Rodriguésia 71: e00052019. 2020 http://rodriguesia.jbrj.gov.br DOI: http://dx.doi.org/10.1590/2175-78602020971106
Original Paper Small Parmeliaceae (liquenized Ascomycota) of Ilhabela State Park and nearby areas, São Paulo state, Brazil
Michel Navarro Benatti1,3,4 & Neli Kika Honda2
Abstract A survey of lichens at Ilhabela State Park and nearby areas in São Sebastião Island revealed the occurrence of 12 taxa belonging to six genera of small foliose Parmeliaceae, which are characterized by usually small thalli (hardly > 10 cm in diameter) with narrow lobes or laciniae less than 1 cm wide. Comments are provided for the species registered. Key words: Atlantic rainforest, lichens, mycobiota, restinga wood, São Sebastião Island. Resumo O levantamento de liquens no Parque Estadual de Ilhabela e seus arredores na Ilha de São Sebastião revelou a ocorrência de 10 táxons pertencentes a seis gêneros de pequenas Parmeliaceae foliosas, caracterizadas pelos talos geralmente pequenos (dificilmente > 10 centímetros de diâmetro), com lobos ou lacíneas estreitas de largura inferior a 1 cm. São apresentados comentários para as espécies registradas. Palavras-chave: Mata Atlântica, liquens, micobiota, restinga, Ilha de São Sebastião.
Introduction diversity and distribution of small Parmeliaceae With the 16th longest coastline in the genera like Bulbothrix Hale, Canoparmelia world, the Brazilian Atlantic coastline extends Elix & Hale, Crespoa Lendemer & Hodkinson, over nearly 7.5 thousand kilometers, comprising Hypotrachyna (Vain.) Hale, Parmelinopsis Elix many geographical features, including beaches, & Hale, Parmelinella Elix & Hale, and Relicina bays, reefs, and islands (CIA 2017). The Atlantic (Hale & Kurok.) Hale (e.g., Benatti 2011, 2012a-h, Rainforest represents the major vegetation type 2013a-c, 2014a-c; Benatti & Elix 2012; Benatti & found in many coastal areas, including the islands. Lendemer 2014; Benatti & Marcelli 2007; Benatti The diversity of lichens still remains poorly et al. 2008; Canêz et al. 2009; Gerlach & Eliasaro investigated in most coastal formations, such as 2012, 2014; Jungbluth et al. 2008; Marcelli & restinga woods, mangroves, and rocky shores. Canêz 2008; Marcelli et al. 2007, 2011; Spielmann Parmeliaceae is the most representative & Marcelli 2008a,b). The small Parmeliaceae family in Brazilian biomes with regard to the comprises species easily recognizable by their diversity of genera and species (Marcelli 1998). small thalli (usually < 10 cm diameter) with narrow During the past two decades, it has been the lobes or laciniae (often < 1 cm wide). focus of Brazilian researchers, who showed the Recently, a survey of foliose lichens in occurrence of hundreds of species, including Cananéia, Cardoso, Comprida, and Ilhabela new records and new species. Several recent Islands (23°45’40”S, 45°24’44”W), São Paulo surveys have significantly contributed to the state, reported 16 species of Leptogium (Kitaura
1 Instituto de Botânica, Núcleo de Pesquisa em Micologia, C.P. 3005, 01061-970, São Paulo, SP, Brasil. 2 Universidade Federal de Mato Grosso do Sul - UFMS, Inst. Química, Av. Sen. Filinto Müller 1555, 79074-460, Campo Grande, MS, Brasil. 3 ORCID:
Material and Methods Species registered Specimens of small foliose Parmeliaceae 1. Bulbothrix ventricosa (Hale & Kurok.) Hale. were collected at Ilhabela (23°45’36”S, Phytologia 28(5): 481. 1974. MB 341620. 45°24’36”W) State Park, São Paulo state, Brazil, Parmelia isidiza var. domingensis Vain., during several field expeditions from 2012 to Annales Academiae Scientarum Fennicae 6A(7): 2013. Vegetational types include mostly Atlantic 17. 1915. Rainforest, with Restinga Wood along the Eastern Species description: Hale (1976b); Benatti Coast. Accordingly to the climate classification of (2012d). Köppen-Geiger, the island is classified as Tropical Specimens examined: Ilhabela, Parque Estadual de Aw. The altitude ranges from sea level up to almost Ilhabela, Ilha de São Sebastião, Cachoeira da Toca 1400 m. The methodology used for the collection old farm, 23º47’S, 45º21’W, 6.XII.2012, leg., M.N. Benatti et al. 3412, 3413, 3418; Cocaia track, entrance and study of lichenized fungi is described in Fink to Costabela, 15.V.2013, leg., M.N. Benatti et al. 3533. (1905), Hale (1979, 1987), Malcolm & Galloway This is one of the most common species of (1997) and Benatti & Marcelli (2007). Collected Bulbothrix in several Brazilian vegetation types specimens were observed under an Eikonal (Benatti 2012d). It is mainly recognized by its EK3ST stereomicroscope and Motic TYPE 102M larger lobed aspect (with rounded and broad lobes, microscope and the macroscopic and microscopic often between 1 and 5 mm wide) compared to other characteristics of somatic and reproductive Bulbothrix species, its distinct bulbate cilia with structures of the thalli were analyzed. Identification simple apices, the varied (often mottled) coloration was performed by comparison of published of the lower cortex and the presence of medullary descriptions of specimens from different locations. norstictic acid (the latter two characteristics also Chemical tests consisted in spot tests, UV light common to the non-isidiate B. viatica Spielmann exposure (360 nm), microcrystal tests and Thin & Marcelli). Our specimens were poorly developed Layer Chromatography (TLC) in the following with 2 to 3 cm in diameter (with the exception of a eluents: (I) toluene: ethyl acetate: acetic acid single larger, 6 cm-wide thallus), and the presence 6:4:1 v/v/v and (II) toluene: acetic acid 85:15 v/v, of laciniae of often small width (only a few > 3 following the methodology described in Asahina mm wide). The laminal ciliar bulbs were scarce & Shibata (1954), Walker & James (1980), White to common, and most specimens showed darkly & James (1985), Huneck & Yoshimura (1996) and mottled lower cortices, with a predominance of Orange et al. (2001). All collected specimens were dark brown and black shades. All specimens have deposited at SP herbarium. plenty of isidia, although no apotheciate material was found. The presence of atranorin and norstictic Results and Discussion acids were confirmed by TLC. Thirty specimens of small Parmeliaceae were studied. We identified ten species belonging 2. Canoparmelia caroliniana (Nyl.) Elix & Hale. to Bulbothrix Hale (one species), Canoparmelia Mycotaxon 27: 278. 1986. MB 128704. Elix & Hale (two), Crespoa Lendemer & Parmelia caroliniana Nylander, Flora 68: Hodkinson (one), Parmelinella Elix & Hale 614. 1885. (two), Parmelinopsis Elix & Hale (three) and Species description: Benatti (2014c). Remototrachyna Divakar & Crespo (one), which Specimens examined: Ilhabela, Ilhabela State Park, Ilha are commented below. de São Sebastião, Cocaia track, entrance to Costabela, Due to the presence of a constantly dense 23º47’S, 45º21’W, 15.V.2013, leg., M.N. Benatti, L.B. ombrophilous forest, it was difficult to find thalli Moro & C. Mayumi 3532, 3538, 3555, 3357. that were mature or not damaged by chlorosis or The isidiate C. caroliniana together with necrosis. Even with a high search effort, almost all the sorediate C. texana (Tuck.) Elix & Hale are thalli in the study area were found in small open among the most common Canoparmelia species
Rodriguésia 71: e00052019. 2020 Small Parmeliaceae from Ilhabela (Brazil) 3 de 7 found in Brazil, even in urbanized or other types the specimens found by Jungbluth (2006), our of anthropized areas. Interestingly, the specimen specimens did not have ascomata or pycnidia. M.N. Benatti et al. 3357 presented a more accentuate medullary reaction to spot tests (almost 4. Crespoa cf. scrobicularis (Kremp.) Benatti & as reddish as expected for C. sanguinea Marcelli, Lendemer, Brittonia 66: 288. 2014. MB 802265. Benatti & Elix) but TLC confirmed traces of Parmelia scrobicularis Kremp., perlatolic acid derivatives. Although confirmed by Videnskabelige Meddelelser Naturhistorik TLC, the perlatolic acid was not clearly evidenced Forening Kjöbenhavn 25: 10. 1873. due to the low concentration found. This might due Species description: Benatti & Lendemer to the contact with other species that are growing (2014). on the same substrate and have similar compounds Specimens examined: Ilhabela, Ilhabela State Park, which could have been leached by rainfall. The southern part of the island, 27.VI.2012, 23º47’S, atranorin and chloroatranorin acids might have 45º21’W, leg., M.N. Benatti, L. Moro & M. Boro 3335. occurred at low concentrations or even been We collected a single specimen that was absent in our material, as they were not detected growing together with a specimen of Heterodermia on the plates. sp. This species is characterized by the scrobiculate thallus. Atranorin, stictic and constictic acids 3. Canoparmelia cryptochlorophaea (Hale) Elix were confirmed by TLC and menegaziaic acid & Hale. Mycotaxon 27: 278. 1986. MB 128708. was not present. An unidentified substance with Parmelia cryptochlorophaea Hale, The Rf close to 43 was found solely in eluent I, but it Bryologist 62: 18. 1959. could not be determined. As the specimen of C. Species description: Hale (1976a, as scorbicularis was growing together with a species Pseudoparmelia cryptochlorophaea). of Heterodermia, the substance might have leached Specimens examined: Ilhabela, Ilhabela State Park, from the later to our specimen. The thallus did not track close to the meteorological station near the lookout, produce apothecia, pycnidia, soredia or isidia, as 23º47’S, 45º21’W, 4.IX.2012, leg., M.N. Benatti et in the case of several other specimens found in the al. 3370; municipal plant nursery Cachoeira da Água study area and as the propagule-producing species Branca, 23º47’S, 45º21’W, 6.XII.2012, leg., M.N. C. crozalsiana (B. de Lesd. ex Harm.) Lendemer & Benatti et al. 3425; SABESP area, southern part of the Hodk. and C. carneopruinata (Zahlbr.) Lendemer island, Bairro Bixiga, 23º47’S, 45º21’W, 06.XII.2012, & Hodk. Therefore, it could only be identified leg., M.N. Benatti et al. 3456 (p.min.p.); Bairro da as Crespoa cf. scrobicularis, which has been Feiticeira, 23º47’S, 45º21’W, 6.XII.2012, leg., M.N. previously reported for other areas in the state of Benatti et al. 3461. São Paulo (Jungbluth 2006; Benatti 2014b). This species was cited for the first time for the state of São Paulo by Jungbluth (2006), who 5. Parmelinella cinerascens (Lynge) Benatti & collected specimens at several spots of Cerrado Marcelli. Opuscula Philolichenum 11: 27. 2012. vegetation in the interior of the state. This is MB 563647. the first record for coastal areas. The presence Parmelia cinerascens Lynge, Arkiv før of capitate and raised marginal soralia and the Botanik 13 (13): 104. 1914. medullary reaction to spot tests (K+ faintly rose Species description: Benatti (2012h). and KC+ purple rose) are characteristic of this Specimens examined: Ilhabela, Ilhabela State Park, species. The KC reaction for the specimen M.N. Cocaia track, entrance to Costabela, 15.V.2013, 23º47’S, Benatti 3370 gave a more purple-reddish tone. 45º21’W, leg., M.N. Benatti, I.H. Schoenlein-Crusius & The presence of cryptochlorophaeic acid was C. Mayumi 3548. confirmed, although atranorin might have occurred We found only a single specimen at the study at low concentrations as it was not detected in area. This species is easy recognizable due to the the TLC plate. We examined several specimens presence of small lobes, axillary or marginally of different species from the study area that sparse cilia that are very short and simple, a black presented low concentrations of atranorin, which lower cortex and medullary salazinic acid. It is has a solar light filter function, and interestingly, similar to Parmelinella salacinifera, from which all these specimens were collected from relatively it differs by the paler and brown lower cortex, and shaded places and reacted to K spot tests, showing the scarce to absent simple cilia. This material the presence, albeit weak, of the substance. Like was one of the few well-developed thalli of small
Rodriguésia 71: e00052019. 2020 4 de 7 Benatti MN & Honda NK Parmeliaceae found (approximately 8 cm wide), with Rf 43 in the eluent 2. According to literature very isidiate and with a single, relatively mature and simultaneous experiments, this substance apothecium. The hymenia, however, did not present might be 2,4-di-O-metilgiroforic acid, also found asci with mature ascospores. by Jungbluth (2006) for P. damaziana growing on Cerrado vegetation. Besides the perceptible but 6. Parmelinella salacinifera (Hale) Marcelli & evanescent medullary reaction KC+ reddish-rose, Benatti. Mycosphere 5: 780. 2014. MB 810474. other components, even possibly giroforic acid, Parmelia salacinifera Hale. Contributions were at too low concentrations in the extract to from the U.S. National. Herbarium 36: 157. 1964. be detected. Species description: Benatti (2014a). Specimens examined: Ilhabela, Ilhabela State Park, 8. Parmelinopsis cf. minarum (Vain.) Elix & Hale. Cocaia track, entrance to Costabela, 15.V.2013, 23º47’S, Mycotaxon 29: 243. 1987. MB 130590. 45º21’W, leg., M.N. Benatti, I.H. Schoenlein-Crusius & Parmelia minarum Vain., Acta Societatis pro C. Mayumi 3540. Fauna et Flora Fennica 7: 48. 1890. This isidiate species is similar to P. Species description: Benatti (2012e). cinerascens, but is promptly identified by its Specimens examined: Ilhabela, Parque Estadual de pale brown lower cortex and the very scarce to Ilhabela, track close to the meteorological station near absent marginal or axillary simple short cilia. It the lookout, 4.IX.2012, 23º47’S, 45º21’W, leg., M.N. also presented medullary salazinic acid, which is Benatti, L. Moro, M. Boro & C. Mayumi 3358, 3368, common for Parmelinella spp. We were not able 3371; Municipal plant nursery Cachoeira da Água to elucidate if all specimens identified under this Branca, 6.XII.2012, 23º47’S, 45º21’W, leg., M.N. Benatti, L. Moro & C. Mayumi 3447; eastern part of name belong to a single species, although they are the island, around Praia de Castelhanos and restinga overall nearly identical in morphology, anatomy with houses, 14.V.2013, 23º47’S, 45º21’W, leg., M.N. and chemistry to all specimens described in Benatti Benatti, H. Schoenlein-Crusius, L. Moro & C. Mayumi (2014a). The only difference found was regarding 3500, 3509; Cocaia track, road to Costabela, 15.V.2013, the frequency of the tiny marginal cilia, with 23º47’S, 45º21’W, leg., M.N. Benatti, I.H. Schoenlein- specimens completely eciliate, with a few cilia, Crusius & C. Mayumi 3556. to some with cilia in a few parts of their marginal This species, together with P. spumosa, are area (Benatti 2014a). As in the case of most species one of the most common small Parmeliaceae found registered in the present study, we only found one at the study area. It is easily recognizable in the specimen. field due its narrow and short laciniate thallus and the isidiate upper cortex. Most specimens collected, 7. Parmelinopsis damaziana (Zahlb.) Elix & Hale. however, consisted of very small thalli of less than Mycotaxon 29: 242. 1987. MB 130583. 4 cm wide, except for a single one of approximately Parmelia damaziana Zahlbr. Bulletin de 7 cm wide. The chromatographic analysis showed l´Herbier Boissier 5: 541. 1905. a few differences between specimens. Atranorin Species description: Hale (1976c) was overall present but some specimens presented Specimens examined: Ilhabela, Ilhabela State Park, three medullary compounds while others had two track close to the meteorological station near the lookout, substances of the gyrophoric tridepsides group. 04.IX.2012, 23º47’S, 45º21’W, leg., M.N. Benatti, L. Analysis by microcrystalization did not show the Moro, M. Boro & C. Mayumi 3365. presence of gyrophoric acid. We were not able to The only specimen collected was fertile with compare the chromatographic behaviour due to the plenty of mature apothecia. This species commonly absence of data in the literature, but it appears to be present hyaline, simple, ellipsoid to subglobose related to the P. horrescens complex. In this study, ascospores that measure (8–)10–15(–16) × 8–12 we found only one specimen (M.N. Benatti et al. µm, and does not produce neither soredia nor 3368) that had mature apothecia but unfortunately, isidia. Its morphological and chemical varieties are the hymenium was damaged. The specimens discussed in detail by Jungbluth (2006), but overall M.N. Benatti et al. 3500 and 3368 both showed a the single specimen examined herein was similar similar chromatographical profile. The collection to those described by this author for Cerrado areas of more specimens and the use of other analytical of São Paulo state. The chromatographic analysis techniques such as Liquid Chromatography-Mass showed the presence of atranorin and also of an Spectrometry (LC-MS) are needed for a conclusive unidentified substance (with a well-marked spot) characterization of these substances.
Rodriguésia 71: e00052019. 2020 Small Parmeliaceae from Ilhabela (Brazil) 5 de 7 9. Parmelinopsis spumosa (Asahina) Elix & Hale. Species description: Spielmann & Marcelli Mycotaxon 29: 243. 1987. MB 130596. (2008b). Parmelia spumosa Asahina, Journal of Specimens examined: Ilhabela, Ilhabela State Park, Japanese Botany 26: 259. 1951. southern part of the island, 27.VI.2012, 23º53’S, Species description: Benatti (2012e). 45º25’W, leg., M.N. Benatti, L. Moro & M. Boro 3336; Specimens examined: Ilhabela, Ilhabela State Park, Cachoeira da Toca old farm, 6.XII.2012, 23º47’S, track close to the meteorological station near the lookout, 45º21’W, leg., M.N. Benatti, L. Moro & C. Mayumi 3408; 4.IX.2012, 23º47’S, 45º21’W, leg., M.N. Benatti, L. Cocaia rack, road to Costabela, 15.V.2013, 23º47’S, Moro, M. Boro & C. Mayumi 3354, 3355, 3359, 3360, 45º21’W, leg., M.N. Benatti, I.H. Schoenlein-Crusius & 3372. C. Mayumi 3531. This species is easily recognizable by its This species was the only Parmeliaceae with eciliate thallus with coarse sorediate bursting dichotomously branched rhizines (previously in pustules, differing from similar species such as Hypotrachyna before recent studies confirmed P. subfatiscens, which is also eciliate but has non that a group of species comprised another genus) sorediate pustules. The chromatographical analysis found at the study area. It presented relatively large showed some differences between specimens. All laciniae (up to 5 mm wide, i.e. broader and more specimens examined contained atranorin but most rotund than in other species of Parmelinopsis) and had at least three other medullary compounds abundant isidia. Atranorin and chloroatranorin were (some specimens contained two compounds). not detected by chromatography, possibly due to The low production of some substances and the their low concentrations in the specimens (as the leeching of other substances from other lichens K+ yellow reaction occurred in the spot tests). present on the same substrate could justify these The chromatography showed also three spots (Rfs discrepancies. Using microcrystalization, only around 35, 40 and 45 in eluent I) that we were not one thalli clearly showed presence of gyrophoric able to identify. The chemistry variability is yet acid. Other compounds could not be determined, not fully comprehended (e.g., Nash et al. 2002; as documented by Jungbluth (2006) for specimens Louwhoff & Elix 2002; Jungbluth 2006) but this from Cerrado. The specimens M.N. Benatti is currently the only known isidiate species with et al. 3360 and 3289 were partially different dichotomously branched rhizines that show no chromatographically. The specimen M.N. Benatti medullary reaction to any spot tests (K, C, KC, et al. 3360 showed presence of three tridepsides and P). together with atranorin, whereas the specimen M.N. The specimens M.N. Benatti et al. 3531 and Benatti et al. 3289 showed only two tridepsides 3336 were slightly different chromatographically, with atranorin. Besides this difference, we were not but both contained atranorin. The spots revealed able to make further identifications of substances with the p-anisaldehyde: sulfuric acid indicated using microcrystalization. that the substances might belong to the class The substances present in the specimens of of terpenes, since fatty acids are not revealed both P. minarum and P. spumosa were tridepsides with this substance. Microcrystalization also did derived from orcinol (e.g., Hüneck & Yoshimura not show the presence of fatty acids, including 1996). However, the chromatographical profiles protoliquesterinic and caperatic acids. Constipatic and microcrystalization tests did not show the acid is very difficult to detect with this technique. presence of gyrophoric acid (although they reacted Flakus et al. (2011) reported the presence of C+ and KC+ rose- reddish, as expected for this atranorin, constipatic acid complex (±, only very substance in spot tests), even with the eluents rarely absent) and an unidentified pigment (±, only tested (I and II) and microcrystal preparations. in one specimen). Our results are in agreement Again, most specimens were quite small with a with the substances reported by Flakus et al. few centimetres wide and therefore, they could (2011) in Bolivian specimens. It is possible that not be used for further tests without destroying the some of the specimens collected in South America whole specimens. and identified as R. costaricensis could represent chemotypes, since it is still premature to confirm 10. Remototrachyna cf. costaricensis (Nyl.) that they belong to different species. Divakar & Crespo. Taxon 97: 586. 2010. MB Aside from our work on the genus Leptogium 546535. (Kitaura et al. 2017) there are no other inventories Parmelia costaricensis Nyl. Journal of of lichens in the study area. Therefore, this study Botany British and Foreign 13: 225.1877. adds new and further information to the diversity of
Rodriguésia 71: e00052019. 2020 6 de 7 Benatti MN & Honda NK the local mycobiota. In addition, it represents one of Benatti MN (2014a) An update on the genus Parmelinella the few surveys (e.g., Benatti 2012b,d) performed Elix & Hale (Parmeliaceae, lichenized ascomycetes). hitherto in areas of the Atlantic Rainforest. Mycosphere 5: 770-789. Benatti MN (2014b) Pequenas espécies de Parmeliaceae (Ascomycota) eciliadas no Parque Estadual da Acknowledgements Cantareira, estado de São Paulo, Brasil: gêneros We are indebted to the reviewers for Canoparmelia e Crespoa. Rodriguésia 65: 587-597. their valuable contribution, which contributed Benatti MN & Elix JA (2012) The true identity significantly to the improvement of this final of Bulbothrix goebelii (Zenker) Hale and the version. reestablishment of some of its synonyms as accepted species. The Lichenologist 44: 813-826. References Benatti MN & Lendemer JC (2014) Canoparmelia scrobicularis belongs to the genus Crespoa Asahina Y & Shibata S (1954) Chemistry of Lichen (Parmeliaceae, lichenized Ascomycota). Brittonia Substances. Japan Society for the Promotion of 66: 287-291. Science, Tokyo. 239p. Benatti MN & Marcelli MP (2007) Gêneros de fungos Benatti MN (2011) A simple clearing technique to aid in liquenizados dos manguezais do sul-sudeste do the recognition of cilia and rhizinae structure in the Brasil, com enfoque no manguezal do Rio Itanhaém, Parmeliaceae. Opuscula Philolichenum 9: 21-25. estado de São Paulo. Acta Botanica Brasilica 21: Benatti MN (2012a) Pequenas espécies de Parmeliaceae 863-878. ciliadas no Parque Estadual da Cantareira, estado de Benatti MN, Marcelli MP & Elix JA (2008) Canoparmelia São Paulo, Brasil: gêneros Bulbothrix, Parmelinella sanguinea, a new Parmeliaceae from Brazil. e Parmelinopsis (Parmeliaceae, Ascomycota). Mycotaxon 106: 435-439. Hoehnea 39: 207-218. Canêz LS, Marcelli MP & Elix JA (2009) New Brazilian Benatti MN (2012b) New species of Bulbothrix Hale species of Canoparmelia with medullary olivetoric, containing gyrophoric acid from Brazil. Mycology anziaic, and sekikaic complexes. Mycotaxon 110: 3: 127-131. Benatti MN (2012c) Three resurrected species of the 465-472. genus Bulbothrix Hale (Parmeliaceae, Lichenized CIA - Central Intelligence Agency (2017) “Coastline.” Fungi). Mycosphere 3: 46-55. cia.gov. Central Intelligence Agency. Available Benatti MN (2012d) A review of the genus Bulbothrix at
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Area Editor: Dr. Mauricio Salazar-Yepes Received in January 09, 2019. Accepted in June 10, 2019. This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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