Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T17:09:15.387Z Has data issue: false hasContentIssue false
  • English
  • Français

Physical dormancy in a changing climate

Published online by Cambridge University Press:  13 January 2015

Alice R. Hudson ,
David J. Ayre  and
Mark K. J. Ooi
Alice R. Hudson*
Affiliation:
Institute for Conservation Biology and Environmental Management, School of Biological Sciences, University of Wollongong, NSW 2522, Australia
David J. Ayre
Affiliation:
Institute for Conservation Biology and Environmental Management, School of Biological Sciences, University of Wollongong, NSW 2522, Australia
Mark K. J. Ooi
Affiliation:
Institute for Conservation Biology and Environmental Management, School of Biological Sciences, University of Wollongong, NSW 2522, Australia
*
*Correspondence E-mail: arh785@uowmail.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Species with physically dormant (PY) seeds make up over 25% of plant species in a number of ecologically important ecosystems around the globe, such as savannah and Mediterranean shrublands. Many of these ecosystems are subject to temporally stochastic events, such as fire and drought; but are in areas projected to experience some of the most extreme climatic changes in the future. Given the importance of PY in controlling germination timing for successful recruitment, we ask how plastic the PY trait is, and if changes to the maternal environment from climate change could alter recruitment. This review focuses on: (1) the evidence for inter- and intraspecific variation in PY; (2) the genetic, maternal and environmental controls involved; and (3) the ecological consequences of (1) and (2) above. Evidence for (within-community) interspecific variation in conditions required to break PY is strong, but for intraspecific variation evidence is contradictory and limited by a paucity of studies. Identifying controllers of variation in PY is complex, there is some suggestion that conditions of the maternal environment may be important, but no consensus on the nature of effects. The implications of PY plasticity for the persistence of seed banks, species and communities under climate change are discussed. We highlight a number of key knowledge gaps, such as a lack of research estimating the components of variation in non-agricultural species, and identify a suite of seed attributes relevant to understanding the potential impacts of climate change on the population dynamics of PY species in the future.

Keywords

germinationhardseedednessheritabilitymaternal effectsMediterranean ecosystemsphenotypic variationseed traits
Type
Review Article
Information
Seed Science Research , Volume 25 , Special Issue 2: Seed Dormancy , June 2015 , pp. 66 - 81
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, L.V. and Arblaster, J.M. (2009) Assessing trends in observed and modelled climate extremes over Australia in relation to future projections. International Journal of Climatology 29, 417–435.Google Scholar
Argel, P.J. and Humphreys, L.R. (1983a) Environmental effects on seed development and hardseededness in Stylosanthes hamata cv. Verano. I Temperature. Australian Journal of Agricultural Research 34, 261–270.Google Scholar
Argel, P.J. and Humphreys, L.R. (1983b) Environmental effects on seed development and hardseededness in Stylosanthes hamata cv. Verano. III Storage humidity and seed characteristics. Australian Journal of Agricultural Research 34, 279–287.Google Scholar
Auld, T.D. and O'Connell, M.A. (1991) Predicting patterns of post-fire germination in 35 Australian Fabaceae. Australian Journal of Ecology 16, 53–70.CrossRefGoogle Scholar
Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, biogeography, and evolution of dormancy and germination (2nd edition). New York, USA, Academic Press.Google Scholar
Baskin, J.M., Baskin, C.C. and Li, X. (2000) Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology 15, 139–152.Google Scholar
Bolin, J.F. (2009) Heat shock germination responses of three eastern North American temperate species. Castanea 74, 160–167.Google Scholar
Bolingue, W., Vu, B.L., Leprince, O. and Buitink, J. (2010) Characterization of dormancy behaviour in seeds of the model legume Megicago truncatula . Seed Science Research 20, 97–107.CrossRefGoogle Scholar
Burrows, G.E., Virgona, J.M. and Heady, R.D. (2009) Effect of boiling water, seed coat structure and provenance on the germination of Acacia melanoxylon seeds. Australian Journal of Botany 57, 139–147.CrossRefGoogle Scholar
Cowling, R.M., Rundel, P.W., Lamont, B.B., Arroyo, M.K. and Arianoutsou, M. (1996) Plant diversity in Mediterranean-climate regions. Trends in Ecology and Evolution 11, 362–366.Google Scholar
Davis, M.B., Shaw, R.G. and Etterson, J.R. (2005) Evolutionary responses to changing climate. Ecology 86, 1704–1714.Google Scholar
de Souza, F.H.D. and Marcos-Filho, J. (2001) The seed coat as a modulator of seed–environment relationships in Fabaceae. Revista Brasilivia de Botânica 24, 365–375.Google Scholar
D'hondt, B., Brys, R. and Hoffmann, M. (2010) The incidence, field performance and heritability of non-dormant seeds in white clover (Trifolium repens L.). Seed Science Research 20, 169–177.CrossRefGoogle Scholar
Donnelly, E.D., Watson, J.E. and McGuire, J.A. (1972) Inheritance of hard seed in Vicia . Journal of Heredity 63, 361–365.CrossRefGoogle Scholar
Donohue, K. (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philosophical Transactions of the Royal Society B 364, 1059–1074.Google Scholar
Donohue, K., Rubio de Casas, R., Burghardt, L., Kovach, K. and Willis, C.G. (2010) Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution and Systematics 41, 293–319.Google Scholar
Evenari, M., Koller, D. and Gutterman, Y. (1966) Effects of the environment of the mother plant on germination by control of seed-coat permeability to water in Ononis sicula. Guss. Australian Journal of Biological Sciences 19, 1007–1016.CrossRefGoogle Scholar
Falconer, D.S. (1989) Introduction to quantitative genetics (3rd edition). USA, Longman Scientific and Technical.Google Scholar
Farrell, T.P. and Ashton, D.H. (1978) Population studies on Acacia melanoxylon R. Br. I. Variation in seed and vegetative characteristics. Australian Journal of Botany 26, 365–379.Google Scholar
Fenner, M. (1991) The effects of the parent environment on seed germinability. Seed Science Research 1, 75–84.Google Scholar
Frankham, R., Ballou, J.D., Briscoe, D.A. and McInnes, K.H. (2010) Introduction to conservation genetics (2nd edition). Cambridge, UK, Cambridge University Press.Google Scholar
Furbeck, S.M., Bourland, F.M. and Watson, C.E. Jr (1993) Inheritance of resistance to seed deterioration in cotton. Euphytica 69, 203–209.CrossRefGoogle Scholar
Galloway, L.F. (2001) The effect of paternal and maternal environments on seed characters in the herbaceous plant Campanula americana (Campanulaceae). American Journal of Botany 88, 832–840.CrossRefGoogle ScholarPubMed
Gama-Arachchige, N.S., Baskin, J.M., Geneve, R.L. and Baskin, C.C. (2010) Identification and characterization of the water gap in physically dormant seeds of Geraniaceae, with special reference to Geranium carolinianum . Annals of Botany 105, 977–990.CrossRefGoogle ScholarPubMed
Gama-Arachchige, N.S., Baskin, J.M., Geneve, R.L. and Baskin, C.C. (2011) Acquisition of physical dormancy and ontogeny of the micropyle-water-gap complex in developing seeds of Geranium carolinianum (Geraniaceae). Annals of Botany 108, 51–64.CrossRefGoogle ScholarPubMed
Gama-Arachchige, N.S., Baskin, J.M., Geneve, R.L. and Baskin, C.C. (2013) Identification and characterization of ten new water gaps in seeds and fruits with physical dormancy and classification of water-gap complexes. Annals of Botany 112, 69–84.Google Scholar
Gresta, F., Avola, G. and Abbate, V. (2007) Germination ecology of Scorpiurus subvillosus L. seeds: the role of temperature and storage time. Plant Ecology 190, 123–130.CrossRefGoogle Scholar
Heisler-White, J.L., Blair, J.M., Kelly, E.F., Harmoney, K. and Knapp, A.K. (2009) Contingent productivity responses to more extreme rainfall regimes across a grassland biome. Global Change Biology 15, 2894–2904.CrossRefGoogle Scholar
Herranz, J.M., Ferrandis, P. and Martinez-Sanchez, J.J. (1998) Influence of heat on seed germination of seven Mediterranean Leguminosae species. Plant Ecology 136, 95–13.Google Scholar
Hill, H.J., West, S.H. and Hinson, K. (1986a) Soybean seed size influences expression of the impermeable seed-coat trait. Crop Science 26, 634–637.Google Scholar
Hill, H.J., West, S.H. and Hinson, K. (1986b) Effect of water stress during seedfill on impermeable seed. Crop Science 26, 807–812.Google Scholar
Hof, C., Levinsky, I., Araújo, M.B. and Rahbek, C. (2011) Rethinking species' ability to cope with rapid climate change. Global Change Biology 17, 2987–2990.Google Scholar
Honnay, O., Verheyen, K., Butaye, J., Jacqumyn, H., Bossuyt, B. and Hermy, M. (2002) Possible effects of habitat fragmentation and climate change on the range of forest plants species. Ecology Letters 5, 525–530.Google Scholar
House, C.R., Roth, C., Hunt, J. and Kover, P.X. (2010) Paternal effects in Arabidopsis indicate that offspring can influence their own size. Proceedings of the Royal Society B-Biological Sciences 277, 2885–2893.Google Scholar
Hoyle, G.L., Steadman, K.J., Daws, M.I. and Adkins, S.W. (2008) Pre- and post-harvest influences on seed dormancy status of an Australian Goodeniaceae species Goodenia fasicularis . Annals of Botany 102, 93–101.Google Scholar
Hoyle, G.L., Kravchuk, O.Y., Daws, M.I., Adkins, S.W. and Steadman, K.J. (2011) Replicated versus un-replicated factorial experiments for preliminary investigation of seed germination and dormancy: alternative approaches using fewer seeds. Seed Science and Technology 39, 93–111.CrossRefGoogle Scholar
Humphrey, M.E., Lambrides, C.J., Chapman, S.C., Aitken, E.A.B., Imrie, B.C., Lawn, R.J., McIntyre, C.L. and Liu, C.J. (2005) Relationships between hard-seededness and seed weight in mungbean (Vigna radiata) assessed by QTL analysis. Plant Breeding 124, 292–298.CrossRefGoogle Scholar
IPCC . (2014) Summary for policymakers. In Field, C.B.; Barros, V.R.; Dokken, D.J.; Mach, K.J.; Mastrandrea, M.D.; Bilir, T.E.; Chatterjee, M.; Ebi, K.L.; Estrada, Y.O.; Genova, R.C.; Girma, B.; Kissel, E.S.; Levy, A.N.; MacCracken, S.; Mastrandrea, P.R.; White, L.L. (Eds) Climate change 2014: impacts, adaptation and vulnerability. Part A: Global and sectoral aspects. Contribution of working group II to the 5th assessment report of the Intergovernmental Panel on Climate change. Cambridge, UK, Cambridge University Press.Google Scholar
Isemura, T., Kaga, A., Tomooka, N., Shimizu, T. and Vaughan, D.A. (2010) The genetics of domestication of rice bean, Vigna umbellata . Annals of Botany 106, 927–944.Google Scholar
Isemura, T., Kaga, A., Tabata, S., Somata, P., Srinives, P., Shimizu, T., Uken, J., Vaughan, D.A. and Tomooka, N. (2012) Construction of a genetic linkage map and genetic analysis of domestication related traits in Mungbean (Vigna radiata). PLOS One 7, e41304.Google Scholar
James, A.T., Lawn, R.J., Williams, R.W. and Lambrides, C.J. (1999) Cross fertility of Australian accessions of wild Mungbean (Vigna radiata ssp. sublobata) with green Gram (V. radiata ssp. radiata) and black Gram (V. mungo). Australian Journal of Botany 47, 601–610.Google Scholar
Jayasuriya, K.M.G.G., Baskin, J.M. and Baskin, C.C. (2008a) Cycling of sensitivity to physical dormancy-break in seeds of Ipomoea lacunose (Convolvulaceae) and ecological significance. Annals of Botany 101, 341–352.CrossRefGoogle Scholar
Jayasuriya, K.M.G.G., Baskin, J.M., Geneve, R.L., Baskin, C.C. and Chien, C.T. (2008b) Physical dormancy in seeds of the holoparastic angiosperm Cuscuta australis (Convolvulaceae, Cuscuteae): dormancy-breaking requirements, anatomy of the water gap and sensitivity cycling. Annals of Botany 102, 39–48.CrossRefGoogle ScholarPubMed
Jayasuriya, K.M.G.G., Baskin, J.M., Geneve, R.L. and Baskin, C.C. (2009) A proposed mechanism for physical dormancy break in seeds of Ipomoea lacunosa (Convolvulaceae). Annals of Botany 103, 433–445.CrossRefGoogle ScholarPubMed
Jeffrey, D.J., Holmes, P.M. and Rebelo, A.G. (1988) Effects of dry heat on seed germination in selected indigenous and alien legume species in South Africa. South African Journal of Botany 54, 28–34.Google Scholar
Jump, A.S. and Peñuelas, J. (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8, 1010–1020.CrossRefGoogle ScholarPubMed
Kaga, A., Isemura, T., Tomooka, N. and Vaughan, D.A. (2008) The genetics of domestication of the Azuki bean (Vigna angularis). Genetics 178, 1013–1035.Google Scholar
Keigley, P.J. and Mullen, R.E. (1986) Changes in soybean seed quality from high temperature during seed fill and maturation. Crop Science 26, 1212–1216.Google Scholar
Keim, P., Diers, B.W. and Shoemaker, R.C. (1990) Genetic analysis of soybean hard seededness with molecular markers. Theoretical and Applied Genetics 79, 465–469.Google Scholar
Kilen, T.C. and Hartwig, E.E. (1978) An inheritance study of impermeable seed in soybeans. Field Crops Research 1, 65–70.Google Scholar
Kimball, S., Angert, A.L., Huxman, T.E. and Venable, D.L. (2010) Contemporary climate change in the Sonoran Desert favours cold-adapted species. Global Change Biology 16, 1555–1565.CrossRefGoogle Scholar
Kochanek, J., Buckley, Y.M., Probert, R.J., Adkins, S.W. and Steadman, K.J. (2011) Pre-zygotic parental environment modulates seed longevity. Austral Ecology 35, 837–848.Google Scholar
Lacerda, D.R., Filho, J.P.L., Goulart, M.F., Ribeiro, R.A. and Lovato, M.B. (2004) Seed-dormancy variation in natural populations of two tropical leguminous tree species: Senna multijuga (Caesalpinoideae) and Plathymenia reticulata (Mimosoideae). Seed Science Research 14, 127–135.Google Scholar
Lacey, E.P., Smith, S. and Case, A.L. (1997) Parental effects on seed mass: seed coat but embryo or endosperm effects. Australian Journal of Botany 84, 1617–1620.Google Scholar
Lee, J.A. (1975) Inheritance of hard seed in cotton. Crop Science 15, 149–152.Google Scholar
Li, X., Baskin, J.M. and Baskin, C.C. (1999a) Pericarp ontogeny and anatomy in Rhus aromatica Ait. and R. glabra L. (Anacardiaceae). Journal of the Torrey Botanical Society 126, 279–288.Google Scholar
Li, X., Baskin, J.M. and Baskin, C.C. (1999b) Anatomy of two mechanisms of breaking physical dormancy by experimental treatments in seeds of two north American Rhus species (Anacardiaceae). American Journal of Botany 86, 1505–1511.Google Scholar
Li, X., Buirchell, B., Yan, G. and Yang, H. (2012) A molecular marker linked to the mollis gene conferring soft-seediness for marker-assisted selection applicable to a wide range of crosses in lupin (Lupinus angustifolius L.). Molecular Breeding 29, 361–370.Google Scholar
Majd, R., Aghaie, P., Monfared, E.K. and Alebrahim, M.T. (2013) Evaluation of some treatments on breaking seed dormancy in Mesquite. International Journal of Agronomy and Plant Production 4, 1433–1439.Google Scholar
Martin, R.E., Miller, R.L. and Cushwa, C.T. (1975) Germination response of legume seeds subjected to moist and dry heat. Ecology 56, 1441–1445.Google Scholar
McLaughlin, B.C. and Zavaleta, E.S. (2012) Predicting species responses to climate change: demography and climate microrefugia in California valley oak (Quercus lobata). Global Change Biology 18, 2301–2312.Google Scholar
Meisert, A. (2002) Physical dormancy in Geraniaceae seeds. Seed Science Research 12, 121–128.CrossRefGoogle Scholar
Michael, P.J., Steadman, K.J. and Plummer, J.A. (2006) Climatic regulation of seed dormancy and emergences of Malva parviflora populations from a Mediterranean-type environment. Seed Science Research 16, 273–281.Google Scholar
Moreira, B. and Pausas, J.G. (2012) Tanned or burned: the role of fire in shaping physical seed dormancy. PlosOne 7, e51523.Google Scholar
Moreno, J.M. and Oechel, W.C. (1991) Fire intensity effects on germination of shrubs and herbs in southern California chaparral. Ecology 72, 1993–2004.Google Scholar
Morin, X., Viner, D. and Chuine, I. (2008) Tree species range shifts at a continental scale: new predictive insights from a process-based model. Journal of Ecology 96, 784–794.Google Scholar
Morley, F.H.W. (1958) The inheritance and ecological significance of seed dormancy in subterranean clover (Trifolium subterraneum L.). Australian Journal of Biological Science 11, 261–274.Google Scholar
Nair, R.M., Craig, A.D., Rowe, T.D., Biggins, S.R. and Hunt, C.H. (2004) Genetic variability and heritability estimates for hardseededness and flowering in balansa clover (Trifolium michelianum Savi) populations. Euphytica 138, 197–203.Google Scholar
Nichols, P.G.H., Cocks, P.S. and Francis, C.M. (2009) Evolution over 16 years in a bulk-hybrid population of subterranean clover (Trifolium subterraneum L.) at two contrasting sites in south-western Australia. Euphytica 169, 31–48.CrossRefGoogle Scholar
Nicotra, A.B., Atkin, O.K., Bonser, S.P., Davidson, A.M., Finnegan, E.J., Mathesius, U., Poot, P., Purugganan, M.D., Richards, C.L., Valladares, F. and van Kleunen, M. (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15, 684–692.Google Scholar
Norman, H.C., Cocks, P.S., Smith, F.P. and Nutt, B.J. (1998) Reproductive strategies in Mediterranean annual clovers: germination and hardseedness. Australian Journal of Agricultural Research 49, 973–982.Google Scholar
Norman, H.C., Cocks, P.S. and Galwey, N.W. (2002) Hardseededness in annual clovers: variation between populations from wet and dry environments. Australian Journal of Agricultural Research 53, 821–829.CrossRefGoogle Scholar
Norman, H.C., Smith, F.P., Nichols, P.G.H., Si, P. and Galwey, N.W. (2006) Variation in seed softening patterns and impact of seed production environment on hardseededness in early-maturing genotypes of subterranean clover. Australian Journal of Agricultural Research 57, 65–74.Google Scholar
Ooi, M.K.J. (2012) Seed bank persistence and climate change. Seed Science Research 22, 53–60.CrossRefGoogle Scholar
Ooi, M.K.J, Auld, T.D. and Denham, A.J. (2009) Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Global Change Biology 15, 2375–2386.Google Scholar
Ooi, M.K.J., Auld, T.D. and Denham, A.J. (2012) Projected soil temperature increase and seed dormancy response along an altitudinal gradient: implications for seed bank persistence under climate change. Plant Soil 353, 289–303.Google Scholar
Ooi, M.K.J., Denham, A.J., Santana, V.M. and Auld, T.D. (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.Google Scholar
Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Reviews of Ecology, Evolution and Systematics 37, 637–669.Google Scholar
Paulsen, T.R., Colville, L., Kranner, I., Daws, M.I., Högstedt, G., Vandvik, V. and Thompson, K. (2013) Physical dormancy in seeds: a game of hide and seek? New Phytologist 198, 496–503.Google Scholar
Penman, T.D. and Towerton, A.L. (2008) Soil temperatures during autumn prescribed burning, implications for the germination of fire responsive species. International Journal of Wildland Fire 17, 572–578.CrossRefGoogle Scholar
Pérez-García, F. and Escudero, A. (1997) Role of the seed coat in germination of Cistus populifolius L. Israel Journal of Plant Sciences 45, 329–331.Google Scholar
Piano, E., Pecetti, L. and Carroni, A.M. (1996) Climatic adaptation in subterranean clover populations. Euphytics 92, 39–44.CrossRefGoogle Scholar
Pollard, D.A. (2012) Design and construction of recombinant inbred lines. Methods in Molecular Biology 871, 31–39.Google Scholar
Probert, R.J. (2000) The role of temperature in the regulation of seed dormancy and germination. pp. 261–292 in Fenner, M. (Ed.) Seeds: The ecology of regeneration in plant communities (2nd edition). Wallingford, UK, CABI.Google Scholar
Quinlivan, B.J. and Nicol, H.I. (1971) Embryo dormancy in subterranean clover seeds. Australian Journal of Agricultural Research 22, 599–606.Google Scholar
Ramsay, G. (1997) Inheritance and linkage of a gene for testa-imposed seed dormancy and faba bean (Vicia faba L.). Plant Breeding 116, 287–289.Google Scholar
Rix, K.D., Gracie, A.J., Potts, B.M., Brown, P.H., Spurr, C.J. and Gore, P.L. (2012) Paternal and maternal effects on the response of seed germination to high temperatures in Eucalyptus globulus . Annals of Forest Science 69, 673–679.CrossRefGoogle Scholar
Roach, D.A. and Wulff, R.D. (1987) Maternal effects in plants. Annual Review of Ecology and Systematics 18, 209–235.Google Scholar
Royer, P.D., Cobb, N.S., Clifford, M.J., Huang, C.Y., Breshears, D.D., Adams, H.D. and Villegas, J.C. (2011) Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. Journal of Ecology 99, 714–723.Google Scholar
Sakamoto, S., Abe, J., Kanazawa, A. and Shimamoto, Y. (2004) Marker-assisted analysis for soybean hard seededness with isozyme and simple sequence repeat loci. Breeding Science 54, 133–139.Google Scholar
Salisbury, P.A. and Halloran, G.M. (1983) Inheritance of rate of breakdown of seed coat impermeability in subterranean clover (Trifolium subterraneum L.). Euphytica 32, 807–819.Google Scholar
Skelly, D.K., Joseph, L.N., Possingham, H.P., Freidenburg, L.K., Farrugia, T.J., Kinnison, M.T. and Hendry, A.P. (2007) Evolutionary responses to climate change. Conservation Ecology 21, 1353–1355.Google ScholarPubMed
Slattery, H.D. (1986) Physiological and genetic control of seed coat impermeability in subterranean clover (Trifolium subterraneum L.). The Journal of the Australian Institute of Agricultural Science 52, 58.Google Scholar
Smith, F.P., Cocks, P.S. and Ewing, M.A. (1998) Seed production in cluster clover (Trifolium glomeratum L.) 1. Flowering time, abortion, seed size, and hardseededness along branches. Australian Journal of Agricultural Research 49, 961–964.Google Scholar
Sriphadet, S., Lambrides, C.J. and Srinives, P. (2007) Inheritance of agronomic traits and their interrelationship in Mungbean (Vigna radiata (L.) Wilczek). Journal of Crop Science and Biotechnology 10, 249–256.Google Scholar
Storz, J.F. (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology 14, 671–688.CrossRefGoogle ScholarPubMed
Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Peterson, A.T., Phillips, O.L. and Williams, S.E. (2004) Extinction risk from climate change. Nature 427, 145–148.Google Scholar
Tozer, M.G. and Ooi, M.K.J. (2014) Humidity-regulated dormancy-onset in the Fabaceae: a conceptual model and its ecological implications for the Australian wattle Acacia saligna (Fabaceae (Labill.) H.L.Wendl). Annals of Botany 114, 579–590.Google Scholar
Trabaud, L. and Oustric, J. (1989) Heat requirements for seed germination of three Cistus species in the garrigue of southern France. Flora 183, 321–325.Google Scholar
Van Assche, J.A. and Vandelook, F.E.A. (2006) Germination ecology of eleven species of Geraniaceae and Malvaceae, with special reference to the effects of drying seeds. Seed Science Research 16, 263–290.Google Scholar
Van Assche, J.A. and Vandelook, F.E.A. (2010) Combinational dormancy in winter annual Fabaceae . Seed Science Research 20, 237–242.Google Scholar
Van der Veken, S., Bellemare, J., Verheyen, K. and Hermy, M. (2007) Life-history traits are correlated with geographical distribution patterns of western European forest herb species. Journal of Biogeography 34, 1723–1735.Google Scholar
van Klinken, R.D. and Flack, L. (2005) Wet heat as a mechanism for dormancy release and germination of seeds with physical dormancy. Weed Science 53, 663–669.Google Scholar
Vázquez-Yanes, C. and Orozco-Segovia, A. (1982) Seed germination of a tropical rain forest pioneer tree (Heliocarpus donnell-smithii) in response to diurnal fluctuation of temperature. Physiologia Plantarum 56, 295–298.Google Scholar
Veasey, E.A. and Martins, P.S. (1990) Variability in seed dormancy and germination potential in Desmodium Desv. (Leguminosae). Brazilian Journal of Genetics 14, 527–545.Google Scholar
Venable, D.L. (2007) Bet-hedging in a guild of desert annuals. Ecology 88, 1086–1090.Google Scholar
Walck, J.L., Hidayati, S.N., Dixon, K.W., Thompson, K. and Poschlod, P. (2011) Climate change and plant regeneration from seed. Global Change Biology 17, 2145–2161.Google Scholar
Whelan, R.J. (1995) The ecology of fire. Cambridge, Cambridge University Press.Google Scholar
Wulff, R.D. (1995) Environmental maternal effects on seed quality and germination. pp. 491–506 in Kigel, J.; Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker.Google Scholar
Zeng, L.W., Cocks, P.S., Kailis, S.G. and Kuo, J. (2005) The role of fractures and lipids in the seed coat in the loss of hardseededness of six Mediterranean legume species. Journal of Agricultural Science 143, 43–55.Google Scholar