Ecological Research

, Volume 29, Issue 4, pp 571–581 | Cite as

Vulnerability of phenological synchrony between plants and pollinators in an alpine ecosystem

  • Gaku KudoEmail author
Special Feature Winter Climate Change


The relationship between flowering phenology and abundance of bumble bees (Bombus spp.) was investigated using 2 years of phenological data collected in an alpine region of northern Japan. Abundance of Bombus species was observed along a fixed transect throughout the flowering season. The number of flowering species was closely related to the floral resources for pollinators at the community scale. In the year with typical weather, the first flowering peak corresponded to the emergence time of queen bees from hibernation, while the second flowering peak corresponded to the active period of worker bees. In the year with an unusually warm spring, however, phenological synchrony between plants and bees was disrupted. Estimated emergence of queen bees was 10 days earlier than the first flowering date owing to earlier soil thawing and warming. However, subsequent worker emergence was delayed, indicating slower colony development. The flowering season finished 2 weeks earlier in the warm-spring year in response to earlier snowmelt. A common resident species in the alpine environment, B. hypocrita sapporoensis, flexibly responded to the yearly fluctuation of flowering. In contrast, population dynamics of other Bombus species were out of synchrony with the flowering: their frequencies were highest at the end of the flowering season in the warm-spring year. Therefore, phenological mismatch between flowers and pollinators is evident during warm years, which may become more prevalent in a warmer climate. To understand the mechanism of phenological mismatch in the pollination system of the alpine ecosystem, ground temperature, snowmelt regime, and life cycle of pollinators are key factors.


Alpine plants Bumble bee Flowering phenology Phenological mismatch Temperature 



This study was conducted as Monitoring Sites 1000 Project of Ministry of the Environment, Japan. I appreciate the members of Flower Research Volunteer and Tetsuo Imoto for their great effort for data collection of flowering phenology and bee observations. I am also grateful to Yuka Kawai and Yukihiro Amagai for their help in fieldwork on Mt. Kaun, David Inouye and Jordan Sinclair for their editorial help, and two anonymous reviewers for their valuable comments. This study was partly supported by a Grant-In-Aid from the Japan Society for the Promotion of Science (23405006, 24570015).


  1. Aldridge G, Inouye DW, Forrest JRK, Barr WA, Miller-Rushing J (2011) Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J Ecol 99:905–913CrossRefGoogle Scholar
  2. Alford DV (1969) A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in southern England. J Anim Ecol 38:149–170CrossRefGoogle Scholar
  3. Amin MR, Suh SJ, Kwon YJ (2007) Impact of artificial photoperiodism on the colony development of the bumblebee Bombus terrestris. Ecol Sci 10:315–321Google Scholar
  4. Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. PNAS 108:20645–20649PubMedCentralPubMedCrossRefGoogle Scholar
  5. Beekman M, van Stratum P, Lingeman R (1998) Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entmol Exp Appl 89:207–214CrossRefGoogle Scholar
  6. Bergman P, Molau U, Holmgren B (1996) Micrometeorological impacts on insect activity and plant reproductive success in an alpine environment, Swedish lapland. Arct Alp Res 28:196–202CrossRefGoogle Scholar
  7. Bingham RA (1998) Efficient pollination of alpine plants. Nature 391:238–239CrossRefGoogle Scholar
  8. Diekmann M (1996) Relationship between flowering phenology of perennial herbs and meteorological data in deciduous forests of Sweden. Can J Bot 74:528–537CrossRefGoogle Scholar
  9. Ellwood ER, Diez JM, Ibáñez I, Primack RB, Kobori H, Higuchi H, Silander JA (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168:1161–1171PubMedCrossRefGoogle Scholar
  10. Fitter ML, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691PubMedCrossRefGoogle Scholar
  11. Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky mountain meadows. Ecol Monogr 81:469–491CrossRefGoogle Scholar
  12. Gordo O, Sanz JJ (2003) Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecol Entmol 31:261–268CrossRefGoogle Scholar
  13. Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland Ø (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195PubMedCrossRefGoogle Scholar
  14. Heinrich B (1979) Bumblebee economics. Harvard University Press, CambridgeGoogle Scholar
  15. Høye TT, Forchhammer MC (2008) Phenology of high-arctic arthropods: effects of climate on spatial, seasonal, and inter-annual variation. Adv Ecol Res 40:299–324CrossRefGoogle Scholar
  16. Hülber K, Winkler M, Grabherr G (2010) Intra-seasonal climate and habitat-specific variability controls the flowering phenology of high alpine plant species. Funct Ecol 24:245–252CrossRefGoogle Scholar
  17. Iler AM, Inouye DW, Høye TT, Miller-Rushing AJ, Burkle LA, Johnston EB (2013) Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Glob Change Biol 19:2348–2359CrossRefGoogle Scholar
  18. Inouye DW (2008) Effect of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362PubMedCrossRefGoogle Scholar
  19. Kameyama Y, Kudo G (2009) Flowering phenology influences seed production and outcrossing rate in populations of an alpine snowbed shrub, Phyllodoce aleutica: effects of pollinators and self-incompatibility. Ann Bot 103:1385–1394PubMedCentralPubMedCrossRefGoogle Scholar
  20. Kudo G (1991) Effects of snow-free period on the phenology of alpine plants inhabiting snow patches. Arc Alp Res 23:436–443CrossRefGoogle Scholar
  21. Kudo G (2006) Flowering phenologies of animal–pollinated plants: reproductive strategies and agents of selection. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, New York, pp 139–158Google Scholar
  22. Kudo G, Hirao AS (2006) Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts. Popul Ecol 48:49–58CrossRefGoogle Scholar
  23. Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology (in press)Google Scholar
  24. Kudo G, Imoto T (2012) Monitoring of bumblebee assemblages in the alpine zone of Daisetsuzan national park. Jap J Cons Ecol 17:263–269 (in Japanese with English summary)Google Scholar
  25. Kudo G, Suzuki S (1999) Flowering phenology of alpine plant communities along a gradient of snowmelt timing. Polar Biosci 12:100–113Google Scholar
  26. Kudo G, Suzuki S (2002) Relationships between flowering phenology and fruit-set of dwarf shrubs in alpine fellfields in northern Japan: a comparison with a subarctic heathland in northern Sweden. Arc Antarc Alp Res 34:185–190CrossRefGoogle Scholar
  27. Kudo G, Yokosuka K (2012) Spatiotemporal variations in flowering phenologies of alpine plant communities: long-term volunteer monitoring in an alpine ecosystem. Jpn J Cons Ecol 17:49–62 (in Japanese with English summary)Google Scholar
  28. Kudo G, Hirao AS, Kawai Y (2011) Pollination efficiency of bumblebee queens and workers in the alpine shrub Rhododendron aureum. Int J Plant Sci 172:70–77CrossRefGoogle Scholar
  29. McKinney AM, Caradonna PJ, Inouye DW, Barr B, Bertelsen CD, Waser NM (2012) Asynchronous changes in phenology of migrating broad-tailed hummingbirds and their early season nectar resources. Ecology 93:1987–1993PubMedCrossRefGoogle Scholar
  30. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717PubMedCrossRefGoogle Scholar
  31. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Phil Trans R Soc B 365:3177–3186PubMedCentralPubMedCrossRefGoogle Scholar
  32. Mote PW, Hamlet AF, Clark MP, Lettenmaier DP (2005) Declining mountain snowpack in western North America. Bull Am Meteor Soc 86:39–49CrossRefGoogle Scholar
  33. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872CrossRefGoogle Scholar
  34. Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant–pollinator interactions. Ecol Lett 14:69–74PubMedCrossRefGoogle Scholar
  35. Rixen C, Dawes MA, Wipf S, Hagedorn F (2012) Evidence of enhanced freezing damage in treeline plants during 6 years of CO2 enrichment and soil warming. Oikos 121:1532–1543CrossRefGoogle Scholar
  36. Root TL, Price JF, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming in wild animals and plants. Nature 421:57–60PubMedCrossRefGoogle Scholar
  37. Schmid-Hempel P, Durrer S (1991) Parasites, floral resources and reproduction in natural populations of bumblebees. Oikos 62:343–350CrossRefGoogle Scholar
  38. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna,
  39. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Phil Trans R Soc B 365:3187–3199PubMedCentralPubMedCrossRefGoogle Scholar
  40. Wipf S (2010) Phenology, growth, and fecundity of eight subarctic tundra species in response to snowmelt manipulations. Plant Ecol 207:53–66CrossRefGoogle Scholar
  41. Yoon HJ, Kim SE, Kim YS (2002) Temperature and humidity favorable for colony development of the indoor-reared bumblebee, Bombus ignites. App Entomol Zool 37:419–423CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2013

Authors and Affiliations

  1. 1.Faculty of Environmental Earth ScienceHokkaido UniversitySapporoJapan

Personalised recommendations