Viability of recalcitrant Araucaria angustifolia seeds in storage and in a soil seed bank

Abstract

Araucaria angustifolia (Bertol.) Kuntze is a representative species of the Mixed Ombrophilous Forest in the Atlantic Forest Biome of Brazil. The development of a germplasm conservation protocol for long-term seed bank storage is compromised for this species, as it is sensitive to desiccation. Furthermore, in situ establishment of a soil seed bank in its natural habitat may be limited. This study evaluates the storability of two provenances of A. angustifolia seeds and their behavior in an artificial soil seed bank in two forest environments (understory and edge). Results show that both seed provenances may be stored at 5 °C for approximately 12 months, retaining high viability. The subsequent decrease in germination was associated with a reduction and an increase in seed water content, as well as with increased electrical conductivity. In the understory environment, seed viability was above 85% for the first 60 days, and at the end of the experiment (270 days), seedlings emerged. However, at the forest edge, there was a total loss of seed viability after 120 days associated with a reduction in water content and high predation. It is concluded, therefore, that short-term storage of A. angustifolia seeds is possible in a cold room, which is fundamental to supply seed demand outside the production period. Forest cover conservation is important for regeneration and conservation of the species.

Keywords

Brazilian pine / Desiccation sensitivity / Forest cover / Soil seed bank / Storability

References

[1] Abreu DCA, Medeiros AC de S, Aguiar IB, Banzatto DA (2012) Teste topográfico de tetrazólio em sementes de pinheiro-brasileiro (Araucaria angustifolia (Bertol.) Kuntze). In: 4° Congresso Florestal Paranaense. Curitiba

[2] Avila AL, Araujo MM, Longhi SJ, Gasparin E. Agrupamentos florísticos na regeneração natural em remanescente de Floresta Ombrófila Mista, RS, Brasil. Sci For, 2011, 39: 331-342.

[3] Avila AL, Araujo MM, Gasparin E, Longhi SJ. Mecanismos de regeneração natural em remanescente de Floresta Ombrófila Mista, RS, Brasil. Cerne, 2013, 19: 621-628.

[4] Barbedo CJ, Bilia DAC. Evolution of research on recalcitrant seeds. Sci Agric, 1998, 55: 121-125.

[5] Berjak P, Pammenter NW. What ultrastructure has told us about recalcitrant seeds. Rev Bras Fisiol Veg, 2000, 12: 22-25.

[6] Bewley JD, Bradford KJ, Hilhorst HW, Nonogaki H. Seeds: physiology of development, germination and dormancy, 2013 3 New York: Springer

[7] Bruna EM. Seed germination in rainforest fragments. Nature, 1999, 402: 139.

[8] Caldato SL, Floss PA, Da Croce DM, Longhi SJ. Estudo da regeneração natural, banco de sementes e chuva de sementes na Reserva Genética Florestal de Caçador, Sc. Ciência Florest, 1996, 6: 27-38.

[9] Carvalho PER. Pinheiro-do-paraná. Circ Técnica Embrapa, 2002, 60: 1-17.

[10] da Duarte LS, Dillenburg LR. Ecophysiological responses of Araucaria angustifolia (Araucariaceae) seedlings to different irradiance levels. Aust J Bot, 2000, 48: 531-537.

[11] Daws MI, Garwood NC, Pritchard HW. Prediction of desiccation sensitivity in seeds of woody species: a probabilistic model based on two seed traits and 104 species. Ann Bot, 2006, 97: 667-674.

[12] Dillenburg LR, Franco AMS, Coutinho AL, Korndorfer CL, Clebsch CC, Duarte LS, Ferla L, Rosa LMG, Silva LGR, Garbin ML, Mósena M, Zandavalli RB, Yamasaki S. Fonseca CR, Souza AF, Leal-Zanchet AM, Dutra T, Backes A, Ganado G. Aspectos ecofisiológicos da regeneração e crescimento de Araucaria angustifolia. Floresta de Araucária: Ecologia, Conservação e Desenvolvimento Sustentável, 2009, Ribeirão Preto: Holos 57 65

[13] Eggers S, Erdey D, Pammenter NW, Berjak P. Adkins SW, Ashmore SE, Navie S. Storage and germination response of recalcitrant seeds subjected to mild dehydration. Seeds: biology, development and ecology, 2007, London: CAB International 85 92

[14] Eira MTS, Salomão AN, Cunha R, Carrara DK, Mello CMC. Efeito do teor de água sobre a germinação de sementes de Araucaria angustifolia (BERT.) O. KTZE—Araucariaceae. Rev Bras Sementes, 1994, 16: 71-75.

[15] Espindola LS, Noin M, Corbineau F, Côme D. Cellular and metabolic damage induced by desiccation in recalcitrant Araucaria angustifolia embryos. Seed Sci Res, 1994, 4: 193-201.

[16] Farrant JM, Pammenter NW, Berjak P. Germination-associated events and the desiccation sensitivity of recalcitrant seeds—a study on three unrelated species. Planta, 1989, 178: 189-198.

[17] Fenner M, Thompson K. The ecology of seeds, 2005, New York: Cambridge University Press

[18] Ferraz IDK, Calvi GP. Lima Junior MJ. Teste de Germinação. Manual de Procedimentos de Análise de Sementes Florestais, 2011, Londrina: Abrates 5 36

[19] Ferreira DF. Sisvar: um programa para análises e ensino de estatística. Rev Sympos, 2008, 6: 36-41.

[20] Fotouo-M H, du Toit ES, Robbertse PJ. Germination and ultrastructural studies of seeds produced by a fast-growing, drought-resistant tree: implications for its domestication and seed storage. AoB Plants, 2015, 7: plv016.

[21] García D, Bañuelos M-J, Houle G. Differential effects of acorn burial and litter cover on Quercus rubra recruitment at the limit of its range in eastern North America. Can J Bot, 2002, 80: 1115-1120.

[22] Gardwood NC. Leck M, Parker V, Simpson R. Tropical soil seed banks: a review. Ecology of soil seed banks, 1989, San Diego: Academic Press 149 209

[23] Gasparin E, Faria JMR, José AC, Hilhorst HWM. Physiological and ultrastructural responses during drying of recalcitrant seeds of Araucaria angustifolia. Seed Sci Technol, 2017, 1: 1-18.

[24] Guerra MP, Silveira V, Santos ALW, Astarita LV, Nodari RO. Jain SM, Gupta PK, Newton RJ. Somatic embryogenesis in Araucaria angustifolia (Bert) O. Kuntze. Somatic embryogenesis in woody plants, 2000, Dordrecht: Kluwer Academic Publishers 457 578

[25] Iakovoglou V, Misra MK, Hall RB, Knapp AD. Alterations of seed variables under storage in nitrous oxide (N₂O) atmospheres for two recalcitrant Quercus species. Scand J For Res, 2010, 25: 24-30.

[26] ISTA. International rules for seed testing. Seed Sci Technol, 1996, 24: 48-52.

[27] IUCN (2016) The IUCN red list of threatened species. Version 2015-4. www.iucnredlist.org. Accessed 18 Mar 2016

[28] Lauterjung MB, Bernardi AP, Montagna T, Candido-Ribeiro R, Costa NCF, Mantovani A, Reis MS. Phylogeography of Brazilian pine (Araucaria angustifolia): integrative evidence for pre-Columbian anthropogenic dispersal. Tree Genet Genomes, 2018, 14: 1-12.

[29] Leite PF. Contribuição ao conhecimento fitoecológico do Sul do Brasil. Ciência Ambient, 2002, 1: 51-73.

[30] Long RL, Gorecki MJ, Renton M, Scott JK, Colville L, Goggin DE, Commander LE, Westcott DA, Cherry H, Finch-Savage WE. The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol Rev, 2015, 90: 31-59.

[31] Mattos JR. O pinheiro brasileiro, 2011, Florianópolis: Editora da UFSC.

[32] Moreira-Souza M, Cardoso EJBN. Practical method for germination of Araucaria angustifolia (Bert.) O. Ktze. seeds. Sci Agric, 2003, 60: 389-391.

[33] Moreno JA. Clima do Rio Grande do Sul, 1961, Porto Alegre: Secretaria da Agricultura.

[34] Motete N, Pammenter NW, Berjak P, Frédéric JC. Response of the recalcitrant seeds of Avicennia marina to hydrated storage: events occurring at the root primordia. Seed Sci Res, 1997, 7: 169-178.

[35] Nimer E (1990) Geografia do Brasil: Região Sul. In: IBGE—Instituto Brasileiro de Geografia e Estatística. IBGE, Rio de Janeiro, pp 51–187

[36] Oliveira-Filho A, Fontes MAL. Patterns of floristic differentiation among Atlantic Forests in Southeastern Brazil and the influence of climate. Biotropica, 2000, 32: 793-810.

[37] Pammenter NW, Berjak P. Evolutionary and ecological aspects of recalcitrant seed biology N.W. Seed Sci Res, 2000, 10: 301-306.

[38] Pasquini S, Braidot E, Petrussa E, Vianello A. Effect of different storage conditions in recalcitrant seeds of holm oak (Quercus ilex L.) during germination. Seed Scince Technol, 2011, 39: 165-177.

[39] Probert RJ, Daws MI, Hay FR. Ecological correlates of ex situ seed longevity: a comparative study on 195 species. Ann Bot, 2009, 104: 57-69.

[40] Saatkamp A, Affre L, Dutoit T, Poschlod P. The seed bank longevity index revisited: limited reliability evident from a burial experiment and database analyses. Ann Bot, 2009, 104: 715-724.

[41] Saatkamp A, Poschlod P, Venable DL. Gallagher RS. The functional role of soil seed banks in natural communities. Seeds: the ecology of regeneration in plant communities, 2014 3 Wallingford: CAB International 263 295

[42] Shibata M, Coelho CMM, Steiner N. Physiological quality of Araucaria angustifolia seeds at different stages of development. Seed Sci Technol, 2013, 41: 214-224.

[43] Souza AF, Forgiarini C, Longhi SJ, Brena DA. Regeneration patterns of a long-lived dominant conifer and the effects of logging in southern South America. Acta Oecol, 2008, 34: 221-232.

[44] Souza ML, Nogueira AC, Macedo RLG, Sanquetta CR, Venturin N. Estudos de um banco de sementes no solo de um fragmento florestal com Araucaria angustifolia no estado do Paraná. Floresta, 2011, 41: 335-346.

[45] Thompson K. Fenner M. The functional ecology of soil seeds banks. Seeds: the ecology of regeneration in plant communities, 2000 2 Wallingford: CABI Publishing 215 235

[46] Thompson K, Grime JP. Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. J Ecol, 1979, 67: 893-921.

[47] Thys RCS, Noreña CPZ, Marczak LDF, Aires AG, Cladera-Oliveira F. Adsorption isotherms of pinhão (Araucaria angustifolia seeds) starch and thermodynamic analysis. J Food Eng, 2010, 100: 468-473.

[48] Tompsett PB. The effect of desiccation on the longevity of seeds of Araucaria hunsteinii and A. cunninghamii. Ann Bot, 1982, 50: 693-704.

[49] Tompsett PB. Desiccation studies in relation to the storage of Araucaria seed. Ann Appl Biol, 1984, 105: 581-586.

[50] Tonetti OAO, Faria JMR, José AC, Oliveira TGS, Martins JC. Seed survival of the tropical tree Cryptocarya aschersoniana (Lauraceae): consequences of habitat disturbance. Austral Ecol, 2015

[51] Tweddle JC, Dickie JB, Baskin CC, Baskin JM. Ecological aspects of seed desiccation sensitivity. J Ecol, 2003, 91: 294-304.

[52] Umarani R, Aadhavan EK, Faisal MM. Understanding poor storage potential of recalcitrant seeds. Curr Sci, 2015, 108: 2023-2034.

[53] Vazquez-Yanes C, Orozco-Segovia A. Patterns of seed longevity and germination in the Tropical Rainforest. Annu Rev Ecol Syst, 1993, 24: 69-87.

[54] Viola MR, Mello CR, Acerbi FW Jr, Silva AM. Modelagem hidrológica na bacia hidrográfica do Rio Aiuruoca, MG. Rev Bras Eng Agrícola e Ambient, 2009, 13: 581-590.

[55] Walters C. Orthodoxy, recalcitrance and in-between: describing variation in seed storage characteristics using threshold responses to water loss. Planta, 2015, 242: 397-406.

[56] Walters C, Pammenter NW, Berjak P, Crane J. Desiccation damage, accelerated ageing and respiration in desiccation tolerant and sensitive seeds. Seed Sci Res, 2001, 11: 135-148.

[57] Wendling I, Delgado ME. Produção de mudas de araucária em tubetes. Comun Técnico Embrapa, 2008, 201: 1-18.