Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-28T17:42:07.569Z Has data issue: false hasContentIssue false

From germination to seedling development: the effects of smoke on a native and an invasive grass species of the Cerrado

Published online by Cambridge University Press:  05 August 2022

Luís G.F. Sanchez
Affiliation:
Laboratório de Ecologia do Fogo, Departamento de Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF, Brazil
Ademar B. Dantas-Junior*
Affiliation:
Laboratório de Ecologia do Fogo, Departamento de Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF, Brazil
Ana Clara C.Q. Porto
Affiliation:
Laboratório de Ecologia do Fogo, Departamento de Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF, Brazil
Carolina Musso
Affiliation:
Laboratório de Ecologia do Fogo, Departamento de Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF, Brazil
Margarete N. Sato
Affiliation:
Laboratório de Ecologia do Fogo, Departamento de Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF, Brazil
Heloisa S. Miranda
Affiliation:
Laboratório de Ecologia do Fogo, Departamento de Ecologia, Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, DF, Brazil
*
*Correspondence: Ademar B. Dantas-Junior, E-mail: abarbosadantasjunior@gmail.com

Abstract

The Brazilian Cerrado, a Neotropical savanna, is a fire-prone ecosystem where the ground layer biomass consists mainly of graminoids. However, as for other savannas, the effects of fire cues (such as smoke) on Cerrado grasses do not present a clear pattern, either for germination or seedling development. Smoke can stimulate different stages of the plant life cycle, which can alter the community and invasion processes. So far, most research on the subject focuses on germination, not addressing post-germinative phases, a sensitive stage of plant development. Here, we investigated the effect of smoke on a native (Echinolaena inflexa) and an invasive (Urochloa decumbens) grass species common in the Cerrado. We analysed germinative parameters and seedling mass and length after exposing the seeds to dry smoke for 5, 10, 15 or 20 min. Seedling development was assessed by measuring shoot and root systems after cultivating germinated seeds for 3, 7 or 15 d. Smoke did not affect germination percentages. However, fumigation reduced the mean germination time of both species and the germination onset of E. inflexa. U. decumbens had higher length values in all periods of cultivation, whereas mass values only surpassed that of E. inflexa at 15 d. Smoke exposure reduced the aboveground length of 7-d seedlings of U. decumbens, and mass of 15-d plants of both species. Also, smoke enhanced the root investment of the native and invasive species in different cultivation periods. Therefore, studying post-germinative parameters on seedling development may bring further insights into the smoke effects.

Type
Short Communication
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Aires, SS, Sato, MN and Miranda, HS (2014) Seed characterization and direct sowing of native grass species as a management tool. Grass and Forage Science 69, 470478.CrossRefGoogle Scholar
Andrade, LAZ and Miranda, HS (2014) The dynamics of the soil seed bank after a fire event in a woody savanna in central Brazil. Plant Ecology 215, 11991209.CrossRefGoogle Scholar
Assis, GB, Pilon, NA, Siqueira, MF and Durigan, G (2021) Effectiveness and costs of invasive species control using different techniques to restore Cerrado grasslands. Restoration Ecology 29, e13219.CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Baxter, BJM, Van Staden, J, Granger, JE and Brown, NAC (1994) Plant-derived smoke and smoke extracts stimulate seed germination of the fire-climax grass Themeda triandra. Environmental and Experimental Botany 34, 217223.CrossRefGoogle Scholar
Blank, RR and Young, JA (1998) Heated substrate and smoke: influence on seed emergence and plant growth. Journal of Range Management 51, 577583.CrossRefGoogle Scholar
Bond, WJ and Keeley, JE (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends in Ecology & Evolution 20, 387394.CrossRefGoogle ScholarPubMed
Brasil (2009) Regras para análise de sementes. Brasília, Brazil, Ministério da Agricultura.Google Scholar
Brooks, ME, Kristensen, K, Darrigo, MR, Rubim, P, Uriarte, M, Bruna, E and Bolker, BM (2019) Statistical modeling of patterns in annual reproductive rates. Ecology 100, e02706.CrossRefGoogle ScholarPubMed
Castro, EA and Kauffman, JB (1998) Ecosystem structure in the Brazilian Cerrado: a vegetation gradient of aboveground biomass, root mass and consumption by fire. Journal of Tropical Ecology 14, 263283.CrossRefGoogle Scholar
Clarke, S and French, K (2005) Germination response to heat and smoke of 22 Poaceae species from grassy woodlands. Australian Journal of Botany 53, 445454.CrossRefGoogle Scholar
Correia, GGDS and Martins, SV (2015) Banco de sementes do solo de floresta restaurada, Reserva Natural Vale, ES. Floresta e Ambiente 22, 7987.CrossRefGoogle Scholar
Curtis, NP (1998) A post-fire ecological study of Xanthorrhoea australis following prescribed burning in the Warby Range State Park, North-eastern Victoria, Australia. Australian Journal of Botany 46, 253272.CrossRefGoogle Scholar
Dairel, M and Fidelis, A (2020a) How does fire affect germination of grasses in the Cerrado? Seed Science Research 30, 275283.CrossRefGoogle Scholar
Dairel, M and Fidelis, A (2020b) The presence of invasive grasses affects the soil seed bank composition and dynamics of both invaded and non-invaded areas of open savannas. Journal of Environmental Management 276, 111291.CrossRefGoogle Scholar
Damasceno, G, Souza, L, Pivello, VR, Gorgone-Barbosa, E, Giroldo, PZ and Fidelis, A (2018) Impact of invasive grasses on Cerrado under natural regeneration. Biological Invasions 20, 36213629.CrossRefGoogle Scholar
Dantas, VDL and Pausas, JG (2013) The lanky and the corky: fire-escape strategies in savanna woody species. Journal of Ecology 101, 12651272.CrossRefGoogle Scholar
Dantas-Junior, AB, Musso, C and Miranda, HS (2018) Seed longevity and seedling emergence rate of Urochloa decumbens as influenced by sowing depth in a Cerrado soil. Grass and Forage Science 73, 811814.CrossRefGoogle Scholar
Daws, MI, Davies, J, Pritchard, HW, Brown, NA and Van Staden, J (2007) Butenolide from plant-derived smoke enhances germination and seedling growth of arable weed species. Plant Growth Regulation 51, 7382.CrossRefGoogle Scholar
Dayamba, SD, Tigabu, M, Sawadogo, L and Oden, PC (2008) Seed germination of herbaceous and woody species of the Sudanian savanna-woodland in response to heat shock and smoke. Forest Ecology and Management 256, 462470.CrossRefGoogle Scholar
Diez, JM, Sullivan, JJ, Hulme, PE, Edwards, G and Duncan, RP (2008) Darwin's naturalization conundrum: dissecting taxonomic patterns of species invasions. Ecology Letters 11, 674681.CrossRefGoogle ScholarPubMed
Dunn, PK and Smyth, GK (2018) Models for proportions: binomial GLMs, pp. 333369 in Dunn, PK and Smyth, GK (Eds) Generalized linear models with examples in R. Heidelberg, Springer Texts in Statistics.Google Scholar
Fernandes, AF, Oki, Y, Fernandes, GW and Moreira, B (2021) The effect of fire on seed germination of campo rupestre species in the South American Cerrado. Plant Ecology 222, 4555.CrossRefGoogle Scholar
Flematti, GR, Ghisalberti, EL, Dixon, KW and Trengove, RD (2004) A compound from smoke that promotes seed germination. Science 305, 977977.CrossRefGoogle ScholarPubMed
Florencio, C, Arruda, R and de Figueiredo, RA (2009) Phenology of herbaceous species in Cerrado: comparisons between intact, burnt, and reforested areas. Naturalia 32, 112.Google Scholar
Fontenele, HG, Figueirôa, RN, Pereira, CM, Nascimento, VTD, Musso, C and Miranda, HS (2020) Protected from fire, but not from harm: seedling emergence of savanna grasses is constrained by burial depth. Plant Ecology & Diversity 13, 189198.CrossRefGoogle Scholar
Ghebrehiwot, HM, Kulkarni, MG, Kirkman, KP 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.CrossRefGoogle Scholar
Gorgone-Barbosa, E, Daibes, LF, Novaes, RB, Pivello, VR and Fidelis, A (2020) Fire cues and germination of invasive and native grasses in the Cerrado. Acta Botanica Brasilica 34, 185191.CrossRefGoogle Scholar
Hartig, F (2022) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R Package (Version 0.4.5). Available at: https://CRAN.R-project.org/package=DHARMaGoogle Scholar
Keeley, JE and Pausas, JG (2018) Evolution of ‘smoke’ induced seed germination in pyroendemic plants. South African Journal of Botany 115, 251255.CrossRefGoogle Scholar
Klink, CA (1996) Germination and seedling establishment of two native and one invading African grass species in the Brazilian Cerrado. Journal of Tropical Ecology 12, 139147.CrossRefGoogle Scholar
Klink, CA and Joly, CA (1989) Identification and distribution of C3 and C4 grasses in open and shaded habitats in São Paulo State, Brazil. Biotropica 21, 3034.CrossRefGoogle Scholar
Kochankov, VG, Grzesik, M, Chojnowski, M and Nowak, J (1998) Effect of temperature, growth regulators and other chemicals on Echinacea purpurea (L.) Moench seed germination and seedling survival. Seed Science and Technology 26, 547554.Google Scholar
Kumar, B, Verma, SK, Ram, G and Singh, HP (2012) Temperature relations for seed germination potential and seedling vigor in Palmarosa (Cymbopogon martinii). Journal of Crop Improvement 26, 791801.CrossRefGoogle Scholar
Kutschera, U (2000) Cell expansion in plant development. Brazilian Journal of Plant Physiology 12, 6595.Google Scholar
Labouriau, LG, Valio, IM, Salgado-Labouriau, ML and Handro, W (1963) Nota sobre a germinação de sementes de plantas de cerrados em condições naturais. Revista Brasileira de Biologia 23, 227237.Google Scholar
Lakon, G (1949) The topographical tetrazolium method for determining the germinating capacity of seeds. Plant Physiology 24, 389394.CrossRefGoogle ScholarPubMed
Lamont, BB and Downes, KS (2011) Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa. Plant Ecology 212, 21112125.CrossRefGoogle Scholar
Lange, JH and Boucher, C (1990) Autecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. South African Journal of Botany 56, 700703.CrossRefGoogle Scholar
Leskovar, DI and Stoffella, PJ (1995) Vegetable seedling root systems: morphology, development, and importance. HortScience 30, 11531159.CrossRefGoogle Scholar
Le Stradic, S, Silveira, FA, Buisson, E, Cazelles, K, Carvalho, V and Fernandes, GW (2015) Diversity of germination strategies and seed dormancy in herbaceous species of campo rupestre grasslands. Austral Ecology 40, 537546.CrossRefGoogle Scholar
Light, ME, Daws, MI and Van Staden, J (2009) Smoke-derived butenolide: towards understanding its biological effects. South African Journal of Botany 75, 17.CrossRefGoogle Scholar
Loch, DS (1977) Brachiaria decumbens (signal grass)—a review with particular reference to Australia. Tropical Grasslands 11, 141157.Google Scholar
Lynch, J (1995) Root architecture and plant productivity. Plant Physiology 109, 713.CrossRefGoogle ScholarPubMed
MacArthur, R and Levins, R (1967) The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101, 377385.CrossRefGoogle Scholar
Macedo, MCM (2005) Pastagens no ecossistema cerrados: evolução das pesquisas para o desenvolvimento sustentável, pp. 5684 in 42 Reunião Anual Da Sociedade Brasileira De Zootecnia. Goiânia, Brasil.Google Scholar
Miranda, MI and Klink, CA (1996a) Colonização de campo sujo de cerrado com diferentes regimes de queima pela gramínea Echinolaena inflexa (Poaceae), pp. 4652 in Miranda, HS; Saito, CH and Dias, BFS (Eds) Impactos de queimadas em áreas de cerrado e de resting. Brasília, Universidade de Brasília.Google Scholar
Miranda, MI and Klink, CA (1996b) Influência do fogo na alocação de biomassa de Echinolaena inflexa em duas áreas de campo sujo de cerrado, pp. 3745 in Miranda, HS; Saito, CH and Dias, BFS (Eds) Impactos de queimadas em áreas de cerrado e de restinga. Brasília, Universidade de Brasília.Google Scholar
Miranda, AC, Miranda, HS, Dias, IFO and Dias, BFS (1993) Soil and air temperatures during prescribed cerrado fires in central Brazil. Journal of Tropical Ecology 9, 313320.CrossRefGoogle Scholar
Mojzes, A, Csontos, P and Kalapos, T (2015) Is the positive response of seed germination to plant-derived smoke associated with plant traits? Acta Oecologica 65, 2431.CrossRefGoogle Scholar
Moraes, MG, Carvalho, MAM, Franco, AC, Pollock, CJ and Figueiredo-Ribeiro, RDCL (2016) Fire and drought: soluble carbohydrate storage and survival mechanisms in herbaceous plants from the Cerrado. BioScience 66, 107117.Google Scholar
Moreira, B, Tormo, J, Estrelles, E and Pausas, JG (2010) Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Annals of Botany 105, 627635.CrossRefGoogle ScholarPubMed
Morrison, DA and Morris, EC (2000) Pseudoreplication in experimental designs for the manipulation of seed germination treatments. Austral Ecology 25, 292296.CrossRefGoogle Scholar
Munhoz, CBR and Felfili, JM (2007) Reproductive phenology of an herbaceous-subshrub layer of a Savannah (Campo Sujo) in the Cerrado Biosphere Reserve I, Brazil. Brazilian Journal of Biology 67, 299307.CrossRefGoogle ScholarPubMed
Muniz, DR, Garcia, JS, Braga, TC, Fátima, A and Modolo, LV (2019) Pre-emergence application of (thio)urea analogues compromises the development of the weed species Bidens pilosa, Urochloa brizantha, and Urochloa decumbens. Journal of Advanced Research 17, 95102.CrossRefGoogle ScholarPubMed
Musso, C, Miranda, HS, Aires, SS, Bastos, AC, Soares, AM and Loureiro, S (2015) Simulated post-fire temperature affects germination of native and invasive grasses in Cerrado (Brazilian savanna). Plant Ecology & Diversity 8, 219227.CrossRefGoogle Scholar
Navas, R and Pereira, MRR (2016) Efeito alelopático de Raphanus sativus em Urochloa decumbens e Lactuca sativa. Revista Agro@mbiente On-line 10, 228234.CrossRefGoogle Scholar
Neves, DRM and Damasceno-Junior, GA (2011) Post-fire phenology in a campo sujo vegetation in the Urucum plateau, Mato Grosso do Sul, Brazil. Brazilian Journal of Biology 71, 881888.CrossRefGoogle Scholar
Overbeck, GE, Müller, SC, Pillar, VD and Pfadenhauer, J (2006) No heat-stimulated germination found in herbaceous species from burned subtropical grassland. Plant Ecology 184, 237243.CrossRefGoogle Scholar
Paredes, MV, Cunha, ALD, Musso, C, Aires, SS, Sato, MN and Miranda, HS (2018) Germination responses of native and invasive Cerrado grasses to simulated fire temperatures. Plant Ecology & Diversity 11, 193203.CrossRefGoogle Scholar
Pausas, JG, Lamont, BB, Paula, S, Appezzato-da-Glória, B and Fidelis, A (2018) Unearthing belowground bud banks in fire-prone ecosystems. New Phytologist 217, 14351448.CrossRefGoogle ScholarPubMed
Pereira, MRR, Martins, CC, Souza, GSF and Martins, D (2012) Influence of saline and water stress on germination of Urochloa decumbens and Urochloa ruziziensis. Bioscience Journal 28, 537545.Google Scholar
Pérez-Fernández, MA 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.CrossRefGoogle ScholarPubMed
Pilon, NA, Hoffmann, WA, Abreu, RC and Durigan, G (2018) Quantifying the short-term flowering after fire in some plant communities of a Cerrado grassland. Plant Ecology & Diversity 11, 259266.CrossRefGoogle Scholar
Pilon, NA, Cava, MG, Hoffmann, WA, Abreu, RC, Fidelis, A and Durigan, G (2021) The diversity of post-fire regeneration strategies in the Cerrado ground layer. Journal of Ecology 109, 154166.CrossRefGoogle Scholar
Pires, HRA, Franco, AC, Piedade, MTF, Scudeller, VV, Kruijt, B and Ferreira, CS (2018) Flood tolerance in two tree species that inhabit both the Amazonian floodplain and the dry Cerrado savanna of Brazil. AoB Plants 10, ply065.Google ScholarPubMed
Pivello, VR (2011) The use of fire in the Cerrado and Amazonian rainforests of Brazil: past and present. Fire Ecology 7, 2439.CrossRefGoogle Scholar
Pivello, VR, Carvalho, VMC, Lopes, PF, Peccinini, AA and Rosso, S (1999) Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian Savanna) biological reserve. Biotropica 31, 7182.Google Scholar
R Core Team (2021) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at: https://www.R-project.org/Google Scholar
Ramos, DM, Liaffa, AB, Diniz, P, Munhoz, CB, Ooi, MK, Borghetti, F and Valls, JF (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, 12731280.CrossRefGoogle Scholar
Ramos, DM, Valls, JF, Borghetti, F and Ooi, MK (2019) Fire cues trigger germination and stimulate seedling growth of grass species from Brazilian savannas. American Journal of Botany 106, 11901201.CrossRefGoogle ScholarPubMed
Ries, RE and Svejcar, TJ (1991) The grass seedling: when is it established? Journal of Range Management 44, 574576.CrossRefGoogle Scholar
Salazar, A, Goldstein, G, Franco, AC and Miralles-Wilhelm, F (2011) Timing of seed dispersal and dormancy, rather than persistent soil seed-banks, control seedling recruitment of woody plants in Neotropical savannas. Seed Science Research 21, 103.CrossRefGoogle Scholar
Sarmiento, G (1992) Adaptive strategies of perennial grasses in south American savannas. Journal of Vegetation Science 3, 325336.CrossRefGoogle Scholar
Simon, MF, Grether, R, Queiroz, LP, Skema, C, Pennington, RT and Hughes, CE (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences of the United States of America 106, 2035920364.CrossRefGoogle Scholar
Souza, A, Sandrin, CZ, Calió, MFA, Meirelles, ST, Pivello, VR and Figueiredo-Ribeiro, RCL (2010) Seasonal variation of soluble carbohydrates and starch in Echinolaena inflexa, a native grass species from the Brazilian savanna, and in the invasive grass Melinis minutiflora. Brazilian Journal of Biology 70, 395404.CrossRefGoogle ScholarPubMed
Sparg, SG, Kulkarni, MG, Light, ME and Van Staden, J (2005) Improving seedling vigour of indigenous medicinal plants with smoke. Bioresource Technology 96, 13231330.CrossRefGoogle ScholarPubMed
Stevens, JC, Merritt, DJ, Flematti, GR, Ghisalberti, EL and Dixon, KW (2007) Seed germination of agricultural weeds is promoted by the butenolide 3-methyl-2 H-furo [2, 3-c] pyran-2-one under laboratory and field conditions. Plant and Soil 298, 113124.CrossRefGoogle Scholar
Symstad, AJ (2000) A test of the effects of functional group richness and composition on grassland invasibility. Ecology 81, 99109.CrossRefGoogle Scholar
Tavşanoğlu, Ç, Çatav, ŞS 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.CrossRefGoogle Scholar
Taylor, JLS and van Staden, J (1996) Root initiation in Vigna radiata (L.) Wilczek hypocotyl cuttings is stimulated by smoke-derived extracts. Plant Growth Regulation 18, 165168.CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York, Springer-Verlag.CrossRefGoogle Scholar
Wright, IJ and Westoby, M (2000) Cross-species relationships between seedling relative growth rate, nitrogen productivity and root vs leaf function in 28 Australian woody species. Functional Ecology 14, 97107.CrossRefGoogle Scholar
Xavier, RO, Leite, MB and Matos, DMS (2019) Phenological and reproductive traits and their response to environmental variation differ among native and invasive grasses in a Neotropical savanna. Biological Invasions 21, 27612779.CrossRefGoogle Scholar
Zenni, RD and Ziller, SR (2011) An overview of invasive plants in Brazil. Brazilian Journal of Botany 34, 431446.CrossRefGoogle Scholar
Zirondi, HL, Silveira, FA and Fidelis, A (2019) Fire effects on seed germination: heat shock and smoke on permeable vs impermeable seed coats. Flora 253, 98106.CrossRefGoogle Scholar
Zuur, AF, Ieno, EN, Walker, NJ, Saveliev, AA and Smith, GM (2009) Mixed effects models and extensions in ecology with R, Vol. 574. New York, Springer.CrossRefGoogle Scholar