Delayed effect of thermal treatment on breaking physical seed dormancy: intrapopulation variation and implications for soil seed banks
Miguel A. Copete Carreño A B * , Elena Copete Carreño A B , Pablo Ferrandis Gotor A B and Jose M. Herranz Sanz A BA
B
Abstract
Many studies have focused on the dormancy-breaking response to heat treatment of freshly matured seeds and immediately after thermal shock.
We evaluated whether the full effect of dry heat scarification in freshly matured seeds could be delayed over time and the possible influence of previous storage in the soil.
Adenocarpus argyrophyllus was the model species selected to explore our hypotheses by analysing the: (a) influence of scarification treatments; (b) seedling emergence during 5 years after dry heat scarification of freshly matured seeds, and evaluating intrapopulation variation; (c) seedling emergence after dry heat scarification of seeds rescued from soil; and (d) ability to form persistent soil seed banks.
Dry heat scarification of freshly matured seeds only resulted in 22.5% germination. However, exposure to pre-sowing thermal shock stimulated seedling emergence during the first few years post-planting, with high intrapopulation variation. In seeds recovered from soil, thermal shock before reseeding increased the seedling emergence rate.
Our results show that, to avoid incomplete interpretation, studies of thermal treatment on the breaking of physical seed dormancy should allow the seeds sufficient time to exhibit the complete effects of high temperature treatment, thereby preventing underestimation.
Keywords: Adenocarpus, fire-prone ecosystems, germination, hard-seededness, heat scarification, Leguminosae, Mediterranean climate, post-fire regeneration, seedling emergence, soil seed bank.
References
Auld TD, O’Connell MA (1991) Predicting patterns of post-fire germination in 35 eastern Australian Fabaceae. Australian Journal of Ecology 16, 53-70.
| Crossref | Google Scholar |
Bakker JP, Poschlod P, Strykstra RJ, Bekker RM, Thompson K (1996) Seed banks and seed dispersal: Important topics in restoration ecology. Acta Botanica Neerlandica 45, 461-490.
| Crossref | Google Scholar |
Baskin JM, Baskin CC (1989) Physiology of dormancy and germination in relation to seed bank ecology. In ‘Ecology of soil seed banks’. (Eds MA Leck, VT Thomas, RL Simpson) pp. 53–66. (Academic Press: San Diego) 10.1016/B978-0-12-440405-2.50009-9
Bradstock RA, Auld TD (1995) Soil temperatures during experimental bushfires in relation to fire intensity: consequences for legume germination and fire management in south-eastern Australia. Journal of Applied Ecology 32, 76-84.
| Crossref | Google Scholar |
Brits GJ, Manning JC (2019) Seed structure and physiology in relation to recruitment ecology in Leucospermum (Proteaceae) in fynbos. Australian Journal of Botany 67(4), 290-308.
| Crossref | Google Scholar |
Clemente AS, Rego FC, Correia OA (1996) Demographic patterns and productivity of post-fire regeneration in Portuguese Mediterranean maquis. International Journal of Wildland Fire 6, 5-12.
| Crossref | Google Scholar |
Copete MA, Herranz JM, Ferrandis P, Copete E (2015) Annual dormancy cycles in buried seeds of shrub species: germination ecology of Sideritis serrata (Labiatae). Plant Biology 17, 798-807.
| Crossref | Google Scholar | PubMed |
Cushwa CT, Martin RE, Miller RL (1968) The effects of fire on seed germination. Journal of Range Management 21(4), 250-254.
| Crossref | Google Scholar |
Daibes LF, Pausas JG, Bonani N, Nunes J, Silveira FAO, Fidelis A (2019) Fire and legume germination in a tropical savanna: ecological and historical factors. Annals of Botany 123(7), 1219-1229.
| Crossref | Google Scholar | PubMed |
Fenner M, Thompson K (2005) ‘The ecology of seeds.’ (Cambridge University Press: Cambridge) 10.1017/CBO9780511614101
Ferrandis P, Herranz JM, Martínez-Sánchez JJ (1999a) Effect of fire on hard-coated Cistaceae seed banks and its influence on techniques for quantifying seed banks. Plant Ecology 144, 103-114.
| Crossref | Google Scholar |
Ferrandis P, Herranz JM, Martínez-Sánchez JJ (1999b) Fire impact on a maquis soil seed bank in Cabañeros National Park (Central Spain). Israel Journal of Plant Sciences 47, 17-26.
| Crossref | Google Scholar |
Gama-Arachchige NS, Baskin JM, Geneve RL, Baskin CC (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.
| Crossref | Google Scholar | PubMed |
Gómez-González S, Cavieres LA (2009) Litter burning does not equally affect seedling emergence of native and alien species of the Mediterranean-type Chilean matorral. International Journal of Wildland Fire 18, 213-221.
| Crossref | Google Scholar |
Herranz JM, Ferrandis P, Martínez-Sánchez JJ (1998) Influence of heat on seed germination of seven Mediterranean Leguminosae species. Plant Ecology 136, 95-103.
| Crossref | Google Scholar |
Herranz JM, Ferrandis P, Martínez-Sánchez JJ (1999) Influence of heat on seed germination of nine woody Cistaceae species. International Journal of Wildland Fire 9(3), 173-182.
| Crossref | Google Scholar |
Herranz JM, Ferrandis P, Copete MA (2003a) Influence of light and temperature on seed germination and ability of the endangered plant species Sisymbrium cavanillesianum to form persistent soil seed banks. Écoscience 10(4), 532-541.
| Crossref | Google Scholar |
Herranz JM, Ferrandis P, Copete MA (2003b) Influence of temperature, matorral source, and seed position in fruit on seed germination and ability to form soil seed banks in threatened species of Coincya (Cruciferae). Israel Journal of Plant Sciences 51, 133-141.
| Crossref | Google Scholar |
Holmes PM, Newton RJ (2004) Patterns of seed persistence in South African fynbos. Plant Ecology 172, 143-158.
| Crossref | Google Scholar |
Huerta S, Marcos E, Fernández-García V, Calvo L (2022) Resilience of Mediterranean communities to fire depends on burn severity and type of ecosystem. Fire Ecology 18, 28.
| Crossref | Google Scholar |
Jastrzębowski S, Ukalska J, Kantorowicz W, Klisz M, Wojda T, Sułkowska M (2017) Effects of thermal-time artificial scarification on the germination dynamics of black locust (Robinia pseudoacacia L.) seeds. European Journal of Forest Research 136, 471-479.
| Crossref | Google Scholar |
Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2011) ‘Fire in Mediterranean ecosystems: ecology, evolution and management.’ (Cambridge University Press: New York) 10.1017/CBO9781139033091
Kimura E, Islam MA (2012) Seed scarification methods and their use in forage legumes. Research Journal of Seed Science 5, 38-50.
| Crossref | Google Scholar |
Liao J, De Boeck HJ, Li Z, Nijs I (2015) Gap formation following climatic events in spatially structured plant communities. Scientific Reports 5, 11721.
| Crossref | Google Scholar | PubMed |
Liyanage GS, Ooi MKJ (2015) Intra-population level variation in thresholds for physical dormancy-breaking temperature. Annals of Botany 116, 123-131.
| Crossref | Google Scholar | PubMed |
Magaña Ugarte R, Redondo MM, Sánchez-Mata D (2021) Evaluating the post-fire natural regeneration of Mediterranean-type scrublands in Central Spain. Mediterranean Botany 42, e67331.
| Crossref | Google Scholar |
Martínez-Duro E, Ferrandis P, Herranz JM, Copete MA (2010) Do seed harvesting ants threaten the viability of a critically endangered non-myrmecochorous perennial plant population? A complex interaction. Population Ecology 52, 397-405.
| Crossref | Google Scholar |
Minnich RA, Bahre CJ (1995) Wildland fire and chaparral succession along the California–Baja California boundary. International Journal of Wildland Fire 5, 13-24.
| Crossref | Google Scholar |
Mira S, Schnadelbach A, Correa EC, Pérez-García F, González-Benito ME (2017) Variability of physical dormancy in relation to seed mechanical properties of three legume species. Seed Science and Technology 45, 540-556.
| Crossref | Google Scholar |
Moreno Marcos G, Gómez Gutiérrez JM, Fernández Santos B (1992) Primary dispersal of Cytisus multiflorus seeds. Pirineos 140, 75-88.
| Crossref | Google Scholar |
Ocampo-Zuleta K, Gómez-González S, Paula S (2022) Generalised seed mortality driven by heat shock in woody plants from Mediterranean Chile. International Journal of Wildland Fire 31(11), 1080-1088.
| Crossref | Google Scholar |
Odion DC, Davis FW (2000) Fire, soil heating, and the formation of vegetation patterns in chaparral. Ecological Monographs 70, 149-169.
| Crossref | Google Scholar |
Ooi MKJ (2012) Seed bank persistence and climate change. Seed Science Research 22(S1), S53-S60.
| Crossref | Google Scholar |
Ooi MKJ, Auld TD, Denham AJ (2009) Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Global Change Biology 15(10), 2375-2386.
| Crossref | Google 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(5), 656-671.
| Crossref | Google Scholar | PubMed |
Pausas JG, Keeley JE (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytologist 204, 55-65.
| Crossref | Google Scholar | PubMed |
Pausas JG, Lamont BB (2022) Fire-released seed dormancy – a global synthesis. Biological Reviews 97, 1612-1639.
| Crossref | Google Scholar | PubMed |
Pausas JG, Bradstock RA, Keith DA, Keeley JE, , GCTE Fire Network (2004) Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85, 1085-1100.
| Crossref | Google Scholar |
Pausas JG, Lamont BB, Keeley JE, Bond WJ (2022) Bet-hedging and best-bet strategies shape seed dormancy. New Phytologist 236, 1232-1236.
| Crossref | Google Scholar | PubMed |
Pereiras J, Puentes MA, Casal M (1985) Efecto de las altas temperaturas sobre la germinación de las semillas del tojo (Ulex europaeus L.). Studia Oecologica 6, 125-133 [In Spanish].
| Google Scholar |
Pérez-Fernández MA, Gómez-Gutiérrez JM, Martín-Berrocoso A, Mann R (2002) Effect of seed shape and size on their distribution in the soil seed bank. Journal of Mediterranean Ecology 3(4), 11-17.
| Google Scholar |
Pérez-García F (2009) Germination characteristics and intrapopulation variation in carob (Ceratonia siliqua L.) seeds. Spanish Journal of Agricultural Research 7(2), 398-406.
| Crossref | Google Scholar |
Rivas M, Reyes O, Casal M (2006) Influence of heat and smoke treatments on the germination of six Leguminous shrubby species. International Journal of Wildland Fire 15, 73-80.
| Crossref | Google Scholar |
Robles AB, Castro J, González-Miras E, Ramos ME (2005) Effects of ruminal incubation and goats’ ingestion on seed germination of two legume shrubs: Adenocarpus decorticans Boiss. and Retama sphaerocarpa (L.) Boiss. Options Mèditerranées: Serie A 67, 111-115.
| Google Scholar |
Rolston MP (1978) Water impermeable seed dormancy. The Botanical Review 44, 365-396.
| Crossref | Google Scholar |
Rosbakh S, Carta A, Fernández-Pascual E, Phartyal SS, Dayrell RLC, Mattana E, Saatkamp A, Vandelook F, Baskin J, Baskin C (2023) Global seed dormancy patterns are driven by macroclimate but not fire regime. New Phytologist 240(2), 555-564.
| Crossref | Google Scholar | PubMed |
Shi YF, Shi SH, Jiang YS, Liu J (2022) A global synthesis of fire effects on soil seed banks. Global Ecology and Conservation 36, e02132.
| Crossref | Google Scholar |
Stamp NE, Lucas JR (1983) Ecological correlates of explosive seed dispersal. Oecologia 59, 272-278.
| Crossref | Google Scholar | PubMed |
Tarrega R, Calvo L, Trabaud L (1992) Effect of high temperatures on seed germination of two woody Leguminosae. Vegetatio 102, 139-147.
| Crossref | Google Scholar |
Thanos CA, Georghiou K (1988) Ecophysiology of fire-stimulated seed germination in Cistus incanus ssp. creticus (L.) Hey wood and C. salvifolius L. Plant, Cell and Environment 11, 841-849.
| Crossref | Google Scholar |
Thanos CA, Georghiou K, Kadis C, Pantazi C (1992) Cistaceae: a plant family with hard seeds. Israel Journal of Botany 41, 251-263.
| Crossref | Google Scholar |
Thompson K, Grime JP (1979) Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology 67, 893-921.
| Crossref | Google Scholar |
Thompson K, Bakker J, Bekker R (1997) ‘The soil seed banks of north-west Europe: methodology, density and longevity.’ (Cambridge University Press: Cambridge) 10.1017/S0960258500003676
Trabaud L. (1979) Etude du comportement du feu dans la Garrigue de Chêne kermès à partir des températures et des vitesses de propagation. Annales des Sciences Forestières 36(1), 13-38 [In French].
| Crossref | Google Scholar |
Van Der Burgt XM (1997) Explosive seed dispersal of the rainforest tree Tetraberlinia moreliana (Leguminosae—Caesalpinioideae) in Gabon. Journal of Tropical Ecology 13, 145-151.
| Crossref | Google Scholar |
Van Klinken RD, Lukitsch B, Cook C (2008) Interaction between seed dormancy-release mechanism, environment and seed bank strategy for a widely distributed perennial legume, Parkinsonia aculeata (Caesalpinaceae). Annals of Botany 102(2), 255-264.
| Crossref | Google Scholar | PubMed |