Skip to main content

Landscape Structure of Flowering Phenology in Alpine Ecosystems: Significance of Plant–Pollinator Interactions and Evolutionary Aspects

  • Chapter
  • First Online:
Structure and Function of Mountain Ecosystems in Japan

Part of the book series: Ecological Research Monographs ((ECOLOGICAL))

Abstract

Spatiotemporal variation in flowering phenology at community scale is an important structure in alpine ecosystems. The composition of flowering species at a regional scale changes drastically on a weekly scale during the short summer. In early snowmelt year, flowering more often overlapped among species, and the whole flowering period was shorter than in usual year. The major pollinators in Japanese alpine ecosystems are flies and bees. Approximately 50 % and 30 % of insect-pollinated plant species were predominantly visited by flies and bees, respectively. Bee-pollinated flowers showed a dispersed flowering pattern in which anthesis of early bloomers corresponded with the active period of queen bumblebees, while that of late bloomers with the active period of worker bumblebees. Fly-pollinated flowers showed a peak in their flowering in the middle of the season when the ambient temperature was high. In an extremely warm summer, the flowering season finished earlier, and the synchrony of flowers and pollinators was disrupted because the life cycle of bees did not keep pace with the rapid progression of the flowering season. This phenological mismatch suggested a fragile relationship between plants and bees. Phenological isolation of pollen-mediated gene flow between local plant populations caused a spatial genetic structure within a local area. The restriction of gene flow could accelerate local adaptation. Because pollinator activity often increased as the season progressed, both fruit-set success and outcrossing rate increased in populations in late-snowmelt habitats. Such variations in reproductive success may cause life history variation at the local scale.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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 

  • Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate Andes of central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97

    Article  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. Proc Natl Acad Sci U S A 108:20645–20649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beekman M, van Stratum P, Lingeman R (1998) Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entomol 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 

  • Billings WD, Bliss LC (1959) An alpine snowbank environment and its effects on vegetation, plant development, and productivity. Ecology 40:388–397

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bischofe M, Campbell DR, Lord JM, Robertson AW (2013) The relative importance of solitary bees and syrphid flies as pollinators of two outcrossing plant species in the New Zealand alpine. Austral Ecol 38:169–176

    Article  Google Scholar 

  • Buehler D, Graf R, Holderegger R, Gugerli (2012) Contemporary gene flow and mating system of Arabis alpina in a central European alpine landscape. Ann Bot 109:1359–1367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615

    Article  CAS  PubMed  Google Scholar 

  • Campbell DR, Bischoff M, Lord JM, Robertson AW (2010) Flower color influences insect visitation in alpine New Zealand. Ecology 91:2638–2649

    Article  PubMed  Google Scholar 

  • Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439

    Article  PubMed  Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • Forrest JRK (2015) Plant-pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations? Oikos 124:4–13

    Article  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 

  • Galen C, Stanton ML (1991) Consequences of emergence phenology for reproductive success in Ranunculus adoneus (Ranunculaceae). Am J Bot 78:978–988

    Article  Google Scholar 

  • Gordo O, Sanz JJ (2006) 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 Entomol 31:261–268

    Article  Google Scholar 

  • Goulson D, Wright NP (1998) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav Ecol 9:213–219

    Article  Google Scholar 

  • Heegaard E (2002) A model of alpine species distribution in relation to snowmelt time and altitude. J Veg Sci 13:493–504

    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 (1975) Bee flowers: a hypothesis on flower variety and blooming times. Evolution 29:325–334

    Article  Google Scholar 

  • Heinrich B (1976) The foraging specializations of individual bumblebees. Ecol Monogr 46:105–128

    Article  Google Scholar 

  • Hirao AS, Kudo G (2004) Landscape genetics of alpine-snowbed plants: comparisons along geographic and snowmelt gradients. Heredity 93:290–298

    Article  CAS  PubMed  Google Scholar 

  • Hirao AS, Kudo G (2008) The effect of segregation of flowering time on fine-scale spatial genetic structure in an alpine-snowbed herb Primula cuneifolia. Heredity 100:424–430

    Article  CAS  PubMed  Google Scholar 

  • Hirao AS, Kameyama Y, Ohara M, Isagi Y, Kudo G (2006) Seasonal changes in pollinator activity influence the pollen dispersal and seed production of the alpine shrub Rhododendron aureum (Ericaceae). Mol Ecol 15:1165–1173

    Article  CAS  PubMed  Google Scholar 

  • Holway JG, Ward RT (1965) Phenology of alpine plants in northern Colorado. Ecology 46:73–83

    Article  Google Scholar 

  • Høye TT, Post E, Schmidt NM, Trøjelsgaard K, Forchhammer MC (2013) Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nat Clim Chang 3:759–763

    Article  Google Scholar 

  • Huelber K, Gottfried M, Pauli H, Reiter K, Winkler M, Grabherr G (2006) Phenological responses of snowbed species to snow removal dates in the central Alps: implications for climate warming. Arct Antarct Alp Res 38:99–103

    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 Chang Biol 19:2348–2359

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ishii HS (2005) Analysis of bumblebee visitation sequences within single bouts: implication of the overstrike effect on short-term memory. Behav Ecol Sociobiol 57:599–610

    Article  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  PubMed Central  Google Scholar 

  • Kameyama Y, Kasagi T, Kudo G (2008) A hybrid zone dominated by fertile F1s of two alpine shrub species, Phyllodoce caerulea and Phyllodoce aleutica, along a snowmelt gradient. J Evol Biol 21:588–597

    Article  CAS  PubMed  Google Scholar 

  • Kawai Y, Kudo G (2011) Local differentiation of flowering phenology in an alpine-snowbed herb Gentiana nipponica. Botany 89:361–367

    Article  Google Scholar 

  • Kearns CA (1992) Anthophilous fly distribution across an elevation gradient. Am Midl Nat 127:172–182

    Article  Google Scholar 

  • Kearns CA, Inouye DW (1994) Fly pollination of Linum lewisii (Linaceae). Am J Bot 81:1091–1095

    Article  Google Scholar 

  • Kevan PG, Baker HG (1983) Insects as flower visitors and pollinators. Ann Rev Entomol 28:407–453

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Kudo G (1993) Relationship between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches. Am J Bot 80:1300–1304

    Article  Google Scholar 

  • Kudo G (2014) Vulnerability of phenological synchrony between plants and pollinators in an alpine ecosystem. Ecol Res 29:571–581

    Article  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 94:2311–2320

    Article  PubMed  Google Scholar 

  • Kudo G, Ito K (1992) Plant distribution in relation to the length of the growing season in a snow-bed in the Taisetsu Mountains, northern Japan. Vegetatio 98:165–174

    Article  Google Scholar 

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

    Google Scholar 

  • Kudo G, Suzuki S (2001) Relationship between flowering phenology and fruit-set of dwarf shrubs in alpine fellfields in northern Japan: a comparison with a subarctic heathland in northern Sweden. Arct Antarct 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 Constr Ecol 17:49–62 (in Japanese with English summary)

    Google Scholar 

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

    Article  Google Scholar 

  • Larson BMH, Kevan PG, Inouye DW (2001) Flies and flowers: taxonomic diversity of anthophiles and pollinators. Can Entomol 133:439–465

    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 PC (1982) Environmental and vegetational variation across a snow accumulation area in montane tundra in central Alaska. Holarct Ecol 5:85–98

    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  PubMed Central  Google Scholar 

  • Moeller DA (2004) Facilitative interactions among plants via shared pollinators. Ecology 85:3289–3301

    Article  Google Scholar 

  • Molau U (1993) Relationships between flowering phenology and life history strategies in tundra plants. Arct Alp Res 25:391–402

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Oberbauer SF, Elmendorf SC, Troxler TG et al (2013) Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment. Phil Trans R Soc B 368:20120481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Ann Bot 103:1471–1480

    Article  PubMed  PubMed Central  Google Scholar 

  • Ovaskainen O, Skorokhodova S, Yakovleva M et al (2013) Community-level phenological response to climate change. Proc Natl Acad Sci U S A 110:13434–13439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Pauli H, Gottfried M, Reiter K, Klettner C, Grabherr G (2007) Signals of range expansion and contributions of vascular plants in the high Alps: observations (1994–2004) at the GLORIA master site Schrankogel, Tyrol, Austria. Glob Chang Biol 13:147–156

    Article  Google Scholar 

  • Pleasants JM (1980) Competition for bumblebee pollinators in rocky mountain plant communities. Ecology 61:1446–1459

    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 

  • Rathcke B (1993) Competition and facilitation among plants for pollination. In: Real L (ed) Pollination biology. Academic, Orlando, pp 305–325

    Google Scholar 

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Ann Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • Rixen C, Dawes MA, Wipf S, Hagedorn F (2012) Evidence of enhanced freezing damage in treeline plants during six 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 

  • Schöb C, Kammer PM, Choler P, Veit H (2009) Small-scale plant species distribution in snowbeds and its sensitivity to climate change. Plant Ecol 200:53–66

    Article  Google Scholar 

  • Shimono Y, Kudo G (2003) Intraspecific variations in seedling emergence and survival of Potentilla matsumurae (Rosaceae) between alpine fellfield and snowbed habitats. Ann Bot 91:21–29

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimono Y, Watanabe M, Hirao AS, Wada N, Kudo G (2009) Morphological and genetic variations of Potentilla matsumurae (Rosaceae) between fellfield and snowbed populations. Am J Bot 96:728–737

    Article  PubMed  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Totland Ø (1993) Pollination in alpine Norway: flowering phenology, insect visitors, and visitation rates in two plant communities. Can J Bot 71:1072–1079

    Article  Google Scholar 

  • Totland Ø (1994) Influence of climate, time of day and season, and flower density on insect flower visitation in alpine Norway. Arct Alp Res 26:66–71

    Article  Google Scholar 

  • Waser NM (1986) Flower constancy: definition, cause and measurement. Am Nat 127:593–603

    Article  Google Scholar 

  • Wheeler JA, Hoch G, Cortés AJ, Sedlacek J, Wipf S, Rixen C (2014) Increased spring freezing vulnerability for alpine shrubs under early snowmelt. Oecologia 175:219–229

    Article  CAS  PubMed  Google Scholar 

  • Wilson P, Stine M (1996) Floral constancy in bumble bees: handling efficiency or perceptual conditioning? Oecologia 106:493–499

    Article  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 

  • Ye Z-M, Dai W-K, Jin X-F, Gituru RW, Wang Q-F, Yang C-F (2014) Competition and facilitation among plants for pollination: can pollinator abundance shift the plant-plant interactions? Plant Ecol 215:3–13

    Article  Google Scholar 

  • Yumoto T (1986) The ecological pollination syndromes of insect-pollinated plants in an alpine meadow. Ecol Res 1:83–95

    Article  Google Scholar 

Download references

Acknowledgements

I am grateful to Yuka Kawai, Yukihiro Amagai, and Yuki Mizunaga for their support in field surveys, Hiroshi Ishii for offering data of pollinator assemblages on Mt. Tateyama, and Takao Itino for comments on an early version of the manuscript. This study was funded by the Global Environmental Research Fund of the Ministry of the Environment, Japan (F-092 and D-0904) and by JSPS KAKENHI (23405006, 24570015).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gaku Kudo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Japan

About this chapter

Cite this chapter

Kudo, G. (2016). Landscape Structure of Flowering Phenology in Alpine Ecosystems: Significance of Plant–Pollinator Interactions and Evolutionary Aspects. In: Kudo, G. (eds) Structure and Function of Mountain Ecosystems in Japan. Ecological Research Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55954-2_3

Download citation

Publish with us

Policies and ethics