Temperature variability drives within-species variation in germination strategy and establishment characteristics of an alpine herb

Abstract

Plant establishment and subsequent persistence are strongly influenced by germination strategy, especially in temporally and spatially heterogeneous environments. Germination strategy determines the plant’s ability to synchronise germination timing and seedling emergence to a favourable growing season and thus variation in germination strategy within species may be key to persistence under more extreme and variable future climates. However, the determinants of variation in germination strategy are not well resolved. To understand the variation of germination strategy and the climate drivers, we assessed seed traits, germination patterns, and seedling establishment traits of Oreomyrrhis eriopoda from 29 populations across its range. Germination patterns were then analysed against climate data to determine the strongest climate correlates influencing the germination strategy. Oreomyrrhis eriopoda exhibits a striking range of germination strategies among populations: varying from immediate to staggered, postponed, and postponed-deep. Seeds from regions with lower temperature variability were more likely to exhibit an immediate germination strategy; however, those patterns depended on the timescale of climatic assessment. In addition, we show that these strategy differences extend to seedling establishment traits: autumn seedlings (from populations with an immediate or staggered germination strategy) exhibited a higher leaf production rate than spring seedlings (of staggered or postponed strategy). Our results demonstrate not only substantial within-species variation in germination strategy across the species distribution range, but also that this variation correlates with environmental drivers. Given that these differences also extend to establishment traits, they may reflect a critical mechanism for persistence in changing climate.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Andersson L, Milberg P (1998) Variation in seed dormancy among mother plants, populations and years of seed collection. Seed Sci Res 8:29–38. https://doi.org/10.1017/s0960258500003883

    Article  Google Scholar 

  2. Barclay AM, Crawford RMM (1984) Seedling emergence in the Rowan (Sorbus aucuparia) from an altitudinal gradient. J Ecol 72:627–636. https://doi.org/10.2307/2260072

    Article  Google Scholar 

  3. Barga S, Dilts TE, Leger EA (2017) Climate variability affects the germination strategies exhibited by arid land plants. Oecologia 185:437–452. https://doi.org/10.1007/s00442-017-3958-5

    Article  PubMed  Google Scholar 

  4. Baskin C, Baskin J (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination. Elsevier/Academic Press, San Diego

    Google Scholar 

  5. Beniston M (2003) Climatic change in mountain regions: a review of possible impacts. Clim Change 59:5–31. https://doi.org/10.1023/a:1024458411589

    Article  Google Scholar 

  6. Bernareggi G, Carbognani M, Mondoni A, Petraglia A (2016) Seed dormancy and germination changes of snowbed species under climate warming: the role of pre- and post-dispersal temperatures. Ann Bot 118:529–539. https://doi.org/10.1093/aob/mcw125

    Article  PubMed  PubMed Central  Google Scholar 

  7. Carta A, Probert R, Puglia G, Peruzzi L, Bedini G (2016) Local climate explains degree of seed dormancy in Hypericum elodes L. (Hypericaceae). Plant Biol 18:76–82. https://doi.org/10.1111/plb.12310

    Article  PubMed  Google Scholar 

  8. Cochrane A, Yates CJ, Hoyle GL, Nicotra AB (2015) Will among-population variation in seed traits improve the chance of species persistence under climate change? Global Ecol Biogeogr 24:12–24. https://doi.org/10.1111/geb.12234

    Article  Google Scholar 

  9. Cohen D (1966) Optimizing reproduction in a randomly varying environment. J Theor Biol 12:119–129. https://doi.org/10.1016/0022-5193(66)90188-3

    Article  PubMed  CAS  Google Scholar 

  10. Costin AB, Gray M, Totterdell CJ, Wimbush DJ (2000) Kosciuszko Alpine Flora. CSIRO Publising, Collingwood

    Book  Google Scholar 

  11. Donohue K (2002) Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology 83:1006–1016. https://doi.org/10.1890/0012-9658(2002)083%5b1006:gtinso%5d2.0.co;2

    Article  Google Scholar 

  12. Donohue K (2005) Seeds and seasons: interpreting germination timing in the field. Seed Sci Res 15:175–187

    Article  Google Scholar 

  13. Donohue K et al (2005) The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59:758–770. https://doi.org/10.1111/j.0014-3820.2005.tb01751.x

    Article  PubMed  Google Scholar 

  14. Donohue K et al (2008) Diversification of phytochrome contributions to germination as a function of seed-maturation environment. New Phytol 177:367–379. https://doi.org/10.1111/j.1469-8137.2007.02281.x

    PubMed  Article  Google Scholar 

  15. Fenner M (1991) The effects of the parent environment on seed germinability. Seed Sci Res 1:75–84. https://doi.org/10.1017/s0960258500000696

    Article  Google Scholar 

  16. Fenner M, Thompson K (2005) The Ecology of Seeds. Cambridge University Press, Cambridge

    Book  Google Scholar 

  17. Fernández-Pascual E, Jiménez-Alfaro B, Caujapé-Castells J, Jaén-Molina R, Díaz TE (2013) A local dormancy cline is related to the seed maturation environment, population genetic composition and climate. Ann Bot 112:937–945. https://doi.org/10.1093/aob/mct154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523. https://doi.org/10.2307/4091471

    Article  PubMed  CAS  Google Scholar 

  19. Forbis TA, Floyd SK, de Queiroz A (2002) The evolution of embryo size in angisoperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56:2112–2125. https://doi.org/10.1111/j.0014-3820.2002.tb00137.x

    Article  PubMed  Google Scholar 

  20. Gutterman Y (2000) Maternal effects on seeds during development. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI, Wallingford, pp 59–84

    Google Scholar 

  21. Herman JJ, Sultan SE (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front Plant Sci 2:102. https://doi.org/10.3389/fpls.2011.00102

    Article  PubMed  PubMed Central  Google Scholar 

  22. Honěk A, Martinková Z (1996) Geographic variation in seed dormancy among populations of Echinochloa crus-galli. Oecologia 108:419–423. https://doi.org/10.2307/4221434

    Article  PubMed  Google Scholar 

  23. Hoyle G, Cordiner H, Good RB, Nicotra AB (2014) Effects of reduced winter duration on seed dormancy and germination in six populations of the alpine herb Aciphylla glacialis (Apiaceae). Conserv Physiol 2:cou015. https://doi.org/10.1093/conphys/cou015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Hoyle G, Steadman K, Good R, McIntosh E, Galea L, Nicotra AB (2015) Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits. Front Plant Sci 6:731. https://doi.org/10.3389/fpls.2015.00731

    Article  PubMed  PubMed Central  Google Scholar 

  25. Jobson PK (1999) Oreomyrrhis. In: Walsh NG, Entwisle TJ (eds) Flora of Victoria, vol 4 Cornaceae to Asteraceae. Inkata Press, Melbourne

    Google Scholar 

  26. Kimball S, Angert AL, Huxman TE, Venable DL (2011) Differences in the timing of germination and reproduction relate to growth physiology and population dynamics of Sonoran Desert winter annuals. Am J Bot 98:1773–1781. https://doi.org/10.3732/ajb.1100034

    Article  PubMed  Google Scholar 

  27. Kochanek J, Steadman KJ, Probert RJ, Adkins SW (2011) Parental effects modulate seed longevity: exploring parental and offspring phenotypes to elucidate pre-zygotic environmental influences. New Phytol 191:223–233. https://doi.org/10.1111/j.1469-8137.2011.03681.x

    Article  PubMed  Google Scholar 

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

    Book  Google Scholar 

  29. Lu JJ, Tan DY, Baskin CC, Baskin JM (2016) Effects of germination season on life history traits and on transgenerational plasticity in seed dormancy in a cold desert annual. Sci Rep 6:25076. https://doi.org/10.1038/srep25076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Maruta E (1994) Seedling establishment of Polygonum cuspidatum and Polygonum weyrichii var. alpinum at high altitudes of Mt Fuji. Ecol Res 9:205–213. https://doi.org/10.1007/bf02347496

    Article  Google Scholar 

  31. Mattana E, Stuppy WH, Fraser R, Waller J, Pritchard HW (2014) Dependency of seed dormancy types on embryo traits and environmental conditions in Ribes species. Plant Biol 16:740–747. https://doi.org/10.1111/plb.12115

    Article  PubMed  CAS  Google Scholar 

  32. Mercer KL, Alexander HM, Snow AA (2011) Selection on seedling emergence timing and size in an annual plant, Helianthus annuus (common sunflower, Asteraceae). Am J Bot 98:975–985. https://doi.org/10.3732/ajb.1000408

    Article  PubMed  Google Scholar 

  33. Meyer SE, Kitchen SG (1994) Life history variation in Blue Flax (Linum perenne: linaceae): seed germination phenology. Am J Bot 81:528–535. https://doi.org/10.2307/2445726

    Article  Google Scholar 

  34. Meyer SE, Kitchen SG, Carlson SL (1995) Seed germination timing patterns in intermountain Penstemon (Scrophulariaceae). Am J Bot 82:377–389. https://doi.org/10.2307/2445584

    Article  Google Scholar 

  35. Mondoni A, Rossi G, Orsenigo S, Probert RJ (2012) Climate warming could shift the timing of seed germination in alpine plants. Ann Bot 110:155–164. https://doi.org/10.1093/aob/mcs097

    Article  PubMed  PubMed Central  Google Scholar 

  36. Mondoni A et al (2015) Climate warming could increase recruitment success in glacier foreland plants. Ann Bot 116:907–916. https://doi.org/10.1093/aob/mcv101

    PubMed  PubMed Central  Article  Google Scholar 

  37. Montesinos-Navarro A, Wig J, Xavier Pico F, Tonsor SJ (2011) Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol 189:282–294. https://doi.org/10.1111/j.1469-8137.2010.03479.x

    Article  PubMed  Google Scholar 

  38. Nishitani S, Masuzawa T (1996) Germination characteristics of two species of Polygonum in relation to their altitudinal distribution on Mt. Fuji, Japan. Arct Alp Res 28:104–110. https://doi.org/10.2307/1552092

    Article  Google Scholar 

  39. Parmesan C, Hanley ME (2015) Plants and climate change: complexities and surprises. Ann Bot 116:849–864. https://doi.org/10.1093/aob/mcv169

    Article  PubMed  PubMed Central  Google Scholar 

  40. Parolo G, Rossi G (2008) Upward migration of vascular plants following a climate warming trend in the Alps. Basic Appl Ecol 9:100–107. https://doi.org/10.1016/j.baae.2007.01.005

    Article  Google Scholar 

  41. Pearson RG (2006) Climate change and the migration capacity of species. Trends Ecol Evol 21:111–113. https://doi.org/10.1016/j.tree.2005.11.022

    Article  PubMed  Google Scholar 

  42. Petrů M, Tielbörger K (2008) Germination behaviour of annual plants under changing climatic conditions: separating local and regional environmental effects. Oecologia 155:717–728. https://doi.org/10.1007/s00442-007-0955-0

    Article  PubMed  Google Scholar 

  43. Pluess AR, Schütz W, Stöcklin J (2005) Seed weight increases with altitude in the Swiss Alps between related species but not among populations of individual species. Oecologia 144:55–61. https://doi.org/10.1007/s00442-005-0047-y

    Article  PubMed  Google Scholar 

  44. Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214. https://doi.org/10.2307/2097047

    Article  Google Scholar 

  45. Reyer C et al (2013) A plant’s perspective of extremes: terrestrial plant responses to changing climatic variability. Glob Change Biol 19:75–89. https://doi.org/10.1111/gcb.12023

    Article  Google Scholar 

  46. Schütz W, Milberg P (1997) Seed dormancy in Carex canescens: regional differences and ecological consequences. Oikos 78:420–428. https://doi.org/10.2307/3545604

    Article  Google Scholar 

  47. Simons AM (2014) Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments. J Evol Biol 27:1047–1056. https://doi.org/10.1111/jeb.12378

    Article  PubMed  CAS  Google Scholar 

  48. Simons AM, Johnston MO (2000) Variation in seed traits of Lobelia inflata (Campanulaceae): sources and fitness consequences. Am J Bot 87:124–132

    Article  PubMed  CAS  Google Scholar 

  49. Simons AM, Johnston MO (2006) Environmental and genetic sources of diversification in the timing of seed germination: implications for the evolution of bet hedging. Evolution 60:2280–2292

    Article  PubMed  Google Scholar 

  50. Skordilis A, Thanos CA (1995) Seed stratification and germination strategy in the Mediterranean pines Pinus brutia and P. halepensis. Seed Sci Res 5:151–160. https://doi.org/10.1017/S0960258500002774

    Article  Google Scholar 

  51. Sommerville KD, Martyn AJ, Offord CA (2013) Can seed characteristics or species distribution be used to predict the stratification requirements of herbs in the Australian Alps? Bot J Linn Soc 172:187–204. https://doi.org/10.1111/boj.12021

    Article  Google Scholar 

  52. South Australian Seed Conservation Centre-Botanic Gardens of South Australia (2018) Seeds of South Australia - Oreomyrrhis eriopoda. Department for Environment and Water, South Australia. https://spapps.environment.sa.gov.au/SeedsOfSA/speciesinformation.html?rid=31

  53. Starrfelt J, Kokko H (2012) Bet-hedging a triple trade-off between means, variances and correlations. Biol Rev 87:742–755. https://doi.org/10.1111/j.1469-185X.2012.00225.x

    Article  PubMed  Google Scholar 

  54. Thuiller W et al (2008) Predicting global change impacts on plant species’ distributions: future challenges. Perspect Plant Ecol Evol Syst 9:137–152. https://doi.org/10.1016/j.ppees.2007.09.004

    Article  Google Scholar 

  55. Torres-Martínez L, Weldy P, Levy M, Emery NC (2017) Spatiotemporal heterogeneity in precipitation patterns explain population-level germination strategies in an edaphic specialist. Ann Bot 119:253–265. https://doi.org/10.1093/aob/mcw161

    Article  PubMed  Google Scholar 

  56. Vasseur DA et al (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc Lond B Biol Sci 281:20132612

    Article  Google Scholar 

  57. Vázquez DP, Gianoli E, Morris WF, Bozinovic F (2015) Ecological and evolutionary impacts of changing climatic variability. Biol Rev 92:22–42. https://doi.org/10.1111/brv.12216

    Article  PubMed  Google Scholar 

  58. Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090. https://doi.org/10.1890/06-1495

    Article  PubMed  Google Scholar 

  59. Venable DL, Lawlor L (1980) Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46:272–282. https://doi.org/10.1007/BF00540137

    Article  PubMed  Google Scholar 

  60. Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86:1385–1394. https://doi.org/10.1890/04-1647

    Article  Google Scholar 

  61. Volis S, Bohrer G (2013) Joint evolution of seed traits along an aridity gradient: seed size and dormancy are not two substitutable evolutionary traits in temporally heterogeneous environment. New Phytol 197:655–667. https://doi.org/10.1111/nph.12024

    Article  PubMed  Google Scholar 

  62. Wagmann K, Hautekèete N-C, Piquot Y, Meunier C, Schmitt SE, Van Dijk H (2012) Seed dormancy distribution: explanatory ecological factors. Ann Bot 110:1205–1219. https://doi.org/10.1093/aob/mcs194

    Article  PubMed  PubMed Central  Google Scholar 

  63. Wagner I, Simons AM (2009) Intraspecific divergence in seed germination traits between high- and low-latitude populations of the arctic-alpine annual Koenigia islandica. Arct Antarct Alp Res 40:233–239. https://doi.org/10.1657/1523-0430%2807-003%29%5bwagner%5d2.0.co%3b2

    Article  Google Scholar 

  64. Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011) Climate change and plant regeneration from seed. Glob Change Biol 17:2145–2161. https://doi.org/10.1111/j.1365-2486.2010.02368.x

    Article  Google Scholar 

  65. Wood JA (2014) Royal tasmanian botanical gardens (RTBG) germination database (last updated 2017) - Oreomyrrhis eriopoda. Tasmanian Government. https://gardens.rtbg.tas.gov.au/tscc-germination-database/

  66. Xu T, Hutchinson M (2011) ANUCLIM version 6.1 User Guide Fenner School of Environment and Society, Australian National University, Canberra

  67. Zhou W, Wang Z, Davy AJ, Liu G (2013) Geographic variation and local adaptation in Oryza rufipogon across its climatic range in China. J Ecol 101:1498–1508. https://doi.org/10.1111/1365-2745.12143

    Article  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the seed banks of the Australian National Botanic Gardens Canberra, The Royal Tasmanian Botanical Gardens, Royal Botanic Gardens Victoria, and the Australian Botanic Garden Mount Annan for providing seeds. We thank Pauline Ding and Terry Neeman (Statistical Consulting Unit ANU) for providing statistical advice, members of the Nicotra lab for useful feedback on the manuscript, ANBG staff Tom North for logistical support and Joe McAuliffe for confirming IDs on the accessions, Afiat Sukmaraga and Salamun Kaulam for the graphic editing, and especially Toton Liantoro for assistance during the experiment. The authors declare no conflict of interest. Annisa Satyanti is supported by an Australian Government Research Training Program (RTP) Scholarship.

Author information

Affiliations

Authors

Contributions

AS designed, carried out, analysed, and wrote the manuscript. ABN advised on design and analysis. ABN and LKG advised on the draft and substantially contributed to the revisions.

Corresponding author

Correspondence to Annisa Satyanti.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Research involving human and/or animal participants

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Monica Geber.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 517 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Satyanti, A., Guja, L.K. & Nicotra, A.B. Temperature variability drives within-species variation in germination strategy and establishment characteristics of an alpine herb. Oecologia 189, 407–419 (2019). https://doi.org/10.1007/s00442-018-04328-2

Download citation

Keywords

  • Local adaptation
  • Maternal environment
  • Plastic variation
  • Seedling growth
  • Reproductive ecology