, Volume 178, Issue 1, pp 249–260 | Cite as

Fruitful factors: what limits seed production of flowering plants in the alpine?

  • Jason R. StrakaEmail author
  • Brian M. Starzomski
Community ecology - Original research


Predicting demographic consequences of climate change for plant communities requires understanding which factors influence seed set, and how climate change may alter those factors. To determine the effects of pollen availability, temperature, and pollinators on seed production in the alpine, we combined pollen-manipulation experiments with measurements of variation in temperature, and abundance and diversity of potential pollinators along a 400-m elevation gradient. We did this for seven dominant species of flowering plants in the Coast Range Mountains, British Columbia, Canada. The number of viable seeds set by plants was influenced by pollen limitation (quantity of pollen received), mate limitation (quality of pollen), temperature, abundance of potential pollinators, seed predation, and combinations of these factors. Early flowering species (n = 3) had higher seed set at high elevation and late-flowering species (n = 4) had higher seed set at low elevation. Degree-days >15 °C were good predictors of seed set, particularly in bee-pollinated species, but had inconsistent effects among species. Seed production in one species, Arnica latifolia, was negatively affected by seed-predators (Tephritidae) at mid elevation, where there were fewer frost-hours during the flowering season. Anemone occidentalis, a fly-pollinated, self-compatible species had high seed set at all elevations, likely due to abundant potential pollinators. Simultaneously measuring multiple factors affecting reproductive success of flowering plants helped identify which factors were most important, providing focus for future studies. Our work suggests that responses of plant communities to climate change may be mediated by flowering time, pollination syndrome, and susceptibility to seed predators.


Phenology Reproduction Pollination Pollen limitation Climate change 



Funding was provided by the Natural Sciences and Engineering Research Council of Canada, the Pacific Institute for Climate Solutions, and the University of Victoria. Two anonymous reviewers provided comments that greatly improved the manuscript. We thank Luise Hermanutz, Andrew Trant, Kimberly Carlson, Kira Hoffman, and Katharine Baldwin-Corriveau for comments on earlier versions. Andrew Sheriff and Erika Dort were instrumental in completing the field work. The experiments comply with the current laws of the country (Canada) in which the experiments were performed.

Supplementary material

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  1. Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421. doi: 10.1890/03-8024 CrossRefGoogle Scholar
  2. Barnett DT, Stohlgren TJ (2003) A nested-intensity design for surveying plant diversity. Biodivers Conserv 12:255–278. doi: 10.1023/A:1021939010065 CrossRefGoogle Scholar
  3. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349. doi: 10.2307/1942268 CrossRefGoogle Scholar
  4. Brosi BJ, Briggs HM (2013) Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc Natl Acad Sci 110(13044):13048. doi: 10.1073/pnas.1307438110 Google Scholar
  5. Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139. doi: 10.1007/BF02856594 CrossRefGoogle Scholar
  6. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  7. Cooper EJ, Dullinger S, Semenchuk P (2011) Late snowmelt delays plant development and results in lower reproductive success in the high Arctic. Plant Sci 180:157–167. doi: 10.1016/j.plantsci.2010.09.005 CrossRefPubMedGoogle Scholar
  8. Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. Enviroquest, CambridgeGoogle Scholar
  9. Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects: and on the good effects of intercrossing. Murray, LondonGoogle Scholar
  10. Droege S, Tepedino VJ, Lebuhn G, Link W, Minckley RL, Chen Q, Conrad C (2010) Spatial patterns of bee captures in North American bowl trapping surveys. Insect Conserv Divers 3:15–23. doi: 10.1111/j.1752-4598.2009.00074.x CrossRefGoogle Scholar
  11. Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86. doi: 10.1890/0012-9615(2003)073%5B0069:SMFPRT%5D2.0.CO;2 CrossRefGoogle Scholar
  12. Ehrlén J (1992) Proximate limits to seed production in a herbaceous perennial legume, Lathyrus vernus. Ecology 73:1820–1831. doi: 10.2307/1940033 CrossRefGoogle Scholar
  13. Fabbro T, Körner C (2004) Altitudinal differences in flower traits and reproductive allocation. Flora Morphol Distrib Funct Ecol Plants 199:70–81. doi: 10.1078/0367-2530-00128 CrossRefGoogle Scholar
  14. Forrest J (2011) Plant-pollinator interactions in a changing climate. PhD dissertation, Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, CanadaGoogle Scholar
  15. Forrest J, Thomson JD (2009) Pollinator experience, neophobia and the evolution of flowering time. Proc R Soc B 276:935–943. doi: 10.1098/rspb.2008.1434 CrossRefPubMedCentralPubMedGoogle Scholar
  16. Forrest J, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491. doi: 10.1890/10-1885.1 CrossRefGoogle Scholar
  17. Galen C, Stanton ML (1993) Short-term responses of alpine buttercups to experimental manipulations of growing season length. Ecology 74(4):1052–1058 doi: 10.2307/1940475
  18. García-Camacho R, Totland Ø (2009) Pollen limitation in the alpine: a meta-analysis. Arct Antarct Alp Res 41:103–111. doi: 10.1657/1523-0430-41.1.103 CrossRefGoogle Scholar
  19. Gutierrez A, Ponti L, d’Oultremont T, Ellis C (2008) Climate change effects on poikilotherm tritrophic interactions. Clim Change 87:167–192. doi: 10.1007/s10584-007-9379-4 CrossRefGoogle Scholar
  20. Haig D, Westoby M (1988) On limits to seed production. Am Nat 131:757–759. Article Stable:
  21. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. doi: 10.1890/00129658(1999)080%5B1150:TMAORR%5D2.0.CO2 CrossRefGoogle Scholar
  22. Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195. doi: 10.1111/j.14610248.2008.01269.x CrossRefPubMedGoogle Scholar
  23. Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513. doi: 10.1017/S1464793105006767 CrossRefPubMedGoogle Scholar
  24. Hothorn T, Zeileis A, Millo G, Mitchell D (2012) lmtest: testing linear regression models. R project.orgGoogle Scholar
  25. Hülber K, Winkler M, Grabherr G (2010) Intraseasonal climate and habitat-specific variability controls the flowering phenology of high alpine plant species. Funct Ecol 24:245–252. doi: 10.1111/j.1365-2435.2009.01645.x CrossRefGoogle Scholar
  26. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362. doi: 10.1890/06-2128.1 CrossRefPubMedGoogle Scholar
  27. Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. PNAS 97:1630–1633. doi: 10.1073/pnas.97.4.1630 CrossRefPubMedCentralPubMedGoogle Scholar
  28. Inouye D, Morales M, Dodge G (2002) Variation in timing and abundance of flowering by Delphinium barbeyi; Huth (Ranunculaceae): the roles of snowpack, frost, and La Niña, in the context of climate change. Oecologia 130:543–550. doi: 10.1007/s00442-001-0835-y CrossRefGoogle Scholar
  29. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  30. Kearns CA, Inouye DW (1994) Fly pollination of Linum lewisii (Linaceae). Am J Bot 81:1091–1095. doi: 10.2307/2445470 CrossRefGoogle Scholar
  31. Knight TM, Steets JA, Vamosi JC, et al. (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497. doi: 10.1146/annurev.ecolsys.36.102403.115320 CrossRefGoogle Scholar
  32. Krebs CJ, Boonstra R, Cowcill K, Kenney AJ (2009) Climatic determinants of berry crops in the boreal forest of the southwestern Yukon. Botany 87:401–408. doi: 10.1139/B09-013 CrossRefGoogle Scholar
  33. Kudo G, Hirao A (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. doi: 10.1007/s10144-005-0242-z CrossRefGoogle Scholar
  34. Kudo G, Nishikawa Y, Kasagi T, Kosuge S (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecol Res 19:255–259. doi: 10.1111/j.14401703.2003.00630.x CrossRefGoogle Scholar
  35. Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520. doi: 10.1111/j.10958312.2000.tb01221.x CrossRefGoogle Scholar
  36. Lee TD, Bazzaz FA (1982) Regulation of fruit and seed production in an annual legume, Cassia fasciculata. Ecology 63:1363–1373. doi: 10.2307/1938864 CrossRefGoogle Scholar
  37. Marshall SA (2006) Insects: their natural history and diversity: with a photographic guide to insects of eastern North America. Firefly, BuffaloGoogle Scholar
  38. McCall C, Primack RB (1992) Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am J Bot 79:434–442. doi: 10.2307/2445156 CrossRefGoogle Scholar
  39. Motten AF (1986) Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecol Monogr 56:21–42. doi: 10.2307/2937269 CrossRefGoogle Scholar
  40. Pojar J (1974) Reproductive dynamics of four plant communities of southwestern British Columbia. Can J Bot 52:1819–1834. doi: 10.1139/b74-234 CrossRefGoogle Scholar
  41. Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79:1261–1271. doi: 10.2307/176741 CrossRefGoogle Scholar
  42. Rafferty NE, Ives AR (2012) Pollinator effectiveness varies with experimental shifts in flowering time. Ecology 93:803–814. doi: 10.1890/11-0967.1 CrossRefPubMedCentralPubMedGoogle Scholar
  43. Rafferty NE, CaraDonna PJ, Burkle LA, et al. (2013) Phenological overlap of interacting species in a changing climate: an assessment of available approaches. Ecol Evol 3:3183–3193. doi: 10.1002/ece3.668 CrossRefPubMedCentralPubMedGoogle Scholar
  44. Scheidel U, Röhl S, Bruelheide H (2003) Altitudinal gradients of generalist and specialist herbivory on three montane Asteraceae. Acta Oecol 24:275–283. doi: 10.1016/j.actao.2003.09.004 CrossRefGoogle Scholar
  45. Schemske DW (1977) Flowering phenology and seed set in Claytonia virginica (Portulacaceae). Bull Torrey Bot Club 104:254–263. doi: 10.2307/2484307 CrossRefGoogle Scholar
  46. Straka JR, Starzomski BM (2014) Humming along or buzzing off? The elusive consequences of plant-pollinator mismatches. J Pollinat Ecol [Suppll] 13, Available at:
  47. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos Trans R Soc B Biol Sci 365:3187–3199. doi: 10.1098/rstb.2010.0115 CrossRefGoogle Scholar
  48. Thórhallsdóttir TE (1998) Flowering phenology in the central highland of Iceland and implications for climatic warming in the Arctic. Oecologia 114:43–49. doi: 10.1007/s004420050418 CrossRefGoogle Scholar
  49. 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. doi: 10.2307/1551879 CrossRefGoogle Scholar
  50. Totland Ø (1997) Limitations on reproduction in alpine Ranunculus acris. Can J Bot 75:137–144. doi: 10.1139/b97-016 CrossRefGoogle Scholar
  51. Totland Ø (2001) Environment-dependent pollen limitation and selection on floral traits in an alpine species. Ecology 82:2233–2244. doi: 10.2307/2680228 CrossRefGoogle Scholar
  52. Triplehorn CA, Johnson NF, Borror DJ (2005) Borror and DeLong’s introduction to the study of insects. Thompson Brooks/Cole, BelmontGoogle Scholar
  53. Vander Kloet SP (1988) The genus Vaccinium in North America. Research Branch Agriculture Canada, OttawaGoogle Scholar
  54. Vuong QH (1989) Likelihood ratio tests for model selection and non-nested hypotheses. Econometrica 57:307–333. doi: 10.2307/1912557 CrossRefGoogle Scholar
  55. Willmer P (2012) Ecology: pollinator–plant synchrony tested by climate change. Curr Biol 22:R131–R132. doi: 10.1016/j.cub.2012.01.009 CrossRefPubMedGoogle Scholar
  56. Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Environmental StudiesUniversity of VictoriaVictoriaCanada

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