Pigments synthesized by dark fungi and their impact on the deterioration of documentary heritage on paper
DOI:
https://doi.org/10.31055/1851.2372.v57.n2.36580Keywords:
biodeterioration, conservation, melanins, black fungi, paperAbstract
Background and aims: Paper documents kept in museums and libraries can show noticeable signs of deterioration caused by the activity of different fungi. Some of the main pigments of fungal origin that aesthetically deteriorate this substrate and affect cultural heritage on cellulosic support are the group of dark pigments or melanins. The aim of this work is to provide an updated overview of the state of the art of black fungi that colonize paper and the melanins they synthesize, causing significant damage to documentary heritage, which is a matchless source for the history of indigenous people.
M&M: A bibliographic search of the updated and available information on the dark pigments that synthesize different black fungi that deteriorate paper was carried out. Seventy-four specialized works on the subject have been analyzed; most of them recently published in national and international journals.
Results: Knowledge about the diversity and characteristics of the dark pigments synthesized by the black fungi that deteriorate paper is key to developing prevention and remediation strategies to eliminate these pigments from cellulosic support with heritage value. This paper presents information about the black fungi that deteriorate paper, the types of melanins they can synthetize, the structures where they are accumulated, and their contribution to the aesthetic deterioration of the mentioned materials
Conclusions: This knowledge serves as the basis for developing new restoration strategies that could be effective and sustainable and the ensure the preventive conservation of historical documents and works of art on paper
References
ALMENDROS, M. G., A. T. MARTINEZ, M. F. MARTÍNEZ & F. J. GONZÁLEZ-VILA. 1985. Degradative oxidation products of the melanin of Ulocladium atrum. Soil Biol. Biochem. 17: 723-726.
https://doi.org/10.1016/0038-0717(85)90052-5
ARAI, H. 2000. Foxing caused by Fungi: twenty-ve years of study. Inter. Biodet. Biodegradation 46: 181-188.
https://doi.org/10.1016/S0964-8305(00)00063-9
BABITSKAYA, V. G., V. V. SHCHERBA, T. V. FILIMONOVA, & E. A. GRIGORCHUK. 2000. Melanin pigments from the fungi Paecilomyces variotii and Aspergillus carbonarius. Appl. Biochem. Microbiol. 36: 128-133.
https://doi.org/10.1007/BF02737906
BÁRCENA, A., G. PETROSELLI, S. M. VELASQUEZ, J. M. ESTÉVEZ, R. ERRA-BALSELLS, P. A. BALATTI & M. C. N. SAPARRAT. 2015. Response of the fungus Pseudocercospora griseola f. mesoamericana to Tricyclazole. Mycol. Prog. 14:76.
https://doi.org/10.1007/s11557-015-1102-7
BÁRCENA, A., M. BRUNO, A. GENNARO, M. F. ROZAS, M. V. MIRÍFICO, P. A. BALATTI & M. C. N. SAPARRAT. 2018. Melanins from two selected isolates of Pseudocercospora griseola grown in-vitro: Chemical features and redox activity. J. Photochem. Photobiol. B. Biol. 186: 207-215.
https://doi.org/10.1016/j.jphotobiol.2018.07.019
BELL, A. A. & M. H. WHEELER. 1986. Biosynthesis and functions of fungal melanins. Annu. Rev. Phytopathol. 24: 411-451.
https://doi.org/10.1146/annurev.py.24.090186.002211
BELTRÁN-GARCÍA, M. J., F. M. PRADO, M. S. OLIVEIRA, D. ORTIZ-MENDOZA, A. C. SCALFO, A. PESSOA, M. H. G. MEDEIROS, J. F. WHITE & P. DI MASCIO. 2014. Singlet molecular oxygen generation by light-activated DHN-melanin of the fungal pathogen Mycosphaerella fijiensis in black Sigatoka disease of bananas. PLoS ONE 9:e91616.
https://doi.org/10.1371/journal.pone.0091616
BHARDWAJ, N. & I. K. BHATNAGAR. 2002. Microbial deterioration of paper paintings. Biodeterioration of Materials 2: 132-135.
BODDY, L. & J. HISCOX. 2016. Fungal ecology: principles and mechanisms of colonization and competition by saprotrophic fungi. Microbiology Spectrum 4: FUNK-0019-2016.
https://doi.org/10.1128/microbiolspec.FUNK-0019-2016
BORREGO ALONSO, S. F., & O. HERRERA BARRIOS.2021. Calidad micológica ambiental en archivos cubanos y su impacto en la salud del personal. An. Acad. Cienc. Cuba 11.
CALVO, A. M., R. A. WILSON, J. W. BOK & N. P. KELLER. 2002. Relationship between secondary metabolism and fungal development. Microbiol. Mol. Biol. Rev 66: 447-459.
https://doi.org/10.1128/MMBR.66.3.447-459.2002
CALVO, A. M. C., A. DOCTERS, M. V. MIRANDA & M. C. N. SAPARRAT. 2017. The use of gamma radiation for the treatment of cultural heritage in the Argentine National Atomic Energy Commission: past, present, and future. Top Curr Chem 375: 227-248.
https://doi.org/10.1007/s41061-016-0087-2
CAMACHO, E., R. VIJ, C. CHRISSIAN, R. PRADOS-ROSALES, D. GIL, R. N. O'MEALLY, R. J. B. CORDERO, R. N. COLE, J. M. McCAFFERY, R. E. STARK & A. CASADEVALL. 2019. The structural unit of melanin in the cell wall of the fungal pathogen Cryptococcus neoformans. J. Biol. Chem 294: 10471-10489.
https://doi.org/10.1074/jbc.RA119.008684
CHIEWCHANVIT, S., S. CHONGKAE, P. MAHANUPAB, J. D. NOSANCHUK, S. PORNSUWAN, N. VANITTANAKOM & S. YOUNGCHIM. 2017. Melanization of Fusarium keratoplasticum (F. solani Species Complex) during disseminated fusariosis in a patient with acute leukemia. Mycopathologia 182: 879-885.
https://doi.org/10.1007/s11046-017-0156-2
CHRISSIAN, C., E. CAMACHO, M. S. FU, R. PRADOS-ROSALES, S. CHATTERJEE, R. J. B. CORDERO, J. K. LODGE, A. CASADEVALL & R. E. STARK. 2020. Melanin deposition in two Cryptococcus species depends on cell-wall composition and flexibility. J. Biol. Chem 295: 1815-1828.
https://doi.org/10.1074/jbc.RA119.011949
DADACHOVA, E., R. A. BRYAN, X. HUANG, T. MOADEL, A. D. SCHWEITZER, P. AISEN, J. D. NOSANCHUK & A. CASADEVALL. 2007. Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS ONE 5: e457.
https://doi.org/10.1371/journal.pone.0000457
EVELEIGH, D. E. 1970. Fungal disfigurement of paper, and soft rot of cedar shingles. Applied Microbiology 19: 872-874.
https://doi.org/10.1128/am.19.5.872-874.1970
ELLIS, M. B. 1971. Dematiaceous Hyphomycetes. Commonwealth Mycological Institute. Kew, London.
ELLIS, M. B. 1976. More Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, London.
FERNANDES, C., R. PRADOS-ROSALES, B. M. SILVA, A. NAKOUZI-NARANJO, M., ZUZARTE, S. CHATTERJEE, R. E. STARK, A. CASADEVALL & T. GONÇALVES. 2015. Activation of melanin synthesis in Alternaria infectoria by antifungal drugs. Antimicrob. Agents Chemother. 60 :1646-55.
https://doi.org/10.1128/AAC.02190-15
FERRÁNDIZ-PULIDO, C., M. T. MARTIN-GOMEZ, T. REPISO, C. JUÁREZ-DOBJANSCHI, B. FERRER, I. LÓPEZ-LERMA, G. APARICIO, C. GONZÁLEZ-CRUZ, F. MORESO, A. ROMAN & V. GARCÍA-PATOS. 2019. Cutaneous infections by dematiaceous opportunistic fungi: Diagnosis and management in 11 solid organ transplant recipients. Mycoses 62: 121-127.
https://doi.org/10.1111/myc.12853
FRANCO, E., M. I. TRONCOZO, M. BAEZ, M. V. MIRÍFICO, G. L. ROBLEDO, P. A. BALATTI & M. C. N. SAPARRAT. 2018. Fusarium equiseti LPSC 1166 and its in vitro role in the decay of Heterostachys ritteriana leaf litter. Folia Microbiologica 63: 169-179.
https://doi.org/10.1007/s12223-017-0541-8
FRANDSEN, R. J. N., S. A. RASMUSSEN, P. B. KNUDSEN, S. UHLIG, D. PETERSEN, E. LYSØE, C. H. H, H. GIESE & T. O. LARSEN. 2016. Black perithecial pigmentation in Fusarium species is due to the accumulation of 5-deoxybostrycoidin-based melanin. Scientific Reports 6: 26206.
https://doi.org/10.1038/srep26206
GESSLER, N. N., A. C. EGOROVA & T. A. BELOZERSKAYA. 2014. Melanin pigments of fungi under extreme environmental conditions. Appl. Biochem. Microbiol. 50: 105-113.
https://doi.org/10.1134/S0003683814020094
GMOSER, R, J. A. FERREIRA, P. R. LENNARTSSON & M. J. TAHERZADEH. 2017. Filamentous ascomycetes fungi as a source of natural pigments. Fungal Biol. Biotechnol. 4:4.
https://doi.org/10.1186/s40694-017-0033-2
HU, Y., X. HAO, J. LOU, P. ZHANG, J. PAN & X. ZHU. 2012. A PKS gene, pks-1, is involved in chaetoglobosin biosynthesis, pigmentation and sporulation in Chaetomium globosum. Sci. China Life Sci. 55: 1100-1108.
https://doi.org/10.1007/s11427-012-4409-5
KARAKASIDOU, K., K NIKOLOULI., G. D. AMOUTZIAS, A. PORNOU, CH. MANASSIS, G. TSIAMIS & D. MOSSIALOS. 2017. Microbial diversity in biodeteriorated Greek historical documents dating back to the 19th and 20th century: a case study. Microbiology Open 1: 11.
https://doi.org/10.1002/mbo3.596
KRAKOVÁ, L., K. CHOVANOVÁ, S. A. SELIM, A. ŠIMONOVIČOVÁ, A. PUŠKAROVÁ, A.D. MAKOVÁ & A. PANGALLO. 2012. Multiphasic approach for investigation of the microbial diversity and its biodegradative abilities in historical paper and parchment documents. Inter. Biodet. Biodegradation 70: 117-125.
https://doi.org/10.1016/j.ibiod.2012.01.011
LACEY, M. E. & J. S. WEST. 2006. The Air Spore. Springer. Dordrecht. https://doi.org/10.1007/978-0-387-30253-9
LECOINTE, K., M. CORNU, J. LEROY, P. COULON & B. SENDID. 2019. Polysaccharides cell wall architecture of Mucorales. Front. Microbiol. 10: 469.
https://doi.org/10.3389/fmicb.2019.00469
LEE D, E-H. JANG, M. LEE, S-W. KIM, Y. LEE, K-T. LEE & Y-S. BAHN. 2019. Unraveling melanin biosynthesis and signaling networks in Cryptococcus neoformans.
https://doi.org/10.1128/mBio.02267-19
LLORENTE, C, A. BÁRCENA, J. VERA BAHIMA, M. C. N. SAPARRAT, A. M. ARAMBARRI, M., F. ROZAS, M. V. MIRÍFICO & P. A. BALATTI. 2012. Cladosporium cladosporioides LPSC 1088 produces the 1,8-dihydroxynaphthalene-melanin-like compound and carries a putative pks gene. Mycopathologia 174: 397-408.
https://doi.org/10.1007/s11046-012-9558-3
MALLO, A. C., D. S. NITIU, L. A. ELÍADES & M. C. N. SAPARRAT. 2017. Fungal degradation of cellulosic materials used as support for cultural heritage. Int. J. Conserv. Sci. 8: 619-632.
MEDINA, R., C. G. LUCENTINI, M. E. E. FRANCO, G. PETROSELLI, J. A. ROSSO, R. ERRA-BALSELLS, P. A. BALATTI & M. C. N. SAPARRAT. 2018. Identification of an intermediate for 1,8- dihydroxynaphthalene-melanin synthesis in a race-2 isolate of Fulvia fulva (syn. Cladosporium fulvum). Heliyon.
https://doi.org/10.1016/j.heliyon.2018.e01036
MELO, D., S. O. SEQUEIRA, J. A. LOPES & M. F. MACEDO. 2019. Stains versus colourants produced by fungi colonising paper cultural heritage: A review. J. Cult. Herit 35: 161-182. https://doi.org/10.1016/j.culher.2018.05.013
MELO, D. C. 2017. Fungal Stains on Paper: Melanins produced by fungi. Thesis for the Master degree in Conservation and Restoration. Monte de Caparica, Lisboa: Departamento de Conservação e Restauro, Mestrado em Conservação e Restauro, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa. 57 p.
MESQUITA, N., A. PORTUGAL, S. VIDEIRA, S. RODRÍGUEZ-ECHEVERRÍA, A. M. L. BANDEIRA, M. J. A. SANTOS & H. FREITAS. 2009. Fungal diversity in ancient documents. A case study on the Archive of the University of Coimbra. Int. Biodeterior. Biodegradation. 63: 626-629.
https://doi.org/10.1016/j.ibiod.2009.03.010
MICHAELSEN, A., F. PINZARI, K. RIPKA, W. LUBITZ & G. PIÑAR. 2006. Application of molecular techniques for identification of fungal communities colonizing paper material. Inter. Biodet. Biodegradation 58:133-141.
https://doi.org/10.1016/j.ibiod.2006.06.019
MICHAELSEN, A., G. PIÑAR & F. PINZARI. 2010. Molecular and microscopical investigation of the microflora inhabiting a deteriorated Italian manuscript dated from the thirteenth century. Microbial Ecology 60: 69-80.
https://doi.org/10.1007/s00248-010-9667-9
NOL, L., Y. HENIS & R. G. KENNETH. 2001. Biological factors of foxing in postage stamp paper. Inter. Biodet. Biodegradation 48: 98-104.
https://doi.org/10.1016/S0964-8305(01)00072-5
NG, K.P., S. M. YEW, CH. L. CHAN, T. S. SOO-HOO, S. L. NA, H. HASSAN, Y. F. NGEOW, CH. CH. HOH, K. W. LEE & W. Y. YEE. 2012. Sequencing of Cladosporium sphaerospermum, a dematiaceous fungus isolated from blood culture. Eukaryotic Cell 11: 705-706.
https://doi.org/10.1128/EC.00081-12
NITIU, D. S., A. C. MALLO & M. C. N. SAPARRAT. 2020. Fungal melanins that deteriorate paper cultural heritage: an overview. Mycologia. 112: 859-870. https://doi.org/10.1080/00275514.2020.1788846
NOSANCHUK, J. D., R. E. STARK & A. CASADEVALL. 2015. Fungal melanin: what do we know about structure? Front. Microbiol. 6: 1463.
https://doi.org/10.3389/fmicb.2015.01463
PAL, A. K., D. H. GAJJAR & A. R. VASAVADA. 2014. DOPA and DHN pathway orchestrate melanin synthesis in Aspergillus species. Medical Mycology 52: 10-18.
https://doi.org/10.3109/13693786.2013.826879
PALONEN, E. K., S. RAINA, A. BRANDT, J. MERILUOTO, T. KESHAVARZ & J. T. SOINI. 2017. Melanisation of Aspergillus terreus-Is butyrolactone I involved in the regulation of both DOPA and DHN types of pigments in submerged culture? Microorganisms 5: 22.
https://doi.org/10.3390/microorganisms5020022
PANGALLO, D., K. CHOVANOVA, A. ŠIMONOVIČOVÁ & P. FERIANIC. 2009. Investigation of microbial community isolated from indoor artworks and air environment: identification, biodegradative abilities, and DNA typing. Can. J. Microbiol. 55: 277-287.
https://doi.org/10.1139/w08-136
PAVON FLORES, S. C. 1976. Gamma radiation as fungicide and its effects on paper. Bulletin of the American Institute for Conservation of Historic and Artistic Works 16: 15-44.
https://doi.org/10.1179/019713676806029384
PEREZ-CUESTA, U., L. APARICIO-FERNANDEZ, X. GURUCEAGA, L. MARTIN-SOUTO, A. ABAD-DIAZ-DE-CERIO, A. ANTORAN, I. BULDAIN, F. L. HERNANDO, A. RAMIREZ-GARCIA & A. REMENTERIA. 2019. Melanin and pyomelanin in Aspergillus fumigatus: from its genetics to host interaction. Int. Microbiol. https://doi.org/10.1007/s10123-019-00078-0
PICCOLO, A. 1996. Humic substances in terrestrial ecosystems. 1st ed. Elsevier, Amsterdam,
PINHEIRO, A. C, M. F. MACEDO, V. JURADO, C. SAINZ JIMENEZ, C. VIEGAS, J. BRANDÃO & L. ROSADO. 2011. Mould and yeast identification in archival settings: Preliminary results on the use of traditional methods and molecular biology options in Portuguese archives. Int. Biodeterior. Biodegradation. 65: 619-627.
https://doi.org/10.1016/j.ibiod.2011.02.008
PINZARI, F. & M. MONTANARI. 2011. Mould growth on library materials stored compactus-type shelving units. In: ABDUL-WAHAB SA, ed. Sick Building Syndrome in Public Buildings and Workplaces, p. 196-203. Springer, Berlin.
https://doi.org/10.1007/978-3-642-17919-8_11
POMBEIRO-SPONCHIADO, S. R., G. S. SOUSA, J. C. ANDRADE, H. F. LISBOA & R. C. GONÇALVES. 2017. Production of melanin pigment by fungi and its biotechnological applications. In BLUMENBERG, M. (ed.), Melanin, p; 45-75. InTechOpen, London.
QUAN, Y., B. G. VAN DEN ENDE, D. SHI, F. X. PRENAFETA-BOLDÚ, Z. LIU, A. M. S. AL-HATMI, S. A. AHMED, P. E. VERWEIJ, Y. KANG & S. DE HOOG. 2019. A comparison of isolation methods for black fungi degrading aromatic toxins. Mycopathologia 184: 653-660.
https://doi.org/10.1007/s11046-019-00382-3
RAKOTONIRAINY, M. S., E HEUDE & B. LAVÉDRINE. 2007. Isolation and attempts of biomolecular characterization of fungal strains associated to foxing on a 19th century book. Journal of Cultural Heritage 8 : 126-133.
https://doi.org/10.1016/j.culher.2007.01.003
RAO, M. P. N., M. XIAO & W. J. LI. 2017. Fungal and bacterial pigments: Secondary metabolites with wide application. Front. Microbiol. 8 :1113.
https://doi.org/10.3389/fmicb.2017.01113
REIS-MENESES, A. A., W. GAMBALE, M. C. GIUDICE & M. A. SHIRAKAWA. 2011. Accelerated testing of mold growth on traditional and recycled book paper. Int. Biodeterior. Biodegradation 65: 423-428. https://doi.org/10.1016/j.ibiod.2011.01.006
ROJAS, T. I., M. J. AIRA, A. BATISTA, I. L. CRUZ & S. GONZÁLEZ. 2012. Fungal biodeterioration in historic buildings of Havana (Cuba). Grana 51 (1): 44-51.
https://doi.org/10.1080/00173134.2011.643920
RUIBAL, C., G. PLATAS & G. F. BILLS. 2008. High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia 21: 93-110.
https://doi.org/10.3767/003158508X371379
RUISI, S., D. BARRECA, L. SELBMANN, L. ZUCCONI & S. ONOFRI. 2007. Fungi in Antarctica. Rev. Environ. Sci. Biotechnol. 6: 127-141.
https://doi.org/10.1007/s11157-006-9107-y
SAPARRAT, M. C. N., G. FERMOSELLE, S. STENGLEIN, M. AULICINO & P. A. BALATTI. 2009. Pseudocercospora griseola causing angular leaf spot on Phaseolus vulgaris produces 1,8-dihydroxynaphthalene-melanin. Mycopathologia 168: 41-47.
https://doi.org/10.1007/s11046-009-9194-8
SARI, E., L. ISERI, M. KOÇAK & D. YILDIZ. 2015. Is it Subungual Melanoma? Fungal melanonychia due to Phoma glomerata. Cukurova Medical Journal 40: 162-165.
https://doi.org/10.17826/cutf.44511
SCHMALER-RIPCKE, J., V. SUGAREVA, P. GEBHARDT, R. WINKLER, O. KNIEMEYER, T. HEINEKAMP & A. A. BRAKHAG. 2009. Production of pyomelanin, a second type of melanin, via the tyrosine degradation pathway in Aspergillus fumigatus. Appl. Environ. Microbiol. 75: 493-503.
https://doi.org/10.1128/AEM.02077-08
SMITH, D. F. Q. & A. CASADEVALL. 2019. The role of melanin in fungal pathogenesis for animal hosts. In: RODRIGUES M. (ed.), Fungal Physiology and Immunopathogenesis. Curr. Top. Microbiol. Immunol. Vol. 422, pp. 1-30. Springer, Cham, Switzerland.
https://doi.org/10.1007/82_2019_173
STALEY, J. T., F. E. PALMER & J. B. ADAMS. 1982. Microcolonial fungi: Common inhabitants on desert rocks? Science 215: 1093-1095. https://doi.org/10.1126/science.215.4536.1093
STERFLIGER, K. 2010. Fungi: Their role in deterioration of cultural heritage. Fungal Biology Reviews 24: 47-55.
https://doi.org/10.1016/j.fbr.2010.03.003
SUN, S., X. ZHANG, S. SUN, L. ZHANG, S. SHAN & H. ZHU. 2016. Production of natural melanin by Auricularia auricula and study on its molecular structure. Food Chemistry 190:801-807.
https://doi.org/10.1016/j.foodchem.2015.06.042
SZCZEPANOWSKA, H. & A. R. CAVALIERE. 2012. Conserving our cultural heritage: The role of fungi in biodeterioration. In: JOHANNING E, MOREY P, AUGER P. (eds.), Bioaerosols Fungi, Bacteria, Mycotoxins in Indoor and Outdoor Environments and Human Health, pp. 293-309. Fungal Research Group, Albany
TOLEDO, A. V, M. E. E. FRANCO, S. M. Y. LÓPEZ, M. I. TRONCOZO, M. C. N. SAPARRAT & P. A. BALATTI. 2017. Melanins in fungi: Types, localization and putative biological roles. Physiol. Mol. Plant Pathol. 99: 2-6. https://doi.org/10.1016/j.pmpp.2017.04.004
TUDOR, D., S. C. ROBINSON & P. A. COOPER. 2012. The influence of moisture content variation on fungal pigment formation in spalted wood. AMB Express 2:69.
https://doi.org/10.1186/2191-0855-2-69
TUDOR, D. 2013. Fungal pigment formation in wood substrate. Ph.D. Thesis, University of Toronto, Toronto, ON, Canada, 2013.
WAINWRIGHT, M., T. A. ALI & F. BARAKAH. 1993. A review of the role of oligotrophic micro-organisms in biodeterioration. Int. Biodet. Biodegradation 31: 1-13.
https://doi.org/10.1016/0964-8305(93)90010-Y
WOUDENBERG, J. H. C., M. MEIJER, J. HOUBRAKEN, & R. A. SAMSON. 2017. Scopulariopsis and scopulariopsis-like species from indoor environments. Studies in Mycology 1-35.
https://doi.org/10.1016/j.simyco.2017.03.001
WALKER, C. A., B. L. GÓMEZ, H. M. MORA-MONTES, K. S. MACKENZIE, C. A. MUNRO, A. J. BROWN, N. A. GOW, C. C. KIBBLER & F. C. ODDS. 2010. Melanin externalization in Candida albicans depends on cell wall chitin structures. Eukaryotic Cell 9: 1329-1342.
https://doi.org/10.1128/EC.00051-10
ZHENG, W., B. S. CAMPBELL, B. M. MCDOUGALL & R. J. SEVIOUR. 2008. Effects of melanin on the accumulation of exopolysaccharides by Aureobasidium pullulans grown on nitrate. Bioresource Technology 16: 7480-6.
https://doi.org/10.1016/j.biortech.2008.02.016
ZOTTI, M, A. FERRONI & P. CALVINI. 2008. Microfungal biodeterioration of historic paper: Preliminary FTIR and microbiological analyses. Int. Biodet. Biodegradation. 62: 186-194.
Downloads
Published
Issue
Section
License
Copyright (c) 2022 Daniela Silvana Nitiu, Andrea Cecilia Mallo, Mario Carlos Nazareno Saparrat
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Provides immediate and free OPEN ACCESS to its content under the principle of making research freely available to the public, which fosters a greater exchange of global knowledge, allowing authors to maintain their copyright without restrictions.
Material published in Bol. Soc. Argent. Bot. is distributed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International license.
