Oomycetes (Oomycota) from Maranhão State, Brazil¹

Oomicetos (Oomycota) do Estado do Maranhão, Brasil)

ABSTRACT

This study aimed at enhancing the knowledge on the diversity and distribution of Oomycetes within Parque Natural Municipal Lagoa do Sambico, in Timon municipality, Maranhão State, Brazil as well as their geographical distribution in Brazil as a whole. Of the 98 isolates, 16 were identified as Oomycetes, which belong to six families: Achlyaceae, Leptolegniellaceae s. lat., Pythiaceae s. lat., Olpidiopsidaceae s. lat., Saprolegniaceae s. str. and Verrucalvaceae. We report herewith the first records of Olpidiopsis aphanomycis Cornu and Saprolegnia luxurians (Bhargava & G.C. Srivast) R.L. Seym. for Brazil, as well as Achlya aff. diffusa J.V. Harv. ex T.W. Johnson, Achlya proliferoides Coker, Aphanomyces helicoides Minden, Aplanopsis terrestris Höhnk, Dictyuchus monosporus Leitg., Globisporangium proliferum (Cornu) P.M. Kirk, and Pythiogeton uniforme A. Lund for the State of Maranhão.

Keywords:
diversity; environment; geographic distribution; zoosporic organisms

RESUMO

Este estudo foi realizado a fim de contribuir para o conhecimento da diversidade e distribuição geográfica de oomicetos no Parque Natural Municipal Lagoa do Sambico, na cidade de Timon, Estado do Maranhão, Brasil; bem como a sua distribuição geográfica no Brasil como um todo. De um total de 98 isolamentos, 16 táxons foram identificadas como espécies de oomicetos, pertencentes a seis famílias: Achlyaceae, Leptolegniellaceae s. lat., Pythiaceae s. lat., Olpidiopsidaceae s. lat., Saprolegniaceae s. str. e Verrucalvaceae. Olpidiopsis aphanomycis Cornu e Saprolegnia luxurians (Bhargava & G.C. Srivast) R.L. Seym. são relatadas pela primeira vez para o Brasil e Achlya aff. diffusa J.V. Harv. ex T.W. Johnson, Achlya proliferoides Coker, Aphanomyces helicoides Minden, Aplanopsis terrestris Höhnk, Dictyuchus monosporus Leitg, Globisporangium proliferum (Cornu) P.M. Kirk e Pythiogeton uniforme A. Lund, para o Estado do Maranhão.

Palavras-chave:
ambiente; distribuição geográfica; diversidade; organismos zoospóricos

Introduction

The phylum Oomycota (Kingdom Straminipila), has two classes (Saprolegniomycetes and Peronosporomycetes). Saprolegniomycetes includes three orders, seven families and 33 genera, whereas Peronosporomycetes has three orders, five families and 40 genera. Further several classes, five orders, ten families and 13 genera as classified as incertae sedis (Beakes et al. 2014). The phylum comprises saprobes and parasites found in aquatic and terrestrial ecosystems; its members play an important role in the decomposition of organic matter and participate in the cycling of nutrients. Important parasites attack plants, algae, fish, crustaceans, fungi, mosquito larvae, nematodes, rotifers, mammals, and even humans (Marano et al. 2008, Beakes et al. 2014).

Oomycota are widely distributed and ubiquitous. Saprobic species have extensive enzymatic capacity, with the ability to degrade a wide range of vegetal and animal substrates such as cellulose (algae and plant debris), keratin (snake skin, hair and feather), chitin (exoskeleton of crustaceans and insects), lignin (dead tissue of woody plants) and sporopollenin (pollen grains). Saprotrophic species are abundantly found in decaying plant material, but their occurrence and frequency are underestimated unless specific techniques are applied for their study (Hawksworth 2004, Marano et al. 2011).

The genera Saprolegnia, Achlya and Aphanomyces are commonly found parasitizing fish as well as their eggs. Pythium and Phytophthora species are highly pathogenic in plants of economic interest (Moore-Landecker 1996, Alexopoulos et al. 1996). Pythium insidiosum stands out as equine parasite, but also parasites other animals such as cattle, goats, dogs, cats, as well as human. Subcutaneus ulcerative lesions in animals caused by this species have been consistently reported (Santurio et al. 1998, Leal et al. 2001, Sallis et al. 2003, Rech et al. 2004), including in humans for the first time in Brazil (Bosco et al. 2008) and in horses in Piauí State (Rocha et al. 2010). However, there have been very few reports of Oomycetes in Maranhão State. A single study by Sales (2009), surveyed species of Oomycetes from groundwater wells in three villages within Timon municipality. The present study aimed at increasing the knowledge on the diversity of Oomycetes within Parque Natural Municipal Lagoa do Sambico, municipality Timon, in Maranhão State, Brazil.

Materials and methods

Study area - The municipality of Timon is located on the left bank of Parnaíba River, which borders Piauí State. Timon comprises an area of 1,743,246 km², with a population density of 89,18 individuals per km² and an estimated population of 161,721 inhabitants. The municipality has a warm tropical dry climate with little temperature variation, at times exceeding 40 ºC, the minimum being rarely less than 22 ºC. Centroid coordinates are 5º05'S latitude and 42º50'W longitude, with an elevation of at 69 m.a.s.l., situated 426 km far from the capital of Maranhão State, São Luís (IBGE 2013) (figure 1). The Parque Natural Municipal Lagoa do Sambico was created by Municipal Decree-Law 1754/2012 (Timon 2012). The park comprises an area of 80,502.25 m². Plant communities are dominated by herbaceous vegetation. It has a natural lagoon called Sambico (Rima 2011). Five water and soil samples were obtained every two months from August 2014 to May 2015, at four different points of the lagoon, for a total of 40 samples.

Figure 1
Geographical location of Parque Natural Municipal Lagoa do Sambico, Timon municipality, Maranhão State, Brazil.

Isolation technique - The multiple baiting technique with cellulosic, chitinous and keratinous substrates was applied to isolate Oomycetes from the samples, following Milanez (1989), according to organic material is used as bait for Oomycetes colonization and culture. Water samples were collected from the lake surface with the aid of a plastic cup and then stored in wide-mouth sterile glass flasks (100 ml Wheaton vials), with perforated plastic cover to allow oxygenation of the water. Prior to collection, nine baits were added to each flask: cellulosic substrates (corn straw, sorghum seeds, onion skin, cellophane and paper filter) and chitinous (termite wings) as well as keratinous (snake skin and human hair) items, which served as organic colonization substrates. Soil samples were collected with the aid of a sterile metal spatula, and the surface layers were removed and about 250 g of soil were collected at depth of approximately 20 cm, then packed in 500 g polyethylene bags properly labeled with the respective collection points. The collected material was transported to the Mycology Laboratory of Universidade Federal do Piauí (UFPI) for analysis. 30 ml from water samples were placed into Petri dishes (100 × 20 mm) with organic substrates. Approximately, 20 g from the soil samples were placed into in Petri dishes (100 × 20 mm) with sterile distilled water to decant. After decanting, cellulosic, chitinous and keratinous substrates were added to the plates. Then the plates were incubated with the samples at room temperature (30-32 ºC) for a 7-day period.

We performed microscopic analysis of the samplings in order to assess the presence of Oomycetes, which were then placed into new Petri plates with the respective substrates to be colonized (cellulosic, chitinous or keratinous). Subsequently, sterile distilled water was added to each plate. The plates were incubated for seven days for the identification of developing fungal structures. The maintenance of the strains was done with the exchange of water and adding new substrates to each plate.

Vegetative and reproductive structures were recorded by using an optical microscope (Olympus BX41 model, Tokyo, Japan), and photographed with a Nikon digital camera (Coolpix - S4100). Taxonomic descriptions of isolates were done in accordance with pertinent publications (Sparrow 1956, Johnson Jr. 1960, Scott 1961, Dick 1990, Johnson et al. 2002). Selected strains were deposited in the mycology culture collection at Universidade Federal do Piauí (UFPI).

Results and Discussion

Beakes et al. (2014) carried out an up-to-date phylogenetic and taxonomic review of the Straminipila (Labyrinthulomycota, Hyphochytridiomycota, and Oomycota) based upon molecular sequence data, biology and evolutionary history. This taxonomic revision was adopted in the present study. We obtained 98 isolates of Oomycota, including 16 species, which belong to Achlyaceae (Achlya aff. diffusa J.V. Harv. ex T.W. Johnson, A. proliferoides Coker, A. orion Coker & Couch, Brevilegnia linearis Coker, and Dictyuchus monosporus Leitg.), Leptolegniellaceae s. lat. (Leptolegniella keratinophila Huneycutt), Pythiaceae s. lat. (Globisporangium proliferum (Cornu) P.M. Kirk, Pythiogeton ramosum Minden, P. uniforme A. Lund, P. utriforme Minden, and Pythium graminicola Subram.), Olpidiopsidaceae s. lat. (Olpidiopsis aphanomycis Cornu) Saprolegniaceae s. str. (Aplanopsis terrestris Höhnk, and Saprolegnia luxurians (Bhargava & G.C. Srivast) R.L. Seym.), Verrucalvaceae (Aphanomyces helicoides Minden, and A. keratinophilus Ôokubo & Kobayasi) (table 1).

Table 1
Oomycetes families and species, according Beakes et al. (2014), found within Parque Natural Municipal Lagoa do Sambico, Timon municipality, Maranhão State, Brazil.

Family/Species
Achlyaceae
Achlya aff. diffusa J.V. Harv. ex T.W. Johnson**
Achlya orion Coker & Couch
Achlya proliferoides Coker**
Brevilegnia linearis Coker
Dictyuchus monosporus Leitg.**
Leptolegniellaceae s. lat.
Leptolegniella keratinophila Huneycutt
Pythiaceae s. lat.
Globisporangium proliferum (Cornu) P.M. Kirk**
Pythiogeton ramosum Minden
Pythiogeton uniforme A. Lund**
Pythiogeton utriforme Minden
Pythium graminicola Subram.
Olpidiopsidaceae s.lat.
Olpidiopsis aphanomycis Cornu*
Saprolegniaceae s. str.
Aplanopsis terrestris Höhnk**
Saprolegnia luxurians (Bhargava & G.C. Srivast) R.L. Seym.*
Verrucalvaceae
Aphanomyces helicoides Minden**
Aphanomyces keratinophilus Ôokubo & Kobayasi

• ^*
  First record for Brazil.
• ^**
  First record for Maranhão State.
Source: Direct research (2015).

Achlyaceae

Achlya aff. diffusa J.V. Harv. ex T.W. Johnson, The Genus Achlya: Morphology and Taxonomy: 64. 1956. Figures 2-3

Figures 2-10
Species of oomycetes (Oomycota) from Parque Natural Municipal Lagoa do Sambico, Timon municipality, Maranhão State, Brazil. 2-3. Achlya aff. diffusa. 2.Oogonia young. 3. Globose dilatations. 4. Achlya orion, oogonium with eccentric oospore, antheridium androgynous, and twisted stalk. 5. Achlya proliferoides, oogonium with oospores and antheridial branches involving the main hyphae. 6. Brevilegnia linearis, oogonium with oospore eccentric. 7. Dictyuchus monosporus, oogonia with parthenogenetic oospores. 8. Leptolegniella keratinophylla, resistant spores. 9. Globisporangium proliferum, spherical oogonia with oospore hyaline. 10. Pythiogeton ramosum, bursiform zoosporangium. Bar: 10 µm.

Zoosporangia abundant, 220˗320 × 18˗38 µm, filiform, irregular, sometimes curved. Gemmae abundant. Dilatations spherical or globular, 63-137 µm diâm., large, disposed between the oogonia. Oogonia abundant, 34-53 µm diâm., sessile, lateral, occasionally intercalary, spherical, terminal, globular, smooth-walled, usually with pores. Peduncle simple, 14-32 × 11-19 µm, straight, curved, or bent, not tapering towards the base. Oospores 19˗25 µm diâm., eccentric, usually 2-6 per oogonium, spherical. Antheridia frequent, monoclinous and diclinous, persistent and long. Antheridial cells branched, not persistent, attached by projections.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples in the respective collection spots, 20-X-2014, J.B. Silva (A2/2-S2/2-S3/2-S4/2); 18-XII-2014, J. B. Silva (A2/3-S3/3-S4/3); 23-II-2015, J.B. Silva (S3/4-S4/4).

Geographical distribution in Brazil: Piauí: Parque Nacional de Sete Cidades (Rocha 2002).

Oogonia were abundant in the material, but not observed proliferating oogonia (figure 2), and the dilatations were very large (63˗137 µm diâm.). These two characteristics are not in accordance with the findings by Rocha (2002), which found abundant proliferating oogonia, and dilatations with measurement lower (47˗98 µm diâm.) (figure 3).

Achlya orion Coker & Couch, J. Elisha Mitchell Scient. Soc. 36: 100. 1920. Figure 4

Zoosporangia 235˗294 × 20˗34 µm, filiform, fusiform, sympodial renewal. Zoospores encysted 10˗12 µm diâm. Gemmae present. Oogonia 34-49 µm diâm., lateral or terminal, spherical, proliferating, smooth-walled; twisted stalk, some being straight. Oospheres 29˗39 µm diâm. Oospores 19˗24 µm diâm., eccentric, spherical, some oval, 1-4 per oogonium. Antheridia androgynous and monoclinous, rarely diclinous; simple, some branched. Antheridial cells tubular, simple or branched.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa Sambico, soil and water samples at collection spots, 23-II-2015, J.B. Silva (S3/4-S4/4-A4/4); 20-V-2015, J.B. Silva (A4/5-S1/5-S2/5).

Geographical distribution in Brazil: Amazonas (Silva 2002); Minas Gerais (Oliveira 2004); Pernambuco (Cavalcanti 2001); Piauí (Rocha 2002); São Paulo (Beneke & Rogers 1962, Gomes et al. 2003, Lyra & Milanez 1974, Milanez 1970, Milanez et al. 1994a, Pires-Zottarelli 1990, 1999, Pires-Zottarelli et al. 1996b, Rocha & Pires-Zottarelli 2002).

Species characterized by eccentric oospores with pending oogonium stalk (figure 4). The characteristics of the isolates agree with the descriptions of Johnson (1956), Beneke & Rogers (1962), Pires-Zottarelli (1990, 1996, 1999), Rocha (2002) and Nascimento (2010). Gomes & Pires-Zottarelli (2008) reported the presence of larger spherical oogonia, ranging from 35 to 47.5 µm diâm. Rocha (2002) observed for the first time the formation of intercalary and sessile oogonia in this species. Such species is described as a second record for Maranhão State.

Achlya proliferoides Coker, Saprolegniaceae with notes on other water molds: 115. 1923. Figure 5

Zoosporangia 259˗343 × 19˗34 µm, abundant, filiform or fusiform, straight or curved near the apex. Encysted zoospore 10˗12 µm diâm. Gemmae abundant. Oogonia 47˗55 µm diâm., lateral, spherical, smooth-walled, usually with pores. Peduncle straight smooth, rarely bent. Oosphere often not maturing. Oospore 22˗27 µm diâm., spherical, eccentric; 3-8 per oogonium, often not filling the oogonium, abortive. Fertilization tube not observed. Antheridia with diclinous or monoclinous antheridial branches, irregular, branched, usually involving hyphae and oogonial peduncle and/or oogonia. Antheridial cells tubular, irregular, simple or branched, lateral attached or by projections.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa Sambico, soil and water samples at collection spots, 23-II-2015, J.B. Silva (S1/4-A4); 20-V-2015, J.B. Silva (S1/5-S3/5-S4/5).

Geographical distribution in Brazil: Piauí (Rocha 2002, Pereira 2008, Negreiros 2008, Trindade-Júnior 2013); Amazonas (Silva 2002); Pernambuco (Cavalcanti 2001); Minas Gerais (Beneke & Rogers 1962, Oliveira 2004); São Paulo (Rogers et al. 1970, Schoenlein-Crusius et al. 1990, Pires-Zottarelli 1999, Gomes et al. 2003, Pires-Zottarelli et al. 1996b, Rocha & Pires-Zottarelli 2002, Rocha 2004).

The measures of the structures were relatively lower than those reported by the original description by Johnson (1956) and Pires-Zottarelli (1999). However, the isolates agree in general with the data described by Rocha (2002), Nascimento & Pires-Zottarelli (2012) and Sousa (2014). The species has as a differential characteristic, which is the presence of antheridial branches involving hyphae, the stalk and the oogonium (figure 5). This is the first record for Maranhão State.

Brevilegnia linearis Coker, J. Elisha Mitchell Scient. 42:214. 1927. Figure 6

Zoosporangia 110˗505 × 7˗15 µm, long, curved or irregular. Zoospores displayed in rows. Gemmae absent. Oogonia spherical, 21˗35 µm diâm., lateral or terminal, sometime with papilla. Oospores 1 per oogonia, sphaeric, eccentric, 12˗14 µm diâm. Antheridium 1 per oogonia, antheridial branches androgenous.

Material examined: BRASIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 20-X-2014, J.B. Silva (A1/2- S3/2-S4/2); 23-II-2015, J.B. Silva (A1/4-S1/4-S3/4-S4/4).

Geographical distribution in Brazil: Piauí (Trindade-Júnior & Rocha 2013); Amazonas (Johnson et al. 2002); Minas Gerais (Oliveira 2004); São Paulo (Pires-Zottarelli & Milanez 1993); Maranhão (Sales 2009).

The isolate presented oospore eccentric (Figure 6), and long zoosporangia, in agreement with Trindade-Júnior & Rocha (2013), which were identified as the first occurrence of B. linearis in Piauí State. The taxon was found in groundwater wells in Timon municipality by Sales (2009), being the first record for Maranhão State. This is the second record for this State.

Dictyuchus monosporus Leitg. Jb. Wiss. Bot. 7:374. 1870. Figure 7

Primary zoosporangia produced in the extremity of the main hyphae. Sometimes zoospores germinating of the zoosporangium, leaving the primary cyst wall, forming real network with the wall of zoosporangium. Gemmae absent. Oogonia terminals, 30˗45 µm diâm. or formed in single lateral branches, smooth, spherical, thin wall. Oospores 1 per oogonium, 19˗35 µm diâm., spherical with a large distinctive lipid droplet, eccentric, wall 2 µm thick. Antheridia diclinous or androgynous or sometimes absent.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 20-X-2014, J.B. Silva (S1/2-S3/2- S4/2-A/2); 18-XII-2014, J.B. Silva (S1/4-S3/4).

Geographical distribution in Brazil: Piauí (Pereira 2008, Negreiros 2008); Maranhão (Sales 2009).

It formed oogonia with whole oospores (Figure 7). Antheridia diclinous, sometimes, absent. The species is described as a second record for Maranhão State.

Leptolegniellaceae s. lat.

Leptolegniella keratinophilaHuneycutt, J. Elisha Mitchell Scient. Soc. 68: 110. (1952). Figure 8

Micelium very branched, irregular hypha. Zoosporangia branched. Zoospore not observed. Resistance spores 10˗16 µm diâm., spherical, internally formed hyphae, sometimes ovoid; with eccentric lipid droplet, thick wall.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 17-VIII-2014, J.B. Silva (A2/1-S1/2-S2/2); 20-X-2014, J.B. Silva (S1/3-S2/3-S4/3); 18-XII-2014, J.B. Silva (S3/4-S4/4); 23-II-2015, J.B. Silva (A2/5-S1/5-S2/5).

Geographical distribution in Brazil: Amazonas (Silva 2002); Piauí (Sousa 2014, Rocha 2002); Pernambuco (Cavalcanti 2001); São Paulo (Milanez 1970, Pires-Zottarelli et al. 1996, 1999, Rocha & Pires-Zottarelli 2002); Maranhão (Sales 2009).

The isolate is characterized by resistant spores with thick wall (Figure 8). Description of the isolate agrees with original description of the species by Huneycutt (1952) and the data reported by Rocha (2002), Sales (2009), Trindade-Júnior (2013) and Sousa (2014) in Piauí State. It is the second record for Maranhão State.

Pythiaceae s. lat.

Globisporangium proliferum (Cornu) P.P. Kirk, Index Fungorum 191:1. 2014. Figure 9

Zoosporangia terminal or intercalar, ovoid, elipsoid, globose, with internal proliferation. Oogonia terminal or lateral, spherical, 15˗25 µm diâm., oval. Sometimes with papilla. Oospores hyaline, spherical, 13˗20 µm diâm., smooth-walled. Antheridia 1-2 per oogonium, monoclinous or hypogynous, sometimes sessile, simple or branched. Antheridial cell simples, clavate, attached apically to oogonium.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil sample at collection spots, 20-V-2015, J.B. Silva (S4/5).

Geographical distribution in Brazil: Piauí (Rocha et al. 2001); São Paulo (Pires-Zottarelli 1999).

Isolates produced typical spherical oogonia with oospore hyaline (Figure 9). It agrees with the descriptions of Plaats-Niterink (1981), Pires-Zottarelli (1999) and Rocha (2002) (cited as Pythium middletonii Sparrow). Also, according to Plaats-Niterink (1981), its pathogenicity caused disease on seedlings of soybean (Glycine max), tomato (Solanum lycopersicum), and potato (Solanum tuberosum). This is the first record for Maranhão State.

Pythiogeton ramosum Minden, Falck, Mykol. Untersuch. Ber. 1:243. 1910. Figure 10

Zoosporangia spherical, bursiform, 18˗48 × 20˗60 µm diâm., terminal. Internal proliferation observed, with a straight or winding release tube forming with the supporting hyphae a right angle. Zoospores encysted 8˗11 µm diâm. Sexual reproductive structures not observed.

Material examined: BRASIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 23-II-2015, J.B. Silva (A4/4-S2/4- S4/4).

Geographical distribution in Brazil: Amazonas (Silva 2002); Pernambuco (Cavalcanti 2001); Piauí (Pereira 2008, Rocha 2002, Trindade-Júnior 2013). Rio de Janeiro (Beneke & Rogers 1970); São Paulo (Rocha & Pires-Zottarelli 2002); Maranhão (Sales 2009).

The characteristics observed corroborate the original description. This sample has a larger spherical zoosporangia (Figure 10) than those described by Gomes and Pires-Zottarelli (2008) in which they reported 27˗45 µm diâm. Analyses agree with descriptions of Rocha (2002), Negreiros (2008) and Pereira (2008). This is the second record for Maranhão State.

Pythiogeton uniforme A. Lund, Mém. Acad. Roy. Sci. Lett. Danemark, Copenhague, Sect. Sci., ser., 6:54. 1934. Figure 11

Figures 11-19
Species of oomycetes (Oomycota) from Parque Natural Municipal Lagoa do Sambico, Timon municipality, Maranhão State, Brazil. 11. Pythiogeton uniforme, spherical zoosporangium. 12. Pythiogeton utriformis, spherical oogonium with oospore and very thick wall. 13. Pythium graminicola, oogonia with aplerotic oospore. 14. Olpidiopsis aphanomyces, oospore covered with conical thorns, parasitizing oogonium of Aphanomyces keratinophillus (left). Intact oogonium and oospore of Aphanomyces keratinophillus (right). 15. Aplanopsis terrestris, oogonia with lipid droplet. 16-17. Saprolegnia luxurians. 16. Oogonium with eccentric spores. 17. Zoosporangium with zoospores. 18. Aphanomyces helicoides, antheridial cells attached to young oogonium, and antheridial branches coiling about the peduncle of the oogonium. 19. Aphanomyces keratinophyllus, oogonia with oospore. Bar: 10 µm.

Terminal zoosporangia in lateral long branches, spherical, 29˗30 µm diâm., occasionally intercalary. Internal proliferation. Zoospores reniform, biflagellate. Sexual structures not observed.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 23-II-2015, J.B. Silva (A2/4-A4/4-S1/4-S4/4).

Geographical distribution in Brazil: Piauí: (Rocha 2002, Negreiros 2008, Trindade-Júnior 2013).

Isolate produced zoosporangia spherical (Figure 11). The data corroborate the original description. It was firstly reported in Brazil by Rocha (2002) in samples of water and soil from the Parque Nacional de Sete Cidades, and later found by Negreiros (2008), in Floriano municipality, and Trindade-Júnior (2013), in Teresina municipality; all in the Piauí State. It is the first record for Maranhão State.

Pythiogeton utriforme Minden. Falck, Mykol. Untersuch. Ber. 1:242. 1916. Figure 12

Zoosporangia lateral, bursiform with internal proliferation, septum at the base separating it from the supporting hyphae. Thin release tube, long, originated near the base of zoosporangia, forming right angles with the axis of the supportive hyphae. Oogonia terminal, spherical, 33˗35 µm diâm. Oospore spherical, 18˗19 µm diâm., plerotic or aplerotic, colorless, very thick wall. Antheridia not observed.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil samples at collection spots, 17-VII-2014, J.B. Silva (S1/1); 20-X-2014, J.B. Silva (S3/2).

Geographical distribution in Brazil: Piauí (Rocha 2002).

The data agree with those presented in the original description. They show a remarkable characteristic: oospores with extremely thick walls with irregular layers (Figure 12) and oogonia which can proliferate and originate another oogonium internally with antheridia. This is first record for Maranhão State, and second for Brazil.

Pythium graminicola Subram., Bull. Agric. Res. Inst. Pus. 177:1. 1928. Figure 13

Zoosporangia terminal or intercalary with filamentous inflated complex. Oogonium 22˗26 µm diâm. terminal, globose, smooth. Oospores plerotic, 20˗23 µm diâm. Antheridia 1-2 per oogonium, monoclinous, diclinous with apical attachment to oogonium.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa Sambico, soil and water samples at collection spots, 20-X-2014, J.B. Silva (A2/2-S2/2-S4/2), 23-II-2015, J.B. Silva (S3/4-S4/4).

Geographical distribution in Brazil: São Paulo (Ghini et al. 2002, Baptista et al. 2004); Piauí (Rocha 2002); Maranhão (Sales 2009).

Isolate produced characteristic oogonia and zoosporangia with inflated complex (Figure 13). The species is depicted according to the description of Plaats-Niterink (1981). It is highly pathogenic in crop plants such as corn (Zea mays), potato (Solanum tuberosum), beans (Phaseolus vulgaris), pineapple (Ananas comosus) and onion (Allium cepa). It is second record for Maranhão State.

Olpidiopsidaceae s.lat.

Olpidiopsis aphanomycisCornu, Annls Sci. Nat., Bot., ser. 5(15): 148. 1872. Figure 14

Zoosporangia 15˗45 µm diâm., solitary or numerous; flat; hyaline or granular gray; oval, spindle-shaped, elongated, but generally spherical; release of one to several tubes that may extend beyond the host cell surface. Zoospore 6˗8 µm diâm.; parthenogenetic or sexual; hyaline or brown; oval, spherical. Oospore 2-4 per oogonium, covered with conical thorns; granular content with one or more large refractive droplets. Companion cell or male cell absent.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa Sambico, soil samples at collection spots, 20-X-2014, J.B. Silva (S1/2-S2/2); 23-II-2015, J.B. Silva (S2/4-S3/4); 20-V-2015, J. B. Silva (S3/5, A2/5).

Geographical distribution in Brazil: Maranhão: this is first record to Brazil.

The examined cultures presented measurements within the variations observed by Cornu (1872), Karling (1944) and Sparrow (1960). O. aphanomycis parasite species Aphanomyces laevis (Butler & Bysby 1931) and A. cladogamus (Whiffen 1942). In Aphanomyces keratinophillus the parasite caused severe hypertrophy in the spots of the infected oogonium (Figure 14). This record indicates the need for more sampling efforts in order to get a better understanding of diversity and geographical distribution of the species Olpidiopsis as well as their role in ecosystems. This new record rises to six species of Olpidiopsis recorded in Brazil (Milanez et al. 2007). It enlarges the distribution of O. aphanomycis in South America, where the nearest record was solely located in Buenos Aires, Argentina (Steciow 2012). This is the first record for Brazil.

Saprolegniaceae s. str.

Aplanopsis terrestris Höhnk, Veröff. Inst. Meeresf, Bremerhaven, Sonderband 1:127. 1952. Figure 15

Mycelium diffuse, long hyphae. Zoosporangia not observed. Oogonia lateral or terminal, 24-30 µm diâm., with ornamented wall, spherical, globose or ovoid. Oospores subcentric, 18˗24 µm diâm., spherical, oval, ellipsoid. Antheridia, when present, androgynous.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 23-II-2015, J.B. Silva (S3/4-S4/4); 20-V-2015, J.B. Silva (A2/5-S1/5).

Geographical distribution in Brazil: São Paulo (Rocha et al. 2016).

Isolate produced oogonia with lipid droplet (Figure 15). First record for Maranhão State and second record for Brazil.

Saprolegnia luxurians (Bhargava & G.C. Srivast) R.L. Seym. Nova Hedwigia 19 (1-2): 55. 1970. Figures 16-17

Zoosporangia abundant, 150˗190 × 19˗28 µm, filiform, clavate; straight, rarely bent, renovation by internal proliferation, occasionally basipetalous succession, rarely by simpodial ramification. Zoospore encysted 8˗11 µm diâm. Gemmae rare. Oogonia abundant, 32˗35 µm diâm., lateral, rarely terminal or intercalary; spherical or subspherical, occasionally pyriform, rarely cylindrical; very rarely catenulate, rarely papillary wall. Oospore eccentric, 22˗27 µm diâm., spherical or rarely ellipsoid almost filling the oogonium. Antheridial branch monoclinous or androgynous, often diclinous, rarely branched. Antheridial cell tubular, simple or compound.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa Sambico, soil samples at collection spots, 23-II-2015, J.B. Silva (S3/4-S2/5); 20-V-2015, J.B. Silva (A/3-A/4).

Geographical distribution in Brazil: Maranhão: This is first record for Brazil.

Isolate produced oogonia with eccentric spores (Figure 16), and zoosporangium clavate (Figure 17). The morphological data of this species agree with those presented in the original description.

Verrucalvaceae

Aphanomyces helicoides Minden, Krypt.-Fl.Brandenburg (Leipizig) 5:559. 1912. Figure 18

Zoosporangia with achlyoid release. Oogonia 24˗28 µm diâm., lateral or terminal, spherical, smooth-walled, sometimes it becomes wrinkled. Oospore 23˗26 µm diâm., light brown, spherical, with thin walls, and a finely granular content with a large central oil globule. Antheridia diclinous or monoclinous. Antheridial cells 1-5 per oogonium.

Material examined: BRAZIL. MARANHÃO: Timon, Parque Natural Municipal Lagoa do Sambico, soil samples at collection spots, 20-X-2014, J.B. Silva (S3/2-S4/2).

Geographical distribution in Brazil: Amazonas (Silva 2002); Minas Gerais (Oliveira 2004); Piauí (Rocha 2002); São Paulo (Pires-Zottarelli 1990, Milanez et al. 2007, Miranda & Pires-Zottarelli 2012).

Isolate produced antheridia attached in oogonia (Figure 18) and oospore occasionally hyaline but with a predominance of light brown color. Howard et al. (1970) assumed that A. helicoides and A. laevis were synonymous species. Currently, are not synonymous, second Species Fungorum (2016). This is first record for Maranhão State.

Aphanomyces keratinophilus (M. Ôkubo & Kobayasi) R.L. Seym. & T.W. Johnson, Mycology 65(6): 1317. 1974. Figure 19

Zoosporangia long and filamentous, with achlyoid release of zoospore. Zoospores cylindrical or fusiform. Gemmae absent. Oogonia 16˗28 µm diâm., lateral or terminals in variables length branches, spherical or pyriform, sometimes intercalary. Oospores spherical, 13˗25 µm diâm., thin-walled, light brown, with the presence of a large lipid droplet in the center. Antheridia branched, androgynous and monoclinous, contorted and irregular.

Material examined: BRAZIL. Maranhão: Timon, Parque Natural Municipal Lagoa do Sambico, soil and water samples at collection spots, 17-VIII-2014, J.B. Silva (A1/1-A2/1-S1/1-S3/1); 20-X-2014, J.B. Silva (S1/2-S2/2-S3/2); 8-XII-2014, J.B. Silva (A2/3-S1/3-S2/3-S3/3); 23-II-2015, J.B. Silva (A3/5-A4/5-S1/5-S2/5).

Geographical distribution in Brazil: Piauí (Rocha 2002); Maranhão (Sales 2009).

Isolate produced typical oogonia with oospore (Figure 19). The main distinguishing features of A. keratinophilus are the affinity for keratin substrates and abundant presence of antheridial branches involving oogonium profusely. Furthermore, the data agree with the descriptions by Rocha (2002), who presented the first description in Brazil, isolating soil samples from Parque Nacional de Sete Cidades, Piauí. This is the second record for Maranhão State.

The current anthropic pressure over ecosystems causes a strong environmental disturbance. Despite global commitments to reduce the impacts of human activities on ecosystems worldwide, loss of biodiversity and ecosystem exploitation continues rising. However, it is little known about the biodiversity of ecosystems in Brazil. Based upon this survey research, new records for Maranhão State and Brazilʼs Countrywide have been made. Most of the speciesʼ records presented herewith were commonly found worldwide (Marano et al. 2008, Steciow et al. 2012) and have been previously isolated in Brazil (Gomes et al. 2003, Gomes & Pires-Zottarelli 2008, Milanez et al. 2008, Nascimento & Pires-Zottarelli 2012). Moreover, many other studies were carried out in Piauí State (Negreiros 2008, Pereira 2001, Rocha et al. 2001, Sousa 2014, Trindade-Júnior 2013), but a single study in Maranhão State (Sales 2009).

These new records of Oomycetes occurrences enhanced the knowledge about such organisms in Brazil.

• 1
  Parte da Dissertação de Mestrado do primeiro Autor

Acknowledgements

The authors wish to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship granted to the first author. We also would like to thank the research group from LFZ-UFPI, Amparo Macêdo, Laercio Saraiva, Santina Barbosa, Francynara Pontes, Daniele Oliveira, Geisla Silva, Tamyres Rios, Débora Gabriele, Larissa Pereira, Francisco Silva, Jório Francand, especially, Joseane Lustosa.

Literature cited

• Alexopoulos, C.J., Mims, C.W. & Blackwell, M. 1996. Introductory Mycology. 4 ed. John Wiley & Sons, Inc., New York.
• Baptista, F.R., Pires-Zottarelli, C.L.A., Rocha, M., Milanez, A.I. 2004. The genus Pythium Pringsheim from Brazilian Cerrado areas, in the state of São Paulo, Brazil. Revista Brasileira de Botânica 27: 281-290.
• Beakes, G.W., Honda, D. & Thines, M. 2014. Systematics of the Straminipila: Labyrinthulomycota, Hyphochytridiomycota, and Oomycota. In: Systematics and Evolution, The Mycota, VIII Part A, D.J. McLaughlin and J.W. Spatafora (eds.). 2 ed., Springer-Verlag, Berlin, Heidelberg, pp. 39-97.
• Beneke, E.S. & Rogers, A.L. 1962. Aquatic Phycomycetes isolated in the States of Minas Gerais, São Paulo and Paraná, Brazil. Rickia 1: 181-193.
• Beneke, E.S. & Rogers, A.L. 1970. Aquatic fungi of Parque Nacional de Itatiaia in the State of Rio de Janeiro. Rickia 5: 51-64.
• Bosco, M., Giovannetti, M., Viti, C. 2008. Ruolo dei microrganismi nei cicli biogeochimici. In: B. Biavati, C. Sorlini (eds.). Microbiologia Agroambientale, Casa Editrice Ambrosiana, pp. 1-37.
• Butler, E.J. & Bisby, G.R. 1931. The fungi of India. Imp. Counc. of Agri Res. India, Sci. Mono 1, XVIII. Calcutta.
• Cavalcanti, M.S. 2001. Fungos isolados de água e do solo das margens dos Açudes do Prata e do Meio, na Reserva Florestal de Dois Irmãos. Recife (PE). Tese de Doutorado, Universidade de São Paulo, São Paulo.
• Cornu, M.M. 1872. Monographie des Saprolégniées. Étude physiologique et systématique. Annales des Sciences Naturelles, Botanique, Série 15: 5-198.
• Dick, M.W. 1990. Keys to Pythium College of Estate Management, Whiteknights.
• Dick, M.W. 2001. Straminipilous Fungi: systematics of the Peronosporomycetes including accounts of the marine straminipilous protists, the plasmodiophorids and similar organisms. Kluwer Academic Publishers, Holand.
• Ghini, R., Shoenmaker, I.A.S., Bettiol, W. 2002. Solarização do solo e incorporação de fontes de matéria orgânica no controle de spp. Pesquisa Agropecuária Brasileira 37: 1253-1261.
• Gomes, A.L., Pires-Zottarelli, C.L.A., Rocha, M., Milanez, A.I. 2003. Saprolegniaceae de áreas de Cerrado do estado de São Paulo, Brasil. Hoehnea 30: 95-110.
• Gomes, A.L. & Pires-Zottarelli, C.L.A. 2008. Oomycota (Straminipila) da Reserva Biológica de Parapiacaba, Santo André, SP, Brasil. Acta Botânica Brasílica 22: 373-392.
• Hawksworth, D.L. 2004. Fungal diversity and its implications for genetic resource collections. Studies in Mycology 50: 9-18.
• Hughes, G.C. 1962. Seasonal periodicity of Saprolegniaceae in the South-Eastern United States. Transactions of the British Mycological Society 45: 519-531.
• Huneycutt, M.B. 1952. A new water mold on keratinized materials. Journal of the Elisha Mitchell Scientific Society 68: 109-112.
• Howard, K.L., Seymour, R. & Johnson, Jr. T.W. 1970. Aquatic fungi of Iceland: Saprolegniaceae. Journal of the Elisha Mitchell Scientific Society 86: 63-79.
• IBGE - Instituto Brasileiro de Geografia e Estatística 2013. Contagem da população 2013. IBGE, Rio de Janeiro.
• Johnson Jr., T.W. 1956. The genus Achlya: Morphology and Taxonomy. The University of Michigan Press. Ann Arbor.
• Johnson, Jr. T.W., Seymour, R. L. & Padgett, D.E. 2002. Biology and systematic of the Saprolegniaceae. Available in http://www.uncw.edu/people/padgett/book (access in 13-I-2017).
  » http://www.uncw.edu/people/padgett/book
• Karling, J.S. 1944. Brazilian chytrids, I: Species of Nowakowskiella. Bull. Torrey Botanical Club 71: 374-389.
• Leal, A.B.M., Leal, A.T., Santurio, J.M., Kommers, G.D. & Catto, J.B. 2001. Pitiose eqüina no Pantanal brasileiro: aspectos clínico-patológicos de casos típicos e atípicos. Pesquisa Veterinária Brasileira 21: 151-156.
• Lyra, N.P. & Milanez, A.I. 1974. Notas para o levantamento dos ficomicetos aquáticos do estado de São Paulo. Instituto de Micologia da Universidade Federal de Pernambuco. Publicação 698, pp. 1-27.
• Marano, A.V., Barrera, M.D., Steciow, M.M., Donadelli, J.L., Saparrat, M.C.N. 2008. Frequency, abundance and distribution of zoosporic organisms from Las Canãs stream, Buenos Aires, Argentina. Mycologia 100: 691-700.
• Marano, A.V., Pires-Zottarelli, C.L.A., Barrera, M.D., Steciow, M.M. 2011. Diversity, role in decomposition, and sucession of zoosporic fungi and straminipiles and submerged decaying leaves in a woodland stream. Hydrobiologia 659: 93-109.
• Milanez, A.I. 1970. Contributions to the knowledge of aquatic Phycomycetes of São Paulo State, I: Oomycetes form the west region. Rickia 5: 23-43.
• Milanez, A.I. 1989. Fungos de águas continentais. In: O. Fidalgo, V.L. Bononi (coords.). Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo, pp. 17-20.
• Milanez, A.I., Pires-Zottarelli, C.L.A., Gomes, A.L. 2007. Brazilian zoosporic fungi. Winner Graph, São Paulo.
• Moore-Landecker, E. 1996. Fundamentals of the fungi. 4 ed., Prentice-Hall, New Jersey.
• Nascimento, C.A. & Pires-Zottarelli, C.L.A. 2010. Blastocladiales e Spizellomycetales do Parque Estadual da Serra da Cantareira, São Paulo, Brasil. Revista Brasileira de Botânica 33: 693-704.
• Nascimento, C.A. & Pires-Zottarelli, C.L.A. 2012. Diversidade de fungos zoospóricos da Reserva Biológica de Mogi Guaçu, estado de São Paulo, Brasil. Rodriguésia 63: 587-611.
• Negreiros, N.C. 2008. Uso sustentável de culturas agrícolas suscetíveis a oomicetos (Oomycota) fitopatogênicos às margens do rio Parnaíba no município de Floriano, Piauí. Dissertação de Mestrado, Universidade Federal do Piauí, Teresina.
• Nikolcheva, L.G., Cockshutt, A.M. & Bärlocher, F. 2003. Determining diversity of freshwater fungi on decaying leaves: comparison of traditional and molecular approaches. Applied and Environmental Microbiology 69: 2548-2554.
• Nikolcheva, L.G. & Bärlocher, F. 2004.Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycological Progress 3: 41-49.
• Oliveira, J.M. 2004. Diversidade de fungos zoospóricos da Represa do Boqueirão, Ingaí, MG. Trabalho de Conclusão de Curso, Centro Universitário de Lavras, Minas Gerais.
• Plaats-Niterink AJ, Van Der 1981. Monograph of genus Pythium Studies in Mycology 21: 1-242.
• Pereira, A.A. 2008. Oomicetos (Oomycota) no campo agrícola de Nazária, Piauí: sustentabilidade na prevenção e controle dos fitopatógenos em agricultura familiar. Dissertação de Mestrado, Universidade Federal do Piauí, Teresina.
• Pires-Zottarelli, C.L.A. 1990. Levantamento dos fungos zoospóricos da Represa do Lobo (Broa), São Carlos-SP. Dissertação de Mestrado, Universidade Estadual Paulista, Rio Claro.
• Pires-Zottarelli, C.L.A. & Milanez, A.I. 1993. Fungos zoospóricos da Represa do Lobo (Broa). Novas citações para o Brasil. Revista Brasileira de Botânica, v. 16, pp. 205-220.
• Pires-Zottarelli, C.L.A., Milanez, A.I., Schoenlein-Crusius, I.H. & Lohmann, L.G. 1996. Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP. Fungos, 6: Chytridiales. Hoehnea 23: 77-90.
• Pires-Zottarelli, C.L.A. 1999. Fungos Zoospóricos dos Vales dos Rios Moji e Pilões, Região de Cubatão, São Paulo - SP. Tese de Doutorado, Universidade Estadual Paulista, Rio Claro.
• Rech, R.R., Graça, D.L. & Barros, C.S.L. 2004. Pitiose em um cão: relato de caso e diagnósticos diferenciais. Clínica Veterinária 50: 68-72.
• SEMA - Secretaria do Meio Ambiente 2011. Relatório de Impacto Ambiental da Lagoa do Sambico e entorno, situada na Zona Urbana do município de Timon/MA. v. 1.
• Rocha, J.R.S. 2002. Fungos zoospóricos em área de cerrado no Parque Nacional de Sete Cidades, Piauí, Brasil. Tese de Doutorado, Universidade de São Paulo, São Paulo.
• Rocha, J.R.S, Milanez A.I, & Pires-Zottarelli, C.L.A. 2001. O gênero Pythium (Oomycota) em áreas de cerrado no Parque Nacional de Sete Cidades, Piauí, Brasil. Hoehnea 28: 209-230.
• Rocha, J.R.S., Silva, V.S., Santos, S.L., Dias, L.P., Rodrigues, E.P., Batista Filho, D.M., Feitosa Junior, F.S. & Barbosa, R.D. 2010. Pitiose cutânea equina. Primeiro relato de caso no Piauí. Revista do Conselho Federal de Medicina Veterinária 15: 24-27.
• Rocha, M. 2004. Micota zoospórica de Lagos, com Diferentes trofias do Parque Estadual das Fontes do Ipiranga (PEFI), São Paulo, SP. Dissertação de Mestrado, Universidade de São Paulo, São Paulo.
• Rocha, M. & Pires-Zottarelli, C.L.A. 2002. Chytridiomycota e Oomycota da Represa do Guarapiranga. São Paulo, SP. Acta Botânica Brasilica 16: 287-309.
• Rocha, S.C.O., Jeronimo, G.H., Marano, A,V., Souza, I.J. & Jesus, A.L. 2016. Oomycota from "Parque Estadual da Ilha do Cardoso" (PEIC): first records for São Paulo State and Brazil. Cryptogamie, Mycologie 37: 177-191.
• Rogers, A.L., Milanez, A.I. & Beneke, E.S. 1970. Fungos aquáticos adicionais do Estado de São Paulo. Rickia 5: 93-110.
• Sales, P.C.L. 2009. Potabilidade da água e presença de oomicetos (Oomycota) em poços freáticos nos povoados Banco de Areia, Bacuri e Roncador no município de Timon Maranhão. Dissertação de Mestrado, Universidade Federal do Piauí, Teresina.
• Sallis, E.S.V., Pereira, D.I.B., Raffi, M.B. 2003. Pitiose cutânea em eqüinos: 14 casos, 2001. Ciência Rural 33: 899-903.
• Santurio, J.M., Monteiro, A.B., Leal, A.T. 1998. Cutaneous Pyhtiosis insidiosi in calves from the Pantanal region of Brazil. Mycopathologia 141: 123-125.
• Silva, M.I.L. 2002. Micobiota de água e solo das margens de Igarapés situados na área de mata do campus da Universidade do Amazonas, Manaus, AM, Brasil. Tese de Doutorado, Universidade de São Paulo, São Paulo.
• Schoenlein-Crusius, I.H., Pires-Zottarelli, C.L.A., Milanez, A.I. 1990. Sucessão fúngica em folhas de Quercus robur L. (carvalho) submersas em um lago situado no município de Itapecerica da Serra, São Paulo.
• Scott, W. W. 1961. A monograph of the genus Aphanomyces Virginia Agricultural Esperiments Station. Technical Bulletin 151: 1-95.
• Sparrow, F.K. 1960. The aquatic Phycomycetes. Ann Arbor, University of Michigan Press 2: 1181.
• SSpecies Fungorum 2016. Search Species Fungorum. Available in http://www.speciesfungorum.org/ (access 23-I-2015).
  » http://www.speciesfungorum.org/
• Sousa, C.D.N. 2014. A percepção da poluição e o impacto sobre os organismos zoospóricos no rio Poti, Teresina- PI. Dissertação de Mestrado, Universidade Federal do Piauí, Teresina.
• Steciow, M.M., Milanez, A.I., Pires-Zottarelli, C.L.A., Marano, A.V., Letcher, P.M. & Vélez, C.G. 2012. Zoosporic true fungi, heterotrophic straminipiles and plasmodiophorids: status of knowledge in South America. Darwiniana 50: 25-32.
• Timon 2012. Lei nº 1.754 de 24 de maio 2012. Estabelece o parque natural municipal lagoa do sambico nesta cidade e dá outras medidas. Available in http://www.meionorte.com/cidades/ma/timon/prefeita-cria-o-parque-natural-municipal-lagoa-do-sambico-211758 (access in 23-I-2015).
  » http://www.meionorte.com/cidades/ma/timon/prefeita-cria-o-parque-natural-municipal-lagoa-do-sambico-211758
• Trindade-Júnior, O.C. 2013. Os riscos sociais e ambientais e a diversidade de fungos zoospóricos em lagoas de Teresina, Piauí. Dissertação de Mestrado, Universidade Federal do Piauí, Teresina.
• Trindade-Júnior, O.C, Rocha, J.R.S. 2013. Brevilegnia linearis Coker (Saprolegniales, Oomycota): um novo registro para o Brasil. Pesquisas, Botânica 64: 341-345.
• Whiffen, A.J. 1942. Two new chytrid genera. Mycologia 34: 543-557.

Publication Dates

• Publication in this collection
  Jul-Sep 2017

History

• Received
  28 Jan 2017
• Accepted
  22 May 2017