Impact of extreme heatwaves and life-history traits on seed germination responses in Cumberland Plain Woodland native plant species
Philippa R. Alvarez
A B * , Daniel W. Krix A , Catherine A. Offord B and Brad R. Murray A
+ Author Affiliations
- Author Affiliations
A School of Life Sciences, University of Technology Sydney, PO Box 123, Ultimo, NSW 2007, Australia.
B Australian PlantBank, Botanic Gardens of Sydney, Mount Annan, NSW, Australia.
Australian Journal of Botany - https://doi.org/10.1071/BT22117
Submitted: 13 October 2022 Accepted: 14 June 2023 Published online: 11 July 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: The Cumberland Plain Woodland (CPW) is a threatened ecological community that is expected to experience heatwaves of increasing intensity and frequency into the future. Given the central role that temperature plays in regulating seed germination, understanding the impacts of such heatwaves on key germination attributes is vital to identify potential impacts on plant community structure.
Aims: To determine the impacts of increased heatwave intensity and frequency treatments on seed germination within and across 15 native species of the CPW. We also examined the influence of interspecific variation in life-history traits on germination responses.
Methods: Seeds were exposed to seven heatwave treatments of increasing intensity and frequency. Life-history trait data were also collected for each species’ dormancy type, fire response traits, life form and seed mass.
Key results: There was evidence within the study species of a significant effect of heatwave treatment. Germination duration was prolonged for the two most extreme simulated heatwave events. Life-history traits could not explain germination responses after heatwave treatments, however, larger seeded species had quicker germination onset and shorter periods of germination over small-seeded species; and trees had lower proportions of germination than any other life form.
Conclusions: Increases in heatwave intensity and frequency have an impact on seed germination responses in native species of the CPW. Life-history traits could not explain germination responses across species along the heatwave gradient.
Implications: Projected increases in heatwave intensity and frequency are likely to impact seed germination, and thus community composition, in species from the CPW.
Keywords: biodiversity, climate change, heatwaves, life-history traits, plant communities, seed ecology, seed germination, woodland ecology.
References
Ahrens CW, Challis A, Byrne M, Leigh A, Nicotra AB, Tissue D, Rymer P (2021) Repeated extreme heatwaves result in higher leaf thermal tolerances and greater safety margins. New Phytologist 232, 1212–1225.| Repeated extreme heatwaves result in higher leaf thermal tolerances and greater safety margins.Crossref | GoogleScholarGoogle Scholar |
Barak RS, Lichtenberger TM, Wellman-Houde A, Kramer AT, Larkin DJ (2018) Cracking the case: seed traits and phylogeny predict time to germination in prairie restoration species. Ecology and Evolution 8, 5551–5562.
| Cracking the case: seed traits and phylogeny predict time to germination in prairie restoration species.Crossref | GoogleScholarGoogle Scholar |
Baskin CC, Baskin JM (1988) Germination ecophysiology of herbaceous plant species in a temperate region. American Journal of Botany 75, 286–305.
| Germination ecophysiology of herbaceous plant species in a temperate region.Crossref | GoogleScholarGoogle Scholar |
Baskin CC, Baskin JM (1998) ‘Seeds: ecology, biogeography, and evolution of dormancy and germination.’ (Elsevier)
Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Science Research 14, 1–16.
| A classification system for seed dormancy.Crossref | GoogleScholarGoogle Scholar |
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Bell DT, Plummer JA, Taylor SK (1993) Seed germination ecology in southwestern Western Australia. The Botanical Review 59, 24–73.
| Seed germination ecology in southwestern Western Australia.Crossref | GoogleScholarGoogle Scholar |
Benson DH, Howell J (2002) Cumberland Plain Woodland ecology then and now: interpretations and implications from the work of Robert Brown and others. Cunninghamia 7, 631–650.
Bewley JD (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066.
| Seed germination and dormancy.Crossref | GoogleScholarGoogle Scholar |
Bewley JD, Black M (1994) Seeds. In ‘Seeds: physiology of development and germination’. (Eds JD Bewley, M Black) pp. 1–33. (Springer)
Bewley JD, Black M (2013) ‘Seeds: physiology of development and germination.’ (Springer Science & Business Media)
Bradstock RA, Tozer MG, Keith DA (1997) Effects of high frequency fire on floristic composition and abundance in a fire-prone heathland near Sydney. Australian Journal of Botany 45, 641–655.
| Effects of high frequency fire on floristic composition and abundance in a fire-prone heathland near Sydney.Crossref | GoogleScholarGoogle Scholar |
Bu H, Du G, Chen X, Xu X, Liu K, Wen S (2008) Community-wide germination strategies in an alpine meadow on the eastern Qinghai-Tibet plateau: phylogenetic and life-history correlates. Plant Ecology 195, 87–98.
| Community-wide germination strategies in an alpine meadow on the eastern Qinghai-Tibet plateau: phylogenetic and life-history correlates.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2020) Understanding heatwaves. (Australian Government, Bureau of Meteorology) Available at http://www.bom.gov.au/australia/heatwave/knowledgecentre/understanding.shtml [Accessed 16 June 2020]
Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405, 234–242.
| Consequences of changing biodiversity.Crossref | GoogleScholarGoogle Scholar |
Clarke S, French K (2005) Germination response to heat and smoke of 22 Poaceae species from grassy woodlands. Australian Journal of Botany 53, 445–454.
| Germination response to heat and smoke of 22 Poaceae species from grassy woodlands.Crossref | GoogleScholarGoogle Scholar |
Cochrane A (2017) Are we underestimating the impact of rising summer temperatures on dormancy loss in hard-seeded species? Australian Journal of Botany 65, 248–256.
| Are we underestimating the impact of rising summer temperatures on dormancy loss in hard-seeded species?Crossref | GoogleScholarGoogle Scholar |
Cochrane JA (2020) Thermal requirements underpinning germination allude to risk of species decline from climate warming. Plants 9, 796
| Thermal requirements underpinning germination allude to risk of species decline from climate warming.Crossref | GoogleScholarGoogle Scholar |
Cochrane A, Hoyle GL, Yates CJ, Wood J, Nicotra AB (2014) Predicting the impact of increasing temperatures on seed germination among populations of Western Australian Banksia (Proteaceae). Seed Science Research 24, 195–205.
| Predicting the impact of increasing temperatures on seed germination among populations of Western Australian Banksia (Proteaceae).Crossref | GoogleScholarGoogle Scholar |
Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wotton BM (2001) Climate change and forest disturbances: climate change can affect forests by altering the frequency, intensity, duration, and timing of fire, drought, introduced species, insect and pathogen outbreaks, hurricanes, windstorms, ice storms, or landslides. BioScience 51, 723–734.
| Climate change and forest disturbances: climate change can affect forests by altering the frequency, intensity, duration, and timing of fire, drought, introduced species, insect and pathogen outbreaks, hurricanes, windstorms, ice storms, or landslides.Crossref | GoogleScholarGoogle Scholar |
Davies M, Ecroyd H, Robinson SA, French K (2018) Stress in native grasses under ecologically relevant heat waves. PLoS ONE 13, e0204906
| Stress in native grasses under ecologically relevant heat waves.Crossref | GoogleScholarGoogle Scholar |
Ellis RH, Hong TD, Roberts EH (1987) Comparison of cumulative germination and rate of germination of dormant and aged barley seed lots at different constant temperatures. Seed Science and Technology 15, 717–727.
Environmental Protection and Biodiversity Conservation Act 1999 (Cth)
Fairley A, Moore P (2010) ‘Native plants of the Sydney Region: from Newcastle to Nowra and west to the dividing range.’ (Allen & Unwin)
Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, Firth D, Friendly M, Gorjanc G, Graves S, Heiberger R (2019) Package ‘car’. p. 16. R Foundation for Statistical Computing, Vienna. Available at https://cran.r-project.org/web/packages/car/index.html
French K, Jansens IB, Ashcroft MB, Ecroyd H, Robinson SA (2019) High tolerance of repeated heatwaves in Australian native plants. Austral Ecology 44, 597–608.
| High tolerance of repeated heatwaves in Australian native plants.Crossref | GoogleScholarGoogle Scholar |
Gill AM (1981) Adaptive responses of Australian vascular plant species to fires. In ‘Fire and the Australian biota’. (Eds AM Gill, RH Groves, IR Noble) pp. 243–271. (Australian Academy of Science: Canberra, ACT)
Gill AM, Bradstock RA (1992) A national register for the fire responses of plant species. Cunninghamia 2, 653–660.
Grime JP, Mason G, Curtis AV, Rodman J, Band SR (1981) A comparative study of germination characteristics in a local flora. The Journal of Ecology 69, 1017–1059.
| A comparative study of germination characteristics in a local flora.Crossref | GoogleScholarGoogle Scholar |
Gross KL, Smith AD (1991) Seed mass and emergence time effects on performance of Panicum dichotomiflorum Michx. across environments. Oecologia 87, 270–278.
| Seed mass and emergence time effects on performance of Panicum dichotomiflorum Michx. across environments.Crossref | GoogleScholarGoogle Scholar |
Hansen A, Pate JS, Hansen AP (1991) Growth and reproductive performance of a seeder and a resprouter species of Bossiaea as a function of plant age after fire. Annals of Botany 67, 497–509.
| Growth and reproductive performance of a seeder and a resprouter species of Bossiaea as a function of plant age after fire.Crossref | GoogleScholarGoogle Scholar |
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather and Climate Extremes 10, 4–10.
| Temperature extremes: effect on plant growth and development.Crossref | GoogleScholarGoogle Scholar |
Hirst MJ, Commander LE, Emery NJ, Guja LK, Liyanage GS, Merritt DJ, Norton SL, Stevens A, Turner SR, Wood JA (2021) Chapter 7: Seed germination and dormancy. In ‘Plant germplasm conservation in Australia: strategies and guidelines for developing, managing and utilising ex situ collections’. 3rd edn. (Eds AJ Martyn Yenson, CA Offord, PF Meagher, T Auld, D Bush, DJ Coates, LE Commander, LK Guja, SL Norton, RO Makinson, R Stanley, N Walsh, D Wrigley, L Broadhurst) pp. 187–240. (Australian Network for Plant Conservation: Canberra, ACT)
Hoyle GL, Venn SE, Steadman KJ, Good RB, McAuliffe EJ, Williams ER, Nicotra AB (2013) Soil warming increases plant species richness but decreases germination from the alpine soil seed bank. Global Change Biology 19, 1549–1561.
| Soil warming increases plant species richness but decreases germination from the alpine soil seed bank.Crossref | GoogleScholarGoogle Scholar |
Hulme PE (1998) Post-dispersal seed predation and seed bank persistence. Seed Science Research 8, 513–519.
| Post-dispersal seed predation and seed bank persistence.Crossref | GoogleScholarGoogle Scholar |
Hunter JT (2003) Persistence on inselbergs: the role of obligate seeders and resprouters. Journal of Biogeography 30, 497–510.
| Persistence on inselbergs: the role of obligate seeders and resprouters.Crossref | GoogleScholarGoogle Scholar |
Jiménez-Alfaro B, Silveira FAO, Fidelis A, Poschlod P, Commander LE (2016) Seed germination traits can contribute better to plant community ecology. Journal of Vegetation Science 27, 637–645.
| Seed germination traits can contribute better to plant community ecology.Crossref | GoogleScholarGoogle Scholar |
Jin Y, Qian H (2019) V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography 42, 1353–1359.
| V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants.Crossref | GoogleScholarGoogle Scholar |
Kahmen S, Poschlod P (2008) Does germination success differ with respect to seed mass and germination season? Experimental testing of plant functional trait responses to grassland management. Annals of Botany 101, 541–548.
| Does germination success differ with respect to seed mass and germination season? Experimental testing of plant functional trait responses to grassland management.Crossref | GoogleScholarGoogle Scholar |
Keith DA, Elith J, Simpson CC (2014) Predicting distribution changes of a mire ecosystem under future climates. Diversity and Distributions 20, 440–454.
| Predicting distribution changes of a mire ecosystem under future climates.Crossref | GoogleScholarGoogle Scholar |
Knox KJE, Morrison DA (2005) Effects of inter-fire intervals on the reproductive output of resprouters and obligate seeders in the Proteaceae. Austral Ecology 30, 407–413.
| Effects of inter-fire intervals on the reproductive output of resprouters and obligate seeders in the Proteaceae.Crossref | GoogleScholarGoogle Scholar |
Kubiak PJ (2009) Fire responses of bushland plants after the January 1994 wildfires in northern Sydney. Cunninghamia 11, 131–165.
Lawrence J, Mackey B, Chiew F, Costello MJ, Lansbury N, Hennessy K, Nidumolu U, Pecl G, Rickards L, Tapper N, Woodward A, Wreford A (2022) Chapter 11: Australasia. In ‘Working Group II: Impacts, adaptation and vulnerability, sixth assessment report’. (Eds H-O Pottner, D Roberts) pp. 1–151. (Intergovernmental Panel on Climate Change: Geneva, Switzerland)
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2021) emmeans: estimated marginal means, aka least-squares means. R Package Version 1.7.0. Available at https://CRAN.R-project.org/package=emmeans
Maher T, Mirzaei M, Pascovici D, Wright IJ, Haynes PA, Gallagher RV (2019) Evidence from the proteome for local adaptation to extreme heat in a widespread tree species. Functional Ecology 33, 436–446.
| Evidence from the proteome for local adaptation to extreme heat in a widespread tree species.Crossref | GoogleScholarGoogle Scholar |
Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 92, 372–383.
| Seedling survival and seed size: a synthesis of the literature.Crossref | GoogleScholarGoogle Scholar |
Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113, 91–105.
| Seed size and plant strategy across the whole life cycle.Crossref | GoogleScholarGoogle Scholar |
Mondoni A, Rossi G, Orsenigo S, Probert RJ (2012) Climate warming could shift the timing of seed germination in alpine plants. Annals of Botany 110, 155–164.
| Climate warming could shift the timing of seed germination in alpine plants.Crossref | GoogleScholarGoogle Scholar |
NSW Government (2016) Biodiversity Conservation Act 2016 (Vic.)
Norden N, Daws MI, Antoine C, Gonzalez MA, Garwood NC, Chave J (2009) The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Functional Ecology 23, 203–210.
| The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests.Crossref | GoogleScholarGoogle Scholar |
Olofsson H, Ripa J, Jonzén N (2009) Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proceedings of the Royal Society B: Biological Sciences 276, 2963–2969.
Ooi M, Auld T, Whelan R (2004) Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species. Ecological Management & Restoration 5, 141–143.
| Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species.Crossref | GoogleScholarGoogle Scholar |
Ooi MKJ, Auld TD, Whelan RJ (2007) Distinguishing between persistence and dormancy in soil seed banks of three shrub species from fire-prone southeastern Australia. Journal of Vegetation Science 18, 405–412.
| Distinguishing between persistence and dormancy in soil seed banks of three shrub species from fire-prone southeastern Australia.Crossref | GoogleScholarGoogle Scholar |
Ooi MKJ, Denham AJ, Santana VM, Auld TD (2014) Temperature thresholds of physically dormant seeds and plant functional response to fire: variation among species and relative impact of climate change. Ecology and Evolution 4, 656–671.
| Temperature thresholds of physically dormant seeds and plant functional response to fire: variation among species and relative impact of climate change.Crossref | GoogleScholarGoogle Scholar |
Orsenigo S, Abeli T, Rossi G, Bonasoni P, Pasquaretta C, Gandini M, Mondoni A (2015) Effects of autumn and spring heat waves on seed germination of high mountain plants. PLoS ONE 10, e0133626
| Effects of autumn and spring heat waves on seed germination of high mountain plants.Crossref | GoogleScholarGoogle Scholar |
Palmer HD, Denham AJ, Ooi MKJ (2018) Fire severity drives variation in post-fire recruitment and residual seed bank size of Acacia species. Plant Ecology 219, 527–537.
| Fire severity drives variation in post-fire recruitment and residual seed bank size of Acacia species.Crossref | GoogleScholarGoogle Scholar |
Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528.
| ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R.Crossref | GoogleScholarGoogle Scholar |
Parmesan C, Hanley ME (2015) Plants and climate change: complexities and surprises. Annals of Botany 116, 849–864.
| Plants and climate change: complexities and surprises.Crossref | GoogleScholarGoogle Scholar |
Penman TD, Binns DL, Allen RM, Shiels RJ, Plummer SH (2008) Germination responses of a dry sclerophyll forest soil-stored seedbank to fire related cues. Cunninghamia 10, 547–555.
Pianka ER (1970) On r- and K-selection. The American Naturalist 104, 592–597.
| On r- and K-selection.Crossref | GoogleScholarGoogle Scholar |
PlantNET (The NSW Plant Information Network System) (2019) Royal Botanic Gardens and Domain Trust, Sydney. Available at http://plantnet.rbgsyd.nsw.gov.au [Accessed 11 November 2019]
Pörtner HO, Roberts DC, Adams H, Adler C, Aldunce P, Ali E, Begum RA, Betts R, Kerr RB, Biesbroek R, Birkmann J (2022) Climate change 2022: impacts, adaptation and vulnerability. IPCC sixth assessment report. Intergovernmental Panel on Climate Change, Geneva.
Probert RJ (2000) The role of temperature in the regulation of seed dormancy and germination. In ‘Seeds: the ecology of regeneration in plant communities’. (Ed. M Fenner) pp. 261–292. (CABI: Wallingford, UK)
Ramos DM, Liaffa ABS, Diniz P, Munhoz CBR, Ooi MKJ, Borghetti F, Valls JFM (2016) Seed tolerance to heating is better predicted by seed dormancy than by habitat type in Neotropical savanna grasses. International Journal of Wildland Fire 25, 1273–1280.
| Seed tolerance to heating is better predicted by seed dormancy than by habitat type in Neotropical savanna grasses.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2022) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/ [Accessed 12 August 2022]
Read T, Bellairs S, Mulligan D, Lamb D (1997) Influence of smoke on soil seed bank germination in a native forest community of New South Wales. In ‘Second Australian native seed biology for revegetation workshop’. pp. 81–92. (Australian Centre for Minesite Rehabilitation Research)
Reznick D, Bryant MJ, Bashey F (2002) r- and k- selection revisited: the role of population regulation in life-history evolution. Ecology 83, 1509–1520.
| r- and k- selection revisited: the role of population regulation in life-history evolution.Crossref | GoogleScholarGoogle Scholar |
Roberts EH (1998) Temperature and seed germination. In ‘Plants and temperature: symposia of the society for experimental biology’. (Eds SP Long, FI Woodward) pp. 109–132. (Company of Biologists Ltd.)
Ruiz-Talonia L, Carr D, Smith R, Whalley RDB, Reid N (2018) Effect of temperature and light on germination of 10 species of Eucalyptus from north-western NSW. Australian Journal of Botany 66, 657–666.
| Effect of temperature and light on germination of 10 species of Eucalyptus from north-western NSW.Crossref | GoogleScholarGoogle Scholar |
Shi Z, Sherry R, Xu X, Hararuk O, Souza L, Jiang L, Xia J, Liang J, Luo Y (2015) Evidence for long-term shift in plant community composition under decadal experimental warming. Journal of Ecology 103, 1131–1140.
| Evidence for long-term shift in plant community composition under decadal experimental warming.Crossref | GoogleScholarGoogle Scholar |
Smith SA, Brown JW (2018) Constructing a broadly inclusive seed plant phylogeny. American Journal of Botany 105, 302–314.
| Constructing a broadly inclusive seed plant phylogeny.Crossref | GoogleScholarGoogle Scholar |
Society for Ecological Restoration, International Network for Seed Based Restoration and Royal Botanic Gardens Kew (2023) Seed Information Database (SID). Available at https://ser-sid.org/ [Accessed 20 February 2023]
Tang Y, Boulter SL, Kitching RL (2003) Heat and smoke effects on the germination of seeds from soil seed banks across forest edges between subtropical rainforest and eucalypt forest at Lamington National Park, south-eastern Queensland, Australia. Australian Journal of Botany 51, 227–237.
| Heat and smoke effects on the germination of seeds from soil seed banks across forest edges between subtropical rainforest and eucalypt forest at Lamington National Park, south-eastern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Tangney R, Merritt DJ, Fontaine JB, Miller BP (2019) Seed moisture content as a primary trait regulating the lethal temperature thresholds of seeds. Journal of Ecology 107, 1093–1105.
| Seed moisture content as a primary trait regulating the lethal temperature thresholds of seeds.Crossref | GoogleScholarGoogle Scholar |
Thompson K, Grime JP, Mason G (1977) Seed germination in response to diurnal fluctuations of temperature. Nature 267, 147–149.
| Seed germination in response to diurnal fluctuations of temperature.Crossref | GoogleScholarGoogle Scholar |
Tozer MG, Leishman MR, Auld TD (2015) Ecosystem risk assessment for Cumberland Plain Woodland, New South Wales, Australia. Austral Ecology 40, 400–410.
| Ecosystem risk assessment for Cumberland Plain Woodland, New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Van Der Veken S, Bossuyt B, Hermy M (2004) Climate gradients explain changes in plant community composition of the forest understory: an extrapolation after climate warming. Belgian Journal of Botany 137, 55–69.
Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86, 1385–1394.
| Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416, 389–395.
| Ecological responses to recent climate change.Crossref | GoogleScholarGoogle Scholar |
Watson PJ (2005) Fire frequencies for western Sydney’s woodlands: indications from vegetation dynamics. PhD Thesis (Unpubl.), University of Western Sydney, NSW, Australia.
Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. Journal of Experimental Botany 62, 3289–3309.
| First off the mark: early seed germination.Crossref | GoogleScholarGoogle Scholar |
Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, Davies TJ, Kraft NJB, Ault TR, Bolmgren K, Mazer SJ, McCabe GJ, McGill BJ, Parmesan C, Salamin N, Schwartz MD, Cleland EE (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497.
| Warming experiments underpredict plant phenological responses to climate change.Crossref | GoogleScholarGoogle Scholar |
Woodstock LW (1988) Seed imbibition: a critical period for successful germination. Journal of Seed Technology 12, 1–15.
