Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-25T04:33:06.626Z Has data issue: false hasContentIssue false
  • English
  • Français

Thermal requirements of seed germination of ten tree species occurring in the western Brazilian Amazon

Published online by Cambridge University Press:  31 May 2019

L. Felipe Daibes Open the ORCID record for L. Felipe Daibes [Opens in a new window] ,
Semirian C. Amoêdo ,
Jeane do Nascimento Moraes ,
Natália Fenelon ,
Débora Rosa da Silva ,
Max Jr de Melo Lopes ,
Lidiane A. Vargas ,
Ediléia F. Monteiro  and
Renita B.C. Frigeri
L. Felipe Daibes*
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil Universidade Estadual Paulista (UNESP), I.B. Departamento de Botânica, Av. 24A 1515, 13506-900 Rio Claro, SP, Brazil
Semirian C. Amoêdo
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil Instituto Nacional de Pesquisas da Amazônia (INPA), Laboratório de Sementes, Av. André Araujo 2936, 69087-000 Manaus, AM, Brazil
Jeane do Nascimento Moraes
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil
Natália Fenelon
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil Universidade Federal de Pelotas (UFPel), Centro de Artes, Rua Álvaro Chaves 65, Pelotas, RS, Brazil
Débora Rosa da Silva
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil
Max Jr de Melo Lopes
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil
Lidiane A. Vargas
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil
Ediléia F. Monteiro
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil
Renita B.C. Frigeri
Affiliation:
Universidade Federal de Rondônia (UNIR), Departamento de Biologia, BR-364, Km 9.5, 76801-059 Porto Velho, RO, Brazil Universidade Federal do Espírito Santo (UFES), Departamento de Ciências Biológicas, Av. Fernando Ferrari 514, 29075-910 Vitória, ES, Brazil
*
*Author for correspondence: L. Felipe Daibes, Email: luipedaibes@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Regeneration from seed affects species assembly in plant communities, and temperature is the most important environmental factor controlling the germination process. Thermal dependence of seed germination is thus associated with species occurrence in an ecosystem. Hence, we aimed to investigate the role of temperature on seed germination of ten tree species from the western Brazilian Amazon. Seeds were collected in the state of Rondônia, Brazil, and set to germinate under constant temperatures ranging from 10 to 40°C in germination chambers. We calculated germination capacity (G%), germination rate (GR50, reciprocal of germination time), and thermal parameters, such as cardinal temperatures and thermal time requirements. Most species had a large range of temperatures showing G% ≥80%, with optimal temperature varying from 20 to 40°C. Base temperature ranged from 6 to 12°C and ceiling temperatures were mainly >40°C. Astronium lecointei and Parkia nitida showed high germination capacity under temperatures of 35–40°C, while germination of Theobroma cacao dropped from 100% to zero under temperatures between 37 and 40°C. The climax species Cedrela fissilis had the slowest germination time (10 days) and highest thermal time requirement, while seeds of Enterolobium schomburgkii (a late-successional species) germinated within the first day of the experiment. Rapid recruitment of Amazon species could be favoured with treefall disturbance, which increases temperatures in the understory, but sharp limits might be found in the supra-optimal range of temperatures. Such patterns might indicate different regeneration strategies in the tropical rainforest, providing important information regarding seed germination among Amazon species.

Keywords

Amazoniacardinal temperaturerainforestregeneration nichetemperaturethermal timetropical forest
Type
Research Paper
Information
Seed Science Research , Volume 29 , Issue 2 , June 2019 , pp. 115 - 123
Copyright
Copyright © Cambridge University Press 2019 

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

Alvarado, V. and Bradford, K.J. (2002) A hydrothermal time model explains the cardinal temperatures for seed germination. Plant Cell and Environment 25, 1061–1069.Google Scholar
Amaral, D.D., Vieira, I.C.G., Almeida, S.S., Salomão, R.P., Silva, A.S.L. and Jardim, M.A.G. (2009) Checklist da flora arbórea de remanescentes florestais da região metropolitana de Belém e valor histórico dos fragmentos, Pará, Brasil. Boletim do Museu Paraense Emílio Goeldi, Ciências Naturais 4, 231–289.Google Scholar
Ambrizzi, T., Rocha, R.P., Marengo, J.A., Pisnitchenko, I., Alves, L.M. and Fernandez, J.P.R. (2007) Cenários regionalizados de clima no Brasil para o Século XXI: Projeções de clima usando três modelos regionais. Relatório 3, Brasília: MMA – Ministério do Meio Ambiente. Available at: http://mudancasclimaticas.cptec.inpe.br/~rmclima/pdfs/prod_probio/Relatorio_3.pdf (accessed 7 August 2018).Google Scholar
Amoêdo, S.C. and Ferraz, I.D.K. (2019) A comparative study of the thermal ranges of three germination criteria of a tropical tree with bioeconomic interest: Carapa surinamensis Miq. (Meliaceae). Brazilian Journal of Biology 79, 213–219.Google Scholar
Amorim, I.L., Davide, A.C., Ferreira, R.A. and Chaves, M.M.F. (2008) Morfologia de frutos, sementes, plântulas e mudas de Senna multijuga var. lindleyana (Gardner) H. S. Irwin & Barneby – Leguminosae Caesalpinioideae. Revista Brasileira de Botânica 31, 507–516.Google Scholar
Angeli, A., Barrichelo, L.E.G. and Müller, P.H. (2005) Cedrella fissilis (Cedro). IPEF – Instituto de Pesquisas e Estudos Florestais. Available at: http://www.ipef.br/identificacao/cedrella.fissilis.asp (accessed 3 August 2018).Google Scholar
Aud, F.F. and Ferraz, I.D.K. (2012) Seed size influence on germination responses to light and temperature of seven pioneer tree species from the Central Amazon. Anais da Academia Brasileira de Ciências 84, 759–766.Google Scholar
Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination, 2nd edition. San Diego, USA: Academic Press.Google Scholar
Baskin, J.M., Baskin, C.C. and Li, X. (2000) Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology 15, 139–152.Google Scholar
Bastos, L.L.S., Ferraz, I.D.K., Lima Junior, M.J.V. and Pritchard, H.W. (2017) Variation in limits to germination temperature and rates across the seed-seedling transition in the palm Oenocarpus bataua from the Brazilian Amazon. Seed Science and Technology 45, 1–13.Google Scholar
Bastos, T.X. (1982) O clima da Amazônia Brasileira segundo Köppen. Belém: EMBRAPA-CPATU, Pesquisa em Andamento no. 87, 4 p.Google Scholar
Bastos, T.X. and Diniz, T.D. (1982) Avaliação do clima do Estado de Rondônia para desenvolvimento agrícola. Belém: EMBRAPA-CPATU, Boletim de Pesquisa no. 44, 28 p.Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Benítez-Malvido, J. and Martínez-Ramos, M. (2003) Influence of edge exposure on tree seedling species recruitment in tropical rain forest fragment. Biotropica 35, 530–541.Google Scholar
Bewley, J.D., Bradford, K., Hilhorst, H.W.M. and Nonogaki, H. (2013) Seeds: Physiology of Development, Germination and Dormancy, 3rd edition. New York, USA: Springer Science.Google Scholar
Bonadeu, F. and Santos, J.U.M. (2013) Contribuição ao conhecimento dos gêneros da tribo Ingeae ocorrentes em uma Floresta Nacional da Amazônia Brasileira. Rodriguésia 64, 321–336.Google Scholar
Bradford, K.J. (2002) Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Science 50, 248–260.Google Scholar
Bradford, K.J. (2005) Threshold models applied to seed germination ecology. New Phytologist 165, 338–341.Google Scholar
Braga, L.F., Oliveira, A.C.C. and Sousa, M.P. (2013) Morfometria de sementes e desenvolvimento pós-seminal de Schizolobium amazonicum Huber (Ducke) – Fabaceae. Científica, Jaboticabal 41, 1–10.Google Scholar
Camargo, J.L.C., Ferraz, I.D.K., Mesquita, M.R., Santos, B.A. and Brum, H.D. (2008) Guia de propágulos e plântulas da Amazônia. Manaus: Editora INPA.Google Scholar
Carvalho, P.E.R. (2004) Pau-cigarra – Senna multijuga. Colombo: Embrapa Florestas, Circular Técnica no. 92, 11 p.Google Scholar
Carvalho, P.E.R. (2009) Faveira-Benguê (Parkia multijuga). Colombo: Embrapa Florestas, Comunicado Técnico no. 227.Google Scholar
Chazdon, R.L. and Pearcy, R.W. (1991) The importance of sunflecks for forest understory plants. BioScience 41, 760–766.Google Scholar
Cornejo, F. and Janovec, J. (2010). Seeds of Amazonian Plants. Princeton Field Guides, Princeton University Press.Google Scholar
Covell, S., Ellis, R.H., Roberts, E.H. and Summerfield, R.J. (1986) The influence of temperature on seed germination rate in grain legumes. I. A comparison of chickpea, lentil, soyabean and cowpea at constant temperatures. Journal of Experimental Botany 37, 705–715.Google Scholar
Daibes, L.F. and Cardoso, V.J.M. (2018) Seed germination of a South American forest tree described by linear thermal time models. Journal of Thermal Biology 76, 156–164.Google Scholar
Dalling, J.W., Davis, A.S., Schutte, B.J. and Arnold, A.E. (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99, 89–95.Google Scholar
Daws, M.I., Ballard, C., Mullins, C.E., Garwood, N.C., Murray, B., Pearson, T.R.H. and Burslem, D.F.R.P. (2007) Allometric relationships between seed mass and seedling characteristics reveal trade-offs for neotropical gap-dependent species. Oecologia 154, 445–454.Google Scholar
Daws, M.I., Burslem, D.F.R.P., Crabtree, L.M., Kirkman, P., Mullins, C.E. and Dalling, J.W. (2002) Differences in seed germination responses may promote coexistence of four sympatric Piper species. Functional Ecology 16, 258–267.Google Scholar
Daws, M.I., Crabtree, L.M., Dalling, J.W., Mullins, C.E. and Burslem, D.F.R.P. (2008) Germination responses to water potential in neotropical pioneers suggest large-seeded species take more risks. Annals of Botany 102, 945–951.Google Scholar
Dayrell, R.L.C., Garcia, Q.S., Negreiros, D., Baskin, C.C., Baskin, J.M. and Silveira, F.A.O. (2017) Phylogeny strongly drives seed dormancy and quality in a climatically buffered hotspot for plant endemism. Annals of Botany 119, 267–277.Google Scholar
Denslow, J.S. (1980) Gap partitioning among tropical rainforest trees. Biotropica 12, 47–55.Google Scholar
Díaz-Bardales, M.P. (2001) Caracterização morfológica dos frutos e sementes de algumas espécies de plantas lenhosas da família Leguminosae (Caesalpinioideae, Mimosiodeae, Papilioniodeae), suas relações abióticas e bióticas de dispersão e o papel na dieta da fauna frugívora. PhD thesis, Universidade Federal do Amazonas, Manaus, 178 pp.Google Scholar
Dürr, C., Dickie, J.B., Yang, X.-Y. and Pritchard, H.W. (2015) Ranges of critical temperature and water potential values for the germination of species worldwide: contribution to a seed trait database. Agricultural and Forest Meteorology 200, 222–232.Google Scholar
Ferraz, I.D.K. and Varela, V.P. (2003) Temperatura ótima para a germinação das sementes de trinta espécies florestais da Amazônia. In Higuchi, N., Santos, J., Sampaio, P.T.B., Marenco, R.A, Ferraz, J., Sales, P.C., Saito, M. and Matsumoto, S. (eds), Projeto Jacaranda - fase 2: pesquisas florestais na Amazônia central, pp. 117–127. Manaus: INPA.Google Scholar
Ferraz, I.D.K., Albuquerque, M.C.F., Calvi, G.P. and Farias, D.L. (2012) Critérios morfológicos e temperatura para avaliação da germinação das sementes de cupuaçu. Revista Brasileira de Fruticultura 34, 905–914.Google Scholar
Ferraz, I.D.K., Leal Filho, N., Imakawa, A.M., Varela, V.P. and Piña-Rodrigues, F.C.M. (2004) Características básicas para um agrupamento ecológico preliminar de espécies madeireiras da floresta de terra firme da Amazônia Central. Acta Amazonica 34, 621–633.Google Scholar
Forcella, F., Benech Arnold, R.L., Sanchez, R. and Ghersa, C.M. (2000) Modeling seedling emergence. Field Crops Research 67, 123–139.Google Scholar
Foster, S.A. (1986) On the adaptive value of large seeds for tropical moist forest trees: a review and synthesis. The Botanical Review 52, 260–299.Google Scholar
Freitas, V.L.O., Viegas, F.P. and Lopes, R.M.F. (2014) Biometria de frutos e sementes, germinação e desenvolvimento inicial de barbatimão (Stryphnodendron adstringens). Floresta, Curitiba 44, 21–32.Google Scholar
Garcia-Huidobro, J., Monteith, J.L. and Squire, G.R. (1982) Time, temperature and germination of pearl millet (Pennisetum typhoides S. and H.). Journal of Experimental Botany 33, 288–296.Google Scholar
Geisler, G.E., Pinto, T.T., Santos, M. and Paulilo, M.T.S. (2017) Seed structures in water uptake, dormancy release, and germination of two tropical forest Fabaceae species with physically dormant seeds. Brazilian Journal Botany 40, 67–77.Google Scholar
Grubb, P.J. (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biological Reviews of the Cambridge Philosophical Society 52, 107–145.Google Scholar
Hothorn, T., Bretz, F. and Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.Google Scholar
INMET – Instituto Nacional de Meteorologia (1931–1960 and 1961–1990). Gráficos Climatológicos. Available at: http://www.inmet.gov.br/portal/ (accessed 2 August 2018).Google Scholar
Jiménez-Alfaro, B., Silveira, F.A.O., Fidelis, A., Poschlod, P. and Commander, L.E. (2016) Seed germination traits can contribute better to plant community ecology. Journal of Vegetation Science 27, 637–645.Google Scholar
Labouriau, L.F.G. (1978) Seed germination as a thermobiological problem. Radiation and Environmental Biophysics 15, 345–366.Google Scholar
Larcher, W. (2000) Ecofisiologia Vegetal. São Carlos: RiMa Editora, 531 pp.Google Scholar
Laurence, W.F. and Williamson, G.B. (2001) Positive feedbacks among forest fragmentation, drought, and climate change in the Amazon. Conservation Biology 15, 1529–1535.Google Scholar
Malhi, Y., Roberts, J.T., Betts, R.A., Killeen, T.J., Li, W. and Nobre, C.A. (2008) Climate change, deforestation, and the fate of the Amazon. Science 319, 169–172.Google Scholar
Marengo, J.A., Liebmann, B., Kousky, V.E., Filizola, N.P. and Wainer, I.C. (2001) Onset and end of the rainy season in the Brazilian Amazon Basin. Journal of Climate 14, 833–852.Google Scholar
Marques, A.R., Atman, A.P.F., Silveira, F.A.O. and Lemos-Filho, J.P. (2014) Are seed germination and ecological breadth associated? Testing the regeneration niche hypothesis with bromeliads in a heterogeneous neotropical montane vegetation. Plant Ecology 215, 517–529.Google Scholar
Moreira, F.M.S. and Moreira, F.W. (1996) Características da germinação de sementes de 64 espécies de leguminosas florestais nativas da Amazônia, em condições de viveiro. Acta Amazonica 26, 3–16.Google Scholar
Moreno-Casasola, P., Grime, J.P. and Martínez, M.L. (1994) A comparative study of the effects of fluctuations in temperature and moisture supply on hard coat dormancy in seeds of coastal tropical legumes in Mexico. Journal of Tropical Ecology 10, 67–86.Google Scholar
Orrù, M., Mattana, E., Pritchard, H.W. and Bacchetta, G. (2012) Thermal thresholds as predictors of seed dormancy release and germination timing: altitude-related risks from climate warming for the wild grapevine Vitis vinifera subsp. silvestris. Annals of Botany 110, 1651–1660.Google Scholar
Osunkoya, O.O., Ash, J.E., Hopkins, M.S. and Graham, A.W. (1994) Influence of seed size and seedling ecological attributes on shade-tolerance of rain-forest tree species in northern Queensland. Journal of Ecology 82, 149–163.Google Scholar
Pearson, T.R.H., Burslem, D.F.R.P., Mullins, C.E. and Dalling, G.W. (2002) Germination ecology of neotropical pioneers: interacting effects of environmental conditions and seed size. Ecology 83, 2798–2807.Google Scholar
Pereira, M.O., Navroski, M.C., Hoffmann, P.M., Grabias, J., Blum, C.T., Nogueira, A.C. and Rosa, D.P. (2017) Qualidade de sementes e mudas de Cedrela fissilis Vell. em função da biometria de frutos e sementes em diferentes procedências. Revista de Ciências Agroveterinárias 16, 376–385.Google Scholar
Picciau, R., Pritchard, H.W., Mattana, E. and Bacchetta, G. (2019) Thermal thresholds for seed germination in Mediterranean species are higher in mountain compared with lowland areas. Seed Science Research 29, 44–54.Google Scholar
Porceddu, M., Mattana, E., Pritchard, H.W. and Bacchetta, G. (2013) Thermal niche for in situ seed germination by Mediterranean mountain streams: model prediction and validation for Rhamnus persicifolia seeds. Annals of Botany 112, 1887–1897.Google Scholar
Poschlod, P., Abedi, M., Bartelheimer, M., Drobnik, J., Rosbakh, S. and Saatkamp, A. (2013) Seed ecology and assembly rules in plant communities. pp. 164–202 in van der Maarel, E. and Franklin, J. (eds), Vegetation Ecology, 2nd edition. London, UK: John Wiley and Sons, Ltd.Google Scholar
Probert, R.J. (2000) The role of temperature in the regulation of seed dormancy and germination. pp. 261–292 in Fenner, M. (ed), Seeds: The Ecology of Regeneration in Plant Communities, 2nd edition. Wallingford, UK: CAB International.Google Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org.Google Scholar
Ramos, M.B.P. and Ferraz, I.D.K. (2008) Estudos morfológicos de frutos, sementes e plântulas de Enterolobium schomburgkii Benth. (Leguminosae-Mimosoideae). Revista Brasileira de Botânica 31, 227–235.Google Scholar
Ranieri, B.D., Pezzini, F.F., Garcia, Q.S., Chautems, A. and França, M.G.C. (2012) Testing the regeneration niche hypothesis with Gesneriaceae (tribe Sinningiae) in Brazil: implications for the conservation of rare species. Austral Ecology 37, 125–133.Google Scholar
Reis, A.R.S., Freitas, A.D.D., Leão, N.V.M. and Santos Filho, B.G. (2016) Morphological aspects of fruits, seeds, and seedlings, and anatomy of seedlings of Apuleia molaris Spruce ex Benth. Journal of Seed Science 38, 118–128.Google Scholar
Ribeiro, G.V.T., Teixido, A.L., Barbosa, N.P.U. and Silveira, F.A.O. (2016) Assessing bias and knowledge gaps on seed ecology research: implications for conservation agenda and policy. Ecological Applications 26, 2033–2043.Google Scholar
Rodrigues-Junior, A.G., Baskin, C.C., Baskin, J.M. and Garcia, Q.S. (2018) Sensitivity cycling in physically dormant seeds of the neotropical tree Senna multijuga (Fabaceae). Plant Biology 20, 698–706.Google Scholar
Rolston, M.P. (1978) Water impermeable seed dormancy. The Botanical Review 44, 365–396.Google Scholar
Rosbakh, S. and Poschlod, P. (2015) Initial temperature of seed germination as related to species occurrence along a temperature gradient. Functional Ecology 29, 5–14.Google Scholar
Rubio de Casas, R., Willis, C.G., Pearse, W.D., Baskin, C.C., Baskin, J.M. and Cavender-Bares, J. (2017) Global biogeography of seed dormancy is determined by seasonality and seed size: a case study in the legumes. New Phytologist 214, 1527–1536.Google Scholar
Silva, M.F., Goldman, G.H., Magalhães, F.M. and Moreira, F.W. (1988) Germinação natural de 10 leguminosas arbóreas da Amazônia. Acta Amazonica 18, 9–26.Google Scholar
Soltani, E., Ghaderi-Far, F., Baskin, C.C. and Baskin, J.M. (2015) Problems with using mean germination time to calculate rate of seed germination. Australian Journal of Botany 63, 631–635.Google Scholar
Souza, C.R., Rossi, L.M.B., Azevedo, C.P. and Vieira, A.H. (2003) Paricá: Schizolobium parahyba var. amazonicum (Huber x Ducke) Barneby. Manaus: Embrapa Amazônia Ocidental, Circular Técnica no. 18, 12 p.Google Scholar
Souza, R.P. and Válio, I.F.M. (2001) Seed size, seed germination, and seedling survival of Brazilian tropical tree species differing in successional status. Biotropica 33, 447–457.Google Scholar
Souza, R.P. and Válio, I.F.M. (2003) Seedling growth of fifteen Brazilian tropical tree species differing in successional status. Revista Brasileira de Botânica 26, 35–47.Google Scholar
Steinmaus, S.J., Prather, T.S. and Holt, J.S. (2000) Estimation of base temperatures for nine weed species. Journal of Experimental Botany 51, 275–286.Google Scholar
Swaine, M.D. and Whitmore, T.C. (1988) On the definition of ecological species groups in tropical rain forests. Vegetatio 75, 81–86.Google Scholar
Thompson, K. and Ceriani, R.M. (2003) No relationship between range size and germination niche width in the UK herbaceous flora. Functional Ecology 17, 335–339.Google Scholar
Thompson, K., Gaston, K.J. and Band, S.R. (1999) Range size, dispersal and niche breadth in the herbaceous flora of central England. Journal of Ecology 87, 150–155.Google Scholar
Trudgill, D.L., Honek, A., Li, D. and van Straalen, N.M. (2005) Thermal time – concepts and utility. Annals of Applied Biology 146, 1–14.Google Scholar
Tudela-Isanta, M., Ladouceur, E., Wijayasinghe, M., Pritchard, H.W. and Mondoni, A. (2018) The seed germination niche limits the distribution of some plant species in calcareous or siliceous alpine bedrocks. Alpine Botany, https://doi.org/10.1007/s00035-018-0199-0.Google Scholar
Tweddle, J.C., Dickie, J.B., Baskin, C.C. and Baskin, J.M. (2003) Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91, 294–304.Google Scholar
Vázquez-Yanes, C. and Orozco-Segovia, A. (1984) Ecophysiology of seed germination in the tropical humid forests of the world: a review, pp. 37–50 in Medina, E., Mooney, H.A. and Vázquez-Yanes, C. (eds), Physiological Ecology of Plants of the Wet Tropics. Amsterdam, Springer-Netherlands, Dr W. Junk Publishers.Google Scholar
Venial, L.R., Alexandre, R.S., Camata, H., Lopes, J.C., Zanotti, R.F., Ferreira, A. and Aguilar, M.A.G. (2017) Biometria e armazenamento de sementes de genótipos de cacaueiro. Pesquisa Florestal Brasileira 37, 39–46.Google Scholar