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How regional climate and seed traits interact in shaping stress–tolerance of savanna seeds?

Published online by Cambridge University Press:  02 November 2021

Leandro C. Ribeiro
Affiliation:
Departamento de Ensino, Instituto Federal Goiano, Rodovia Professor Geraldo Silva Nascimento, Km 2.5, Urutaí, Goiás, Brazil Departamento de Ensino, Instituto Federal do Ceará, Rodovia CE 060, Km 332, Acopiara, Ceará, Brazil Departamento de Botânica, Universidade de Brasília, Campus Universitário Darcy Ribeiro, S/N, Brasília, Distrito Federal, Brazil
Eduardo R. M. Barbosa
Affiliation:
Departamento de Botânica, Universidade de Brasília, Campus Universitário Darcy Ribeiro, S/N, Brasília, Distrito Federal, Brazil
Fabian Borghetti*
Affiliation:
Departamento de Botânica, Universidade de Brasília, Campus Universitário Darcy Ribeiro, S/N, Brasília, Distrito Federal, Brazil
*
*Correspondence: Fabian Borghetti, E-mail: borghetti.fabian@gmail.com

Abstract

Functional traits related to regeneration responses to the environment are highly determinants of distribution patterns of plant communities. A large body of studies on seed traits suggests that regional climate may act as a strong filter of plant recruitment; however, few studies have evaluated the relative importance of seed traits and environmental filters for seed persistence at the population level. We tested the role of seed mass, water content and desiccation tolerance, as well as the germination time as proxies for seed tolerance to environmental filters (water deficit, heat shock and high temperatures) by comparing the response of tree species co-occurring in savannas located in different regions: Cerrado biome of Central Brazil and the Rio Branco savannas of northern Brazil. Seeds collected in savannas of Rio Branco showed a higher tolerance to environmental filters than those collected in savannas of the Cerrado. While the germination percentages largely varied in response to the treatments, the germination times were virtually unaffected by them, irrespective of seed origin, seed mass and water content. At the population level, the regional environment was a key determinant of seed tolerance to stress, irrespective of seed traits. Germination time was shown to represent a conservative seed trait and more linked to a species-specific germination strategy than to regional characteristics. Our results suggest that recruitment patterns of Cerrado savannas may be more impacted than Rio Branco savannas by the climate scenarios predicted for the future.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

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
Baraloto, C, Forget, P and Goldberg, DE (2005) Seed mass, seedling size and neotropical tree seedling establishment. Journal of Ecology 93, 11561166.CrossRefGoogle Scholar
Barbosa, RI and Fearnside, PM (2005a) Above-ground biomass and the fate of carbon after burning in the savannas of Roraima, Brazilian Amazonia. Forest Ecology and Management 216, 295316.Google Scholar
Barbosa, RI and Fearnside, PM (2005b) Fire frequency and area burned in the Roraima savannas of Brazilian Amazonia. Forest Ecology and Management 204, 371384.CrossRefGoogle Scholar
Barbosa, RI, Campos, C, Pinto, F and Fearnside, PM (2007) The ‘Lavrados’ of Roraima: biodiversity and conservation of Brazil's Amazonian savannas. Functional Ecosystems and Communities 1, 2941.Google Scholar
Barbosa, ERM, van Langevelde, F, Tomlinson, KW, Carvalheiro, LG, Kirkman, K, de Bie, S and Prins, HHT (2014) Tree species from different functional groups respond differently to environmental changes during establishment. Oecologia 174, 13451357.Google ScholarPubMed
Baskin, CC and Baskin, JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, CA, Academic Press.Google Scholar
Benedetti, UG, Júnior, JFV, Schaefer, CEGR, Melo, VF and Uchôa, SCP (2011) Gênese, química e mineralogia de solos derivados de sedimentos pliopleistocênicos e de rochas vulcânicas básicas em Roraima, norte amazônico. Revista Brasileira de Ciência do Solo 35, 299312.Google Scholar
Berg, H, Becker, U and Matthies, D (2005) Phenotypic plasticity in Carlina vulgaris: effects of geographical origin, population size, and population isolation. Oecologia 143, 220231.CrossRefGoogle ScholarPubMed
Borghetti, F, Barbosa, ERM, Ribeiro, LC, Ribeiro, JF and Walter, BMT (2019) South American savannas, pp. 77122 in Scogings, PF and Sankaran, M (Eds) Savanna woody plants and large herbivores. Chichester, John Wiley and Sons.CrossRefGoogle Scholar
Borghetti, F, Caetano, GHO, Colli, GR, Françoso, R and Sinervo, BR (2021) The firewall between Cerrado and Amazonia: interaction of temperature and fire govern seed recruitment in a neotropical savana. Journal of Vegetation Science 32, e12988.CrossRefGoogle Scholar
Brancalion, PHS, Novembre, ADLC and Rodrigues, RR (2010) Temperatura ótima de germinação de sementes de espécies arbóreas brasileiras. Revista Brasileira de Sementes 32, 1521.CrossRefGoogle Scholar
Brasil (2009) Ministério da Agricultura, Pecuária e Abastecimento. Regras para análise de sementes. Brasília, MAPA/ACS.Google Scholar
Bristow, KL (1998) Measurement of thermal properties and water content of unsaturated sandy soil using dual probe heat-pulse probes. Agricultural and Forest Meteorology 89, 7584.CrossRefGoogle Scholar
Bueno, ML, Pennington, RT, Dexter, KG, Kamino, LHY, Pontara, V, Neves, DM, Ratter, JA and Oliveira-Filho, AT (2017) Effects of quaternary climatic fluctuations on the distribution of neotropical savanna tree species. Ecography 40, 403414.CrossRefGoogle Scholar
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
Chevin, LM, Lande, R and Mace, GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8, e1000357.CrossRefGoogle Scholar
Clauss, MJ and Venable, DL (2000) Seed germination in desert annuals: an empirical test of adaptive bet hedging. The American Naturalist 155, 168186.CrossRefGoogle ScholarPubMed
Cochrane, A, Yates, CJ, Hoyle, GL and Nicotra, AB (2015) Will among-population variation in seed traits improve the chance of species persistence under climate change? Global Ecology and Biogeography 24, 1224.CrossRefGoogle Scholar
Coomes, DA and Grubb, PJ (2003) Colonization, tolerance, competition and seed-size variation within functional groups. Trends in Ecology & Evolution 18, 283291.CrossRefGoogle Scholar
Cromarty, AS, Ellis, RH and Roberts, EH (1985) Designing of seed storage facilities for genetic conservation. Rome, IPGRI.Google Scholar
Daws, MI, Burslem, DFRP, Crabtree, LM, Kirkman, P, Mullins, CE and Dalling, JW (2002) Differences in seed germination responses may promote coexistence of four sympatric Piper species. Functional Ecology 16, 258267.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
DeBano, LF, Neary, DG and Ffolliott, PF (1998) Fire's effects on ecosystems. New York, John Wiley & Sons.Google Scholar
Donohue, K, Casas, KK, Burghart, L, Kovach, LK and Willis, CG (2010) Germination, post germination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution and Systematics 41, 293319.Google Scholar
Escudero, A, Nuñez, Y and Pérez-García, F (2000) Is fire a selective force of seed size in pine species? Acta Oecologica 21, 245256.CrossRefGoogle Scholar
Farooq, M, Basra, SMA, Hafeez, K and Ahmad, N (2005) Thermal hardening: a new seed vigour enhancement tool in rice. Journal of Integrative Plant Biology 47, 187193.CrossRefGoogle Scholar
Fay, PA and Schultz, MJ (2009) Germination, survival, and growth of grass and forb seedlings: effects of soil moisture variability. Acta Oecologica 35, 679684.CrossRefGoogle Scholar
Fenner, M and Thompson, K (2005) The ecology of seeds. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Fidalski, J, Tormena, CA, Alves, SJ and Auler, PAM (2013) Influência das frações de areia na retenção e disponibilidade de água em solos das formações Caiuá e Paranavaí. Revista Brasileira de Ciência do Solo 37, 613621.CrossRefGoogle Scholar
Flores, J and Briones, O (2001) Plant life form and germination in a Mexican inter-tropical desert: effects of soil water potential and temperature. Journal of Arid Environments 47, 485497.Google Scholar
Franco, AC (2002) Ecophysiology of woody plants, pp. 178197 in Oliveira, PS and Marquis, RJ (Eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. New York, Columbia University Press.Google Scholar
Furley, PA (2007) Tropical savannas and associated forests: vegetation and plant ecology. Progress in Physical Geography 31, 203211.CrossRefGoogle Scholar
Galloway, LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytologist 166, 93100.CrossRefGoogle ScholarPubMed
Garcia, QS, Jacobi, CM and Ribeiro, BA (2007) Resposta germinativa de duas espécies de Vellozia (Velloziaceae) dos campos rupestres de Minas Gerais, Brasil. Acta Botanica Brasilica 21, 451456.CrossRefGoogle Scholar
Gomes, JBV, Curi, N, Motta, PEF, Ker, JC, Marques, JJGS and Schulze, DG (2004) Análise de componentes principais de atributos físicos, químicos e mineralógicos de solos do bioma Cerrado. Revista Brasileira de Ciência do Solo 28, 137153.Google Scholar
Gottsberger, G and Silberbauer-Gottsberger, I (2006) Life in the cerrado: a South American tropical seasonal ecosystem: origin, structure, dynamics and plant use. Ulm, Reta Verlag.Google Scholar
Gremer, JR and Venable, DL (2014) Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecology Letters 17, 380387.Google Scholar
Hamilton, KN, Offord, CA, Cuneo, P and Deseo, MA (2013) A comparative study of seed morphology in relation to desiccation tolerance and other physiological responses in 71 Eastern Australian rainforest species. Plant Species Biology 28, 5162.CrossRefGoogle Scholar
Hanley, ME and Lamont, BB (2000) Heat pre-treatment and the germination of soil- and canopy-stored seeds of south-western Australian species. Acta Oecologica 21, 315321.CrossRefGoogle Scholar
Hardegree, SP and Emmerich, WE (1994) Seed germination in response to polyetilene glycol solution. Seed Science and Technology 22, 17.Google Scholar
INMET (2013) Normais climatológicas do Brasil: 1961–1990. Available at: http://www.inmet.gov.br/portal/index.php?r=clima/normaisClimatologicas (accessed 25 September 2013).Google Scholar
INMET (2014) Estações convencionais – gráficos. Available at: http://www.inmet.gov.br/portal/index.php?r=home/page&page=rede_estacoes_conv_graf (accessed 20 October 2014).Google Scholar
Jiménez-Alfaro, B, Silveira, FAO, Fidelis, A, Poschlod, P and Commander, LE (2016) Seed germination traits can contribute better to plant community ecology. Journal of Vegetation Science 27, 637645.Google Scholar
Kauffman, JB, Cummings, DL and Ward, DE (1994) Relationships of fire, biomass and nutrient dynamics along a vegetation gradient in the Brazilian Cerrado. Journal of Ecology 82, 519531.CrossRefGoogle Scholar
Keeley, JE (2009) Fire intensity, fire severity and burn severity: a brief review. International Journal of Wildland Fire 18, 116126.CrossRefGoogle Scholar
Kos, M and Poschlod, P (2008) Correlates of inter-specific variation in germination response to water stress in a semi-arid savannah. Basic and Applied Ecology 9, 645652.CrossRefGoogle 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 ScholarPubMed
Labouriau, LG (1983) A germinação das sementes. Washington, DC, Secretaria Geral da Organização dos Estados Americanos.Google Scholar
Leishman, MR and Westoby, M (1994) The role of large seeds in seedling establishment in dry soil conditions: experimental evidence for semi-arid species. Journal of Ecology 82, 249258.CrossRefGoogle Scholar
Leishman, MR, Wright, IJ, Moles, AT and Westoby, M (2000) The evolutionary ecology of seed size, pp. 3157 in Fenner, M (Ed.) Seeds: the ecology of regeneration in plant communities. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Meneses, MENS, Costa, ML and Behling, H (2013) Late Holocene vegetation and fire dynamics from a savanna-forest ecotone in Roraima state, northern Brazilian Amazon. Journal of South American Earth Sciences 42, 1726.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.Google Scholar
Miranda, HS, Sato, MN, Neto, WN and Aires, FS (2009) Fires in the Cerrado, the Brazilian savanna, pp. 427450 in Cochrane, MA (Ed.) Tropical fire ecology: climate change, land use, and ecosystem dynamics. Chichester, Springer-Praxis Publishing.CrossRefGoogle Scholar
Miranda, HS, Nascimento-Neto, W and Castro-Neves, BM (2010) Caracterização das queimadas de Cerrado, pp. 2333 in Miranda, HS (Org.)Efeitos do regime do fogo sobre a estrutura de comunidades de cerrado: resultados do projeto fogo, Brasília, Ibama.Google Scholar
Moles, AT, Ackerly, DD, Webb, CO, Tweddle, JC, Dickie, JB and Westoby, M (2005) A brief history of seed size. Science 307, 576580.Google ScholarPubMed
Moles, AT, Ackerly, DD, Tweddle, JC, Dickie, JB, Smith, R, Leishman, MR, Mayfield, MM, Pitman, A, Wood, JT and Westoby, M (2007) Global patterns in seed size. Global Ecology and Biogeography 16, 109116.CrossRefGoogle Scholar
Moore, RP (1973) Tetrazolium staining for assessing seed quality, pp. 347366 in Heydecker, W (Ed.) Seed ecology. London, Butterworths.Google Scholar
Muller-Landau, HC (2010) The tolerance-fecundity trade-off and the maintenance of diversity in seed size. Proceedings of the National Academy of Sciences of the USA 107, 42424247.CrossRefGoogle ScholarPubMed
Nardoto, GB, Souza, MP and Franco, AC (1998) Estabelecimento e padrões sazonais de produtividade de Kielmeyera coriacea (Spr) Mart. nos cerrados do Planalto Central: efeitos do estresse hídrico e sombreamento. Revista Brasileira de Botânica 98, 313319.Google Scholar
Norden, N, Daws, MI, Antoine, C, et al. (2009) The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Functional Ecology 23, 203210.CrossRefGoogle Scholar
Nwadibia, N, Ugwu, E and Aduloju, K (2010) Theoretical analysis of the influence of the thermal diffusivity of clay soil on the thermal energy distribution in clay soil of Abakaliki, Nigeria. Research Journal of Applied Sciences, Engineering and Technology 3, 216221.Google Scholar
Oliveira, ME and Silva, IL (1994) Efeitos do fogo sobre o solo. Floresta e Ambiente 1, 142145.Google Scholar
Ooi, MKJ (2012) Seed bank persistence and climate change. Seed Science Research 22, S53S60.CrossRefGoogle Scholar
Ooi, MKJ, Auld, TD and Denham, AJ (2009) Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Global Change Biology 15, 23752386.Google Scholar
Ooi, MKJ, Auld, T and Denham, A (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.CrossRefGoogle Scholar
Pammenter, NW and Berjak, P (2000) Evolutionary and ecological aspects of recalcitrant seed biology. Seed Science Research 10, 301306.CrossRefGoogle Scholar
Peel, MC, Finlayson, BL and McMahon, TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Science 11, 16331644.CrossRefGoogle Scholar
Pivello, VR, Oliveras, I, Miranda, HS, Haridasan, M, Sato, MN and Meirelles, ST (2010) Effect of fires on soil nutrient availability in an open savanna in Central Brazil. Plant and Soil 337, 111123.CrossRefGoogle Scholar
Poschlod, P, Abedi, M, Bartelheimer, M, Drobnik, J, Rosbakh, S and Saatkamp, A (2013) Seed ecology and assembly rules in plant communities, pp. 164202 in van der Maarel, E and Franklin, J (Eds) Vegetation ecology. Chichester, Wiley-Blackwell.Google Scholar
Prance, GT (2006) Tropical savannas and seasonally dry forests: an introduction. Journal of Biogeography 33, 385386.CrossRefGoogle Scholar
Pritchard, HW, Daws, MI, Fletcher, BJ, Gaméné, CS, Msanga, HP and Omondi, W (2004) Ecological correlates of seed desiccation tolerance in tropical African dry land trees. American Journal of Botany 91, 863870.CrossRefGoogle Scholar
Ranieri, BD, Lana, TC, Negreiros, D, Araújo, LM and Fernandes, GW (2003) Germinação de sementes de Lavoisiera cordata Cogn. e Lavoisiera francavillana Cogn. (Melastomataceae), espécies simpátricas da Serra do Cipó, Brasil. Acta Botanica Brasilica 17, 523530.CrossRefGoogle Scholar
R Core Team (2020) R: a language and environment for statistical computing. Vienna, R Foundation for Statistical Computing.Google Scholar
Rees, M and Venable, DL (2007) Why do big plants make big seeds? Journal of Ecology 95, 926936.Google Scholar
Rees, M and Westoby, M (1997) Game-theoretical evolution of seed mass in multi-species ecological models. Oikos 78, 116126.CrossRefGoogle Scholar
Ribeiro, LC and Borghetti, F (2014) Comparative effects of desiccation, heat shock and high temperatures on seed germination of savanna and forest tree species. Austral Ecology 39, 267278.Google Scholar
Ribeiro, LC, Pedrosa, M and Borghetti, F (2013) Heat shock effects on seed germination of five Brazilian savanna species. Plant Biology 15, 152157.CrossRefGoogle ScholarPubMed
Ribeiro, LC, Barbosa, ERM, van Langevelde, F and Borghetti, F (2015) The importance of seed mass for the tolerance to heat shocks of savanna and forest tree species. Journal of Vegetation Science 26, 11021111.CrossRefGoogle Scholar
Saatkamp, A, Affre, L, Dutoit, T and Poschlod, P (2011) Germination traits explain soil seed persistence across species: the case of Mediterranean annual plants in cereal fields. Annals of Botany 107, 415426.Google ScholarPubMed
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, 103116.CrossRefGoogle Scholar
Sales, NM, Pérez-García, F and Silveira, FAO (2013) Consistent variation in seed germination across an environmental gradient in a Neotropical savanna. South African Journal of Botany 87, 129133.CrossRefGoogle Scholar
Sano, EE, Rosa, R, Brito, JLS and Ferreira, LG (2010) Land cover mapping of the tropical savanna region in Brazil. Environmental Monitoring and Assessment 166, 113124.CrossRefGoogle ScholarPubMed
Schütz, W, Milberg, P and Lamont, BB (2002) Germination requirements and seedling responses to water availability and soil type in four eucalypt species. Acta Oecologica 23, 2330.Google Scholar
Scott, K, Setterfield, S, Douglas, M and Andersen, A (2010) Soil seed banks confer resilience to savanna grass-layer plants during seasonal disturbance. Acta Oecologica 36, 202210.CrossRefGoogle Scholar
Silva, JMC and Bates, JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52, 225233.Google Scholar
Simons, AM and Johnston, MO (2006) Environmental and genetic sources of diversification in the timing of seed germination: implications for the evolution of bet hedging. Evolution 60, 22802292.CrossRefGoogle ScholarPubMed
Spina, AP (2004) Estudos taxonômico, micro-morfológico e filogenético do gênero Himatanthus Willd. Ex Schult. (Apocynaceae: Rauvolfioideae - Plumerieae). PhD dissertation, University of Campinas, Campinas, São Paulo.Google Scholar
Spina, AP, Bittrich, V and Kinoshita, LS (2013) Typifications, new synonyms and a new combination in Himatanthus (Apocynaceae). Taxon 62, 13041307.Google Scholar
Sy, A, Grouzis, M and Danthu, P (2001) Seed germination of seven Sahelian legume species. Journal of Arid Environments 49, 875882.CrossRefGoogle Scholar
Tambelini, M and Perez, SCJGA (1999) Temperature limits on germination of Stryphnodendron polyphyllum Mart. Journal of Tropical Forestry Science 11, 630636.Google Scholar
Thomas, PB, Morris, EC and Auld, TA (2007) Response surfaces for the combined effects of heat shock and smoke on germination of 16 species forming soil seed banks in south-east Australia. Austral Ecology 32, 605616.CrossRefGoogle Scholar
Tielbörger, K, Petru, M and Lampei, C (2012) Bet-hedging germination in annual plants: a sound empirical test of the theoretical foundations. Oikos 121, 18601868.CrossRefGoogle Scholar
Tweddle, JC, Dickie, JB, Baskin, CC and Baskin, JM (2003) Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91, 294304.CrossRefGoogle Scholar
Villela, FA, Doni-Filho, L and Siqueira, EL (1991) Tabela de potencial osmótico em função da concentração de polietilenoglicol 6000 e da temperatura. Pesquisa Agropecuária Brasileira 26, 19571968.Google Scholar
Westoby, M, Falster, DS, Moles, AT, Vesk, PA and Wright, IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33, 125159.CrossRefGoogle Scholar
Zaidan, LBP and Carreira, RC (2008) Seed germination in Cerrado species. Brazilian Journal of Plant Physiology 20, 167181.CrossRefGoogle Scholar