Ramalina Lacera (With.) J

n Extending the distribution of Ramalina lacera (With.) J. R. Laundon (Ramalinaceae, lichen forming Ascomycota): First

istributio record from eastern South America D

1* 2 1

raphic , Sionara Eliasaro g

eo Emerson Luiz Gumboski and Rosa Mara Borges da Silveira G n o

1 Universidade Federal do Rio Grande do Sul, Programa de Pós-Graduação em Botânica, Av. Bento Gonçalves, 9500, Agronomia, 91501-970, Porto * CorrAlegrespondinge, RS, Brazil. author. E-mail: [email protected]

otes 2 Universidade Federal do Paraná, Setor de Ciências Biológicas, Departamento de Botânica, 81531-980, Curitiba, PR, Brazil. N

Abstract: The lichen forming fungus Ramalina lacera

is reported for the first time from Brazil. The specimens were collected in the State of Rio Grande do Sul (Southern of Brazil), only on rocks and between 210 m to 350 m altitude. A distribution map, figure and comments on the species are provided.

Ramalina Ach. is a cosmopolitan genus with ca. 150 member of the genus due to the absence of a supportive to 200 species (Kashiwadani and Nash 2004; Sérusiaux hyphal layer called chondroid tissue (Kashiwadani and et al. 2010). Generally the species have a greenish gray Kalb 1993, Kashiwadani and Nash 2004). This layer is to yellowish-green fruticose thallus, always producing present in the majority of species of Ramalina. The species is also unusual within the genus because of the production from solid to hollow, and often produces pseudocyphellae of bourgeanic acid in the medulla (Kashiwadani and Nash (usnice.g. Krogacid. The and branches James 1977; may vary Krog from and flat Østhagen to cylindrical, 1980; 2004), a compound that is rarely produced in Ramalina. Kashiwadani and Kalb 1993). The anatomy of the Although Laundon (1984) considered Ramalina duriaei branches is also variable, which can often present a R. lacera, many authors cortical layer followed by a chondroid tissue and a medulla have continued using the name R. duriaei (e.g. Canaani et (Kashiwadani and Kalb 1993; Kashiwadani and Nash al(De. 1984; Not.) EpsteinBagl. to etbe al a .synonym 1986; Garty of 1987; Lurie and Garty 2004). The ascospores are hyaline, usually 2-celled and 1991; Garty et al. 1993; 1997; Silberstein et al. 1996); varying from ellipsoid to fusiform (e.g. Krog and James thus, most records of R. lacera remain under the synonym. 1977; Kashiwadani and Nash 2004). Ramalina lacera has a broad but somewhat spotted Ramalina lacera (With.) J. R. Laundon is a remarkable distribution (Figure 1). It is known from Europe (e.g. Krog

Figure 1. Worldwide distribution map of Ramalina lacera

(red stars) based on previous publications and the new records. Source: Modified from Software DIVA-GIS, Version 7.5. 195 Gumboski et al. | First record of Ramalina lacera from eastern South America and James 1977; Jatta 1889, 1911; Follmann 1980; Jones 716. 1776. et al. 2001), west of Asia (e.g. Canaani et al. 1984; Epstein et al et1980; al. 2011), Bruyn Africa2000; (Alvareze.g Lectotype (designated by Laundon, 1984): Dillenius . 1986; Sipman 2002; Yazıcı pale(1742: stramineous 163): tab. 21, in fig. herbaria, 57B (OXF). growing from a common . De Notaris 1846; Baglietto 1879;et holdfast,Description: irregularly thallus palmate solid, shrubby, branched, up to dichotomous 6.0 cm tall, Doidgeal. 1994; 1950; Egea Krog 1996; and Aptroot Østhagen 2012), 1980; southwest Follmann andof North Mies 1986; Follmann and Sanchez-Pintoet al1987;. 1972; Van Kashiwadani Haluwyn branches up to 1.3 cm wide and terminal branches up to 1.0in mm narrow wide, branches, 200–500 µm branches thick, surface flatted, weakly bifacial, to clearly main etAmerica al. 1972). (Howe In South 1913; America Rundel it was reported only from northernand Nash Chile2004) (Rundel and Central 1978). America In this (Howestudy, we1913; report Rundel the occurrence of R. lacera laminal,scrobiculate; mainly pseudocyphellae in upper parts very of thallus, rare, orbicular, laminal flat,soralia up Rio Grande do Sul, in two sites located at approximately growingto 0.1 mm mainly in diam.; on topsoralia of the at wrinkle,first marginal soredia then (300–) becoming 400– the same latitude as the in Chileanthe most specimen, southern andstate extending of Brazil, 600 µm in diam. Cortex dirty yellow, continuous, 25–45 its distribution to the east of South America. µm thick, chondroid tissue absent, medulla white, dense, 120–380 µm thick, algal layer almost continuous, 50–60

The study is based on unidentified specimens collected 5.0 mm in diam., without pruina, with marginal to rarely (ICN).by Dr. Mariana They were Fleig examined between 1989 using and standard 1998 housed stereoscopic in the submarginalµm thick. Apothecia soralia, orbicular, up to 0.6 concave mm long. to mainly Epihymenium flat, up to (20–40×)Herbarium and of Universidadelight microscopic Federal (400–1000×) do Rio Grande techniques. do Sul brownish, 10–15 µm thick, hymenium hyaline, 35–40 µm Sections of thallus and apothecia were mounted in water. thick, subhymenium hyaline to weakly grayish, 25–35 µm thick, algal layer under the hymenium present, continuous, 50–55 µm thick; ascospores hyaline, 1-septate, weakly solventChemical system constituents C (Orange were et identifiedal. 2001). by spot tests, under curved to straight, 10–14 × 4–5 µm. Pycnidia not found. UV light and thin layer chromatography (TLC) using Ramalina lacera (With.) J. R. Laundon, Lichenologist 16: 220. 1984. Figure 2 SubstrateSpot tests: and cortex ecology: K-, C-, AccordingKC+ yellow, to UV-; Kashiwadani medulla K-, and C-, Lichen lacerus NashKC-, UV-. (2004) TLC: thisbourgeanic species acid occurs (in medulla) mainly on and branches usnic acid. of

Basionym: With., Bot. Arr. Veg. Gr. Brit.:

Figure 2. Thallus of Ramalina lacera algal layer. The gray central area in the thallus is the dense medulla. (M. Fleig 7247). B. Anatomical section of branches. Black arrows indicate the cortex. White arrows indicate the

196 Gumboski et al. | First record of Ramalina lacera from eastern South America various trees and rarely on rock, and Krog and Østhagen Acknowledgments: We are grateful to the curators of O, UPS and W for (1980) stated it can be corticolous or saxicolous, occurring the loan of the type specimens; to the curator and staff of ICN for all the in rather dry, well lit sites and often in man-made habitats. procedures; to Dr. Adriano Afonso Spielmann (Universidade Federal do reviewMato Grosso and comments; do Sul, Brazil) and to for CAPES providing (Coordenadoria valuable bibliography; de Aperfeiçoamento to MSc. between 210 m to 350 m alt. Manuela Dal-Forno (George Mason University, U.S.A.) for the English The specimens from Brazil wereState growing of Rio only Grande on rocks, do Sul Literaturedo Pessoal do Cited Ensino Superior) for financial support to E. L. Gumboski. Material examined: BRAZIL. , M. Fleig quimiotaxonómico del género Ramalina Ach. (Lecanorales, 3907: Municipality (ICN), ibid of Bagé, Casa deM. Pedra, Fleig 400114 Km (ICN), in parallel ibid., AlvarezAscomycotina) J., G. Paz-Bermúdez en Galicia and(NW M.J.de España). Sánchez-Biezma. Cryptogamie, 2001. Mycologie Estudio road to highway BR 153,M. 210 Fleig m 4144alt., 03.XI.1989(ICN); Municipality 22(4): 271–287. of Caçapava do Sul,., 04.XI.1989, Pedra do Segredo, undisturbed place, Aptroot A. 2012. Lichens of St. Helena. Kew: SCES Publications. 116 pp. Nuovo 350 m alt., 15.XII.1989,M. Fleig 5948 (ICN), ibid., on rock protected by Giornale Botanico Italiano 11: 50–123. M. Fleig 7247 (ICN). Baglietto F. 1879. Lichenes Insulae Sardiniae recensit E. Baglietto. 27.XI.1993, nördlichen Weser-Ems-Gebiet. Oldenburger Jahrbuch 100: 281–318. Additional species examined: Ramalina canariensis Bruyn U. 2000. Zur aktuellen Verbreitung epiphytischer Flechten im shrubs, 300 m alt., 15.IX.1998, Photoacoustic study of the green alga Trebouxia in the lichen J. Bornmüller, Pl. Canar. No. 3500 (W, isolectotype). CanaaniRamalina O., R. duriaei Ronen, in J. vivo. Garty, Photosynthesis D. Cahen, S. MalkinResearch and 5: 297–306. M. Galun. 1984. J. Steiner: GRAN CANARIA, Tafira, 400 m, 22 May 1900, Ramalina mollis Giornale Botanico Italiano 1: 174–224. De Notaris G. 1846. Frammenti lichenografici di un lavoro inedito. 1975, Krog and Østhagen Krog and 1055 Østh.: (O, UPS,THE isotypes).CANARY ISLANDS, Bothalia [Pretoria] 5: 1–1094. Lanzarote, La Geria, ca. 5 Km ENE of Yaiza, 320 m, 13 Apr. Doidge E.M. 1950. The South African fungi and lichens to the end of 1945. Morocco. Bocconea 6: 19–114. Notes: The presence of fertile apothecia (i.e., with Egea J.M. 1996. Catalogue of lichenized and lichenicolous fungi of mature asci and ascospores) in R. lacera is evidently very ethylene in the lichen Ramalina duriaei. Plant Physiology 82: 1122– rare (Krog and James 1977; Krog and Østhagen 1980). In Epstein1125. E., O. Sagee, J.D. Cohen and J. Garty. 1986. Endogenous auxin and Fleig M. 1988. Líquens da Estação Ecológica do Taim, Rio Grande, RS, specimens from Canary Islands, Krog and Østhagen (1980) Napaea 6: 9–16. found apothecia, but without mature ascospores; whereas Follmann, G. 1980. Schedae ad Lichenes Exsiccati Selecti a Museo Brasil. Philippia 4(3): 204–212. Historiae Naturalis Casselensi Editi. XVI Fasiculus. KrogKashiwadani and James and (1977) Nash mentioned (2004) did the not presence find specimens of mature ascosporeswith apothecia in European in the material, Greater Sonorangiving the Desert dimensions Region. as Follmann G. and B. Mies. 1986. ContributionsJournal of to the the Hattori lichen floraBotanical and Laboratorylichen vegetation 61: 499–523. of the Cape Verde Islands. IV. New lichen records and their chorological significance.

10–15According × 3–5 µm. to This the size literature range matches and the our dimensions analyses, Follmann G. and L. Sanchez-Pinto. 1987. Zur Kenntnis der Flechtenflora und FlechtenvegetationCourrier Forschungsinstitut der Kapverdischen Seneckenberg Inseln 95: Ramalinaof the ascospores mollis found is very in Brazilian similar tospecimens. R. lacera in their 175–188.III. Neue Flechtenfunde und ihre Bedeutung fur die Floren- und chemistry, ecological features and overall morphology. GartyVegetationsgeschichte. J. 1987. Metal amounts in the lichen Ramalina duriaei Krog and Østhagen (1980) distinguished from R. lacera power station after 1 year of operation. Environmental (De Research Not.) R. mollis by the presence of soralia and rare presence of 43(1):Bagl. transplanted 104–116. at biomonitoring sites around a new coal-fired apothecia in the former, and by the absence of soralia and to usual presence of apothecia in the latter species. integrity of cell membranes and chlorophyll in the lichen Ramalina Gartyduriaei J., Y. Karary and J. Harel. 1993. The impact of air pollution on the Archives of Environmental Contamination and Toxicology 24(4): 455– molecular studies are needed to clarify the relationships 460. (De Not.) Bagl. transplanted to industrial sites in Israel. betweenBoth are these identical two species in anatomical (i.e., whether features they too, represent however, a Garty J., Y. Cohen, N. Kloog and A. Karnieli. 1997. Effects of air pollution monophyletic group) and whether they represent a pair of concentrations in lichens. Environmental Toxicology and Chemistry monophyletic clades that correspond to the presence and 16(7):on cell 1396–1402.membrane integrity, spectral reflectance and metal and sulfur absence of soralia. While has been reported from Ramalina. Part II. R. lacera The Bryologist 16(6): 81–89. various localities around the world, R. mollis is known JattaHowe A. R.H. 1889. 1913. Monographia North American lichenum Species Italiae of Meridionalis the Genus only from the Canary Islands and parts of Spain (Krog and 261 pp. Østhagen 1980; Stolley and Kappen 2002). Jatta A. 1911. Lichenes. Flora Italica Cryptogama . Trani: V. Vecchi. 4-6: 461–958. According to Kashiwadani and Nash (2004), Ramalina Jones M.P. 1980. Epiphytic macrolichens of , the Firenze, Algarve, Pars Portugal.III, Fasc. lacera might also be confused with R. canariensis Lichenologist 12: 253–275. has monophyllous main laciniae with marginal Ramalina R. lacera Lichenologist 25(1): 1–31. secondary branches, no chondroid tissue, a single-layered. However, Kashiwadani H. and K. Kalb. 1993. TheRamalina genus in Brazil. cortex and produces bourgeanic acid in the medulla. Lichen KashiwadaniFlora of the H. Greaterand T.H. Sonoran Nash. 2004. Desert Region ; pp. 440–455, in: T.H. Whereas R. canariensis has palmately or irregularly Nash, B.D. Ryan, P. Diederich, C. Gries and F. Bungartz. (ed.). branched laciniae, chondroid tissue present, a two-layered , Vol. 2. Tempe: Lichens cortex and produces divaricatic acid in the medulla. Unlimited,genus Ramalina Arizona (Ascomycotina: State University. Ramalinaceae) from South America; As conclusion, considering the previous studies ( , Kashiwadanipp. 335–340 H., T.H. in: Nash I. Kärnefeltand K.H. Moon. and A.2007. Thell Two (ed.). new Lichenologicalspecies of the e.g. Contributions in Honour of David Galloway

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