Skip to main content
SpringerLink
Log in

Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): single-visit effectiveness, overnight sheltering and responses to flower colour

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Solitary bees often form specialised mutualisms with particular plant species, while honeybees are considered to be relatively opportunistic foragers. Thus, it may be expected that solitary bees are more effective pollinators than honeybees when foraging on the same floral resource. To test this, we studied two Wahlenbergia species (Campanulaceae) in South Africa that are visited by both social honeybees and solitary bees, and which are shown here to be genetically self-incompatible and thus reliant on pollinator visits for seed production. Contrary to expectation, the solitary bee Lipotriches sp. (Halictidae) and social bee Apis mellifera (Apidae), which were the two most frequent visitors to flowers of the study species, were equally effective pollinators in terms of the consequences of single visits for fruit and seed set. Both bee species preferentially visited female phase flowers, which contain more nectar than male phase flowers. Male solitary bees of several genera frequently shelter overnight in flowers of both Wahlenbergia species, but temporal exclusion experiments showed that this behaviour makes little contribution to either seed production or pollen dispersal (estimated using a dye particle analogue). Manipulation of flower colour using a sunscreen that removed UV reflectance strongly reduced visits by both bee groups, while neither group responded to Wahlenbergia floral odour cues in choice tests. This study indicates that while flowers of Wahlenbergia cuspidata and W. krebsii are pollinated exclusively by bees, they are not under strong selection to specialise for pollination by any particular group of bees.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aigner PA (2001) Optimality modeling and fitness trade-offs: when should plants become pollinator specialists? Oikos 95:177–184

    Article  Google Scholar 

  • Alves-dos-Santos I, Gaglianone MC, Naxara SRC, Engels MS (2009) Male sleeping aggregations of solitary oil-collecting bees in Brazil (Centridini, Tapinotaspidini, and Tetrapediini; Hymenoptera: Apidae). Gene Mol Res 8:515–524

    Article  CAS  Google Scholar 

  • Anderson GJ, Bernardello G, Stuessy TF, Crawford DJ (2001) Breeding system and pollination of selected plants endemic to Juan Fernandez Islands. Am J Bot 88:220–233

    Article  PubMed  CAS  Google Scholar 

  • Andersson S, Amundsen T (1997) Ultraviolet colour vision and ornamentation in bluethroats. Proc R Soc Lond B 264:1587–1591

    Article  Google Scholar 

  • Arnold SEJ, Savolainen V, Chittka L (2009) Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod Plant Interact 3:27–43

    Article  Google Scholar 

  • Beattie AJ (1971) A technique for the study of insect-borne pollen. Pan Pac Entomol 47:82

    Google Scholar 

  • Bell G (1985) On the function of flowers. Proc R Soc of Lond B Biol Sci 224:223–265

    Article  Google Scholar 

  • Bernardello G, Anderson GJ, Stuessy TF, Crawford DJ (2001) A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernandez Islands (Chile). Bot Rev 67:255–308

    Article  Google Scholar 

  • Bogdan AV (1962) Grass pollination by bees in Kenya. Proc Linn Soc Lond 173:57–60

    Article  Google Scholar 

  • Butz Huryn VM (1997) Ecological impacts of introduced honey bees. Q Rev Biol 72:275–297

    Article  Google Scholar 

  • Carthew SM (1993) An assessment of pollinator visitation to Banksia spinulosa. Aust J Ecol 18:257–268

    Article  Google Scholar 

  • Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A (Sens Neural Behav Physio) 170:533–543

    Google Scholar 

  • Chittka L, Kevan PG (2005) Flower colour as advertisement. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest Ltd, Cambridge, pp 157–196

    Google Scholar 

  • Chittka L, Wells H (2004) Color vision in bees: mechanisms, ecology, and evolution. In: Prete FR (ed) Complex worlds from simpler nervous systems. The MIT Press, Massachusetts, pp 165–191

    Google Scholar 

  • Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377

    Article  CAS  Google Scholar 

  • Dafni A, Ivri Y, Brantjes NBM (1981) Pollination of Serapias vomeracea Briq. (Orchidaceae) by imitation of holes for sleeping solitary male bees (Hymenoptera). Acta Bot Neerl 30:69–73

    Google Scholar 

  • Dyer AG, Chittka L (2004) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:759–763

    Article  PubMed  Google Scholar 

  • Free JB (1963) The flower constancy of honeybees. J Anim Ecol 32:119–131

    Article  Google Scholar 

  • Freitas BM, Paxton RJ (1998) A comparison of two pollinators: the introduced honey bee Apis mellifera and an indigenous bee Centris tarsata on Cashew Anacardium occidentale in its native range of NE Brazil. J Appl Ecol 35:109–121

    Article  Google Scholar 

  • Gess SK (1999) South African Bluebells. Wasps and bees, stars and bells: an intricate pollination study of Wahlenbergia. Veld Flora 85:80–81

    Google Scholar 

  • Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91:228–231

    Article  PubMed  CAS  Google Scholar 

  • Goulson D (2003) Effects of introduced bees on native ecosystems. Ann Rev Ecol Evol Syst 34:1–26

    Article  Google Scholar 

  • Grant V (1950) The flower constancy of bees. Bot Rev 16:379–398

    Article  Google Scholar 

  • Gumbert A, Kunze J (2001) Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi. Biol J Linn Soc 72:419–433

    Article  Google Scholar 

  • Hargreaves AL, Harder LD, Johnson SD (2010) Native pollen thieves reduce the reproductive success of a hermaphroditic plant, Aloe maculate. Ecology 91:1693–1703

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hood GM (2008) PopTools version 3.0.6. Available on the internet. URL:http://www.csl.csiro.au/poptools

  • Howell AD, Alarcon R (2007) Osmia bees (Hymenoptera: Megachilidae) can detect nectar-rewarding flowers using olfactory cues. Anim Behav 74:199–205

    Article  Google Scholar 

  • Immelman K, Eardley CD (2000) Gathering of grass pollen by solitary bees (Halictidae, Lipotriches) in South Africa. Mitt Mus Nat.kd Berl Zool Reihe 76:263–268

    Google Scholar 

  • Johnson SD (2000) Batesian mimicry in the non-rewarding orchid Disa pulchra, and its consequences of pollinator behaviour. Biol J Linn Soc 71:119–132

    Google Scholar 

  • Johnson SD, Hargreaves AL, Brown M (2006) Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87:2709–2716

    Article  PubMed  Google Scholar 

  • Kevan PG (1972) Insect pollination of high arctic flowers. J Ecol 60:831–847

    Article  Google Scholar 

  • Klein A-M, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Pro Roy Soc Lon B 270:955–961

    Article  Google Scholar 

  • Larsson M (2005) Higher pollinator effectiveness by specialist than generalist flower-visitors of unspecialized Knauita arvensis (Dipsacaceae). Oecologia 146:394–403

    Article  PubMed  Google Scholar 

  • Lau JA, Galloway LF (2004) Effects of low-efficiency pollinators on plant fitness and floral trait evolution in Campanula americana (Campanulaceae). Oecologia 141:577–583

    Article  PubMed  Google Scholar 

  • Le Corff J, Agren J, Schemske DW (1998) Floral display, pollination discrimination and female reproductive success in two monoecious Begonia species. Ecology 79:1610–1619

    Article  Google Scholar 

  • Linsley EG (1958) The ecology of solitary bees. Hilgardia 27:543–599

    Google Scholar 

  • Lloyd DG, Yates JMA (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36:903–913

    Article  Google Scholar 

  • Loper GM, Berdel RL (1980) The effects of nine pollen diets on brood rearing of honeybees. Apidologie 11:351–359

    Article  Google Scholar 

  • Michener CD (1965) A classification of the bees of the Australian and South Pacific regions. Bull Am Mus Nat Hist 130:1–324

    Google Scholar 

  • Michener CD (2000) The bees of the world. John Hopkins University Press, Baltimore

    Google Scholar 

  • Moritz RFA, Southwick EE (1992) Bees as superorganisms: an evolutionary reality. Springer, Berlin

    Book  Google Scholar 

  • Müller A (1996) Host-plant specialization in western palearctic anthidiine bees (Hymenoptera: Apoidea: Megachilidae). Ecol Monogr 66:235–257

    Article  Google Scholar 

  • Olsen KM (1997) Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109:114–121

    Google Scholar 

  • Pellmyr O (2002) Pollination by animals. In: Herrara CM, Pellmyr O (eds) Plant-animal interactions: an evolutionary approach. Blackwell, Oxford, pp 157–184

    Google Scholar 

  • Peter CI, Johnson SD (2008) Mimics and magnets: the importance of colour and ecological facilitation in floral deception. Ecology 89:1583–1595

    Article  PubMed  Google Scholar 

  • Petterson JA (1997) Revision of the genus Wahlenbergia (Campanulaceae) in New Zealand. New Zeal J Bot 35:9–54

    Article  Google Scholar 

  • Pimentel De Carvalho A, Message D (2004) A scientific note on the toxic pollen of Stryphnodendron polyphyllum (Fabaceae, Mimosoideae) which causes sacbrood-like symptoms. Apidologie 35:89–90

    Article  Google Scholar 

  • Rader R, Howlett BG, Cunninghams SA, Westcott DA, Newstrom-Lloyd LE, Walker MK, Teulon DAJ, Edwards W (2009) Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J Appl Ecol 46:1080–1087

    Article  Google Scholar 

  • Raine NE, Ings TC, Dornhaus A, Saleh N, Chittka L (2006) Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Adv Stud Behav 36:305–354

    Article  Google Scholar 

  • Ribbands CR (1953) The behaviour and social life of honeybees. Bee Research Associates, London

    Google Scholar 

  • Sapir Y, Shmida A, Ne’eman G (2005) Pollination of Oncocylus irises (Iris: Iridaceae) by night-sheltering male bees. Plant Biol 7:417–424

    Article  PubMed  CAS  Google Scholar 

  • Schlindwein C, Wittman D, Martins CF, Hamm A, Siqueira JA, Schiffler D, Machado IC (2005) Pollination of Campanula rapunculus L. (Campanulaceae): how much pollen flows into pollination and into reproduction of oligolectic pollinators? Plant Syst Evol 250:147–156

    Article  Google Scholar 

  • Scopece G, Cozzolino S, Johnson SD, Schiestl FP (2010) Pollination efficiency and the evolution of specialized deceptive pollination systems. Am Nat 175:98–105

    Article  PubMed  Google Scholar 

  • Sedivy C, Müller A, Dorn S (2001) Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digist pollen. Funct Ecol 25:718–725

    Article  Google Scholar 

  • Seeley TD (1985) Honeybee ecology: a study of adaptation in social life. Princeton University Press, Princeton

    Google Scholar 

  • Seeley TD (1989) The honey bee colony as a superorganism. Am Sci 77:546–553

    Google Scholar 

  • Shuttleworth A, Johnson SD (2009) The importance of scent and nectar filters in a specialized wasp-pollination system. Funct Ecol 23:931–940

    Article  Google Scholar 

  • Simpson BB, Neff JL (1981) Floral rewards: alternatives to pollen and nectar. Ann Mo Bot Gard 68:301–322

    Article  Google Scholar 

  • Snodgrass RE (1956) Anatomy of the honey bee. Cornell University Press, New York

    Google Scholar 

  • Soderstrom TR, Calderon CE (1971) Insect pollination in tropical rain forests. Biotropica 3:1–16

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1994) Biometry: the principles and practices of statistics in biological research, 3rd edn. W.H. Freeman, New York

    Google Scholar 

  • Spears EE Jr (1983) A direct measure of pollinator effectiveness. Oecologia 57:196–199

    Article  Google Scholar 

  • Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst 1:307–326

    Article  Google Scholar 

  • Steiner KE, Whitehead VB (1988) The association between oil-producing flowers and oil-collecting bees in the Drakensberg of southern Africa. Monogr Syst Bot Mo Bot Gard 25:259–277

    Google Scholar 

  • Strickler K (1979) Specialization and foraging efficiency of solitary bees. Ecology 60:998–1009

    Article  Google Scholar 

  • Thomson JD, Goodell K (2001) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. J Appl Ecol 38:1032–1044

    Article  Google Scholar 

  • von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge

    Google Scholar 

  • Waser NM (1983) The adaptive nature of floral traits: ideas and evidence. In: Real LK (ed) Pollination biology. Academic Press, Orlando, pp 242–286

    Google Scholar 

  • Waser NM (1986) Flower constancy: definition, cause, and measurement. Am Nat 127:593–603

    Article  Google Scholar 

  • Weatherwax PB (1986) Why do honeybees reject certain flowers? Oecologia 69:567–570

    Article  Google Scholar 

  • Wells H, Wells PH (1983) Honey bee foraging ecology: optimal diet, minimal uncertainty or individual constancy? J Anim Ecol 52:829–836

    Article  Google Scholar 

  • Westerkamp C (1991) Honeybees are poor pollinators—why? Plant Syst Evol 177:71–75

    Article  Google Scholar 

  • Williams NM (2003) Use of novel pollen species by specialists and generalist solitary bees (Hymenoptera: Megachilidae). Oecologia 134:228–237

    PubMed  Google Scholar 

  • Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507

    Article  Google Scholar 

  • Winston L (1991) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

  • Wright GA, Schiestl FP (2009) Floral scent in a whole-plant context. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851

    Article  Google Scholar 

Download references

Acknowledgments

Many thanks to C. Eardley, ARC-plant protection research institute for identifying the bees to species. For their valuable assistance in this study, Dr. A. Juergens, S-L. Steenhuisen, A. Shutterworth, J. Rodger and M. Mgobozi are thanked. Ezumvelo KZN Wildlife, in particular Dr. I. Rushworth, the Pierce family and Mondi-Shanduka are thanked for permission to work at Midmar Reserve, Midmar farmlands and Gilboa Estate, respectively. Lars Chittka and three anonymous reviewers are thanked for their comments and suggestions. R. Welsford is thanked for his company and support during field work at Gilboa Estate. This study was supported by the National Research Foundation of South Africa.

Author information

Authors and Affiliations

  1. Faculty of Science and Agriculture, School of Biological and Conservation Sciences, University of KwaZulu-Natal, Pietermaritzburg Campus, Private Bag X01, Scottsville, 3209, South Africa

    Megan R. Welsford & Steven D. Johnson

Authors
  1. Megan R. Welsford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven D. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Megan R. Welsford.

Additional information

Handling Editor: Lars Chittka.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 472 kb)

Appendix

Appendix

See Table 3.

Table 3 The observed versus expected number of visits by bees to male and female phase flowers in patches of W. cuspidata and W. krebsii
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Welsford, M.R., Johnson, S.D. Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): single-visit effectiveness, overnight sheltering and responses to flower colour. Arthropod-Plant Interactions 6, 1–14 (2012). https://doi.org/10.1007/s11829-011-9149-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-011-9149-0

Keywords

Search

Navigation