Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-23T16:04:23.567Z Has data issue: false hasContentIssue false

Multiple fire-related cues stimulate germination in Chaenorhinum rubrifolium (Plantaginaceae), a rare annual in the Mediterranean Basin

Published online by Cambridge University Press:  12 January 2017

Çağatay Tavşanoğlu*
Affiliation:
Fire Ecology and Seed Research Laboratory, Division of Ecology, Department of Biology, Hacettepe University, Beytepe 06800, Ankara, Turkey
Gökhan Ergan
Affiliation:
Fire Ecology and Seed Research Laboratory, Division of Ecology, Department of Biology, Hacettepe University, Beytepe 06800, Ankara, Turkey
Ş. Serter Çatav
Affiliation:
Department of Biology, Muğla University, Kötekli 48000, Muğla, Turkey
Golshan Zare
Affiliation:
Division of Botany, Department of Biology, Hacettepe University, Beytepe 06800, Ankara, Turkey
Köksal Küçükakyüz
Affiliation:
Department of Biology, Muğla University, Kötekli 48000, Muğla, Turkey
Barış Özüdoğru
Affiliation:
Division of Botany, Department of Biology, Hacettepe University, Beytepe 06800, Ankara, Turkey
*
*Correspondence Email: ctavsan@hacettepe.edu.tr

Abstract

In Mediterranean fire-prone ecosystems, annual species specific to post-fire habitats should have a soil seed bank and should be able to germinate after a fire. Therefore, various fire-related cues can be expected to stimulate germination in post-fire annuals. Germination patterns of the rare annual Chaenorhinum rubrifolium (Plantaginaceae) were examined in response to mechanical scarification, heat shock, aqueous smoke, nitrogenous compounds, gibberellic acid, karrikinolide (KAR1), and mandelonitrile (a cyanohydrin analogue, MAN) under dark and photoperiod conditions in the laboratory. Combinations of these treatments were also included in the experiment. Strong physiological dormancy in the seeds of C. rubrifolium was partially broken by several fire-related germination cues, including smoke and nitrate, under light conditions. KAR1 and MAN also stimulated germination, and the highest improvement in germination was achieved in the KAR1 treatment in the presence of light. Heat shock + smoke and KAR1 + MAN combinations had positive synergetic and additive effects on germination under light conditions, respectively. The light played a crucial role in the promotion of germination. The results suggest that multiple fire-related cues operate to stimulate germination in C. rubrifolium, an annual species from the Mediterranean Basin. However, the species may have a broader germination niche than a fire-restricted one.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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

Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination, 2nd edition. San Diego, Elsevier/Academic Press.Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2015) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–9. See: https://CRAN.R-project.org/package=lme4 Google Scholar
Bell, D.T., King, L.A. and Plummer, J.A. (1999) Ecophysiological effects of light quality and nitrate on seed germination in species from Western Australia. Australian Journal of Ecology 24, 210.Google Scholar
Bethke, P.C., Libourel, I.G., Reinöhl, V. and Jones, R.L. (2006) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223, 805812.Google Scholar
Brown, N.A.C. (1993) Promotion of germination of fynbos seeds by plant-derived smoke. New Phytologist 123, 575583.Google Scholar
Çatav, Ş.S., Küçükakyüz, K., Akbaş, K. and Tavşanoğlu, Ç. (2014) Smoke-enhanced seed germination in Mediterranean Lamiaceae. Seed Science Research 24, 257264.Google Scholar
Çatav, Ş.S., Küçükakyüz, K., Tavşanoğlu, Ç. and Akbaş, K. (2015) Effects of aqueous smoke and nitrate treatments on the germination of 12 eastern Mediterranean plants. Annales Botanici Fennici 52, 93100.Google Scholar
Cembrowska-Lech, D. and Kępczyński, J. (2016) Gibberellin-like effects of KAR1 on dormancy release of Avena fatua caryopses include participation of non-enzymatic antioxidants and cell cycle activation in embryos. Planta 243, 531548.Google Scholar
Céspedes, B., Torres, I., Pérez, B., Luna, B. and Moreno, J.M. (2014) Burning season does not affect post-fire regeneration but fire alters the balance of the dominant species in a seeder-dominated Mediterranean shrubland. Applied Vegetation Science 17, 711725.Google Scholar
Cowling, R.M., Rundel, P.W. and Lamont, B.B. (1996) Plant diversity in Mediterranean-climate regions. Trends in Ecology and Evolution 11, 362366.Google Scholar
Daws, M.I., Davies, J., Pritchard, H.W., Brown, N.A. and Van Staden, J. (2007) Butenolide from plant-derived smoke enhances germination and seedling growth of arable weed species. Plant Growth Regulation 51, 7382.Google Scholar
Dixon, K.W., Merritt, D.J., Flematti, G.R. and Ghisalberti, E.L. (2009) Karrikinolide – a phytoreactive compound derived from smoke with applications in horticulture, ecological restoration and agriculture. Acta Horticulturae 813, 155170.CrossRefGoogle Scholar
Downes, K.S., Lamont, B.B., Light, M.E. and Van Staden, J. (2010) The fire ephemeral Tersonia cyathiflora (Gyrostemonaceae) germinates in response to smoke but not the butenolide 3-methyl-2H-furo [2, 3-c] pyran-2-one. Annals of Botany 106, 381384.Google Scholar
Downes, K.S., Light, M.E., Pošta, M., Kohout, L. and Van Staden, J. (2013) Comparison of germination responses of Anigozanthos flavidus (Haemodoraceae), Gyrostemon racemiger and Gyrostemon ramulosus (Gyrostemonaceae) to smoke-water and the smoke-derived compounds karrikinolide (KAR1) and glyceronitrile. Annals of Botany 111, 489497.Google Scholar
Downes, K.S., Light, M.E., Pošta, M., Kohout, L. and Van Staden, J. (2014) Do fire-related cues, including smoke-water, karrikinolide, glyceronitrile and nitrate, stimulate the germination of 17 Anigozanthos taxa and Blancoa canescens (Haemodoraceae)? Australian Journal of Botany 62, 347358.Google Scholar
Downes, K.S., Light, M.E., Pošta, M. and Van Staden, J. (2015) Fire-related cues and the germination of eight Conostylis (Haemodoraceae) taxa, when freshly collected, after burial and after laboratory storage. Seed Science Research 25, 286298.Google Scholar
Fichino, B.S., Dombroski, J.R., Pivello, V.R. and Fidelis, A. (2016) Does fire trigger seed germination in the Neotropical Savannas? Experimental tests with six Cerrado species. Biotropica 48, 181187.Google Scholar
Flematti, G.R., Merritt, D.J., Piggott, M.J., Trengove, R.D., Smith, S.M., Dixon, K.W. and Ghisalberti, E.L. (2011) Burning vegetation produces cyanohydrins that liberate cyanide and stimulate seed germination. Nature Communications 2, 360. doi: 10.1038/ncomms1356.Google Scholar
Flematti, G.R., Waters, M.T., Scaffidi, A., Merritt, D.J., Ghisalberti, E.L., Dixon, K.W. and Smith, S.M. (2013) Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds. Molecular Plant 6, 2937.Google Scholar
Ghebrehiwot, H.M., Kulkarni, M.G., Light, M.E., Kirkman, K.P. and Van Staden, J. (2011) Germination activity of smoke residues in soils following a fire. South African Journal of Botany 77, 718724.CrossRefGoogle Scholar
Ghebrehiwot, H.M., Kulkarni, M.G., Kirkman, K.P. and Van Staden, J. (2012) Smoke and heat: influence on seedling emergence from the germinable soil seed bank of mesic grassland in South Africa. Plant Growth Regulation 66, 119127.Google Scholar
Herranz, J.M., Ferrandis, P. and Copete, M.A. (2003) Influence of light and temperature on seed germination and ability of the endangered plant species Sisymbrium cavanillesianum to form persistent soil seed banks. Ecoscience 10, 532541.Google Scholar
Jäger, A.K., Light, M.E. and Van Staden, J. (1996) Effects of source of plant material and temperature on the production of smoke extracts that promote germination of light-sensitive lettuce seeds. Environmental and Experimental Botany 36, 421429.Google Scholar
Kavgacı, A., Čarni, A., Başaran, S., Başaran, M.A., Košir, P., Marinšek, A. and Šilc, U. (2010) Long-term post-fire succession of Pinus brutia forest in the east Mediterranean. International Journal of Wildland Fire 19, 599605.CrossRefGoogle Scholar
Kazanis, D. and Arianoutsou, M. (2004) Long-term post-fire vegetation dynamics in Pinus halepensis forests of Central Greece: a functional group approach. Plant Ecology 171, 101121.Google Scholar
Keeley, J.E. and Bond, W.J. (1997) Convergent seed germination in South African fynbos and Californian chaparral. Plant Ecology 133, 153167.Google Scholar
Keeley, J.E. and Fotheringham, C.J. (1998a). Mechanism of smoke-induced seed germination in a post fire chaparral annual. Journal of Ecology 86, 2736.Google Scholar
Keeley, J.E. and Fotheringham, C.J. (1998b) Smoke-induced seed germination in California chaparral. Ecology 79, 23202336.Google Scholar
Keeley, J.E. and Fotheringham, C.J. (2000) Role of fire in regeneration from seed. In Fenner, M. (ed), Seeds: The Ecology of Regeneration in Plant Communities, 2nd edition, pp. 311330. CAB International.Google Scholar
Keeley, J.E. and Pausas, J.G. (2016) Evolution of ‘smoke’ induced seed germination in pyroendemic plants. South African Journal of Botany. doi:10.1016/j.sajb.2016.07.012 Google Scholar
Keeley, J.E., Morton, B.A., Pedrosa, A. and Trotter, P. (1985) Role of allelopathy, heat and charred wood in the germination of chaparral herbs and suffrutescents. Journal of Ecology 73, 445458.Google Scholar
Keeley, J.E., Fotheringham, C.J. and Baer-Keeley, M. (2005) Factors affecting plant diversity during post-fire recovery and succession of mediterranean-climate shrublands in California, USA. Diversity and Distributions 11, 525537.Google Scholar
Keeley, J.E., Bond, W.J., Bradstock, R.A., Pausas, J.G. and Rundel, P.W. (2012) Fire in Mediterranean Ecosystems: Ecology, Evolution and Management. Cambridge, UK, Cambridge University Press.Google Scholar
Keith, D.A. (1997) Combined effects of heat shock, smoke and darkness on germination of Epacris stuartii Stapf., an endangered fire-prone Australian shrub. Oecologia 112, 340344.Google Scholar
Kȩpczyński, J. and Sznigir, P. (2014) Participation of GA3, ethylene, NO and HCN in germination of Amaranthus retroflexus L seeds with various dormancy levels. Acta Physiologiae Plantarum 36, 14631472.Google Scholar
Kos, M. and Poschlod, P. (2010) Why wait? Trait and habitat correlates of variation in germination speed among Kalahari annuals. Oecologia 162, 549559.Google Scholar
Koutsovoulou, K., Daws, M.I. and Thanos, C.A. (2014) Campanulaceae: a family with small seeds that require light for germination. Annals of Botany 113, 135143.Google Scholar
Light, M.E., Burger, B.V., Staerk, D., Kohout, L. and Van Staden, J. (2010) Butenolides from plant-derived smoke: Natural plant-growth regulators with antagonistic actions on seed germination. Journal of Natural Products 73, 267269.Google Scholar
Long, R.L., Stevens, J.C., Griffiths, E.M., Adamek, M., Gorecki, M.J., Powles, S.B. and Merritt, D.J. (2011) Seeds of Brassicaceae weeds have an inherent or inducible response to the germination stimulant karrikinolide. Annals of Botany 108, 933944.Google Scholar
Luna, B. and Moreno, J.M. (2009) Light and nitrate effects on seed germination of Mediterranean plant species of several functional groups. Plant Ecology 203, 123135.Google Scholar
Luna, B., Pérez, B., Torres, I. and Moreno, J.M. (2012) Effects of incubation temperature on seed germination of Mediterranean plants with different geographical distribution ranges. Folia Geobotanica 47, 1727.Google Scholar
Merritt, D.J., Kristiansen, M., Flematti, G.R., Turner, S.R., Ghisalberti, E.L., Trengove, R.D. and Dixon, R.D. (2006) Effects of a butenolide present in smoke on light-mediated germination of Australian Asteraceae. Seed Science Research 16, 2935.Google Scholar
Moreira, B. and Pausas, J.G. (2016) Shedding light through the smoke on the germination of Mediterranean Basin flora. South African Journal of Botany. doi:10.1016/j.sajb.2016.10.008 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
Moreira, B., Tavsanoglu, Ç. and Pausas, J.G. (2012) Local versus regional intraspecific variability in regeneration traits. Oecologia 168, 671677.Google Scholar
Paula, S., Arianoutsou, M., Kazanis, D., Tavsanoglu, Ç., Lloret, F., Buhk, C., Ojeda, F., Luna, B., Moreno, J.M., Rodrigo, A., Espelta, J.M., Palacio, S., Fernández-Santos, B., Fernandes, P.M. and Pausas, J.G. (2009) Fire-related traits for plant species of the Mediterranean Basin. Ecology 90, 1420.Google Scholar
Pausas, J.G. and Keeley, J.E. (2009) A burning story: the role of fire in the history of life. BioScience 59, 593601.Google Scholar
Pausas, J.G. and Keeley, J.E. (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytologist 204, 5565.Google Scholar
Pérez-Fernández, M.A. and Rodríguez-Echeverría, S. (2003) Effect of smoke, charred wood, and nitrogenous compounds on seed germination of ten species from woodland in central-western Spain. Journal of Chemical Ecology 29, 237251.Google Scholar
Peinado, M., Bartolomé, C. and Martínez-Parraz, J.M. (1985) Notas sobre vegetación nitrófila, I. Studia Botanica 4, 2733.Google Scholar
Preston, C.A. and Baldwin, I.T. (1999) Positive and negative signals regulate germination in the post-fire annual, Nicotiana attenuata . Ecology 80, 481494.Google Scholar
Roy, J. and Arianoutsou-Faraggitaki, M. (1985) Light quality as the environmental trigger for the germination of the fire-promoted species Sarcopoterium spinosum L. Flora 177, 345349.Google Scholar
Tavşanoğlu, Ç., Çatav, Ş.S. and Özüdoğru, B. (2015) Fire-related germination and early seedling growth in 21 herbaceous species in Central Anatolian steppe. Journal of Arid Environments 122, 109116.Google Scholar
Thanos, C.A. (1993) Germination ecophysiology of Mediterranean aromatic plants. In Come, D. and Corbineau, F. (eds), Proceedings of the Fourth International Workshop on Seeds, pp. 281287. Basic and Applied Aspects of Seed Biology. Paris, ASFIS.Google Scholar
Thanos, C.A. and Rundel, P.W. (1995) Fire-followers in chaparral: nitrogenous compounds trigger seed germination. Journal of Ecology 83, 207216.Google Scholar
Thomas, P.B., Morris, E.C. and Auld, T.D. (2003) Interactive effects of heat shock and smoke on germination of nine species forming soil seed banks within the Sydney region. Austral Ecology 28, 674683.Google Scholar
Tieu, A., Dixon, K.W., Meney, K.A. and Sivasithamparam, K. (2001) The interaction of heat and smoke in the release of seed dormancy in seven species from southwestern Western Australia. Annals of Botany 88, 259265.Google Scholar
Todorović, S., Božić, D., Simonović, A., Filipović, B., Dragićević, M., Giba, Z. and Grubišić, D. (2010) Interaction of fire-related cues in seed germination of the potentially invasive species Paulownia tomentosa Steud. Plant Species Biology 25, 193202.Google Scholar
Tormo, J., Moreira, B. and Pausas, J.G. (2014) Field evidence of smoke-stimulated seedling emergence and establishment in Mediterranean Basin flora. Journal of Vegetation Science 25, 771777.Google Scholar
Traba, J., Azcárate, F.M. and Peco, B. (2004) From what depth do seeds emerge? A soil seed bank experiment with Mediterranean grassland species. Seed Science Research 14, 297303.Google Scholar
Van Staden, J., Jäger, A.K., Light, M.E., Burger, B.V., Brown, N.A.C. and Thomas, T.H. (2004) Isolation of the major germination cue from plant-derived smoke. South African Journal of Botany 70, 654659.Google Scholar
Venable, D.L. and Brown, J.S. (1988) The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. American Naturalist 131, 360384.Google Scholar
Venable, D.L. and Brown, J.S. (1993) The population-dynamic functions of seed dispersal. Plant Ecology 107, 3155.Google Scholar
Williams, P.R., Congdon, R.A., Grice, A.C. and Clarke, P.J. (2003) Fire-related cues break seed dormancy of six legumes of tropical eucalypt savannas in north-eastern Australia. Austral Ecology 28, 507514.Google Scholar