Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees

Authors

  • Alessandro Fisogni Department of Biological, Geological and Environmental Sciences, University of Bologna, via Irnerio 42, 40126, Bologna
  • Gherardo Bogo Department of Biological, Geological and Environmental Sciences, University of Bologna, via Irnerio 42, 40126, Bologna
  • François Massol Université de Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, F-59000 Lille
  • Laura Bortolotti CREA Research Centre for Agriculture and Environment, via di Saliceto 80, 40128, Bologna
  • Marta Galloni Department of Biological, Geological and Environmental Sciences, University of Bologna, via Irnerio 42, 40126, Bologna

DOI:

https://doi.org/10.26496/bjz.2021.93

Keywords:

Bombus, flower-visiting behaviour, Gentiana lutea, plant-pollinator interactions, Psithyrus

Abstract

Cuckoo bumblebees are a monophyletic group within the genus Bombus and social parasites of free-living bumblebees, upon which they rely to rear their offspring. Cuckoo bumblebees lack the worker caste and visit flowers primarily for their own sustenance and do not collect pollen. Although different flower-visiting behaviours can be expected between cuckoo and free-living bumblebees due to different biological constraints, no study has yet quantified such differences. Here, we provide the first empirical evidence of different flower-visiting behaviours between cuckoo and free-living bumblebees. We recorded the flower-visiting behaviour of 350 individual bumblebees over two years in a wild population of the entomophilous plant Gentiana lutea, of which they are among the main pollinators. In cuckoo bumblebees (28.9% of the total), we only found males, while we found both workers and males in free-living bumblebees. Cuckoo bumblebees visited significantly more flowers for longer time periods than both free-living bumblebee workers and males within whorls, while differences at the whole-plant level were less marked. Free-living bumblebee males visited more flowers and performed slightly longer flower visits than workers. Behavioural differences between cuckoo male bumblebees and free-living bumblebee workers are likely related to different foraging needs, while differences between cuckoo and free-living bumblebee males may be caused by differences in colony development and a delayed mating period of free-living bumblebees. The longer visits made by cuckoo male bumblebees will likely negatively affect plant reproductive success through increased within-plant pollen flow.

References

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

Andrikopoulos C. & Cane J. (2018). Comparative pollination efficacies of five bee species on raspberry. Journal of Economic Entomology 111: 2513–2519. https://doi.org/10.1093/jee/toy226

Barton K. (2019). MuMIn: Multi-Model Inference. R package version 1.43.17. Avalaible from https://CRAN.R-project.org/package=MuMIn

Bateman R. & Rudall P. (2014). Bumblebee-mediated pollination of English populations of the Military Orchid (Orchis militaris): its possible relevance to functional morphology, life history and climate change. New Journal of Botany 4: 122–133. https://doi.org/10.1179/2042349714Y.0000000048

Bates D., Mächler M., Bolker B.M. & Walker S.C. (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 67: 1–48. https://doi.org/10.18637/jss.v067.i01

Bogo G., de Manincor N., Fisogni A., Galloni M., Zavatta L. & Bortolotti L. (2018). Different reproductive strategies and their possible relation to inbreeding risk in the bumble bee Bombus terrestris. Insectes Sociaux 65: 289–295. https://doi.org/10.1007/s00040-018-0611-1

Brunet J. (2005). Plant–pollinator interactions and pollen dispersal. In: Dafni A., Kevan P.G. & Husband B. (eds) Practical pollination biology: 56–82. Enviroquest Ltd, Cambridge, Ontario, Canada.

Burnham K. & Anderson D. (2002). Information and likelihood theory: a basis for model selection and inference. In: Model Selection And Multimodel Inference: a Practical Information-Theoretic Approach: 49–97. Springer-Verlag, New York.

Fisher R. (1987). Queen-worker conflict and social parasitism in bumble bees (Hymenoptera: Apidae). Animal Behaviour 35: 1026–1036. https://doi.org/10.1016/S0003-3472(87)80159-8

Fründ J., Dormann C.F., Holzschuh A. & Tscharntke T. (2013). Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology 94: 2042–2054. https://doi.org/10.1890/12-1620.1

Goulson D. (2010). Bumblebees. Behaviour, Ecology, and Conservation. Oxford University Press, Oxford.

Goulson D., Lye G.C. & Darvill B. (2008). Decline and conservation of bumble bees. Annual Review of Entomology 53: 191–208. https://doi.org/10.1146/annurev.ento.53.103106.093454

Hodges C. & Wolf L. (1981). Optimal foraging in bumblebees: why is nectar left behind in flowers? Behavioral Ecology and Sociobiology 9: 41–44. https://doi.org/doi:10.1007/bf00299851

Jennersten O., Morse D.H. & O’Neil P. (1991). Movements of Male and Worker Bumblebees on and between Flowers. Oikos 62: 319–324. https://doi.org/10.2307/3545496

Kreuter K., Bunk E., Lückemeyer A., Twele R., Francke W. & Ayasse M. (2012). How the social parasitic bumblebee Bombus bohemicus sneaks into power of reproduction. Behavioral Ecology and Sociobiology 66: 475–486. https://doi.org/10.1007/s00265-011-1294-z

Küpper G. & Schwammberger K. (1995). Social parasitism in bumble bees (Hymenoptera, Apidae): observations of Psithyrus sylvestris in Bombus pratorum nests. Apidologie 26: 245–254. https://doi.org/10.1051/apido:19950306

Lenth R. (2020). Emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.1. Available from https://CRAN.R-project.org/package=emmeans

Lhomme P. & Hines H.M. (2019). Ecology and evolution of cuckoo bumble bees. Annals of the Entomological Society of America 112: 122–140. https://doi.org/10.1093/aesa/say031

Lhomme P., Sramkova A., Kreuter K., Lecocq T., Rasmont P. & Ayasse M. (2013). A method for year-round rearing of cuckoo bumblebees (Hymenoptera: Apoidea: Bombus subgenus Psithyrus). Annales de la Société Entomologique de France 49: 117–125. https://doi.org/10.1080/00379271.2013.774949

Lhomme P., Williams S.D., Ghisbain G., Martinet B., Gérard M. & Hines H.M. (2021). Diversification pattern of the widespread Holarctic cuckoo bumble bee, Bombus flavidus (Hymenoptera: Apidae): the east side story. Insect Systematics and Diversity 5: 1–15. https://doi.org/10.1093/isd/ixab007

Ogilvie J.E. & Thomson J.D. (2015). Male bumble bees are important pollinators of a late-blooming plant. Arthropod-Plant Interactions 9: 205–213. https://doi.org/10.1007/s11829-015-9368-x

Ollerton J., Killick A., Lamborn E., Watts S. & Whiston M. (2007). Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56: 717–728. https://doi.org/10.2307/25065855

Ostevik K.L., Manson J.S. & Thomson J.D. (2010). Pollination potential of male bumble bees (Bombus impatiens): movement patterns and pollen-transfer efficiency. Journal of Pollination Ecology 2:21–26. https://doi.org/10.26786/1920-7603(2010)3

Pellissier V., Muratet A., Verfaillie F. & Machon N. (2012). Pollination success of Lotus corniculatus (L.) in an urban context. Acta Oecologica 39: 94–100. https://doi.org/10.1016/j.actao.2012.01.008

Prys-Jones O. & Corbet S. (1991). Bumblebees. Richmond Publishing Company, Slough, UK.

Pyke G.H. (1984). Optimal foraging theory: A critical review. Annual Review of Ecology and Systematics 15: 523–575. https://doi.org/10.1146/annurev.es.15.110184.002515

R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Rossi M., Fisogni A. & Galloni M. (2015). Biosystematic studies on the mountain plant Gentiana lutea L. reveal variability in reproductive traits among subspecies. Plant Ecology & Diversity 9: 97–104. https://doi.org/10.1080/17550874.2015.1074625

Rossi M., Fisogni A. & Galloni M. (2016). The effect of pollination mode on seed performance of Gentiana lutea: a laboratory evaluation of seed germinability. Nordic Journal of Botany 34: 761–768. https://doi.org/10.1111/njb.01177

Rossi M., Fisogni A., Nepi M., Quaranta M. & Galloni M. (2014). Bouncy versus idles: On the different role of pollinators in the generalist Gentiana lutea L. Flora 209: 164–171. https://doi.org/10.1016/j.flora.2014.02.002

Russell A.L., Morrison S.J., Moschonas E.H. & Papaj D.R. (2017). Patterns of pollen and nectar foraging specialization by bumblebees over multiple timescales using RFID. Scientific Reports 7: 42448. https://doi.org/10.1038/srep42448

Smith G.P., Bronstein J.L. & Papaj D.R. (2019). Sex differences in pollinator behavior: Patterns across species and consequences for the mutualism. Journal of Animal Ecology 88: 971–985. https://doi.org/10.1111/1365-2656.12988

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. https://doi.org/10.1046/j.1365-2664.2001.00657.x

Velthuis H. & van Doorn A. (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37: 421–451. https://doi.org/10.1051/apido:2006019

Wickham H. (2016). ggplot2: elegant graphics for data analysis. Springer-Verlag, New York.

Wolf S. & Chittka L. (2016). Male bumblebees, Bombus terrestris, perform equally well as workers in a serial colour-learning task. Animal Behaviour 111: 147–155. https://doi.org/10.1016/j.anbehav.2015.10.009

Wolf S & Moritz R. (2014). The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera: Apidae). Apidologie 45: 440–450. https://doi.org/10.1007/s13592-013-0259-9

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Published

2021-12-15

How to Cite

Fisogni, A., Bogo, G., Massol, F., Bortolotti, L., & Galloni, M. (2021). Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees. Belgian Journal of Zoology, 151. https://doi.org/10.26496/bjz.2021.93

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