Big bees do a better job: intraspecific size variation influences pollination effectiveness.

Pat Willmer; Kathryn Finlayson

doi:10.26786/1920-7603(2014)22

Authors

Pat Willmer School of Biology, University of St Andrews Fife, Scotland, UK
Kathryn Finlayson As above

DOI:

https://doi.org/10.26786/1920-7603(2014)22

Abstract

Bumblebees (Bombus spp.) are efficient pollinators of many flowering plants, yet the pollen deposition performance of individual bees has not been investigated. Worker bumblebees exhibit large intraspecific and intra-nest size variation, in contrast with other eusocial bees; and their size influences collection and deposition of pollen grains.
Laboratory studies with B. terrestris workers and Vinca minor flowers showed that pollen grains deposited on stigmas in single visits (SVD) were significantly positively related to bee size; larger bees deposited more grains, while the smallest individuals, with proportionally shorter tongues, were unable to collect or deposit pollen in these flowers. Individuals did not increase their pollen deposition over time, so handling experience does not influence SVD in Vinca minor.
Field studies using Geranium sanguineum and Echium vulgare, and multiple visiting species, confirmed that individual size affects SVD. All bumblebee species showed size effects, though even the smallest individuals did deposit pollen, whereas there was no detectable effect with Apis with its limited size variation. Two abundant hoverfly species also showed size effects, particularly when feeding for nectar.
Mean size of foragers also varied diurnally, with larger individuals active earlier and later, so that pollination effectiveness varies through a day; flowers routinely pollinated by bees may best be served by early morning dehiscence and visits from larger individuals.
Thus, while there are well-documented species-level variations in pollination effectiveness, the fine-scale individual differences between foragers should also be taken into account when assessing the reproductive outputs of biotically-pollinated plants.

References

Alford DV (1975) Bumblebees. Davis-Poynter, London.

Baron GL, Raine NE & Brown MJF (2014) Impact of chronic exposure to a pyrethroid pesticide on bumblebees and interactions with a trypanosome parasite. Journal of Applied Ecology 51:460-469. DOI: https://doi.org/10.1111/1365-2664.12205

Benton T (2006) Bumblebees. Harper Collins, London.

Bishop JA & Armbruster WS (1999) Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Functional Ecology 13:711–724. DOI: https://doi.org/10.1046/j.1365-2435.1999.00351.x

Butz Huryn VM (1997) Ecological impacts of introduced honeybees. Quarterly Review of Biology 72:275-297. DOI: https://doi.org/10.1086/419860

Cane JH & Sipes S (2006) Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Waser NM & Ollerton J (eds) Plant pollinator interactions: from specialization to generalization, Chicago University Press, Chicago, pp 99-112.

Castellanos MD, Wilson P, Keller SJ, Wolfe AD & Thomson JD (2006) Anther evolution: pollen presentation strategies when pollinators differ. American Naturalist 167:288-296. DOI: https://doi.org/10.1086/498854

Couvillon MJ & Dornhaus A (2009) Location, location, location: larvae position inside the nest is correlated with adult body size in worker bumble-bees (Bombus impatiens). Proceedings of the Royal Society B 276:2411-2418. DOI: https://doi.org/10.1098/rspb.2009.0172

Couvillon MJ & Dornhaus A (2010). Small worker bumblebees (Bombus impatiens) are hardier against starvation than their larger sisters. Insectes Sociaux 57:193-197. DOI: https://doi.org/10.1007/s00040-010-0064-7

Darwin C (1861) Fertilization of Vincas. Gardeners' Chronicle 552

Dawson EH, Avargues-Weber A, Chittka L & Leadbeater E (2013) Learning by observation emerges from simple associations in an insect model. Current Biology 23:727-730. DOI: https://doi.org/10.1016/j.cub.2013.03.035

del Castillo RC & Fairbairn D (2011) Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection. Ecology & Evolution 2:46-57. DOI: https://doi.org/10.1002/ece3.65

Durisko Z, Shipp L & Dukas R (2011) Effects of experience on short and long-term foraging performance in Bumblebees. Ethology 117:49-55. DOI: https://doi.org/10.1111/j.1439-0310.2010.01842.x

Fjell I (1983) Anatomy of the xeromorphic leaves of Allamanda neriifolia, Thevetia peruviana and Vinca minor (Apocynaceae). Nordic Journal of Botany 3:383-392. DOI: https://doi.org/10.1111/j.1756-1051.1983.tb01953.x

Fontaine C, Collin CL & Dajoz I (2008) Generalist foraging of pollinators: diet expansion at high density. Journal of Ecology 96:1002-1010. DOI: https://doi.org/10.1111/j.1365-2745.2008.01405.x

Fryxell P (1957) Mode of reproduction of higher plants. Botanical Review 23:135-233. DOI: https://doi.org/10.1007/BF02869758

Gonzalez A, Rowe CL, Weeks PJ, Whittle D, Gilbert FS & Barnard CJ (1995) Flower choice by honeybees (Apis mellifera L) – sex phase of flowers and preferences among nectar and pollen foragers. Oecologia 101:258-264. DOI: https://doi.org/10.1007/BF00317292

Goulson D (2010) Bumblebees: behaviour, ecology, and conservation (2nd ed.) Oxford University Press, Oxford. DOI: https://doi.org/10.1093/oso/9780199553068.001.0001

Goulson D, Peat J, Stout JC, Tucker J, Darvill B, Derwent LC & Hughes WOH (2002) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Animal Behaviour 64:123-130. DOI: https://doi.org/10.1006/anbe.2002.3041

Goulson D & Sparrow KR (2009) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. Journal of Insect Conservation 13:177-181. DOI: https://doi.org/10.1007/s10841-008-9140-y

Greenleaf S, Williams N, Winfree R & Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. DOI: https://doi.org/10.1007/s00442-007-0752-9

Harder L (1982) Measurement and estimation of functional proboscis length in bumblebees (Hymenoptera: Apidae). Canadian Journal of Zoology 60:1073-1079. DOI: https://doi.org/10.1139/z82-148

Heinrich B (1979) ‘Majoring’ and ‘minoring’ by foraging bumblebees, Bombus vagans; an experimental analysis. Ecology 60:245-255. DOI: https://doi.org/10.2307/1937652

Heinrich B & Heinrich MJE (1983) Size and caste in temperature regulation by bumblebees. Physiological Zoology 56:552–562. DOI: https://doi.org/10.1086/physzool.56.4.30155878

Horwood A (1919) British Wild Flowers – In Their Natural Haunts. Gresham Publ Co. DOI: https://doi.org/10.5962/bhl.title.10759

Inoue MI & Yokoyama J (2006) Morphological variation in relation to flower use in bumblebees. Entomological Science 9:147–159. DOI: https://doi.org/10.1111/j.1479-8298.2006.00162.x

Jander R (1976) Grooming and pollen manipulation in bees (Apoidea): the nature and evolution of movements involving the foreleg. Physiological Entomology 1:179-194. DOI: https://doi.org/10.1111/j.1365-3032.1976.tb00960.x

Kandori I (2002) Diverse visitors with various pollinator importance and temporal change in the important pollinators of Geranium thunbergii (Geraniaceae). Ecological Research 17:283-294. DOI: https://doi.org/10.1046/j.1440-1703.2002.00488.x

Kapustjanskij A, Streinzer M, Paulus HF & Spaethe J (2007) Bigger is better: implications of body size for flight ability under different light conditions and the evolution of alloethism in bumblebees. Functional Ecology 21:1130-1136. DOI: https://doi.org/10.1111/j.1365-2435.2007.01329.x

King C, Ballantyne G & Willmer P (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology & Evolution 4:811-818. DOI: https://doi.org/10.1111/2041-210X.12074

Klinkhamer PGL, de Jong TJ & Wesselingh RA (1991) Implications of differences between hermaphrodite and female flowers for attractiveness to pollinators and seed prodcution. Netherlands Journal of Zoology 41:130-143. DOI: https://doi.org/10.1163/156854291X00081

Laverty TM (1994) Bumblebee learning and flower morphology. Animal Behaviour 47:531-545. DOI: https://doi.org/10.1006/anbe.1994.1077

Leadbeater E & Chittka L (2009) Bumble-bees learn the value of social cues through experience Biology Letters 5:310-312. DOI: https://doi.org/10.1098/rsbl.2008.0692

Macuda T, Gegear RJ, Laverty TM & Timney B (2001) Behavioural assessment of visual acuity in bumblebees (Bombus impatiens). Journal of Experimental Biology 204:559–564. DOI: https://doi.org/10.1242/jeb.204.3.559

Mares S, Ash L & Gronenberg W (2005) Brain allometry in bumblebee and honey bee workers. Brain Behaviour & Evolution 66:50-61. DOI: https://doi.org/10.1159/000085047

Morse D (1977) Estimating proboscis length from wing length in bumblebees (Bombus spp.). Annals of the Entomological Society of America 70:311-315. DOI: https://doi.org/10.1093/aesa/70.3.311

Morse DH (1978) Size-related foraging differences of bumble-bee workers. Ecological Entomology 3:189-192. DOI: https://doi.org/10.1111/j.1365-2311.1978.tb00918.x

Ne'eman G, Jürgens A, Newstrom-Lloyd L, Potts S, & Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biological Reviews 85:435-451. DOI: https://doi.org/10.1111/j.1469-185X.2009.00108.x

Peat J, Darvill B, Ellis J & Goulson D (2005) Effects of climate on intra- and interspecific size variation in bumble-bees. Functional Ecology 19:145-151. DOI: https://doi.org/10.1111/j.0269-8463.2005.00946.x

Peat J & Goulson D (2005) Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris. Behavioral Ecology & Sociobiology 58:152-156. DOI: https://doi.org/10.1007/s00265-005-0916-8

Peat J, Tucker J & Goulson D (2005) Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers? Ecological Entomology 30:176–181. DOI: https://doi.org/10.1111/j.0307-6946.2005.00676.x

Persson AS & Smith HG (2011) Bumblebee colonies produce larger foragers in complex landscapes. Basic & Applied Ecology 12:695-702. DOI: https://doi.org/10.1016/j.baae.2011.10.002

Plowright RC & Jay SC (1968) Caste differentiation in bumblebees (Bombus latr.: Hym.) I. The determination of female size. Insectes Sociaux 2:171–192. DOI: https://doi.org/10.1007/BF02223465

Pouvreau A (1989) Contribution à l'étude du polyéthisme chez les bourdons, Bombus Latr. (Hymenoptera, Apidae). Apidologie 20:229-244. DOI: https://doi.org/10.1051/apido:19890305

Rademaker MCJ, de Jong TJ & Klinkhamer PGL (1997) Pollen dynamics of bumble-bee visitation on Echium vulgare. Functional Ecology 11:554-563. DOI: https://doi.org/10.1046/j.1365-2435.1997.00124.x

Rademaker MCJ, de Jong TJ & van der Meijden E (1999) Selfing rates in natural populations of Echium vulgare: a combined empirical and model approach. Functional Ecology 13:828-837. DOI: https://doi.org/10.1046/j.1365-2435.1999.00384.x

Raine N & Chittka L (2007). Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris). Naturwissenschaften 94:459-464. DOI: https://doi.org/10.1007/s00114-006-0184-0

Roulston TH & Cane JH (2000) The effect of diet breadth and nesting ecology on body size variation in bees (Apiformes). Journal of the Kansas Entomological Society 73:129–142.

Sahli HF & Conner JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanismum (Brassicaceae). American Journal of Botany 94: 203-209. DOI: https://doi.org/10.3732/ajb.94.2.203

Seeley TD (1982) Significance of the age polyethism schedule in honeybee colonies. Behavioral Ecology & Sociobiology 11:287-293. DOI: https://doi.org/10.1007/BF00299306

Shelly TE & Villalobos E (2000) Buzzing bees (Hymenoptera: Apidae, Halictidae) on Solanum (Solanaceae): floral choice and handling time track pollen availability. Florida Entomologist 83:180-187. DOI: https://doi.org/10.2307/3496153

Smeets P & Duchateau M (2003) Longevity of Bombus terrestris workers (Hymenoptera: Apidae) in relation to pollen availability, in the absence of foraging. Apidologie 34:333-337. DOI: https://doi.org/10.1051/apido:2003026

Spaethe J, Brockmann A, Halbig C & Tautz J (2007) Size determines antennal sensitivity and behavioural threshold to odors in bumblebee workers. Naturwissenschaften 94:733-739. DOI: https://doi.org/10.1007/s00114-007-0251-1

Spaethe J & Weidenmüller A (2002) Size variation and foraging rate in bumblebees (Bombus terrestris) Insectes Sociaux 49:142-146. DOI: https://doi.org/10.1007/s00040-002-8293-z

Stout JC (2000) Does size matter? Bumblebee behaviour and the pollination of Cytisus scoparius L. (Fabaceae). Apidologie 31:129-139. DOI: https://doi.org/10.1051/apido:2000111

Sutcliffe GH & Plowright RC (1988) The effects of food supply on adult size in the bumble bee Bombus terricola Kirby (Hymenoptera: Apidae). The Canadian Entomologist 120:1051–1058. DOI: https://doi.org/10.4039/Ent1201051-12

Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85: 458-470. DOI: https://doi.org/10.1890/02-0626

Thomson J & Goodell K (2001) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. Journal of Applied Ecology 38:1032-1044. DOI: https://doi.org/10.1046/j.1365-2664.2001.00657.x

Thomson JD & PlowrightRC (1980) Pollen carryover, nectar rewards and pollinator behaviour with special reference to Diervilla lonicera. Oecologia 46:68-74. DOI: https://doi.org/10.1007/BF00346968

Tur C, Vigalondo B, Trojelsgaard K, Olesen J & Traveset A (2014) Downscaling pollen-transport networks to the level of individuals. Journal of Animal Ecology 83:306-317. DOI: https://doi.org/10.1111/1365-2656.12130

Waddington KD, Herbst LH & Roubik DW (1986) Relationship between recruitment systems of stingless bees and within-nest worker size variation. Journal of the Kansas Entomological Society 59:95–102.

Willmer PG (1983) Thermal constraints on activity patterns in nectar-feeding insects. Ecological Entomology 8:455-469. DOI: https://doi.org/10.1111/j.1365-2311.1983.tb00524.x

Willmer PG (2011) Pollination and floral ecology. Princeton University Press, Princeton. DOI: https://doi.org/10.23943/princeton/9780691128610.001.0001

Willmer PG, Bataw AAM & Hughes JP (1994) The superiority of bumblebees to honeybees as pollinators: insect visits to raspberry flowers. Ecological Entomology 19:271-284. DOI: https://doi.org/10.1111/j.1365-2311.1994.tb00419.x

Willmer PG & Stone GN (2005) Behavioural, ecological and physiological determinants of the activity patterns of bees. Advances in the Study of Behavior 34:347-466. DOI: https://doi.org/10.1016/S0065-3454(04)34009-X

Worden BD, Skemp AK, & Papaj DR (2005) Learning in two contexts: the effects of interference and body size in bumblebees. Journal of Experimental Biology 208:2045-2053. DOI: https://doi.org/10.1242/jeb.01582