Abstract
Differences in the pollinator performance of flower visitor sexes are rarely considered. In bumble bees, males differ from workers in morphology and behaviour in ways that may affect their contribution to pollination. We compared the abundance, foraging behaviour, and pollen transfer ability of worker and male bumble bees on late-blooming Gentiana parryi (Gentianaceae) in subalpine meadows of the Colorado Rocky Mountains. Male bees mostly outnumbered female workers throughout blooming of the gentian. Males and workers foraged similarly, though individual males were more faithful to small foraging areas than workers. During single flower visits, males and workers caused similar levels of pollen deposition and seed production, yet female bees left fewer pollen grains in anthers to be transferred to other stigmas in the plant population. Overall, male bumble bees are common and capable pollinators of G. parryi and in some years and sites could be more important than workers. Male bumble bees may be important but unrecognized pollinators of other late-season plant species, and animal sexes may differ in their pollinator performance in other systems.
Similar content being viewed by others
References
Agosta SJ, Janzen DH (2005) Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology. Oikos 108:183–193
Alarcón R, Riffell JA, Davidowitz G, Hildebrand JG, Bronstein JL (2010) Sex-dependent variation in the floral preferences of the hawkmoth Manduca sexta. Anim Behav 80:289–296
Alford DV (1975) Bumblebees. Davis-Poynter, London
Bates D, Maechler M, Bolker BM, Walker S (2013) Linear mixed-effects models using Eigen and S4. R Package, version 1.0–5. http://lme4.r-forge.r-project.org/
Bertsch A (1984) Foraging in male bumblebees (Bombus lucorum L.): Maximizing energy or minimizing water load? Oecologia 62:325–336
Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354
Bourke AFG (1997) Sex ratios in bumble bees. Philos T Roy Soc B 352:1921–1933
Brittain C, Williams N, Kremen C, Klein AM (2013) Synergistic effects of non-Apis bees and honey bees for pollination services. Proc R Soc B Biol Sci 280:20122767
Cane JH, Sampson BJ, Miller SA (2011) Pollination value of male bees: the specialist bee Peponapis pruinosa (Apidae) at summer squash (Cucurbita pepo). Environ Entomol 40:614–620
Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742–2752
Colla SR, Dumesh S (2010) The bumble bees of southern Ontario: notes on natural history and distribution. J Entomol Soc Ont 141:38–67
de Jager ML, Ellis AG (2012) Gender-specific pollinator preference for floral traits. Funct Ecol 26:1197–1204
del Castillo RC, Fairbairn DJ (2011) Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection. Ecol Evol 2:46–57
Dressler RL (1968) Pollination by euglossine bees. Evolution 22:202–210
Garibaldi LA, Steffan-Dewenter I, Winfree R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611
Gaskett AC (2011) Orchid pollination by sexual deception: pollinator perspectives. Biol Rev 86:33–75
Gögler J, Stökl J, Sramkova A et al (2009) Ménage à trois—two endemic species of deceptive orchids and one pollinator species. Evolution 63:2222–2234
Goulson D (2010) Bumblebees: behaviour, ecology, and conservation. Oxford University Press, Oxford
Harder LD, Wilson WG (1998) Theoretical consequences of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79:2789–2807
Heinrich B (1976) The foraging specializations of individual bumblebees. Ecol Monogr 46:105–128
Herrera CM (1987) Components of pollinator “quality”: comparative analysis of a diverse insect assemblage. Oikos 50:79–90
Jennersten O, Morse DH, O’Neil P (1991) Movements of male and worker bumblebees on and between flowers. Oikos 62:319–324
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot
Kearns CA, Thomson JD (2001) The natural history of bumblebees. University Press of Colorado, Boulder
Kraus FB, Wolf S, Moritz RFA (2009) Male flight distance and population substructure in the bumblebee Bombus terrestris. J Anim Ecol 78:247–252
Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore
Motten AF, Campbell DR, Alexander DE, Miller HL (1981) Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica. Ecology 62:1278–1287
Ogilvie JE (2014) Bee foraging in space and time: linking individual behaviour to pollination. PhD Dissertation, University of Toronto, Canada
Osborne JL, Williams IH (2001) Site constancy of bumble bees in an experimentally patchy habitat. Agric Ecosyst Environ 83:129–141
Ostevik KL, Manson JS, Thomson JD (2010) Pollination potential of male bumble bees (Bombus impatiens): movement patterns and pollen-transfer efficiency. J Poll Ecol 2:21–26
Pelletier L, McNeil JN (2003) The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos 103:688–694
Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland
Prŷs-Jones OE, Corbet SA (2011) Bumblebees. Pelagic Publishing, Exeter
Pyke GH (1978) Optimal foraging in bumblebees and coevolution with their plants. Oecologia 36:281–293
Pyke GH, Inouye DW, Thomson JD (2011) Activity and abundance of bumble bees near Crested Butte, Colorado: diel, seasonal, and elevation effects. Ecol Entomol 36:511–521
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/
Ranta E, Lundberg H (1981) Resource utilization by bumblebee queens, workers and males in a subarctic area. Ecography 4:145–154
Sahli HF, Conner JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae). Am J Bot 94:203–209
Skaug H, Fournier A, Nielsen A, Magnusson A, Bolker BM (2011) glmmADMB: generalized linear mixed models using AD model builder. R Package, version 0.7. http://glmmadmb.r-forge.r-project.org, http://admb-project.org
Sladen FW (1912) The humble-bee, its life-history and how to domesticate it. Macmillan, London
Stiles EW (1979) Evolution of colour pattern and pubescence characteristics in male bumblebees: automimicry vs. thermoregulation. Evolution 33:941–957
Svensson BG (1979) Patrolling behavior of bumble bee males (Hymenoptera, Apidae) in a subalpine-alpine area, Swedish Lapland. Zoon 7:67–94
Temeles EJ, Kress WJ (2003) Adaptation in a plant-hummingbird association. Science 300:630–633
Thomson JD (1981) Field measures of flower constancy in bumblebees. Am Midl Nat 105:377–380
Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. J Ecol 74:329–341
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
Thomson JD, Plowright RC (1980) Pollen carryover, nectar rewards, and pollinator behaviour with special reference to Diervilla lonicera. Oecologia 46:68–74
Thomson JD, Forrest JRK, Ogilvie JE (2011) Pollinator exclusion devices permitting easy access to flowers of small herbaceous plants. J Poll Ecol 4:24–25
Vereecken NJ, Dorchin A, Dafni A, Hötling S, Schulz S, Watts S (2013) A pollinators’ eye view of a shelter mimicry system. Ann Bot 111:1155–1165
Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–709
Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507
Wolf S, Moritz RFA (2014) The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera: Apidae). Apidologie 45:440–450
Wolf S, Toev T, Moritz RLV, Moritz RFA (2012) Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae). Popul Ecol 54:115–124
Acknowledgments
We thank the RMBL for field support, especially Jennie Reithel and billy barr; Brett Harris for field help; and Kareem Jarrah, Sarah Kim, and Patricia Lee for help with laboratory work. We are grateful to Jessica Forrest, Ben Gilbert, Takashi Makino, Randy Mitchell, Ali Parker, and an anonymous reviewer, for helpful discussion or manuscript comments. We also thank Neal Williams and his laboratory for assistance and use of the particle counter, and Megan Frederickson and her laboratory for use of the dissecting microscope. This work was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to JDT.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Lars Chittka.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ogilvie, J.E., Thomson, J.D. Male bumble bees are important pollinators of a late-blooming plant. Arthropod-Plant Interactions 9, 205–213 (2015). https://doi.org/10.1007/s11829-015-9368-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-015-9368-x