364–370

    Google Scholar 

  • Laverty TM (1994) Bumble bee learning and flower morphology. Anim Behav 47:531–545. doi:10.1006/anbe.1994.1077

    Article  Google Scholar 

  • Maeta Y (2000) Tajima Gakuonji-no Utsugi-himehanabachi. Kaiyusya, Tokyo

    Google Scholar 

  • Marden JM (1984) Remote perception of floral nectar by bumblebees. Oecologia 64:232–240. doi:10.1007/BF00376876

    Article  Google Scholar 

  • Michener CD (2000) The bees of the world. Johns Hopkins, Baltimore

    Google Scholar 

  • 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, Chicago, pp 69–98

    Google Scholar 

  • Nuttman CV, Semida FM, Zalat S, Willmer PG (2006) Visual cues and foraging choices: bee visits to floral colour phases in Alkanna orientalis (Boraginaceae). Biol J Linn Soc Lond 87:427–435. doi:10.1111/j.1095-8312.2006.00582.x

    Article  Google Scholar 

  • Reader T, MacLeod I, Elliott PT, Robinson OJ, Manica A (2005) Inter-order interactions between flower-visiting insects: Foraging bees avoid flowers previously visited by hoverflies. J Insect Behav 18:51–57. doi:10.1007/s10905-005-9346-8

    Article  Google Scholar 

  • Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220. doi:10.1007/s00265-006-0252-7

    Article  Google Scholar 

  • Saleh N, Ohashi K, Thomson JT, Chittka L (2006) Facultative use of repellent scent mark in foraging bumblebees: complex vs. simple flowers. Anim Behav 71:847–854. doi:10.1016/j.anbehav.2005.06.014

    Article  Google Scholar 

  • Schmitt U, Bertsch A (1990) Do foraging bumblebees scent-mark food sources and does it matter? Oecologia 82:137–144. doi:10.1007/BF00318545

    Article  Google Scholar 

  • Schmidt VM, Zucchi R, Barth FG (2005) Scent marks left by Nannotrigona testaceicornis at the feeding site: cues rather than signals. Apidologie 36:285–291

    Article  Google Scholar 

  • Stout JC, Goulson D (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183–189. doi:10.1006/anbe.2001.1729

    Article  Google Scholar 

  • 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 52:239–246. doi:10.1007/s00265-002-0510-2

    Article  Google Scholar 

  • Stout JC, Goulson D, Allen JA (1998) Repellent scent-marking of flowers by a guild of foraging bumblebees (Bombus spp.). Behav Ecol Sociobiol 43:317–326. doi:10.1007/s002650050497

    Article  Google Scholar 

  • Thorpe RW, Briggs DL, Estes JR, Ericksin EH (1975) Nectar fluorescence under ultraviolet irradiation. Science 189:476–478. doi:10.1126/science.189.4201.476

    Article  Google Scholar 

  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. doi:10.2307/2265575

    Article  Google Scholar 

  • Weiss MR (1991) Floral colour changes as cues for pollinators. Nature 354:227–229. doi:10.1038/354227a0

    Article  Google Scholar 

  • Wetherwax PB (1986) Why do honeybees reject certain flowers? Oecologia 69:567–570. doi:10.1007/BF00410364

    Article  Google Scholar 

  • Williams CS (1998) The identity of the previous visitor influences flower rejection by nectar-collecting bees. Anim Behav 56:673–681. doi:10.1006/anbe.1998.0794

    Article  PubMed  Google Scholar 

  • Williams CS, Poppy GM (1997) Responses of individual honey bees to artificial feeders visited by themselves and to feeders visited by hivemates. J Apic Res 36:105–108

    Google Scholar 

  • Wilms J, Eltz T (2007) Foraging scent marks of bumblebees: footprint cues rather than pheromone signals. Naturwissenschaften. doi:10.1007/s00114-007-0298-z

  • Witjes S, Eltz T (2007) Influence of scent deposits on flower choice: experiments in an artificial flower array with bumblebees. Apidologie (Celle) 38:12–18. doi:10.1051/apido:2006048

    Article  Google Scholar 

  • Yokoi T, Fujisaki K (2007) Repellent scent-marking behaviour of the sweat bee Halictus (Seladonia) aerarius during flower foraging. Apidologie (Celle) 38:482–504. doi:10.1051/apido:2007034

    Article  Google Scholar 

  • Yokoi T, Goulson D, Fujisaki K (2007) The use of heterospecific scent marks by the sweat bee Halictus aerarius. Naturwissenschaften 94:1021–1024. doi:10.1007/s00114-007-0285-4

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dave Goulson, School of Biological and Environmental Science, University of Stirling, and Pablo J. Perez-Goodwyn, Laboratory of Insect Ecology, Kyoto University, for careful proofreading of the manuscript. We thank Takayoshi Nishida and members of the Laboratory of Insect Ecology, Kyoto University, for helpful comments on an early draft of the manuscript. We are also grateful to Tsuyoshi Sugimoto, Yasuyuki Sakuratani, and Ikuo Kandori, Laboratory of Entomology, Kinki University, for valuable advice and permission to use the university campus. This work was supported in part by the Twenty-First Century COE Program for Innovative Food and Environmental Studies Pioneered by Entomomimetic Sciences from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Author information

Authors and Affiliations

  1. Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Kitashirakawa, Sakyo, Kyoto, 606-8502, Japan

    Tomoyuki Yokoi & Kenji Fujisaki

Authors
  1. Tomoyuki Yokoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenji Fujisaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomoyuki Yokoi.

About this article

Cite this article

Yokoi, T., Fujisaki, K. Recognition of scent marks in solitary bees to avoid previously visited flowers. Ecol Res 24, 803–809 (2009). https://doi.org/10.1007/s11284-008-0551-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-008-0551-8

Keywords

Search

Navigation