, Volume 50, Issue 3, pp 340–352 | Cite as

Colour patterns, distribution and food plants of the Asian bumblebee Bombus bicoloratus (Hymenoptera: Apidae)

  • Guiling Ding
  • Shiwen Zhang
  • Jiaxing Huang
  • Muhammad Naeem
  • Jiandong AnEmail author
Original article


Bombus bicoloratus is an important pollinator of wild flowers in the oriental region. We confirmed a total of 451 specimens of B. bicoloratus from China based on DNA sequences from mitochondrial cytochrome oxidase subunit I (COI) barcodes. Bombus bicoloratus is distributed mainly in tropical and subtropical areas of southern China. This species exhibits a striking intraspecific colour-pattern polymorphism both in females and males. The distribution frequency of the different colour patterns is heavily skewed, with 50.9% of the workers sharing the same colour pattern that predominates in most locations. Workers from the islands of Hainan and Taiwan possess a very distinct colour pattern, and its spatial distribution is correlated with the climate factor irradiance. Bombus bicoloratus has been recorded to collect nectar and pollen from 14 plant families, indicating that this species is polylectic. This study will be helpful for recognising bumblebee species with variable colour patterns, especially B. bicoloratus, in Asia.


Bombus bicoloratus Colour pattern COI Distribution Food plants 



We are grateful to Cheng Liang, Yiheng Qin, Liping Yao, Zongwen Hu, Deqin Zong, Huanxian Lu, Hongmu Zhao, Xuewen Zhang, Zhiyong Zhao, Dongxu Zhao, Jianrong Dai, Jiamin Qin, Qun Luo, Youping Yang, Fanggui Xi, Wenhua Luo, Duansheng Wang, Jun Gao, Jun Guo, Yaning Zhang, Xinyu Liu, Zhengying Miao, Aiping Han, Zhiyong Zhou, Xiaolong Yuan, Huanli Xu and Yanjie Liu for their help in collecting bumblebees. We thank Dr. Paul H. Williams for his help in identifying the specimens to species and Yumei Zhang for her help in DNA barcoding. We also thank Dr. Lei Meng of China Agricultural University for her assistance in identifying the food plants.

Author contributions

J.A. conceived this research. G.D., S.Z., M.N. and J.H. performed the experiments and the analyses. G.D. wrote the paper. All authors read and approved the final manuscript.

Funding information

This work was financially supported by the Natural Science Foundation of China (31672500) and the Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2015-IAR).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. An, J.-D., Huang, J.-X., Shao, Y.-Q., Zhang, S.-W., Wang, B., Liu, X.-Y., Wu, J., Williams, P.H. (2014) The bumblebees of North China (Apidae, Bombus Latreille). Zootaxa 3830(1): 1–89.PubMedCrossRefGoogle Scholar
  2. Cameron, S.A., Hines, H.M., Williams, P.H. (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linnean Soc. 91(1): 161–188.CrossRefGoogle Scholar
  3. Cao, G.-X., Xue, L., Li, Y., Pan, K.-W. (2011) The relative importance of architecture and resource competition in allocation to pollen and ovule number within inflorescences of Hosta ventricosa varies with the resource pools. Ann. Bot. 107(8): 1413–1419.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Carolan, J.C., Murray, T.E., Fitzpatrick, Ú., Crossley, J., Schmidt, H., Cederberg, B., Mcnally, L., Paxton, R.J., Williams, P.H., Brown, M.J.F. (2012) Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. PLoS One 7(1): e29251.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Darriba, D., Taboada, G.L., Doallo, R., Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9(8): 772.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Darvill, B., Ellis, J.S., Lye, G.C., Goulson, D. (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol. Ecol. 15(3): 601–611.PubMedCrossRefGoogle Scholar
  7. Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29(8): 1969–1973.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Duennes, M.A., Lozier, J.D., Hines, H.M., Cameron, S.A. (2012) Geographical patterns of genetic divergence in the widespread Mesoamerican bumble bee Bombus ephippiatus (Hymenoptera: Apidae). Mol. Phylogenet. Evol. 64(1): 219–231.PubMedCrossRefGoogle Scholar
  9. Frison, T.H. (1934) Records and descriptions of Bremus and Psithyrus from Formosa and the Asiatic mainland. Trans. Nat. Hist. Soc. Formosa 24: 150–185.Google Scholar
  10. Fujisawa, T., Barraclough, T.G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst. Biol. 62(5): 707–724.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Gjershaug, J.O., Staverløkk, A., Kleven, O., Ødegaard, F. (2013) Species status of Bombus monticola Smith (Hymenoptera: Apidae) supported by DNA barcoding. Zootaxa 3716(3): 431–440.PubMedCrossRefGoogle Scholar
  12. Goulson, D., Lye, G.C., Darvill, B. (2008) Decline and conservation of bumble bees. Annu. Rev. Entomol. 53: 191–208.PubMedCrossRefGoogle Scholar
  13. Hall, T.A. (1999) BioEdit : a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, in: Series, N.A.S. (Ed.), Nucl. Acids. Symp. Ser. 41: 95–98.Google Scholar
  14. Hammer, Ø., Harper, D.A., Ryan, P.D. (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4(1): 1–9.Google Scholar
  15. Hebert, P.D.N., Ratnasingham, S., deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. Lond. B. 270 (Suppl): S96–99.Google Scholar
  16. Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H., Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. U.S.A. 101(41): 14812–14817.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Hines, H.M., Williams, P.H. (2012) Mimetic colour pattern evolution in the highly polymorphic Bombus trifasciatus (Hymenoptera: Apidae) species complex and its comimics. Zool. J. Linn. Soc. 166(4): 805–826.CrossRefGoogle Scholar
  18. Ho, K.-K., Yang, P.-S., Chiang, C.-H. (2002) The study of artificial rearing Taiwan bumble bee. Taiwan Insect [Spec. Issue] 4: 151–164.Google Scholar
  19. Huang, J.-X., An, J.-D. (2018) Species diversity, pollination application and strategy for conservation of the bumblebees of China. Biodivers Sci 26(5): 486–497.CrossRefGoogle Scholar
  20. Huang, J.-X., An, J.-D., Wu, J., Williams, P.H. (2015a) Extreme food-plant specialisation in Megabombus bumblebees as a product of long tongues combined with short nesting seasons. PLoS One 10(8): e0132358.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Huang, J.-X., Wu, J., An, J.-D., Williams, P.H. (2015b) Newly discovered colour-pattern polymorphism of Bombus koreanus females (Hymenoptera: Apidae) demonstrated by DNA barcoding. Apidologie 46(2): 250–261.CrossRefGoogle Scholar
  22. Julier, H.E., Roulston, T.H. (2009) Wild bee abundance and pollination service in cultivated pumpkins: farm management, nesting behavior and landscape effects. J. Econ. Entomol. 102(2): 563–573.PubMedCrossRefGoogle Scholar
  23. Kawakita, A., Sota, T., Ito, M., Ascher, J.S., Tanaka, H., Kato, M., Roubik, D.W. (2004) Phylogeny, historical biogeography, and character evolution in bumble bees (Bombus: Apidae) based on simultaneous analysis of three nuclear gene sequences. Mol. Phylogenet. Evol. 31(2): 799–804.PubMedCrossRefGoogle Scholar
  24. Kumar, S., Stecher, G., Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33(7): 1870–1874.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Lozier, J.D., Strange, J.P., Koch, J.B. (2013) Landscape heterogeneity predicts gene flow in a widespread polymorphic bumble bee, Bombus bifarius (Hymenoptera: Apidae). Conserv. Genet. 14(5): 1099–1110.CrossRefGoogle Scholar
  26. Lozier, J.D., Jackson, J.M., Dillon, M.E., Strange, J.P. (2016) Population genomics of divergence among extreme and intermediate color forms in a polymorphic insect. Ecol. Evol. 6(4): 1075–1091.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Murray, T.E., Fitzpatrick, Ú., Brown, M.J.F., Paxton, R.J. (2008) Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conserv. Genet. 9(3): 653–666.CrossRefGoogle Scholar
  28. Naeem, M., Yuan, X.-L., Huang, J.-X., An, J.-D. (2018) Habitat suitability for the invasion of Bombus terrestris in East Asian countries: A case study of spatial overlap with local Chinese bumblebees. Sci. Rep. 8(1): 11035.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Owen, R.E., Plowright, R.C. (1988) Inheritance of metasomal pile colour variation in the bumble bee Bombus rufocinctus Cresson (Hymenoptera: Apidae). Can. J. Zool. 66(5): 1172–1178.CrossRefGoogle Scholar
  30. Pimsler, M.L., Jackson, J.M., Lozier, J.D. (2017) Population genomics reveals a candidate gene involved in bumble bee pigmentation. Ecol. Evol. 7(10): 3406–3413.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Puillandre, N., Lambert, A., Brouillet, S., Achaz, G. (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol. Ecol. 21(8): 1864–1877.PubMedCrossRefGoogle Scholar
  32. Pywell, R.F., Warman, E.A., Hulmes, L., Hulmes, S., Nuttall, P., Sparks, T.H., Critchley, C.N.R., Sherwood, A. (2006) Effectiveness of new agri-environment schemes in providing foraging resources for bumblebees in intensively farmed landscapes. Biol. Conserv. 129(2): 192–206.CrossRefGoogle Scholar
  33. Rapti, Z., Duennes, M.A., Cameron, S.A. (2014) Defining the colour pattern phenotype in bumble bees (Bombus): a new model for evo devo. Biol. J. Linnean Soc. 113(2): 384–404.CrossRefGoogle Scholar
  34. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61(3): 539–542.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Schmid-Hempel, P., Schmid-Hempel, R., Brunner, P.C., Seeman, O.D., Allen, G.R. (2007) Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck. Heredity 99(4): 414–422.PubMedCrossRefGoogle Scholar
  36. Shao, Z.-Y., Mao, H.-X., Fu, W.-J., Ono, M., Wang, D.-S., Bonizzoni, M., Zhang, Y.-P. (2004) Genetic structure of Asian populations of Bombus ignitus (Hymenoptera: Apidae). J. Hered. 95(1): 46–52.PubMedCrossRefGoogle Scholar
  37. Stiles, E.W. (1979) Evolution of color pattern and pubescence characteristics in male bumblebees: automimicry vs. thermoregulation. Evolution 33(3): 941–957.PubMedCrossRefGoogle Scholar
  38. Sung, I.-H., Lu, S.-S., Chan, M.-L., Lin, M.-Y., Chiang, C.-H., Li, C.-C., Yang, P.-S. (2011) A study on the size and morphological difference, seasonal occurrence and distribution features of four bumblebees from Taiwan (Hymenoptera, Apidae). Formosan Entomol. 31(4): 309–323.Google Scholar
  39. Thompson, J.D., Higgins, D.G., Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22(22): 4673–4680.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Velthuis, H.H.W., van Doorn, A. (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37(4): 421–451.CrossRefGoogle Scholar
  41. Vesterlund, S.R., Sorvari, J., Vasemägi, A. (2014) Molecular identification of cryptic bumblebee species from degraded samples using PCR-RFLP approach. Mol. Ecol. Resour. 14(1): 122–126.PubMedCrossRefGoogle Scholar
  42. Waters, J., Darvill, B., Lye, G.C., Goulson, D. (2011) Niche differentiation of a cryptic bumblebee complex in the Western Isles of Scotland. Insect. Conserv. Divers. 4(1): 46–52.CrossRefGoogle Scholar
  43. Williams, P.H. (1998) An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bull. Nat. Hist. Mus. Lond. (Ent.) 67(1): 79–152.Google Scholar
  44. Williams, P. (2007) The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry. Biol. J. Linnean Soc. 92(1): 97–118.CrossRefGoogle Scholar
  45. Williams, P., Tang, Y., Yao, J., Cameron, S. (2009) The bumblebees of Sichuan (Hymenoptera: Apidae, Bombini). Syst. Biodivers. 7(2): 101–189.CrossRefGoogle Scholar
  46. Williams, P.H., Brown, M.J.F., Carolan, J.C., An, J.-D., Goulson, D., et al. (2012) Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). Syst. Biodivers. 10(1): 21–56.CrossRefGoogle Scholar
  47. Williams, P.H., Byvaltsev, A., Sheffield, C., Rasmont, P. (2013) Bombus cullumanus-an extinct European bumblebee species? Apidologie 44(2): 121–132.CrossRefGoogle Scholar
  48. Williams, P.H., Bystriakova, N., Huang, J.-X., Miao, Z.-Y., An, J.-D. (2015) Bumblebees, climate and glaciers across the Tibetan plateau (Apidae: Bombus Latreille). Syst. Biodivers. 13(2): 164–181.CrossRefGoogle Scholar
  49. Williams, P.H., Huang, J.-X., Rasmont, P., An, J.-D. (2016) Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae). Zootaxa 4204(1): 1–72.CrossRefGoogle Scholar
  50. Williams, P.H., Huang, J.-X., An, J.-D. (2017) Bear wasps of the Middle Kingdom: a decade of discovering China's bumblebees. Antenna 41(1): 21–24.Google Scholar
  51. Zhang, J., Kapli, P., Pavlidis, P., Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22): 2869–2876.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory for Insect-Pollinator Biology of the Ministry of Agriculture and Rural Affairs, Institute of Apicultural ResearchChinese Academy of Agricultural SciencesBeijingChina
  2. 2.Gansu Institute of ApicultureTianshuiChina

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