Honey bee and native solitary bee foraging behavior in a crop with dimorphic parental lines

Autoři: María Cecilia Estravis Barcala aff001;  Florencia Palottini aff001;  Walter Marcelo Farina aff001
Působiště autorů: Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Laboratorio de Insectos Sociales, Buenos Aires, Argentina aff001;  CONICET-Universidad de Buenos Aires, Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE), Buenos Aires, Argentina aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223865


Insect pollination is issential for hybrid seed production systems, among which, introduced and native bees are the primary pollinating agents transferring pollen from male fertile (MF) to male sterile (MS) lines. On a highly dimorphic sunflower (Helianthus annuus) crop, we assessed the foraging behavior of solitary Melissodes bees and honey bees Apis mellifera. We found that Melissodes spp. were dominant in and showed fidelity to MF plants, gathering sunflower pollen efficiently throughout the day. In contrast, honey bees dominated on MS lines, mostly gathered nectar and exhibited high floral constancy, even after interacting with a second visitor. Also, honey bees carried sunflower pollen on their bodies while visiting MS inflorescences. This study highlights the need for a thorough understanding of the factors involved in a pollinator-dependent agroecosystem crop to assess the contribution of native bees on pollination of crops which offer resources spatially separated in two highly dimorphic parental lines.

Klíčová slova:

Crops – Flowering plants – Foraging – Honey bees – Inflorescences – Sunflower – Pollen – Pollination


1. McGregor SE. Insect pollination of cultivated crop plants. Vol. 496. Washington DC: Agricultural Research Service, US Department of Agriculture; 1976.

2. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci. 2007; 274(1608): 303–313. doi: 10.1098/rspb.2006.3721 17164193

3. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science. 2013; 339(6127): 1608–1611. doi: 10.1126/science.1230200 23449997

4. Mallinger RE, Gratton C. Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. J Appl Ecol. 2015; 52(2): 323–330. doi: 10.1111/1365-2664.12377

5. Rader R, Bartomeus I, Garibaldi LA, Garratt MP, Howlett BG, Winfree R, et al. Non-bee insects are important contributors to global crop pollination. P Natl Acad Sci. USA. 2016; 113(1): 146–151. doi: 10.1073/pnas.1517092112 26621730

6. Brosi BJ, Briggs HM. Single pollinator species losses reduce floral fidelity and plant reproductive function. P Natl Acad Sc. USA. 2013; 110(32): 13044–13048. doi: 10.1073/pnas.1307438110 23878216

7. Degrandi-Hoffman G, Chambers M. Effects of honey bee (Hymenoptera: Apidae) foraging on seed set in self-fertile sunflowers (Helianthus annuus L.). Environmental Entomology. 2006; 35(4), 1103–1108. doi: 10.1603/0046-225X-35.4.1103

8. Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay GB, Pirk CWW, Donaldson JS, et al. Natural and within-farmland biodiversity enhances crop productivity. Ecol Lett. 2011; 14(3): 251–259. doi: 10.1111/j.1461-0248.2010.01579.x 21244594

9. Mallinger RE, Bradshaw J, Varenhorst AJ, Prasifka JR. Native Solitary Bees Provide Economically Significant Pollination Services to Confection Sunflowers (Helianthus annuus L.)(Asterales: Asteraceae) Grown Across the Northern Great Plains. J Econ Entomol. 2018. doi: 10.1093/jee/toy322 30346534

10. DeGrandi-Hoffman G, Watkins JC. The foraging activity of honey bees Apis mellifera and non—Apis bees on hybrid sunflowers (Helianthus annuus) and its influence on cross—pollination and seed set. J Apicult Res. 2000; 39(1–2): 37–45. doi: 10.1080/00218839.2000.11101019

11. Greenleaf SS, Kremen C. Wild bees enhance honey bees’ pollination of hybrid sunflower. P. Natl. Acad. Sci. USA. 2006; 103(37): 13890–13895. doi: 10.1073/pnas.0600929103 16940358

12. Torretta JP, Medan D, Roig Alsina A, Montaldo NH. Visitantes florales diurnos del girasol (Helianthus annuus, Asterales: Asteraceae) en la Argentina. Rev. Soc. Entomol. Argent. 2010; 69(1–2): 17–32.

13. Cilla G, Caccavari M, Bartoloni NJ, Roig-Alsina A. The foraging preferences of two species of Melissodes Latreille (Hymenoptera, Apidae, Eucerini) in farmed sunflower in Argentina. Grana. 2012; 51(1):63–75. doi: 10.1080/00173134.2011.644324

14. Parker F.D. Sunflower pollination: abundance, diversity, and seasonality of bees on male-sterile and male-fertile cultivars. Environ Entomol. 1981; 10(6): 1012–1017. doi: 10.1093/ee/10.6.1012

15. Sardiñas HS, Kremen C. Pollination services from field-scale agricultural diversification may be context-dependent. Agric Ecosyst Environ. 2015; 207, 17–25. doi: 10.1016/j.agee.2015.03.020

16. Mallinger RE, Prasifka JR. Bee visitation rates to cultivated sunflowers increase with the amount and accessibility of nectar sugars. J Appl Entomol. 2017; 141(7): 561–573. doi: 10.1111/jen.12375

17. Gumbert A, Kunze J. Inflorescence height affects visitation behavior of bees–a case study of an aquatic plant community in Bolivia. Biotropica. 1999; 31(3): 466–477. doi: 10.1111/j.1744-7429.1999.tb00389.x

18. Ishii HS. Floral display size influences subsequent plant choice by bumble bees. Funct Ecol. 2006; 20(2): 233–238. doi: 10.1111/j.1365-2435.2006.01106.x

19. Sapkale RB, Shinde SR, Pawar RM. Heterosis studies in sunflower (Helianthus annus L.). Internat J Plant Sci. 2016; 11(1), 22–27. doi: 10.15740/HAS/IJPS/11.1/22-27

20. Vear F. Changes in sunflower breeding over the last fifty years. OCL. 2016; 23(2), D202. doi: 10.1051/ocl/2016006

21. Susic Martin C, Farina WM. Honeybee floral constancy and pollination efficiency in sunflower (Helianthus annuus) crops for hybrid seed production. Apidologie. 2016; 47(2): 161–170. doi: 10.1007/s13592-015-0384-8

22. Gabai-Hazera A, Vaissière BE, Blacquière T, Freitas BM, Allsopp M, Chabert S, et al. Protocol for using pollinators in hybrid vegetable seed production. ISF Working Group Vegetable Seed Production. 2018.

23. Vaissière BE, Freitas BM, Gemmill-Herren B. Protocol to detect and assess pollination deficits in crops: a handbook for its use. Rome: FAO (Food and Agriculture Organization of the United Nations). 2011

24. Degrandi-Hoffman G, Thorp R, Loper G, Eisikowitch D. Identification and distribution of cross-pollinating honey-bees on almonds. J Appl Ecol. 1992; 238–246.

25. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. [Internet]. 2018.

26. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015; 67(1): 1–48.

27. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–137, https://CRAN.R-project.org/package=nlme [Internet]. 2018.

28. Russell L. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.2.3. https://CRAN.R-project.org/package=emmeans [Internet]. 2018.

29. Venables WN, Ripley BD. Modern Applied Statistics with S—Fourth Edition. New York: Springer. ISBN 0-387-95457-0; 2002.

30. Chambers JM, Hastie TJ. Statistical Models in S. New York, NY: Chapman and Hall; 1992.

31. McDonald J.H. Handbook of Biological Statistics (3rd ed.). Baltimore: Sparky House Publishing; 2014.

32. Sokal RR, Rohlf FJ. Biometry: the principles and practice of statistics in biological research. p.715. New York: State University of New York; 1995.

33. DeGrandi-Hoffman G, Martin JH. The size and distribution of the honey bee (Apis mellifera L.) cross-pollinating population on male-sterile sunflowers (Helianthus annuus L.). J Apicult Res. 1993; 32(3–4): 135–142. doi: 10.1080/00218839.1993.11101298

34. Louveaux J. Recherches sur la récolte du pollen par les abeilles (Apis mellifica L)(Fin). Ann. Abeille. 1959; 1: 13–111.

35. von Frisch K. The dance language and orientation of bees. Cambridge: Harvard University Press: 1967.

36. Tepedino VJ, Parker FD. Interspecific differences in the relative importance of pollen and nectar to bee species foraging on sunflowers. Environ Entomol. 1982; 11(1): 246–250. doi: 10.1093/ee/11.1.246

37. FAO [Internet]. Food and Agriculture Organization of the United Nations–FAOSTATS. Available from: http://www.fao.org/faostat/en/#data. [last accessed 27 December 2018].

38. Winfree R, Fox JW, Williams NM, Reilly JR, Cariveau DP. Abundance of common species, not species richness, drives delivery of a real‐world ecosystem service. Ecol Lett. 2015; 18(7), 626–635. doi: 10.1111/ele.12424 25959973

39. Fijen TP, Scheper JA, Boom TM, Janssen N, Raemakers I, Kleijn D. Insect pollination is at least as important for marketable crop yield as plant quality in a seed crop. Ecol Lett. 2018; 21(11), 1704–1713. doi: 10.1111/ele.13150 30189466

40. DeGrandi-Hoffman G, Martin JH. Does a honey bee (Apis mellifera) colony's foraging population on male-fertile sunflowers (Helianthus annuus) affect the amount of pollen on nestmates foraging on male-steriles?. J Apicult Res. 1995; 34: 109–114.

41. Parker AJ, Williams NM, Thomson JD. Specialist pollinators deplete pollen in the spring ephemeral wildflower Claytonia virginica. Ecol Evol. 2016; 6(15): 5169–5177. doi: 10.1002/ece3.2252 27551374

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2019 Číslo 10
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