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.
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References
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
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
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
Baskin C, Baskin J (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination. Elsevier/Academic Press, San Diego
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
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
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
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
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
Costin AB, Gray M, Totterdell CJ, Wimbush DJ (2000) Kosciuszko Alpine Flora. CSIRO Publising, Collingwood
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
Donohue K (2005) Seeds and seasons: interpreting germination timing in the field. Seed Sci Res 15:175–187
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
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
Fenner M (1991) The effects of the parent environment on seed germinability. Seed Sci Res 1:75–84. https://doi.org/10.1017/s0960258500000696
Fenner M, Thompson K (2005) The Ecology of Seeds. Cambridge University Press, Cambridge
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
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
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
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
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
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
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
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
Jobson PK (1999) Oreomyrrhis. In: Walsh NG, Entwisle TJ (eds) Flora of Victoria, vol 4 Cornaceae to Asteraceae. Inkata Press, Melbourne
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
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
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin
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
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
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
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
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
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
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
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
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
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
Parmesan C, Hanley ME (2015) Plants and climate change: complexities and surprises. Ann Bot 116:849–864. https://doi.org/10.1093/aob/mcv169
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
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
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
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
Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214. https://doi.org/10.2307/2097047
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
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
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
Simons AM, Johnston MO (2000) Variation in seed traits of Lobelia inflata (Campanulaceae): sources and fitness consequences. Am J Bot 87:124–132
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
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
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
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
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
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
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
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
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
Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090. https://doi.org/10.1890/06-1495
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
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
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
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
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
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
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/
Xu T, Hutchinson M (2011) ANUCLIM version 6.1 User Guide Fenner School of Environment and Society, Australian National University, Canberra
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
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.
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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.
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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
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DOI: https://doi.org/10.1007/s00442-018-04328-2