Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T06:04:30.707Z Has data issue: false hasContentIssue false

Do dormancy-breaking temperature thresholds change as seeds age in the soil seed bank?

Published online by Cambridge University Press:  29 December 2016

Ganesha S. Liyanage*
Affiliation:
Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
Mark K.J. Ooi
Affiliation:
Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia
*
*Correspondence Email: [email protected]

Abstract

In fire-prone ecosystems, many species regenerate after fire from persistent soil seed banks. Species with physically dormant (PY) seeds have dormancy broken by fire-related heat. The magnitude of post-fire recruitment, to predict response to varying fire severity, is commonly estimated by testing dormancy-breaking temperature thresholds of fresh PY seeds. However, seeds spend years in the soil during the inter-fire period, and determining whether dormancy-breaking thresholds change over time is essential to accurately predict population persistence. Germination of four south-eastern Australian PY species from the Fabaceae family (Acacia linifolia, Aotus ericoides, Bossiaea heterophylla and Viminaria juncea) were studied. Dormancy-breaking temperature thresholds vary inter-specifically and the species represented either high or low dormancy-breaking threshold classes. Freshly collected seeds, and seeds that had been buried in the field or stored in dry laboratory conditions for 6 and 18 months were subjected to a fire-related range of heat treatments (40–100°C). Seed ageing increased germination response to heat treatments, effectively lowering the dormancy-breaking thresholds of three species. The fourth species, A. linifolia, initially had a relatively large non-dormant fraction which was lost as seeds aged, with older seeds then displaying PY broadly similar to the other study species. Patterns of threshold decay were species-specific, with the thresholds and viability of low-threshold species declining more rapidly than high-threshold species. The non-dormant fraction did not increase over time for any of our study species. Instead of increasing their non-dormant fraction, as is common in other vegetation types, these fire-prone PY species displayed a change of dormancy-breaking temperature thresholds. This is an important distinction, as maintaining dormancy during the inter-fire period is essential for population persistence. While changes in sensitivity to dormancy-breaking treatments have previously been reported as seeds age, our study provides the first test of changes to temperature thresholds, which increases the range of germination response from the seed bank under varying fire severity.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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

Akaike, H. (1973) Information theory as an extension of the maximum likelihood principle. In Petrov, B.N. and Csaki, F. (eds), Proceedings of the Second International Symposium on Information Theory, pp. 267281. Budapest, Akademiai Kiado.Google Scholar
Auld, T.D. (1986) Population dynamics of the shrub Acacia suaveolens (SM) Willd.: Dispersal and the dynamics of the soil seed-bank. Australian Journal of Ecology 11, 235254.CrossRefGoogle Scholar
Auld, T.D. and Bradstock, R.A. (1996) Soil temperatures after the passage of a fire: Do they influence the germination of buried seeds? Australian Journal of Ecology 21, 106109.Google Scholar
Auld, T.D. and O'Connell, M.A. (1991) Predicting patterns of post-fire germination in 35 eastern Australian Fabaceae. Australian Journal of Ecology 16, 5370.Google Scholar
Auld, T.D., Keith, D.A. and Bradstock, R.A. (2000) Patterns in longevity of soil seedbanks in fire-prone communities of South-eastern Australia. Annals of Botany 48, 539548.Google Scholar
Australian Government Bureau of Meteorology (2016) Climate Data Online. Available at: http://www.bom.gov.au/climate/data Google Scholar
Baker, K.S., Steadman, K.J., Plummer, J.A., Merritt, D.J. and Dixon, K.W. (2005) Dormancy release in Australian fire ephemeral seeds during burial increases germination response to smoke water or heat. Seed Science Research 15, 339348.Google Scholar
Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination. San Diego, Academic Press.Google Scholar
Benvenuti, S. (2007) Natural weed seed burial: effect of soil texture, rain and seed characteristics. Seed Science Research 17, 211219.Google Scholar
Bond, W.J., Honig, M. and Maze, K.E. (1999) Seed size and seedling emergence: an allometric relationship and some ecological implications. Oecologia 120, 132136.Google Scholar
Bradstock, R.A. and Auld, T.D. (1995) Soil temperatures during experimental bushfires in relation to fire intensity: consequences for legume and fire management in south-eastern Australia. Journal of Applied Ecology 32, 7684.Google Scholar
Bradstock, R.A. and Kenny, B.J. (2003) An application of plant functional types to fire management in a conservation reserve in south-eastern Australia. Journal of Vegetation Science 14, 345354.Google Scholar
Bradstock, R.A., Auld, T.D., Ellis, M.E. and Cohn, J.S. (1992) Soil temperatures during bushfire in semi-arid, mallee shrublands. Australian Journal of Ecology 17, 433440.Google Scholar
Chambers, J.C. and MacMahon, J.A. (1994) A day in the life of a seed: Movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25, 263292.CrossRefGoogle Scholar
Fenner, M. and Thompson, K. (2005) The Ecology of Seeds. Cambridge, Cambridge University Press.Google Scholar
Galíndez, G., Ortega-Baes, P., Seal, C.E., Daws, M.I., Scopel, A.L. and Pritchard, H.W. (2010) Physical seed dormancy in Collaea argentina (Fabaceae) and Abutilon pauciflorum (Malvaceae) after 4 years storage. Seed Science and Technology 38, 777782.CrossRefGoogle Scholar
González-Rabanal, F. and Casal, M. (1995) Effect of high-temperature and ash on germination of 10 species from Gorse shrubland. Vegetation 116, 123131.Google Scholar
Hanley, M.E., Unna, J.E. and Darvill, B. (2003) Seed size and germination response: a relationship for fir-following plant species exposed to thermal shock. Oecologia 134, 1822.Google Scholar
Hudson, A.R., Ayre, D.J. and Ooi, M.K.J. (2015) Physical dormancy in a changing climate. Seed Science Research 25, 6681.Google Scholar
Jeffery, 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, 2834.CrossRefGoogle Scholar
Keeley, J.E. (1991) Seed germination and life-history syndromes in the California chaparral. Botanical Review 57, 81116.Google Scholar
Keith, D.A., Williams, J.E. and Woinarski, J.C.Z. (2002) Fire management and biodiversity conservation: key approaches and principles. In Bradstock, R.A., Williams, J.E. and Gill, M.A. (eds), Flammable Australia: the Fire Regimes and Biodiversity of a Continent, pp. 401428. London, Cambridge University Press.Google Scholar
Liyanage, G.S. and Ooi, M.K.J. (2015) Intra-population level variation in threshold for physical dormancy-breaking temperature. Annals of Botany 116, 123131.Google Scholar
Liyanage, G.S., Ayre, D.J. and Ooi, M.K.J. (2016) Seedling performance covaries with dormancy thresholds: maintaining cryptic seed heteromorphism in a fire-prone system. Ecology 97, 30093018.Google Scholar
Marthews, T.R., Mullins, C.E., Dalling, J.W. and Burslem, D.F.R.P. (2008) Burial and secondary dispersal of small seeds in a tropical forest. Journal of Tropical Ecology 24, 595605.Google Scholar
McLoughlin, L.C. (1998) Season of burning in the Sydney region: the historical records compared with recent prescribed burning. Australian Journal of Ecology 23, 393404.Google Scholar
Moreira, B., Tormo, J., Estrelles, E. and Pausas, J.G. (2010) Disentangling the role of heat and smoke as germination cues in Mediterranean basin flora. Annals of Botany 105, 627635.Google Scholar
Morrison, D.A., Auld, T.D., Rish, S., Porter, C. and McClay, K. (1992) Patterns of testa-imposed seed dormancy in native Australian legumes. Annals of Botany 70, 157163.Google Scholar
Ooi, M.K.J. (2015) Seed bank dynamics and climate change in semi-arid ecosystems: a focus on physically dormant species. Revista Brasileira de Geografia Física 8, 651659.Google Scholar
Ooi, M.K.J. (2007) Dormancy classification and potential dormancy-breaking cues for shrub species from fire-prone south-eastern Australia. In Adkins, S.W., Ashmore, S. and Navie, S.C. (eds), Seed: Biology, Development and Ecology, pp. 205216. Wallingford, CABI Publishing.Google 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, 23752386.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 and Soil 353, 289303.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, 656671.CrossRefGoogle ScholarPubMed
Orscheg, C.K. and Enright, N.J. (2011) Patterns of seed longevity and dormancy in obligate seeding legumes of box-ironbark forests, south-eastern Australia. Austral Ecology 36, 185194.Google Scholar
Parmesan, C. and Hanley, M.E. (2015) Plants and climate change: complexities and surprises. Annals of Botany 116, 849864.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, 496503.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 5, 572578.Google Scholar
Pukittayacamee, P. and Hellum, A.K. (1988) Seed germination in Acacia auriculiformis: developmental aspects. Canadian Journal of Botany 66, 388393.Google Scholar
R Core Development Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. See: http://www.R-project.org/ Google Scholar
Roche, S., Dixon, K.W. and Pate, J.S. (1997) Seed ageing and smoke: Partner cues in the amelioration of seed dormancy in selected Australian native species. Australian Journal of Botany 45, 783815.Google Scholar
Santana, V.M., Baeza, M.J. and Blanes, M.C. (2013) Clarifying the role of heat and daily temperature fluctuations as germination cues for Mediterranean Basin obligate seeders. Annals of Botany 111, 127134.Google Scholar
Santana, V.M., Bradstock, R.A., Ooi, M.K.J., Denham, A.J., Auld, T.D. and Baeza, M.J. (2010) Effects of soil temperature regimes after fire on seed dormancy and germination in six Australian Fabaceae species. Australian Journal of Botany 58, 539545.Google Scholar
Schatral, A. (1996) Dormancy in seeds of Hibbertia hypericoides (Dilleniaceae). Australian Journal of Botany 44, 213222.Google Scholar
Thanos, C.A., Georghiou, K., Kadis, C. and Pantazi, C. (1992) Cistaceae: a plant family with hard seeds. Israel Journal of Botany 41, 251263.Google Scholar
Tieu, A., Dixon, K.W., Meney, K.A. and Sivasithamparam, K. (2001) Interaction of soil burial and smoke on germination patterns in seeds of selected Australian native plants. Seed Science Research 11, 6976.Google Scholar
Tozer, M. 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 . Annals of Botany 114, 579590.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, 321325.Google Scholar
Turner, S.R., Steadman, K.J., VIahos, S., Koch, J.M. and Dixon, K.W. (2013) Seed treatment optimizes benefits of seed bank storage for restoration-ready seeds: the feasibility of pre-storage dormancy alleviation for mine-site revegetation. Restoration Ecology 21, 186192.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, 283290.Google Scholar
van Staden, J., Kelly, K.M. and Bell, W.E. (1994) The role of natural agents in the removal of coat-imposed dormancy in Dichrostachys cinerea (L.) Wight et Arn. Seeds. Plant Growth Regulation 14, 5159.Google Scholar
Whelen, R.J. (1995) The Ecology of Fire, London, Cambridge University Press.Google Scholar
Williams, R.J., Congdon, R.A., Grice, A.C. and Clarke, P. (2004) Soil temperature and depth of legume germination during early and late dry season fires in a tropical eucalypt savannah of north-east Australia . Australian Journal of Ecology 29, 258263.Google Scholar
Wills, T.J. and Read, J. (2002) Effects of heat and smoke on germination of soil-stored seed in a south-eastern Australian sand heathland. Australian Journal of Botany 50, 197206.Google Scholar
Wright, B.R., Latz, P.K. and Zuur, A.F. (2015) Fire severity mediates seedling recruitment patterns in slender mulga (Acacia aptaneura), a fire-sensitive Australian desert shrub with heat-stimulated germination. Plant Ecology 217, 789800.Google Scholar
Zalamea, P., Sarmiento, C., Arnold, A.E., Davis, A.S. and Dalling, J.W. (2015) Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers? Frontiers in Plant Science 5. See: https://doi.org/10.3389/fpls.2014.00799 4355.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 hradseededness of six Mediterranean legume species. Journal of Agricultural Science 143, 4355.Google Scholar