A diversidade dos Hyphomycetes aquáticos nas águas continentais da América do Sul

bjm Brazilian Journal of Microbiology Braz. J. Microbiol. 1517-8382 1678-4405 Sociedade Brasileira de Microbiologia São Paulo, SP, Brazil Os Hyphomycetes aquáticos, também denominados fungos "Ingoldeanos", constituem grupo de fungos anamórficos tipicamente aquáticos, que produzem conídios tetrarradiados, sigmóides ou esféricos sobre substratos vegetais submersos (folhedo, pecíolos, cortiça, etc.). Ocorrendo principalmente em sistemas lóticos, estes fungos são considerados como um dos grupos de organismos mais ativos na decomposição de folhedo, assumindo papel crucial na cadeia trófica. Na América do Sul os Hyphomycetes aquáticos são mencionados para a Argentina, Brasil, Chile, Equador, Peru e Venezuela, totalizando a citação de aproximadamente 90 espécies. Quase todos os estudos são taxonômicos, com ilustrações adequadas e descrições completas, porém ainda não foram elaboradas chaves sistemáticas ou coleções de culturas de linhagens específicas. Os artigos publicados ainda são esporádicos e dispersos, enfatizando-se a grande necessidade de aperfeiçoamento dos conhecimentos sobre a diversidade dos Hyphomycetes aquáticos na América do Sul. A presente revisão contém listas das espécies mencionadas até o momento e tem o objetivo de encorajar a pesquisa destes fungos em áreas ainda não investigadas no continente. MINI REVIEW The diversity of aquatic Hyphomycetes in South America A diversidade dos Hyphomycetes aquáticos nas águas continentais da América do Sul Iracema Helena Schoenlein-Crusius*; Rosely Ana Piccolo Grandi Instituto de Botânica, Seção de Micologia e Liquenologia, São Paulo, SP, Brasil ABSTRACT Aquatic Hyphomycetes, also named Ingoldian or freshwater fungi, constitute a group of anamorphic fungi that are typically aquatic, producing tetraradiate, sigmoid or spherical conidia on submerged plant debris (leaf litter, petioles, bark, etc.). Mainly occurring in lotic systems, these fungi are considered to be one of the most active groups of organisms in the decomposition of leaf litter, and play a crucial role in the trophic chain. In South America, aquatic Hyphomycetes are mentioned for Argentina, Brazil, Chile, Ecuador, Peru and Venezuela, totalizing the report of about 90 species. Almost all studies are taxonomical, some with proper drawings and complete descriptions, but no keys have been provided yet, nor there is a specific culture collection for preserved strains. The published papers are still sporadic and dispersed, emphasizing a great need to improve the knowledge of the diversity of South American aquatic Hyphomycetes. The present review contents the check list of reported species until now, and has the aim to encourage the research concerned with aquatic Hyphomycetes in non explored regions of the continent. Key words: anamorphic fungi, aquatic Hyphomycetes, biodiversity, Brazil, South America. RESUMO Os Hyphomycetes aquáticos, também denominados fungos "Ingoldeanos", constituem grupo de fungos anamórficos tipicamente aquáticos, que produzem conídios tetrarradiados, sigmóides ou esféricos sobre substratos vegetais submersos (folhedo, pecíolos, cortiça, etc.). Ocorrendo principalmente em sistemas lóticos, estes fungos são considerados como um dos grupos de organismos mais ativos na decomposição de folhedo, assumindo papel crucial na cadeia trófica. Na América do Sul os Hyphomycetes aquáticos são mencionados para a Argentina, Brasil, Chile, Equador, Peru e Venezuela, totalizando a citação de aproximadamente 90 espécies. Quase todos os estudos são taxonômicos, com ilustrações adequadas e descrições completas, porém ainda não foram elaboradas chaves sistemáticas ou coleções de culturas de linhagens específicas. Os artigos publicados ainda são esporádicos e dispersos, enfatizando-se a grande necessidade de aperfeiçoamento dos conhecimentos sobre a diversidade dos Hyphomycetes aquáticos na América do Sul. A presente revisão contém listas das espécies mencionadas até o momento e tem o objetivo de encorajar a pesquisa destes fungos em áreas ainda não investigadas no continente. Palavras-chave: fungos anamórficos, Hyphomycetes aquáticos, biodiversidade, Brasil, América do Sul. INTRODUCTION The group of the aquatic Hyphomycetes comprises fungi that produce conidia exclusively in the aquatic environment or in the interstitial water among soil particles. Their habitats are preferencially streams with clear, clean, well-aerated waters, with moderate turbulence, and also reservoirs and lakes with different kinds or levels of pollution. The conidia may be trapped in foam, dispersed in the water, floating on the water surface or are associated to organic decomposing substrates as leaf litter and twigs (36). From the taxonomical point of view, the aquatic Hyphomycetes constitute an artificial phylogenetically heterogenous group, being anamorphs of Ascomycota and Basidiomycota (1,60). Identification of the species has been mainly based on the morphological features of the conidia (40,60). The term "tetraradiate fungi"has been also frequently used to name this fungal group because many species produce conidia with a radiate or star-like shape, build by a central part, from which three or four arms are projected in divergent positions (18,59). The hydrodynamic shapes of the conidia confers to these fungi higher ability to remain suspended in the water for extended periods of time and improve the chances of the propagules to become attached to organic substrates, available for colonization. However, among the aquatic Hyphomycetes there are species that produces sigmoid, fusiform, coiled and spherical conidia too, which are also dependent of the aquatic environment to complete their life cycle (22,40). This fungal group has been also named "Ingoldian fungi"in honour to Prof. Dr. C. T. Ingold, who was one of the most important pioneers in the study of aquatic Hyphomycetes (18). The eminent Professor studied these fungi in several aquatic environments in the United Kingdom and other countries starting from 40's, describing species that are now considered cosmopolitan (36,40). According to their form and life-cycle, a classification of the freshwater fungi (22) into the following groups was proposed: Ingoldian Hyphomycetes (fungi that present conidia with hydrodynamic shape and are exclusively dependent on aquatic environment for reproduction); aero-aquatic Hyphomycetes (fungi that may support submerged conditions but reproduce out of aquatic environments), and terrestrial-aquatic Hyphomycetes and submerged-aquatic Hyphomycetes, which are observed in aquatic and terrestrial environments as facultative organisms. One year later three groups were better distinguished among the former: Ingoldian fungi, aero-aquatic fungi and lignicolous aquatic fungi (21). In the present revision representants of all these group were considered. In tropical and equatorial climates the leaf litter and the soil are constantly wetted by heavy daily rainfalls, which may reach more than 3,000 mm/year in certain regions. In such conditions, it can be difficult to distinguish aquatic from terrestrial fungi only on basis of the habitat. It has been observed that some typical geofungi isolated from such areas, like Epicoccum nigrum Link and Trichoderma viride Rifai are able to produce spores in submerged cultures (51). Beltrania, Camposporium, Chaetendophragmia, Cladosporium, Cryptophiale, Dactylella, Dictyochaeta, Kionochaeta, Phaeoisaria, Subulispora, Tetraploa and other well-known terrestrial genera of Hyphomycetes are usually found on submerged litter as "facultative aquatic fungi"(21). On the other hand, some typical aquatic species such as Sporidesmium and Articulispora has been isolated from non aquatic environments. One can speculate about the reason for this behavior, considering the possibility of adaptations or tolerance of the fungi to drastic habitat changes and/or climatic conditions of the ecosystem. Fact is that, besides of the polemic discussion about which fungi are truly aquatic and if the terrestrial fungi may keep their saprophytic hability even in submerged conditions, the recognition of the importance of the aquatic Hyphomycetes has been continuously increased since many years. These fungi are considered predominant in the leaf decomposition process in aquatic environments. There is an evidence that aquatic Hyphomycetes are able to degrade several plant cell polymers such as cellulose, hemicellulose, pectin (16) and probably lignin (35,40), producing amylase, cellulase, pectinase, protease, pyrocatechol oxidase, triacyl glycerol lipase and xylanase (17,40,58). Such degradative enzymes may cause breakdown of leaf tissues and increase the palatability to leaf-eating invertebrates, besides their biomass is an important component in the diet of aquatic invertebrates (9,18,57,58). Some aquatic fungi are able to degrade animal parts like insect exoskeletons, hair and fish scales (22). Excellent considerations and descriptions of methods to perform ecological studies concerning aquatic Hyphomycetes may be consulted in Bärlocher (9), Suberkropp (58), Dix and Webster (18) and Marvanová (40). During the autumn in temperate climates, streams receive a great supply of tree leaves which may be densily colonize by a high diversity of aquatic Hyphomycetes (9). In the tropics the richness of these fungi is probably influenced by the type of substrates, chemical and physical changes in the streams (35) as well as due complex interactions among several climatic and limnological factors (9,40). Thus, it has been considered that in the tropics, the analysis of the seasonal behavior of these fungi may be more difficult (50). Based on accumulative results of several worldwide studies, about 100 anamorphic genera and 300 species of aquatic Hyphomycetes are known until now (37). In the revision for tropical freshwater Hyphomycetes Goh (21) listed 19 taxa to South America without specifying the countries. The quantification of the taxa in revisions concerned with fungal diversity in the tropics may result different numbers in function of several definitions of aquatic fungi and also depends on the availability of the literature. There may be many interesting additional data in regional journals, monographs, thesis and reports. As the aquatic Hyphomycetes has been characterized as one of the most active fungi in the mineralization of leaf litter, and consequently important dynamizers of the nutrient cycling in the aquatic environments, it has been considered relevant to increase the knowledge of the species diversity in terms of geographic distribution. The aim of this revision is to present the state of the art of the studies concerned with aquatic Hyphomycetes in Brazil, in the context of South America, to encourage the conduction of surveys in unexplored areas of the continent. SOUTH AMERICA For South America, reports of aquatic Hyphomycetes are low and mainly from Argentina, Chile, Ecuador, Peru, Venezuela (Table 1) and Brazil (Table 2). In Argentina the sampling of submerged mixed leaf litter, leaves of definied species such as Salix sp., Nothofagus dombeyi, N. pumillio, foam, wood, cork and plant debris, mainly from sites at Santiago River and Tierra Del Fuego, resulted in the report of about 25 fungal taxa (Table 1). Dead leaves of Nothofagus dombeyi (Mirb.) Blume sampled at Negro River, Nahuel Huapi National Park were analysed and the aero-aquatic fungus Candelabrum spinulosum v. Bev. was described (19). Campylospora chaetocladia Ranzoni, Clathrosphaerina zalewskii v. Bev. and Gyoerffyella gemellipara Marvanová were described from leaves of Nothofagus pumilio (Poepp. et Endl.) Oerst. and foam samples taken from streams in Neuquén, San Martín de los Andes (2). Among the mycota associated with grass leaves, dicotyledoan leaf litter, wood and foam samples, 12 aquatic Hyphomycetes were reported in some streams and lakes in Tierra del Fuego (20). Surveys were performed in the subtropical region of Santiago River in Buenos Aires (5,6,7), resulting in the description of 19 Hyphomycetes including nine new species and one new combination, Dictyochaeta assamica (Agnihothrudu) Arambarri, Cabello and Mengascini. Furthering the studies with Hyphomycetes from Santiago River, Cabello et al. (13) described Camposporium antillanum Castañeda Ruiz and Cazau et al. (15) published two new species: Dwayaangam gamundiae Cazau, Arambarri and Cabello and Diplocladiella taurina Cazau, Arambarri and Cabello. The taxonomical descriptions are complete and well documented by drawings. Besides, several other studies were performed at several localities in Argentina, involving the sampling of leaf litter or woody debris, from which many not typical aquatic fungi were isolated (3,4,11,12,14). In Chile (Table 1), samples of wood, leaf litter and insects were collected in several streams and lakes in the temperate region of Osorno (10). The authors observed 14 taxa of Ingoldian fungi, identified nine at specific level and documented their taxonomic features by spore drawings. Matsushima (41,42) greatly contributed to the knowledge of Hyphomycetes in South America. Several decaying palmae petioles mainly but also leaf litter, fruits and soil samples were collected in the vicinity of some rivers in the equatorial Amazon region of Ecuador and Peru. In Ecuador (Table 1) 5 species were reported (41). Many fungi with star-like conidia or considered aquatic were isolated but it is not clear if they were obtained from really submerged substrates. In Peru 30 taxa were described (42). Among them, 8 known species considered aquatic to Ingold (36) or Marvanová (40) were found, including Campylospora filicladia Nawawi and Condylospora spumigena Nawawi and also new taxa such as Isthmolongispora biramifera Matsushima, Triscelophorus curviramifer Matsushima, Trinacrium incurvum Matsushima, Trinacrium angamosense Matsushima, Trinacrium sp. (MPF-9P323), and one new combination, Triscelophorus deficiens (Matsushima) Matsushima. The Hyphomycetes were fully described and documented through excellent photographs and drawings. In Venezuela (Table 1) 11 taxa of aquatic Hyphomycetes were isolated from submerged leaf litter, branches and petioles of Casuarina in streams, pools and waterfalls in the surroundings of Caracas (44). 2 new genera and 2 new species were proposed: Angulospora aquatica S. Nilss. and Pyramidospora casuarinae S. Nilss., with complete descriptions and drawings. BRAZIL In Brazil studies of aquatic Hyphomycetes in freshwater were initiated at the end of the 80's mainly in the state of São Paulo (Table 2). Thus, some species were observed during fungal decomposition of leaves of Ficus microcarpa L. f. submerged in an artificial lake in the "Parque Estadual das Fontes do Ipiranga", municipality of São Paulo (47). Later, aquatic Hyphomycetes were observed during the decomposition of leaves of Quercus robur L. in a lake in the municipality of Itapecerica da Serra (52). In the "cerrado"(a kind of Brazilian savannah), municipality of Corumbataí, a strain of Lemonniera was found in terrestrial leaf litter (8). The first reports, besides the observation of fungi in mixed leaf litter collected in waterfalls ("Cachoeira do Altarújo", municipality of Rio Claro) and streams ("Recanto dos Nefelibatas", municipality of Águas de Lindóia) are mentioned in the taxonomical description of the Brazilian species (48,49). Besides some interesting aquatic Hyphomycetes, such as Dictyochaeta fertilis Hughes and Kendrick, Sporidesmiella hyalosperma (Corda) P. M. Kirk var. hialosperma P. M. Kirk and Tetraploa aristata Berkeley and Broome were isolated from Marantaceae roots in the "Parque Estadual das Fontes do Ipiranga"(23,24,25,26). Camposporium antennatum Harkn. and Kionochaeta ramifera (Matsushima) P. M. Kirk and B. Sutton were observed during the decomposition of leaves of Cedrela fissilis Vell. in the urban Forest reservation of the University of São Paulo (30). On the same plant species, but in the reservation of "Horto Florestal Dr. Luiz Teixeira Mendes", in the municipality of Maringá, State of Paraná, Wiesneriomyces laurinus (Tassi) P. M. Kirk was reported (33). At the surface of the leaves of Alchornea triplinervia (Spreng.) M. Arg., in the forest reservation of "Juréia-Itatins"Kionochaeta ramifera, Phaeoisaria clematidis (Fckl.) Hughes and Subulispora procurvata Tubaki were observed (29). In the "Reserva Biológica do Alto da Serra de Paranapiacaba", municipality of Santo André, many species of aquatic Hyphomycetes were observed during the fungal succession on decomposing submerged leaves of A. triplinervia (51). In the same region, the mycota associated with leaves of Ficus microcarpa, Alchornea triplinervia and Quercus robur were compared, evaluating the diversity (53), the methods for fungal quantification to express the colonization intensity (45) and the correlation between fungal diversity (zoosporic fungi and aquatic Hyphomycetes) and macro and microelements during the decomposition (54,55). In the same Reserve, Dendrosporomyces splendens (Nawawi) Nawawi, a typical species from water, was isolated from Alchornea triplinervia and Euterpe edulis Mart. leaf litter (27,28). More recently 9 taxa were isolated from decomposing leaves of Miconia cabussu (34). On Tibouchina pulchra leaves six Hyphomycetes were observed on leaves (31) and 11 were involved in the fungal succession during the decomposition of submerged leaf litter (43). Studies of aquatic Hyphomycetes and zoosporic fungi associated with submerged leaf litter in the "cerrado"region were intensified through surveys conducted in the Monjolinho River in the municipality of São Carlos in the State of São Paulo (38). Afterwards, the fungal diversity, biomass production and ergosterol content of submerged leaves were compared between the Monjolinho River and Jacaré-Guaçú River (lotic system) and the reservoir Represa do Guarapiranga (lentic system) in the city of São Paulo. The results were not clear in relation to the correlation between ergosterol / biomass content and fungal diversity, but the aquatic Hyphomycetes were more frequent in the rivers than in the reservoir regardless to the eutrophization level of the environments (39). A survey of aquatic Hyphomycetes in four "cerrado"regions in the State of São Paulo was concluded recently, obtaining 14 taxa, with three new records for Brazil (46). Recently, a taxonomical revision of some species of Subulispora (S. longirostrata, S. procurvata and S. rectilineata) was accomplished base on the reports of collections of leaf litter at several localities of the State of São Paulo (32). Until now, almost all sites are situated mainly in the state of São Paulo, approaching collections in streams, rivers of medium size, waterfalls, lakes and reservoirs in subtropical climatic conditions. Although the number of taxa and studies are higher in Brazil than in other South American countries, no new species have been described until now. Also the quality of the taxonomical descriptions and drawings must be improved. The Brazilian Amazonian region, where water bodies are plenty is still almost unknown. Only 1 record, Helicosporium sp. has been cited until now (56). Comparing the results among the countries, one may observe that some species such as Anguillospora longissima (Sacc. and Sydow) Ingold, Articulispora tetracladia Ingold, Clavariopsis aquatica Wildeman, Lunulospora curvula Ingold, and Triscelophorus monosporus Ingold are commonly mentioned as they are in other subtropical and tropical areas. Since in many countries no data about this fungal group have been published, and the studies are very scarce, sporadic and dispersed, it is difficult to draw conclusions about the geographic distribution of aquatic Hyphomycetes in South America. In Brazil, as well as probably in other countries of South America, the interest of researchers and students in the taxonomy of aquatic Hyphomycetes has come from the observation of the species in ecological studies about leaf litter decomposition and fungal succession. However, the scarcity of taxonomical keys with tropical species and the difficulty of obtaining cultures on agar media has disencouraged further initiatives. Marvanová (40) published a key to tropical and subtropical species but it was based on Indian and Malaysian material. So, the publication of keys and the improvement of the isolation techniques of these fungi in tropical waters may stimulate the interest of more taxonomists in the systematics and ecology of aquatic Hyphomycetes. Considering the dimension of the Continent, with the high variability of vegetation, habitats and abundance of rivers, streams and waterfalls, the number of aquatic Hyphomycetes in South America, around 90, is still very low. More effort is needed in terms of surveys and taxonomical studies to improve the knowledge of these fungi. ACKNOWLEDGEMENTS The author would like to thank to CNPq for financial support and Prof. Dr. Felix Bärlocher for the suggestions and revision of the text. Submitted: May 13, 2003; Approved: July 08, 2003 * Corresponding author. Mailing address: Instituto de Botânica, Seção de Micologia e Liquenologia. Caixa Postal 4005. 01061-970, São Paulo, SP, Brasil. Tel.: [phone], r. 260. E-mail: [e-mail] 1. Alexopoulos, C.J.; Mims, C.W.; Blackwell, M. Introductory Mycology, John Wiley & Sons, Inc., New York, 4ş ed., 1996. Introductory Mycology 1996 Alexopoulos C.J Mims C.W Blackwell M 2. Arambarri, A.M.; Spinedi, H.A. Micoflora de la hojarasca de Nothofagus pumilio. III. Darwiniana, 25(1-4):321-330, 1984. Micoflora de la hojarasca de Nothofagus pumilio. III. Darwiniana 1984 321 330 1-4 25 Arambarri A.M. Spinedi H.A. 3. Arambarri, A.M.; Cabello, M.N.; Cazau, M.C. Gyrothrix flagelliramosa sp. nov., a new hyphomycete from Argentina. Mycol. Res., 101(12):1529-1530, 1997. Gyrothrix flagelliramosa sp. nov., a new hyphomycete from Argentina. Mycol. Res. 1997 1529 1530 12 101 Arambarri A.M. Cabello M.N. Cazau M.C. 4. Arambarri, A.M.; Cabello, M.N.; Cazau, M.C. Dictyosporium triramosum, a new Hyphomycete from Argentina. Mycotaxon, 78:185-189, 2001. Dictyosporium triramosum, a new Hyphomycete from Argentina Mycotaxon 2001 185 189 78 Arambarri A.M. Cabello M.N. Cazau M.C. 5. Arambarri, A.M.; Cabello, M.N.; Mengascini, A. Estudio sistematico de los Hyphomycetes del Rio Santiago (prov. Buenos Aires, Argentina). Darwiniana, 28(1-4):293-301, 1987a. Estudio sistematico de los Hyphomycetes del Rio Santiago (prov. Buenos Aires, Argentina). Darwiniana 1987 293 301 1-4 28 Arambarri A.M. Cabello M.N. Mengascini A. 6. Arambarri, A.M.; Cabello, M.N.; Mengascini, A. New Hyphomycetes from Santiago River (Buenos Aires Province, Argentina). Mycotaxon, 29:29-35, 1987b. New Hyphomycetes from Santiago River (Buenos Aires Province, Argentina) Mycotaxon 1987 29 35 29 Arambarri A.M. Cabello M.N. Mengascini A. 7. Arambarri, A.M.; Cabello, M.N.; Mengascini, A. New Hyphomycetes from Santiago River II. (Buenos Aires Province, Argentina). Mycotaxon, 30:263-267, 1987c. New Hyphomycetes from Santiago River II Mycotaxon 1987 263 267 30 Arambarri A.M. Cabello M.N. Mengascini A. 8. Attili, D.S.; Tauk-Tornisiello, S.M. Occurrence of microfungi during leaf litter decomposition in a cerrado sensu strictu area of São Paulo, Brazil. Rev. Microbiol., 25(3):188-194, 1994. Occurrence of microfungi during leaf litter decomposition in a cerrado sensu strictu area of São Paulo, Brazil Rev. Microbiol. 1994 188 194 3 25 Attili D.S. Tauk-Tornisiello S.M. 9. Bärlocher, F. Research on aquatic Hyphomycetes: historical background and overview. In: Bärlocher, F. (ed.). The ecology of aquatic Hyphomycetes. Springer Verlag, Berlin, 1992, p.1-15. The ecology of aquatic Hyphomycetes 1992 1 15 Bärlocher F. Bärlocher F. 10. Burgos, J.E.; Riffart, R.G. Hongos saprobios en Chile: ambiente limnico. Noticiario Mensual del Museo Nacional de Historia Natural, Chile, 306-307:5-8, 1982. Hongos saprobios en Chile: ambiente limnico Noticiario Mensual del Museo Nacional de Historia Natural 1982 5 8 306-307 Burgos J.E. Riffart R.G. 11. Cabello, M.N.; Arambarri, A.M.; Cazau, M.C. Minimidochium parvum, a new species of hyphomycete from Argentina. Mycol. Res., 102(3):383-384, 1998. Minimidochium parvum, a new species of hyphomycete from Argentina Mycol. Res. 1998 383 384 3 102 Cabello M.N. Arambarri A.M. Cazau M.C. 12. Cabello, M.N.; Cazau, M.C.; Arambarri, A.M. New Hyphomycetes from Santiago River. III. (Buenos Aires Province, Argentina). Mycotaxon, 38:15-19, 1990. New Hyphomycetes from Santiago River. III. (Buenos Aires Province, Argentina). Mycotaxon 1990 15 19 38 Cabello M.N. Cazau M.C. Arambarri A.M. 13. Cabello, M.N.; Cazau, M.C.; Arambarri, A.M. Estudio sistematico de los Hyphomycetes del Rio Santiago. VI. (Buenos Aires, Argentina). Bol. Soc. Argent. Bot., 29:11-14, 1993. Estudio sistematico de los Hyphomycetes del Rio Santiago. VI. (Buenos Aires, Argentina). Bol. Soc. Argent. Bot. 1993 11 14 29 Cabello M.N. Cazau M.C. Arambarri A.M. 14. Cazau, M.C.; Arambarri, A.M.; Cabello, M.N. New Hyphomycetes from Santiago River. IV (Buenos Aires Province, Argentina). Mycotaxon, 38:21-25, 1990. New Hyphomycetes from Santiago River. IV (Buenos Aires Province, Argentina). Mycotaxon 1990 21 25 38 Cazau M.C. Arambarri A.M. Cabello M.N. 15. Cazau, M.C.; Arambarri, A.M.; Cabello, M.N. New Hyphomycetes from Santiago River. VI. (Buenos Aires Province, Argentina). Mycotaxon, 46:235-240, 1993. New Hyphomycetes from Santiago River. VI. (Buenos Aires Province, Argentina). Mycotaxon 1993 235 240 46 Cazau M.C. Arambarri A.M. Cabello M.N. 16. Chamier, C.A. Cell-wall degrading enzymes of aquatic Hyphomycetes: a review. Bot. J. Linn Soc., 1:67-81, 1985. Cell-wall degrading enzymes of aquatic Hyphomycetes: a review Bot. J. Linn Soc. 1985 67 81 1 Chamier C.A. 17. Chandrashekar, K.R.; Kaveriappa, K.M. Production of extra-cellular cellulase by Lunulospora curvula and Flagellospora penicillioides. Ibid, 33:55-58, 1991. Production of extra-cellular cellulase by Lunulospora curvula and Flagellospora penicillioides Ibid 1991 55 58 33 Chandrashekar K.R. Kaveriappa K.M. 18. Dix, N.J.; Webster, J. Fungal Ecology. Chapman & Hall, London, 1995, 549p. Fungal Ecology 1995 549p Dix N.J. Webster J. 19. Gamundi, I.J.; Arambarri, A.M.; Giaiotti, A. Micoflora de la hojarasca de Nothofagus dombeyi. Darwiniana, 21(1):81-114, 1977. Micoflora de la hojarasca de Nothofagus dombeyi Darwiniana 1977 81 114 1 21 Gamundi I.J. Arambarri A.M. Giaiotti A. 20. Godeas, A.M. Hifomicetes (Deuteromycotina) acuaticos de Tierra del Fuego. Physis, Secc. B, 43(104):7-9, 1985. Hifomicetes (Deuteromycotina) acuaticos de Tierra del Fuego Physis, Secc. B 1985 7 9 104 43 Godeas A.M. 21. Goh, T.K. Tropical Freshwater Hyphomycetes. In: Hyde, K.D. (ed). Biodiversity of Tropical Microfungi. Hong Kong University Press, p.189-227, 1997. Biodiversity of Tropical Microfungi 1997 189 227 Goh T.K. Hyde K.D. 22. Goh, T.K.; Hyde, K.D. Biodiversity of freshwater fungi. J. Ind. Microbiol., 17:328-345, 1996. Biodiversity of freshwater fungi J. Ind. Microbiol. 1996 328 345 17 Goh T.K. Hyde K.D. 23. Grandi, R.A.P. Hyphomycetes decompositores. 1. Espécies associadas às raízes de Calathea stromata (Horticultural). Rev. Bras. Biol., 50(1):123-132, 1990. Hyphomycetes decompositores. 1. Espécies associadas às raízes de Calathea stromata (Horticultural). Rev. Bras. Biol. 1990 123 132 50(1) Grandi R.A.P. 24. Grandi, R.A.P. Hyphomycetes decompositores. 2. Táxons associados às raízes de Maranta bicolor Ker. Rev. Bras. Biol., 5(1):133-141, 1991a. Hyphomycetes decompositores. 2. Táxons associados às raízes de Maranta bicolor Ker. Rev. Bras. Biol. 1991 133 141 1 5 Grandi R.A.P. 25. Grandi, R.A.P. Hyphomycetes decompositores. 4. Espécies associadas às raízes de Ctenanthe oppenheimiana Sond. Acta Botanica Brasilica, 5(1):13-23, 1991b. Hyphomycetes decompositores. 4. Espécies associadas às raízes de Ctenanthe oppenheimiana Sond. Acta Botanica Brasilica 1991 13 23 1 5 Grandi R.A.P. 26. Grandi, R.A.P. Hyphomycetes decompositores. 3. Espécies associadas às raízes de Stromanthe sanguinea Sond. Rev. Bras. Biol., 52(2):275-282, 1992. Hyphomycetes decompositores. 3. Espécies associadas às raízes de Stromanthe sanguinea Sond. Rev. Bras. Biol. 1992 275 282 2 52 Grandi R.A.P. 27. Grandi, R.A.P. Hyphomycetes decompositores do folhedo de Alchornea triplinervia (Spreng.) Müll. Arg. Hoehnea, 25:133-148, 1998. Hyphomycetes decompositores do folhedo de Alchornea triplinervia (Spreng.) Müll. Arg. Hoehnea 1998 133 148 25 Grandi R.A.P. 28. Grandi, R.A.P. Hifomicetos decompositores do folhedo de Euterpe edulis Mart. Hoehnea, 26:87-101, 1999. Hifomicetos decompositores do folhedo de Euterpe edulis Mart Hoehnea 1999 87 101 26 Grandi R.A.P. 29. Grandi, R.A.P.; Attili, D.S. Hyphomycetes on Alchornea triplinervia (Spreng.) Muell. Arg. Leaf litter from the ecological reserve Juréia-Itatins, State of São Paulo, Brazil. Mycotaxon, 60:373-386, 1996. Hyphomycetes on Alchornea triplinervia (Spreng.) Muell. Arg. Leaf litter from the ecological reserve Juréia-Itatins, State of São Paulo, Brazil Mycotaxon 1996 373 386 60 Grandi R.A.P. Attili D.S. 30. Grandi, R.A.P.; Grandi, A.C.; Delitti, W.B.C. Hyphomycetes sobre folhas em decomposição de Cedrela fissilis Vell. Hoehnea, 22(1-2): 27-37, 1995. Hyphomycetes sobre folhas em decomposição de Cedrela fissilis Vell Hoehnea 1995 1 2 22 Grandi R.A.P. Grandi A.C. Delitti W.B.C. 31. Grandi, R.A.P.; Gusmão, L.F.P. Hyphomycetes decompositores do folhedo de Tibouchina pulchra Cogn. Revista Brasileira de Botânica, 25(1):79-87, 2002a. Hyphomycetes decompositores do folhedo de Tibouchina pulchra Cogn Revista Brasileira de Botânica 2002 79 87 1 25 Grandi R.A.P. Gusmão L.F.P. 32. Grandi, R.A.P.; Gusmão, L.F.P. O gênero Subulispora Tubaki (fungos mitospóricos Hyphomycetes) sobre folhas em decomposição no estado de São Paulo, Brasil. Hoehnea, 29(1):31-36, 2002b. O gênero Subulispora Tubaki (fungos mitospóricos - Hyphomycetes) sobre folhas em decomposição no estado de São Paulo, Brasil Hoehnea 2002 31 36 1 29 Grandi R.A.P. Gusmão L.F.P. 33. Gusmão, L.F.P.; Grandi, R.A.P. Hyphomycetes com conidioma dos tipos esporodóquio e sinema associados a folhas de Cedrela fissilis Vell. (Meliaceae) em Maringá, PR, Brasil. Acta Botanica Brasilica, 11(2):123-134, 1997. Hyphomycetes com conidioma dos tipos esporodóquio e sinema associados a folhas de Cedrela fissilis Vell. (Meliaceae) em Maringá, PR, Brasil Acta Botanica Brasilica 1997 123 134 2 11 Gusmão L.F.P. Grandi R.A.P. 34. Gusmão, L.F.P.; Grandi, R.A.P.; Milanez, A.I. Hyphomycetes from leaf litter of Miconia cabussu in the Brazilian Atlantic Rain forest. Mycotaxon, 79:201-213, 2001. Hyphomycetes from leaf litter of Miconia cabussu in the Brazilian Atlantic Rain forest Mycotaxon 2001 201 213 79 Gusmão L.F.P Grandi R.A.P Milanez A.I 35. Hasija, S.K.; Singhal, P.K. Degradation of Plant Litter by Aquatic Hyphomycetes. In: Arora, D.K.; Rai, B.; Mukerji, K.G.; Knudsen, G. (eds.). Handbook of Applied Mycology: soils and plants. Marcel Dekkerm New York, 1991, p.481-505. Handbook of Applied Mycology: soils and plants 1991 481 505 Hasija S.K. Singhal P.K. Arora D.K. Rai B. Mukerji K. G Knudsen G 36. Ingold, C.T. An Illustrated Guide to Aquatic and Water-borne Hyphomycetes (Fungi Imperfecti) with notes on their Biology. Freshwater Biological Association, Ambleside, 1975. 96p. An Illustrated Guide to Aquatic and Water-borne Hyphomycetes (Fungi Imperfecti) with notes on their Biology 1975 Ingold C.T 37. Kirk, P.M.; Cannon, P.F.; David, J.C.; Stalpers, J.A. Ainsworth & Bisby's Dictionary of the Fungi. 9th. ed. CAB International, 2001, 655p. Ainsworth & Bisby's Dictionary of the Fungi Kirk P.M. Cannon P.F. David J.C. Stalpers J.A. 38. Malosso, E. Ocorrência de Hyphomycetes (Fungi Imperfecti) e Fungos Zoospóricos em Ambientes Aquáticos (Rio do Monjolinho, São Carlos, SP). São Carlos, 1995, 54p. (Bachelor Thesis, Universidade Federal de São Carlos, SP, Brasil). Ocorrência de Hyphomycetes (Fungi Imperfecti) e Fungos Zoospóricos em Ambientes Aquáticos (Rio do Monjolinho, São Carlos, SP) 1995 Malosso E. 39. Malosso, E. Hyphomycetes em ambientes aquáticos lótico e lêntico ocorrência e biomassa. São Carlos, 1999, 98p. (MSc. Thesis, Universidade Federal de São Carlos, SP, Brasil). Hyphomycetes em ambientes aquáticos lótico e lêntico - ocorrência e biomassa 1999 Malosso E. 40. Marvanová, L. Freshwater Hyphomycetes: a survey with remarks on tropical taxa. In: Janardhanan, K.K.; Rajendran, C.; Natarajan, K.; Hawksworth, D.L. (Eds.). Tropical Mycology, Science Publishers, Inc., 1997, p.169-226. Tropical Mycology 1997 169 226 Marvanová L. Janardhanan K.K. Rajendran C. Natarajan K. Hawksworth D.L. 41. Matsushima, T. Matsushima Mycological Memoirs no. 7, 75p. - 131 plates, September 1993. Matsushima Mycological Memoirs 09 1993 75p. 131 7 Matsushima T. 42. Matsushima, T. Matsushima Mycological Memoirs no. 8, 54p. - 120 plates, August 1995. Matsushima Mycological Memoirs 08 1995 54p. 120 8 Matsushima T. 43. Moreira, C.G. Sucessão de fungos (Hyphomycetes aquáticos e geofungos) associados a folhas de Tibouchina pulchra Cogn. submersas em um riacho da mata atlântica. (Bachelor Thesis, Universidade de Santo Amaro, São Paulo, Brasil). Sucessão de fungos (Hyphomycetes aquáticos e geofungos) associados a folhas de Tibouchina pulchra Cogn. submersas em um riacho da mata atlântica. Moreira C.G. 44. Nilsson, S. Some Aquatic Hyphomycetes from South America. Svensk Botanisk Tidskrift, 56(2):351-361, 1962. Some Aquatic Hyphomycetes from South America Svensk Botanisk Tidskrift 1962 351 361 2 56 Nilsson S. 45. Pires-zottarelli, C.L.; Schoenlein-Crusius, I.H.; Milanez, A.I. Quantitative estimation of zoosporic fungi and aquatic Hyphomycetes on leaves submerged in a stream in the atlantic rainforest, in the state of São Paulo, Brazil. Rev. Microbiol., 24(3): 192-197, 1993. Quantitative estimation of zoosporic fungi and aquatic Hyphomycetes on leaves submerged in a stream in the atlantic rainforest, in the state of São Paulo, Brazil Rev. Microbiol. 1993 192 197 3 24 Pires-zottarelli C.L. Schoenlein-Crusius I.H. Milanez A.I. 46. Schoenlein-Crusius, I.H. Aquatic Hyphomycetes from cerrado regions in the state of São Paulo, Brazil. Mycotaxon, 81:457-462, 2002. Aquatic Hyphomycetes from cerrado regions in the state of São Paulo, Brazil Mycotaxon 2002 457 462 81 Schoenlein-Crusius I.H. 47. Schoenlein-Crusius, I.H.; Milanez, A.I. Sucessão fúngica em folhas de Ficus microcarpa L. F., submersas no Lago Frontal situado no Parque Estadual das Fontes do Ipiranga, São Paulo. Rev. Microbiol., 20(1):95-101, 1989. Sucessão fúngica em folhas de Ficus microcarpa L. F., submersas no Lago Frontal situado no Parque Estadual das Fontes do Ipiranga, São Paulo. Rev. Microbiol 1989 95 101 1 20 Schoenlein-Crusius I.H. Milanez A.I. 48. Schoenlein-Crusius, I.H.; Milanez, A.I. Hyphomycetes aquáticos no Estado de São Paulo, Brasil. Revista Brasileira de Botânica, 13(1):61-68, 1990a. Hyphomycetes aquáticos no Estado de São Paulo, Brasil Revista Brasileira de Botânica 1990 61 68 1 13 Schoenlein-Crusius I.H. Milanez A.I. 49. Schoenlein-Crusius, I.H.; Milanez, A.I. Aquatic Hyphomycetes in São Paulo State, Brazil. I First observations. Hoehnea, 17:111-115. 1990b. Aquatic Hyphomycetes in São Paulo State, Brazil: I First observations Hoehnea 1990 111 115 17 Schoenlein-Crusius I.H Milanez A.I 50. Schoenlein-Crusius, I.H.; Milanez, A.I. Diversity of aquatic fungi in Brazilian Ecosystems. In: Bicudo, C.; Menezes, N.A. (eds.), Biodiversity in Brazil, a first approach, 1996, p.31-48, 1996. Biodiversity in Brazil, a first approach 1996 31 48 Schoenlein-Crusius I.H. Milanez A.I. Bicudo C. Menezes N.A. 51. Schoenlein-Crusius, I.H.; Milanez, A.I. Fungal succession on leaves of Alchornea triplinervia (Spreng.) M. Arg. Submerged in a stream of an Atlantic Rainforest in the State of São Paulo, Brazil. Revista Brasileira de Botânica, 21(3):253-259, 1998. Fungal succession on leaves of Alchornea triplinervia (Spreng.) M. Arg. Submerged in a stream of an Atlantic Rainforest in the State of São Paulo, Brazil. Revista Brasileira de Botânica 1998 253 259 3 21 Schoenlein-Crusius I.H. Milanez A.I. 52. Schoenlein-Crusius, I.H.; Pires-Zottarelli, C.L.A.; Milanez, A.I. Sucessão fúngica em folhas de Quercus robur L. (carvalho) submersas em um lago situado no município de Itapecerica da Serra, SP. Rev. Microbiol., 21(1):61-67, 1990. Sucessão fúngica em folhas de Quercus robur L. (carvalho) submersas em um lago situado no município de Itapecerica da Serra, SP Rev. Microbiol 1990 61 67 1 21 Schoenlein-Crusius I.H. Pires-Zottarelli C.L.A. Milanez A.I. 53. Schoenlein-Crusius, I.H.; Pires-Zottarelli, C.L.A.; Milanez, A.I. Aquatic fungi in leaves submerged in a stream in the Atlantic Rainforest. Rev. Microbiol., 23(3):167-171, 1992. Aquatic fungi in leaves submerged in a stream in the Atlantic Rainforest Rev. Microbiol. 1992 167 171 3 23 Schoenlein-Crusius I.H. Pires-Zottarelli C.L.A. Milanez A.I. 54. Schoenlein-Crusius, I.H.; Pires-Zottarelli, C.L.A.; Milanez, A.I.; Humphreys, R.D. Influence of nutrients concentration on the aquatic mycota of leaves submerged in a stream in the Atlantic rainforest. Verh. Internat. Verein. Limnol., 1125-1128, 1998. Influence of nutrients concentration on the aquatic mycota of leaves submerged in a stream in the Atlantic rainforest Verh. Internat. Verein. Limnol 1998 1125 1128 Schoenlein-Crusius I.H Pires-Zottarelli C.L.A Milanez A.I Humphreys R.D 55. Schoenlein-Crusius, I.H.; Pires-Zottarelli, C.L.A.; Milanez, A.I.; Humphreys, R.D. Interaction between the mineral content and the occurrence number of aquatic fungi in leaves submerged in a stream in the Atlantic rainforest, São Paulo, Brazil. Revista Brasileira de Botânica, 22(2):133-139, 1999. Interaction between the mineral content and the occurrence number of aquatic fungi in leaves submerged in a stream in the Atlantic rainforest, São Paulo, Brazil Revista Brasileira de Botânica 1999 133 139 2 22 Schoenlein-Crusius I.H. Pires-Zottarelli C.L.A. Milanez A.I. Humphreys R.D. 56. Silva, M.I.L. Micobiota de água e do solo das margens de igarapés situados na área de mata do campus da Universidade do Amazonas, AM. São Paulo, 2002, 175p. (PhD. Thesis, Instituto de Ciências Biológicas, USP). Micobiota de água e do solo das margens de igarapés situados na área de mata do campus da Universidade do Amazonas, AM 2002 Silva M.I.L. 57. Sridhar, K.R.; Bärlocher, F. Initial colonization, nutrient supply, and fungal activity on leaves decaying in streams. Appl. Environ. Microbio., 66(3):1114-1119, 2000. Initial colonization, nutrient supply, and fungal activity on leaves decaying in streams Appl. Environ. Microbio. 2000 1114 1119 3 66 Sridhar K.R. Bärlocher F. 58. Suberkropp, K. Aquatic Hyphomycete Communities. In: Carroll, G.C.; Wicklow, D.T. The Fungal Community Its organization and role in the ecosystem. Marcel Dekker, New York, Mycology Series n.9, 1992, p.729-747. The Fungal Community - Its organization and role in the ecosystem 1992 729 747 9 Suberkropp K. Carroll G.C. Wicklow D.T. 59. Subramanian, C.V. Hyphomycetes Taxonomy and Biology. Academic Press, London, 1983, 502p. Hyphomycetes - Taxonomy and Biology 1983 Subramanian C.V. 60. Webster, J. Anamorph-teleomorph relationaships. In: Bärlocher, F. (ed.), The ecology of aquatic Hyphomycetes. Springer-Verlag, Berlin, 1992, p.99-117. The ecology of aquatic Hyphomycetes 1992 99 117 Webster J. Bärlocher F.