Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X0921
Acta Limnologica Brasiliensia
Original Article

Diversity of hyphomycetes on submerged leaf litter in two Atlantic Forest areas in the Northeast of Brazil with comments on the water quality

Diversidade de hifomicetos em folhedo submerso em duas áreas de Mata Atlântica no nordeste do Brasil com comentários sobre a qualidade da água

Elder George Rodrigues do Nascimento; Marcela Alves Barbosa; Wanderson Luiz Tavares; Elaine Malosso

Downloads: 0
Views: 1057

Abstract

Abstract:: Aim: The Atlantic Forest is a Brazilian biome whose biota plays a fundamental role in the preservation of water quality. Hyphomycetes play an important role in aquatic ecosystems as they can decompose organic matter and, consequently, contribute to nutrient cycling, maintaining aquatic life. The aim of this work was to determine the diversity and composition of the aquatic hyphomycetes community in two areas of Atlantic Forest in the state of Pernambuco (Charles Darwin Ecological Refuge) and Alagoas (Pedra Talhada Biological Reserve), in addition to comparing these communities with the water abiotic factors.

Methods: For this, four collections of submerged decomposing leaves, for evaluation of the fungi community, and water for measuring the parameters: acidity, alkalinity, chlorides, electrical conductivity, total coliforms, color, BOD, COD, DO, total nitrogen, pH, total solids, sulfates, temperature and turbidity, and calculation of the Water Quality Index (WQI) were carried out. The samplings took place between July/2018 and May/2019, at six points along a stream in each study area.

Results: Fifty-three taxa were identified, and 1926 occurrences were recorded in 2592 leaf fragments. There was a predominance of Blodgettia aquatica, Blodgettia indica, Flagellospora penicillioides, Flagellospora sp., Mycoleptodiscus disciformis, Triscelophorus monosporus and Xylomyces acerosisporus, with similarity of these and other species between the studied areas. In the rainy season, there was a greater occurrence of aquatic hyphomycetes in both areas; however, the diversity of fungi was greater in the Charles Darwin Refuge. Abiotic factors such as temperature, DO and rainfall influence the occurrence of hyphomycetes, however, no community structure was detected or strongly correlated with the studied abiotic variables.

Conclusions: The areas presented adequate values ​​for the variables indicative of water quality and high richness of hyphomycetes species, demonstrating the importance of legal protection for the conservation of natural areas.

Keywords

Ascomycota, conidial fungi, aquatic ecosystems, water quality

Resumo

Resumo: : Objetivo: A Mata Atlântica é um bioma brasileiro cuja biota desempenha um papel fundamental na preservação da qualidade da água. Os hifomicetos têm um papel importante nos ecossistemas aquáticos, pois são capazes de decompor a matéria orgânica e, consequentemente, contribuem com a ciclagem de nutrientes, mantendo a vida aquática. O objetivo deste trabalho foi determinar a diversidade e composição da comunidade de hifomicetos aquáticos em duas áreas de Mata Atlântica no estado de Pernambuco (Refúgio Ecológico de Charles Darwin) e Alagoas (Reserva Biológica de Pedra Talhada), além de comparar essas comunidades com os fatores abióticos da água.

Métodos: Para isso, foram realizadas quatro coletas de folhas submersas em decomposição, para avaliação da comunidade de fungos, e água para aferição dos parâmetros: acidez, alcalinidade, cloretos, condutividade elétrica, coliformes totais, cor, DBO, DQO, OD, nitrogênio total, pH, sólidos totais, sulfatos, temperatura e turbidez, e cálculo do Índice de Qualidade da Água (IQA). As coletas foram realizadas entre julho/2018 e maio/2019, em seis pontos ao longo de um riacho em cada área de estudo.

Resultados: Foram identificados 53 táxons e registradas 1926 ocorrências em 2592 fragmentos foliares. Houve predomínio de Blodgettia aquatica, Blodgettia indica, Flagellospora penicillioides, Flagellospora sp., Mycoleptodiscus disciformis, Triscelophorus monosporus e Xylomyces acerosisporus, havendo similaridade dessas e de outras espécies entres as áreas estudadas. No período chuvoso houve maior ocorrência de hifomicetos aquáticos nas duas áreas, porém, a diversidade de fungos foi maior no Refúgio Charles Darwin. Fatores abióticos como temperatura, OD e pluviosidade influenciam na ocorrência de hifomicetos, no entanto, nenhuma estrutura de comunidade foi detectada ou fortemente correlacionada com as variáveis abióticas estudadas.

Conclusões: As áreas apresentaram valores adequados para as variáveis indicativas da qualidade da água e alta riqueza de espécies de hifomicetos, demonstrando a importância da proteção legal para conservação de áreas naturais.
 

Palavras-chave

Ascomycota, fungos conidiais, ecossistemas aquáticos, qualidade da água

References

AGÊNCIA NACIONAL DE ÁGUAS – ANA. Portal da qualidade das águas: indicadores de qualidade da água: Índice de Qualidade das Águas (IQA) [online]. 2020 [viewed 24 Mar. 2020]. Available from: http://portalpnqa.ana.gov.br/indicadores-indice-aguas.aspx

ALMEIDA, D.A.C., BARBOSA, F.R. and GUSMÃO, L.F.P. Alguns fungos conidiais aquáticos-facultativos do bioma Caatinga. Acta Botanica Brasílica, 2012, 26(4), 924-932. http://dx.doi.org/10.1590/S0102-33062012000400021.

ALMEIDA, D.A.C., IZABEL, T.S.S. and GUSMÃO, L.F.P. Fungos conidiais do bioma Caatinga I. Novos registros para o continente americano, Neotrópico, América do Sul e Brasil. Rodriguésia, 2011, 62(1), 43-53. http://dx.doi.org/10.1590/2175-7860201162104.

AMERICAN PUBLIC HEALTH ASSOCIATION – APHA. American Water Works Association – AWWA. Water Environment Federation – WEF. Standard methods for the examination of water and wastewater. 19th ed. Washington: APHA/AWWA/WEF, 1995.

BARBOSA, F.R. and GUSMÃO, L.F.P. Conidial fungi from semi-arid Caatinga Biome of Brazil. Rare freshwater hyphomycetes and other new records. Mycosphere, 2011, 2(4), 475-485.

BARBOSA, F.R., GUSMÃO, L.F.P. and BARBOSA, F. Fungos anamórficos (Hyphomycetes) no semi- árido do Estado da Bahia, Brasil. Acta Botanica Brasílica, 2008, 22(1), 29-36. http://dx.doi.org/10.1590/S0102-33062008000100004.

BÄRLOCHER, F. and ROSSET, J. Aquatic hyphomycete spora of two Black Forest and two Swiss Jura streams. Transactions of the British Mycological Society, 1981, 76(3), 479-483. http://dx.doi.org/10.1016/S0007-1536(81)80076-9.

BÄRLOCHER, F. Water-borne conidia of aquatic hyphomycetes: seasonal and yearly patterns in Catamaran Brook, New Brunswick, Canada. Canadian Journal of Botany, 2000, 78(2), 157-167. http://dx.doi.org/10.1139/b99-172.

BÄRLOCHER, F., HELSON, J.E. and WILLIAMS, D.D. Aquatic hyphomycete communities across a land-use gradient of Panamanian streams. Fundamental and Applied Limnology, 2010, 177(3), 209-221. http://dx.doi.org/10.1127/1863-9135/2010/0177-0209.

BAUDOIN, J., GUEROLD, F., FELTEN, V., CHAUVET, E., WAGNER, P.Y. and ROUSSELLE, P. Elevated aluminium concentration in acidified headwater streams lowers aquatic hyphomycetes diversity and impairs leaf-litter breakdown. Microbial Ecology, 2008, 56(2), 260-269. http://dx.doi.org/10.1007/s00248-007-9344-9. PMid:18202885.

BELLIVEAU, M.J.R. and BÄRLOCHER, F. Molecular evidence confirms multiple origins of aquatic hyphomycetes. Mycological Research, 2005, 109(12), 1407-1417. http://dx.doi.org/10.1017/S0953756205004119. PMid:16353640.

BRASIL. Ministério do Meio Ambiente – MMA. Conselho Nacional do Meio Ambiente – CONAMA. Resolução CONAMA nº 357, de 17 de março de 2005. Diário Oficial da União [da] República Federativa do Brasil, Poder Executivo, Brasília, DF, 18 mar. 2005, no. 53, pp. 58-63.

BRASIL. Ministério do Meio Ambiente – MMA. Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis – IBAMA. 2006. Plano operativo de prevenção e combate aos incêndios florestais da Reserva Biológica da Pedra Talhada. Brasília.

BRASIL. Ministério da Saúde. Portaria nº 2914, de 12 de dezembro de 2011. Dispõe sobre os procedimentos de controle e de vigilância da qualidade da água para consumo humano e seu padrão de potabilidade. Diário Oficial da União [da] República Federativa do Brasil, Poder Executivo, Brasília, DF, 14 dez. 2011, Seção 1, no. 239, pp. 39-46.

CASTAÑEDA-RUIZ, R.F., HEREDIA, G., GUSMÃO, L.F.P. and LI, D.-W. Fungal diversity of Central and South America In: D.-W. LI, ed. Biology of microfungi. Switzerland: Springer International Publishing, 2016, pp. 197-217. http://dx.doi.org/10.1007/978-3-319-29137-6_9.

CAVALCANTI, M.S. and MILANEZ, A.I. Hyphomycetes from water and soil at the Dois Irmãos Forest Reserve, Recife, Pernambuco State, Brazil. Acta Botanica Brasílica, 2007, 21(4), 857-862. http://dx.doi.org/10.1590/S0102-33062007000400010.

CHAMIER, A.-C. Water chemistry. In: F. BÄRLOCHER, ed. The ecology of aquatic hyphomycetes. Berlin: Springer, 1992, pp. 152-172. http://dx.doi.org/10.1007/978-3-642-76855-2_8.

CHAUVET, E. and SUBERKROPP, K. Temperature and sporulation of aquatic hyphomycetes. Applied and Environmental Microbiology, 1998, 64(4), 1522-1525. http://dx.doi.org/10.1128/AEM.64.4.1522-1525.1998. PMid:16349551.

CHAUVET, E. Aquatic hyphomycete distribution in South-Western France. Journal of Biogeography, 1991, 18(6), 699-706. http://dx.doi.org/10.2307/2845551.

CHAUVET, E., CORNUT, J., SRIDHAR, K.R., SELOSSE, M. and BÄRLOCHER, F. Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecology, 2016, 19, 112-127. http://dx.doi.org/10.1016/j.funeco.2015.05.014.

CHENG, Z.L., ANDRE, P. and CHIANG, C. Hyphomycetes and macroinvertebrates colonizing leaf litter in two Belgian streams with contrasting water quality. Limnetica, 1997, 13, 57-63.

CZECZUGA, B., MAZALSKA, B., GODLEWSKA, A. and MUSZYŃSKA, E. Aquatic fungi growing on dead fragments of submerged plants. Limnologica, 2005, 35(4), 283-297. http://dx.doi.org/10.1016/j.limno.2005.07.002.

DANGER, M., GESSNER, M.O. and BÄRLOCHER, F. Ecological stoichiometry of aquatic fungi: current knowledge and perspectives. Fungal Ecology, 2016, 19, 100-111. http://dx.doi.org/10.1016/j.funeco.2015.09.004.

DESCALS, E. and MORALEJO, E. Water and asexual reproduction in the Ingoldian fungi. Botanica Complutensis, 2001, 25, 13-71.

DESCALS, E. Diagnostic characters of propagules of Ingoldian fungi. Mycological Research, 2005, 109(Pt 5), 545-555. http://dx.doi.org/10.1017/S0953756205002728. PMid:16018309.

DUARTE, S., BÄRLOCHER, F., PASCOAL, C. and CASSIO, F. Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives. Fungal Ecology, 2016, 19, 169-181. http://dx.doi.org/10.1016/j.funeco.2015.06.002.

DUARTE, S., PASCOAL, C., CÁSSIO, F. and BÄRLOCHER, F. Aquatic hyphomycete diversity and identity affect leaf litter decomposition in microcosms. Oecologia, 2006, 147(4), 658-666. http://dx.doi.org/10.1007/s00442-005-0300-4. PMid:16496184.

ELLIS, M.B. Dematiaceous Hyphomycetes. Kew: Commonwealth Mycological Institute, 1971.

ELLIS, M.B. More Dematiaceous Hyphomycetes. Kew: Commonwealth Mycological Institute, 1976.

FERNANDES, I., UZUN, B., PASCOAL, C. and CÁSSIO, F. Responses of aquatic fungal communities on leaf litter to temperature-change events. International Review of Hydrobiology, 2009, 94(4), 410-418. http://dx.doi.org/10.1002/iroh.200811163.

FERNÁNDEZ, R., VINCENZO, S. and SMITH, G. Evaluación de los hifomicetos acuáticos como bioindicadores de calidad ambiental en el río Chirgua (Bejuma, Venezuela). Gestion y Ambiente, 2017, 20(1), 82-94. http://dx.doi.org/10.15446/ga.v20n1.62241.

FIUZA, P., PÉREZ, T.C., GULIZ, V. and GUSMÃO, L.F.P. Ingoldian fungi of Brazil: some new records and a review including a checklist and a key. Phytotaxa, 2017, 306(3), 171-200. http://dx.doi.org/10.11646/phytotaxa.306.3.1.

FIUZA, P.O. and GUSMÃO, L.F.P. Ingoldian fungi from the semi-arid Caatinga biome of Brazil. Mycosphere, 2013, 4(6), 1133-1150. http://dx.doi.org/10.5943/mycosphere/4/6/10.

FIUZA, P.O., COSTA, L.A., MEDEIROS, A.O., GULIS, V. and GUSMÃO, L.F.P. Diversity of freshwater hyphomycetes associated with leaf litter of Calophyllum brasiliense in streams of the semiarid region of Brazil. Mycological Progress, 2019, 18(7), 907-920. http://dx.doi.org/10.1007/s11557-019-01501-6.

FIUZA, P.O., OTTONI-BOLDRINI, B.M.P., MONTEIRO, J.S., CATENA, N.R., HAMADA, N. and GUSMÃO, L.F.P. First records of Ingoldian fungi from the Brazilian Amazon. Brazilian Journal of Botany, 2015, 38(3), 615-621. http://dx.doi.org/10.1007/s40415-015-0157-7.

GARDNER, G. The challenge for Johannesburg: creating a more secure world. In: L. STARKE, ed. State of the world: a worldwatch institute report on progress toward a sustainable society. New York: W. W. Norton, 2002.

GOH, T.K. and HYDE, K.D. Biodiversity of freshwater fungi. Journal of Industrial Microbiology, 1996, 17(5-6), 328-345. http://dx.doi.org/10.1007/BF01574764.

GONÇALVES JUNIOR, J.F., GRAÇA, M.A.S. and CALLISTO, M. Litter decomposition in a Cerrado savannah stream is retarded by leaf toughness, low dissolved nutrients and a low density of shredders. Freshwater Biology, 2007, 52(8), 1440-1451. http://dx.doi.org/10.1111/j.1365-2427.2007.01769.x.

GOTELLI, N.J. and ELLISON, A.M. Princípios de estatística em Ecologia. Porto Alegre: Artmed, 2011.

GRAÇA, M.A.S. Effects of water pollution on assemblages of aquatic fungi. Limnetica, 1994, 10(2), 41-43.

GRAÇA, M.A.S., HYDE, K. and CHAUVET, E. Aquatic hyphomycetes and litter decomposition in tropical – subtropical low order streams. Fungal Ecology, 2015, 19, 182-189. http://dx.doi.org/10.1016/j.funeco.2015.08.001.

GRATTAN II, R.M. and SUBERKROPP, K. Effects of nutrient enrichment on yellow poplar leaf decomposition and fungal activity in streams. Journal of the North American Benthological Society, 2001, 20(1), 33-43. http://dx.doi.org/10.2307/1468186.

GUIMARÃES, J.R. A., STUDER, A., TRIVELLATO, C. Educação ambiental no entorno da reserva biológica de Pedra Talhada. X Fórum Ambiental da Alta Paulista, 2014, 10(6), 32-45.

GULIS, V. and SUBERKROPP, K. Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshwater Biology, 2003, 48(1), 123-134. http://dx.doi.org/10.1046/j.1365-2427.2003.00985.x.

HAIR JUNIOR, J.F., BLACK, W.C., BABIN, B.J., ANDERSON, R.E. and TATHAN, R.L. Análise multivariada de dados. 6. ed. Porto Alegre: Bookman, 2009.

INGOLD, C.T. An illustrated guide to aquatic and water-borne hyphomycetes (Fungi Imperfecti) with notes on their biology. Ambleside: Freshwater Biological Association, 1975. Scientific Publication, vol. 30.

INGOLD, C.T. The tetraradiate aquatic fungal spore. Mycologia, 1966, 58(1), 43-56. http://dx.doi.org/10.2307/3756987.

ITTNER, L.D., JUNGHANS, M. and WERNER, I. Aquatic fungi: a disregarded trophic level in ecological risk assessment of organic fungicides. Frontiers in Environmental Science, 2018, 6, 105. http://dx.doi.org/10.3389/fenvs.2018.00105.

JÖRDENING, H.J. and WINTER, J. Environmental biotechnology. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA, 2005.

KRAUSE, L.M., FIUZA, P.O. and BARBOSA, F.R. Xylomyces (Aliquandostipitaceae, Jahnulales) freshwater hyphomycetes from the Brazilian Amazon. Nova Hedwigia, 2020, 111(1-2), 1-12. http://dx.doi.org/10.1127/nova_hedwigia/2020/0590.

KRAUSS, G., SRIDHAR, K.R., JUNG, K., WENNRICH, R., EHRMAN, J. and BÄRLOCHER, F. Aquatic Hyphomycetes in Polluted Groundwater Habitats of Central Germany. Microbial Ecology, 2003, 45(4), 329-339. PMid:12704555.

LIBÂNIO, M. Fundamentos de qualidade e tratamento de água. Campinas: Átomo, 2005.

LOMBARD, L., van der MERWE, N.A., GROENEWALD, J.Z. and CROUS. P.W. Generic concepts in Nectriaceae. Studies in Mycology, 2015, 80, 189-245. http://dx.doi.org/10.1016/j.simyco.2014.12.002.

MACÊDO, J.A. Métodos laboratoriais de análise físicos químicos e microbiológicos. 3. ed. Belo Horizonte: Jorge Macêdo, 2005.

MAGALHÃES, M.R.L. Concentrações naturais de elementos químicos da classe Insecta do fragmento florestal de Mata Atlântica reserva Charles Darwin [Dissertação de Mestrado em Tecnologias Energéticas e Nucleares]. Recufe: Universidade Federal de Pernambuco, 2015.

MALOSSO, E. Hyphomycetes em ambientes aquáticos lótico e lêntico: ocorrência e biomassa [Dissertação de Mestrado em Ecologia e Recursos Naturais]. São Carlos: Universidade Federal de São Carlos, 1999.

MARVANOVÁ, L. Freshwater Hyphomycetes: a survey with remarks on tropical taxa. In: K.K. JANARDHANAN, C. RAJENDRAN, K. NATARAJAN and D. L. HAWSWORTH, eds. Tropical mycology. Enfield: Science Publishers, 1997, pp. 169-226.

MATSUSHIMA, T. Matsushima Mycological Memoirs. Published by the author. Kobe, 1985.

MEDEIROS, A.O., PASCOAL, C. and GRAÇA, M.A.S. Diversity and activity of aquatic fungi under low oxygen conditions. Freshwater Biology, 2009, 54(1), 142-149. http://dx.doi.org/10.1111/j.1365-2427.2008.02101.x.

MONTEIRO, J.S. and GUSMÃO, L.F.P. An emendation of Fusticeps and two new species from the Brazilian Amazon Forest. Mycotaxon, 2013, 123(1), 431-437. http://dx.doi.org/10.5248/123.431.

MOREIRA, C.G. and SCHOENLEIN-CRUSIUS, I.H. Nova espécie e novos registros para o Brasil de hifomicetos em folhedo submersos coletados no Parque Municipal Alfredo Volpi, São Paulo, SP, Brasil. Hoehnea, 2012, 39(4), 521-527. http://dx.doi.org/10.1590/S2236-89062012000400001.

MOREIRA, C.G. Sucessão de hifomicetos e avaliação da biomassa fúngica durante a decomposição de folhedo de Caesalpinia echinata Lam. e Campomanesia phaea (O. Berg.) Landrum submersos em lagos artificiais na cidade de São Paulo, SP [Tese de Doutorado em Biodiversidade Vegetal e Meio Ambiente]. São Paulo: Instituto de Botânica de São Paulo, 2011.

MORO, L.B. and SCHOENLEIN-CRUSIUS, I.H. Freshwater hyphomycetes in a preserved insular system from Brazil: first records at the Parque Estadual da Ilha do Cardoso, municipality of Cananéia, São Paulo State, Brazil. Hoehnea, 2020, 47, e832018. http://dx.doi.org/10.1590/2236-8906-83/2018.

MULHOLLAND, P.J., ELWOOD, J.W., NEWBOLD, J.D., WEBSTER, J.R., FERREN, L.A. and PERKINS, R.E. Phosphorus uptake by decomposing leaf detritus: effect of microbial biomass and activity. Internationale Vereinigung für Theoretische und Angewandte Limnologie: Verhandlungen, 1984, 22(3), 1899-1905. http://dx.doi.org/10.1080/03680770.1983.11897591.

NILSSON, S. Freshwater hyphomycetes. Symbolae Botanicae Upsalienses, 1964, 18, 1-130.

OLIVEIRA, M.S. Micobiota em folhas submersas em dois mananciais sob proteção ambiental no estado de Pernambuco [Dissertação de Mestrado em Biologia de Fungos]. Recife: Universidade Federal de Pernambuco, 2016.

ORTIZ-VERA, M.P., OLCHANHESKI, L.R., SILVA, E.G., LIMA, F.R., MARTINEZ, L.R.P.R., SATO, M.I.Z., JAFFÉ, R., ALVES, R., ICHIWAKI, S., PADILLA, G. and ARAÚJO, W.L. Influence of water quality on diversity and composition of fungal communities in a tropical river. Scientific Reports, 2018, 8(1), 14799. http://dx.doi.org/10.1038/s41598-018-33162-y. PMid:30287878.

PASCOAL, C., MARVANOVÁ, L. and CÁSSIO, F. Aquatic hyphomycete diversity in streams of Northwest Portugal. Fungal Diversity, 2005, 19, 109-128.

POHLING, R. Reações químicas na análise de água. Fortaleza: Arte Visual Gráfica e Editora, 2009.

RAJASHEKHAR, M. and KAVERIAPPA, K.M. Diversity of aquatic hyphomycetes in the aquatic ecosystems of the Western Ghats of India. Hydrobiologia, 2003, 501(1-3), 167-177. http://dx.doi.org/10.1023/A:1026239917232.

RASVAILER, V.S., SCOARIZE, M.M.R. and BENEDITO, E. Diversidade de fungos aquáticos em uma lagoa urbana da Mata Atlântica. Arquivos do Mudi, 2020, 24(2), 84-97. http://dx.doi.org/10.4025/arqmudi.v24i2.52474.

ROSEMOND, A.D., PRINGLE, C.M., RAMÍREZ, A., MICHAEL, J.P. and JUDY, L.M. Landscape variation in phosphorus concentration and effects on detritus-based tropical streams. Limnology and Oceanography, 2002, 47(1), 278-289. http://dx.doi.org/10.4319/lo.2002.47.1.0278.

ROSSMAN, A.Y., ALLEN, W.C., BRAUN, U., CASTLEBURY, L.A., CHAVERRI, P., CROUS, P.W., HAWKSWORTH, D.L., HYDE, K.D., JOHNSTON, P., LOMBARD, L., ROMBERG, M., SAMSON, R.A., SEIFERT, K.A., JEFFREY, K.S., UDAYANGA, D. and WHITE, J.F. Overlooked competing asexual and sexually typified generic names of Ascomycota with recommendations for their use or protection. IMA Fungus, 2016, 7(2), 289-308. http://dx.doi.org/10.5598/imafungus.2016.07.02.09.

SALES, M.A., GONÇALVES JÚNIOR, J.F., DAHORA, J.S. and MEDEIROS, A.O. Influence of leaf quality in microbial decomposition in a headwater stream in the Brazilian Cerrado: a 1-year study. Microbial Ecology, 2015, 69(1), 84-94. http://dx.doi.org/10.1007/s00248-014-0467-5. PMid:25096988.

SANTIAGO, A.C.P. and BARROS, I.C.L. Pteridoflora do Refúgio Ecológico Charles Darwin (Igarassu, Pernambuco, Brasil). Acta Botanica Brasílica, 2003, 17(4), 597-604. http://dx.doi.org/10.1590/S0102-33062003000400011.

SCHOENLEIN-CRUSIUS, I.H. and GRANDI, R.A.P. A diversidade dos Hyphomycetes aquáticos nas águas continentais da América do Sul. Brazilian Journal of Microbiology, 2003, 34(3), 183-193.

SCHOENLEIN-CRUSIUS, I.H. and MILANEZ, A.I. Sucessão fúngica em folhas de Ficus microcarpa Lf submersas no lago frontal situado no Parque Estadual das Fontes do Ipiranga, São Paulo, SP. Revista de Microbiologia, 1989, 32(3), 411-426.

SCHOENLEIN-CRUSIUS, I.H. Aquatic hyphomycetes from Cerrado regions in the state of São Paulo, Brazil. Mycotaxon, 2002, 81, 457-462.

SCHOENLEIN-CRUSIUS, I.H., DINIZ, B.F., COSTA, R.T., SABINO, A.P.R., MORO, L.B., BORO, M., ISHIDA, C.M., JESUS, A.L. and PIRES-ZOTTARELLI, C.L.A. Diversity of conidial fungi and some abiotic variables of the water after the reopening of the Pirarungaua stream in the Jardim Botânico, São Paulo, São Paulo State, Brazil. Hoehnea, 2016, 43(1), 57-75. http://dx.doi.org/10.1590/2236-8906-58/2015.

SCHOENLEIN-CRUSIUS, I.H., MOREIRA, C.G. and BICUDO, D.C. Aquatic Hyphomycetes in the Parque Estadual das Fontes do Ipiranga – PEFI, São Paulo, Brazil. Brazilian Journal of Botany, 2009, 32(3), 411-426. http://dx.doi.org/10.1590/S0100-84042009000300003.

SCHOENLEIN-CRUSIUS, I.H., MOREIRA, C.G. and GOMES, E.P.C. Riqueza dos fungos ingoldianos e dos fungos aquáticos facultativos do Parque Municipal da Aclimação, São Paulo, SP, Brasil. Hoehnea, 2015, 42(2), 239-251. http://dx.doi.org/10.1590/2236-8906-52/2014.

SCHOENLEIN-CRUSIUS, I.H., MOREIRA, C.G. and GOMES, E.P.C. Riqueza de fungos ingoldianos e de fungos aquático-facultativos no Parque Municipal do Carmo, São Paulo, SP, Brasil. Hoehnea, 2018, 45(3), 379. http://dx.doi.org/10.1590/2236-8906-24/2018.

SCHOENLEIN-CRUSIUS, I.H., MOREIRA, C.G., TAKAHASHI, J.P. and GOMES, E.P.C. Riqueza dos fungos ingoldianos e aquáticos facultativos no Parque Municipal do Ibirapuera, São Paulo, SP, Brasil. Hoehnea, 2014, 41(1), 61-76. http://dx.doi.org/10.1590/S2236-89062014000100006.

SCOARIZE, M.M.R. Distribuição e diversidade de hifomicetos aquáticos em riachos Neotropicais [Dissertação de Mestrado em Ecologia de Ambientes Aquáticos Continentais]. Maringá: Universidade Estadual de Maringá, 2018.

SEIFERT, K., MORGAN-JONES, G., GAMS, W. and KENDRICK, B. The genera of Hyphomycetes. Utrecht: CBS-KNAW Fungal Biodiversity Centre, 2011. CBS Biodiversity Series, no. 9.

SEKERKA, I. and LECHNER, J.F. Determination of alkalinity and acidity of water by conductometric acid-base titration. Journal - Association of Official Analytical Chemists, 1984, 67(5), 893-895. http://dx.doi.org/10.1093/jaoac/67.5.893.

SHEARER, C.A., DESCALS, E., KOHLMEYER, B., KOHLMEYER, J., MARVANOVÁ, L., PADGETT, D., PORTER, D., RAJA, H.A., SCHMIT, J.P., THORTON, H.A. and VOGLYMAYR, H. Fungal biodiversity in aquatic habitats. Biodiversity and Conservation, 2007, 16(1), 49-67. http://dx.doi.org/10.1007/s10531-006-9120-z.

SILVA, G.V.R., CASTAÑEDA-RUIZ, R.F. and MALOSSO, E. Comparison of aquatic hyphomycetes communities between lotic and lentic environments in the Atlantic rain forest of Pernambuco, Northeast Brazil. Fungal Biology, 2019, 123(9), 660-668. http://dx.doi.org/10.1016/j.funbio.2019.05.013. PMid:31416585.

SRIDHAR, K.R. and BÄRLOCHER, F. Initial colonization, nutrient supply, and fungal activity on leaves decaying in streams. Applied and Environmental Microbiology, 2000, 66(3), 1114-1119. http://dx.doi.org/10.1128/AEM.66.3.1114-1119.2000. PMid:10698779.

SRIDHAR, K.R. and RAVIRAJA, N.S. Aquatic hyphomycetes and leaf litter processing in unpolluted and polluted habitats. In: J.K. MISRA and B.W. HORN, eds. Trichomycetes and other fungal groups. Enfield: Science Publishers, 2001. http://dx.doi.org/10.13140/RG.2.1.3809.9602.

SRIDHAR, K.R., ARUN, A.B., MARIA, G.L. and MADHYASATHA, M.N. Diversity of fungi on submerged leaf and woody litter in river Kali, South-west India. Environmental Research Journal, 2011, 5, 701-714.

SUBERKROPP, K. and CHAUVET, E. Regulation of Leaf breakdown by fungi in streams: influences of water chemistry. Ecology, 1995, 76(5), 1433-1445. http://dx.doi.org/10.2307/1938146.

SUBERKROPP, K. Interactions with invertebrates. In: F. BÄRLOCHER, ed. The ecology of aquatic hyphomycetes. Berlin: Springer-Verlag, 1992, pp. 118-134. http://dx.doi.org/10.1007/978-3-642-76855-2_6.

SURESHA, H.R., KRISHNAPPA, M., DESCALS, E., RAJU, G.H. and TAYLOR, B.R. Diversity of aquatic hyphomycetes in Kalathgiri Falls of Chikmagalur District, Karnataka, India. International Journal of Microbiology Research, 2013, 5(3), 410-416. http://dx.doi.org/10.9735/0975-5276.5.3.410-416.

SUZUKI, S. and NIMURA, H. Relation between the distribution of aquatic hyphomycetes in Japanese lakes and lake types. Botanical Magazine Tokyo, 1961, 74(872), 51-55. http://dx.doi.org/10.15281/jplantres1887.74.51.

SUZUKI, S. and NIMURA, H. The microbiological studies of the lakes of Volcano Bandai II. Ecological study on aquatic hyphomycetes in the Goshikinuma and Akanuma Lake group. Botanical Magazine Tokyo, 1960, 73(867), 360-364. http://dx.doi.org/10.15281/jplantres1887.73.360.

WEIß, C.H. StatSoft, Inc., Tulsa, O.K. STATISTICA, Version 8.0. AStA Advances in Statistical Analysis, 2007, 91(3), 339-341. http://dx.doi.org/10.1007/s10182-007-0038-x.

WONG, M.K.M., GOH, T.-K., HODGKISS, I.J., HYDE, K.D., RANGHOO, V.M., TSUI, C.K.M., HO, W.-H., WONG, W.S.W. and YUEN, T.-K. Role of fungi in freshwater ecosystems. Biodiversity and Conservation, 1998, 7(9), 1187-1206. http://dx.doi.org/10.1023/A:1008883716975.

WOOD-EGGENSCHWILER, S. and BÄRLOCHER, F. Geographical distribution of Ingoldian fungi. Internationale Vereinigung für Theoretische und Angewandte Limnologie: Verhandlungen, 1985, 22, 2780-2785.

ZHANG, Y., GUO, L.D. and LIU, R.J. Survey of arbuscular mycorrhizal fungi in deforested and natural forest land in the subtropical region of Dujiangyan, Southwest China. Plant and Soil, 2004, 261(1-2), 257-263. http://dx.doi.org/10.1023/B:PLSO.0000035572.15098.f6.
 


Submitted date:
02/19/2021

Accepted date:
11/01/2021

Publication date:
04/28/2022

626a8fa4a9539537b2658d32 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections