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

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  • Winter Climate Change
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Ecological Research

Abstract

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.

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References

  • 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 99:905–913

    Article  Google Scholar 

  • Alford DV (1969) A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in southern England. J Anim Ecol 38:149–170

    Article  Google Scholar 

  • Amin MR, Suh SJ, Kwon YJ (2007) Impact of artificial photoperiodism on the colony development of the bumblebee Bombus terrestris. Ecol Sci 10:315–321

    Google Scholar 

  • 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 108:20645–20649

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beekman M, van Stratum P, Lingeman R (1998) Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entmol Exp Appl 89:207–214

    Article  Google Scholar 

  • 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 28:196–202

    Article  Google Scholar 

  • Bingham RA (1998) Efficient pollination of alpine plants. Nature 391:238–239

    Article  Google Scholar 

  • Diekmann M (1996) Relationship between flowering phenology of perennial herbs and meteorological data in deciduous forests of Sweden. Can J Bot 74:528–537

    Article  Google Scholar 

  • 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 168:1161–1171

    Article  PubMed  Google Scholar 

  • Fitter ML, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691

    Article  CAS  PubMed  Google Scholar 

  • Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky mountain meadows. Ecol Monogr 81:469–491

    Article  Google Scholar 

  • 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 31:261–268

    Article  Google Scholar 

  • Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland Ø (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195

    Article  PubMed  Google Scholar 

  • Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge

    Google Scholar 

  • Høye TT, Forchhammer MC (2008) Phenology of high-arctic arthropods: effects of climate on spatial, seasonal, and inter-annual variation. Adv Ecol Res 40:299–324

    Article  Google Scholar 

  • 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 24:245–252

    Article  Google Scholar 

  • 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 19:2348–2359

    Article  Google Scholar 

  • Inouye DW (2008) Effect of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362

    Article  PubMed  Google Scholar 

  • 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 103:1385–1394

    Article  PubMed Central  PubMed  Google Scholar 

  • Kudo G (1991) Effects of snow-free period on the phenology of alpine plants inhabiting snow patches. Arc Alp Res 23:436–443

    Article  Google Scholar 

  • 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 139–158

    Google Scholar 

  • 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 48:49–58

    Article  Google Scholar 

  • Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology (in press)

  • 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 

  • Kudo G, Suzuki S (1999) Flowering phenology of alpine plant communities along a gradient of snowmelt timing. Polar Biosci 12:100–113

    Google Scholar 

  • 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 34:185–190

    Article  Google Scholar 

  • 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 

  • Kudo G, Hirao AS, Kawai Y (2011) Pollination efficiency of bumblebee queens and workers in the alpine shrub Rhododendron aureum. Int J Plant Sci 172:70–77

    Article  Google Scholar 

  • 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 93:1987–1993

    Article  PubMed  Google Scholar 

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717

    Article  PubMed  Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Phil Trans R Soc B 365:3177–3186

    Article  PubMed Central  PubMed  Google Scholar 

  • Mote PW, Hamlet AF, Clark MP, Lettenmaier DP (2005) Declining mountain snowpack in western North America. Bull Am Meteor Soc 86:39–49

    Article  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872

    Article  Google Scholar 

  • Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant–pollinator interactions. Ecol Lett 14:69–74

    Article  PubMed  Google Scholar 

  • 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 121:1532–1543

    Article  Google Scholar 

  • Root TL, Price JF, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming in wild animals and plants. Nature 421:57–60

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P, Durrer S (1991) Parasites, floral resources and reproduction in natural populations of bumblebees. Oikos 62:343–350

    Article  Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, http://www.R-progect.org

  • Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Phil Trans R Soc B 365:3187–3199

    Article  PubMed Central  PubMed  Google Scholar 

  • Wipf S (2010) Phenology, growth, and fecundity of eight subarctic tundra species in response to snowmelt manipulations. Plant Ecol 207:53–66

    Article  Google Scholar 

  • Yoon HJ, Kim SE, Kim YS (2002) Temperature and humidity favorable for colony development of the indoor-reared bumblebee, Bombus ignites. App Entomol Zool 37:419–423

    Article  Google Scholar 

Download references

Acknowledgments

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).

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  1. Faculty of Environmental Earth Science, Hokkaido University, Sapporo, 060-0810, Japan

    Gaku Kudo

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Correspondence to Gaku Kudo.

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Kudo, G. Vulnerability of phenological synchrony between plants and pollinators in an alpine ecosystem. Ecol Res 29, 571–581 (2014). https://doi.org/10.1007/s11284-013-1108-z

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  • DOI: https://doi.org/10.1007/s11284-013-1108-z

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