versión On-line ISSN 1852-5962
Kurtziana vol.37 no.1 Córdoba ene./jun. 2012
Clavulina amazonensis, an Amazonian fungus discovered in the Atlantic Forest
Universidade Federal de Pernambuco, Departamento de Micologia, Av. Prof. Nelson Chaves, s/n° CEP: 50670-901, Recife, PE, BRAZIL. Current address: Universidade Federal da Paraíba, Departamento de Sistemática e Ecologia, CEP: 58051-970, João Pessoa, PB, BRAZIL. E-mail: email@example.com
Clavulina amazonensis is reported for the first time in the Atlantic Forest of Northeastern Brazil from herbarium material. C. amazonensis is characterized by branched basidiomes with, hymenium, small subglobose basidiospores, frequency of three sterigmata per basidia and context bearing orange-brown hyphae. Description, drawings, and discussion on its biogeography are provided here.
Key words: Cantharellaceae; Clavulinaceae; Neotropical; Brazil.
Clavulina amazonensis, un hongo amazónico descubierto en la Mata Atlántica
Se reporta Clavulina amazonensis por primera vez para la Selva Atlántica del Nordeste de Brasil con base en material de herbario. La especie se caracteriza por basidiosporas subglobosas pequeñas, basidios con dos a tries esterigmas cornudos y contexto con hifas marrón anaranjadas. Se presenta descripción, ilustraciones y una discusión sobre su distribución.
Palabras clave: Cantharellaceae; Clavulinaceae; Neotropical; Brasil.
Clavulina J. Schröt. (Cantharellales) is a clavariod genus easily segregated by its pale, smooth basidiospores and mostly two cornute sterigmate basidia (Corner 1950). Recent studies indicated this genus as one of the conspicuous ectomycorrhizal fungi in the tropical zones of the Neotropical (Thaker & Henkel 2004, Henkel et al. 2005, 2011). From the Amazonas State, Corner (1950) reported four species: C. connata (Berk.) Corner, C. delicia (Berk.) Corner, C. panurensis (Berk.) Corner and C. sprucei (Berk.) Corner. Later, Corner (1970) described C. amazonensis Corner from Manaus in the same state. More recently Gomes-Silva & Gibertoni (2009) reported C. cirrhata (Berk.) Corner from the Amazonas State. From the northeastern Brazilian state of Pernambuco, only C. incrustata Wartchow is known (Wartchow 2012).
The Atlantic Forest is treated as one of the worldwide hotspots for conservation and is drastically reduced to several small fragments since beginning of the colonization of Brazil by the Portuguese in 1500 A.D. (Kimmel et al. 2008). The"Refúgio Ecológico Charles Darwin" (07º48'37"-07º49'02" S and 34º27'25"-34º56'52"W), where an exsiccatum identified as Clavulina vinaceocervina (Cleland) Corner was collected, is a 60 ha protected private area located at the municipality of Igarassu, in the State of Pernambuco, Northeast Brazil (Costa- Lima 1998), and correspond to an Atlantic Forest fragment with an arborous stratum of about 8 to 15 m (Santiago & Barros 2003), surrounded by agricultural areas. Alves-Araújo et al. (2008) reported from Atlantic Forest of Pernambuco about 650 species of angiosperms, including taxa of Leguminosae (including Caesalpinoideae), Euphorbiaceae, Nyctaginaceae and Polygonaceae, groups with ectomycorrhizal trees genera (Smith & Read 2008).
I refer here a new and interesting report of Clavulina from Atlantic Forest of the State of Pernambuco Northeast Brazil, based on herbarium material, and discussion about the distribution of that fungus in the Neotropical zone.
Material and Methods
The description of the macroscopic characters was realized from dry material (exsiccatum). Basidiospores description follows the methodology proposed by Tulloss et al. (1992), but utilizing a single basidiome Wartchow (2009). Twenty five basidiospores were measured for statistics. Abbreviations include L (W) = basidiospore length (width) average from a single basidiome, Q = the length: width ratio range as determined from all measured basidiospores, and Q = the Q value averaged from all basidiospores measured within a single basidiome. Color code follows Online Auction Color - OAC (2004).
The exsiccatum examined is deposited at Herbarium Camille Torrend (URM) of the Department of Mycology of the Universidade Federal de Pernambuco (Thiers 2011).
Figs. 1-2. Clavulina amazonensis. 1. Basidiospores. 2. Basidia. Scale bar is 10 µm.
Fig. 3. Clavulina amazonensis. Basidiomes. Scale bar is 10 mm.
Basidiomes gregarious, 20-45 mm high and 18 mm wide, with stipes of some individuals with an apparent caespitose habit with fused stipes; tough consistency in dried state; dichotomously branched, on which the main axis begin to branch and from that arise two or three short branches; tips acute, sometimes with small spurs, only occasionally flabellate. Hymenium cream (OAC 814-815) to brownish orange (OAC 713), ochraceous brown (OAC 713) at the tips. Stipe 3-8 × 1-2.5 mm, cream (OAC 814) to ochraceous brown (OAC 713); more or less cylindric in cross section, smooth, glabrous. Odor not distinguished.
Basidiospores (5.5-) 5.8-7.2 × (5-) 5.5-6.5 µm, L = 6.5 µm; W = 6 µm, Q = 1.00-1.22 (-1.24), Q = 1.09, globose to subglobose then sometimes broadly ellipsoid, hyaline, thin walled; presenting a large guttule; hilar appendix sublateral or subapical, rounded-obtuse. Basidia 43-51 × 6.5-7 µm (measured at apex), clavate-elongated, with two or three cornuted sterigmata to 5 µm high; thick walled up to 1 µm, clampless. Basidioles slender clavate, widespread among basidia. Subh ymenium up to 100 µm thick composed of slender, colorless thin walled hyphae up to 5 µm wide. Hymenial trama hyphae 2-6 µm wide, interwoven, wall up to 1 µm thick, orange brown in 3% KOH, individually slightly paler; inflated hyphae absent. Clamp connections absent to very rare (only two observed).
Material examined: BRAZIL. Pernambuco. Mun. Igarassu: Refúgio Ecológico Charles Darwin, J. Kimbrough s.n.,V-1995 (URM 75693, as C. vinaceocervina).
Distribution: Neotropical. In the Amazonian Forest in Brazil, State of Amazonas (Corner 1970) and Venezuela (Petersen 1988), and Guyana (Henkel et al. 2011). This is the first record from Atlantic Forest of Pernambuco, Northeast Brazil.
Remarks: Clavulina amazonensis, is a unusual member of Clavulina due its somewhat frequent 3-spored (rather than exclusively 2-spored) and mostly thick-walled basidia, and brownish ferruginous hymenial context. However, the hyaline subglobose basidiospores plus the cornuted sterigmata fit these specimens in this genus (Corner 1970, Petersen 1988, Henkel et al. 2011). Clavulina vinaceocervina, the name which this exsiccate was identified, is an Australian clampless taxon segregate due the irregular branches mostly as short prongs, irregular apices, presence of cystidia in the hymenium and larger basidiospores measuring 7.8-10 × 6.1-9.1 µm (Petersen 1984).
The distribution pattern of C. amazonensis was estimated after Corner (1970) discovery in Manaus, Amazonas State, North Brazil. Petersen (1988) recorded it as far north as Venezuela. More recently, Henkel et al. (2011) recorded it as an abundant fruiter in the Pakaraima Mountains in Guyana, mostly under Dicymbe and Aldinia spp., and estimated a triangular area of distribution of C. amazonensis linking the type locality in Manaus, Venezuela and Guyana. My finding now represent the eastern distribution for C. amazonensis, 3000 km from the type locality, and reinforce the idea suggested by Henkel et al. (2011) about a putative widespread association of C. amazonensis with diverse host plants over a broad area in the South American tropics, with the Leguminosae genera Dicymbe and Aldinia in Guyana for example. Based on molecular identification of fungal mantle using Blast on GenBank website, clavulinas were also reported as fungal partner of Pakaraimea diperocarpaceae in Venezuela (Moyersoen 2006), and Coccoloba, Guapira and Neea in Ecuadorian Amazon (Tedersoo et al. 2010).
In Northeastern Brazil, Ducke (1953) and Andrade-Lima (1966) already observed the simultaneous occurrence of some leguminous species trees belonging to all subfamilies in both the Amazon and Atlantic Forests of Pernambuco and Paraíba. In addition, recent studies suggest that the center of endemism of the Atlantic Forest located in Pernambuco is floristically more related to the Amazon than to the rest of Atlantic Forest (Melo-Santos et al. 2007). Within the fungi, the putative ectomycorrhizal species Amanita crebresulcata Bas occurs simultaneously in the Amazon and Atlantic Forests in Northeastern Brazil (Wartchow & Maia 2007). In the Atlantic Forest of State of São Paulo, in Southeast Brazil, another Amazonian taxon was found, A. coacta Bas (Menolli et al. 2008). Recently, Vellinga et al. (2009) affirmed that introduced ectomycorrhizal fungi accompanying their respective introduced tree hosts (mostly Pinus and Eucalyptus). If ectomycorrhizal putative entities occur simultaneously in Amazon and Atlantic Forests, as well as floristic evidences linking both biogeographic areas, we can hypothesized that some ectomycorrhizal fungi (including the one studied here) might have a pattern of distribution accompanying their tree hosts.
Other organisms also present similar distribution patterns to those shown above. Costa (2003) observed that rodents and marsupial distribution was influenced by central Brazilian forests connections. These forests, Cerrado and Caatinga suffered influence during glacial ages in the Quaternary, when retreat of the glacial resulted wet periods, that promoted expansion of the wet forests (i.e. Atlantic and Amazon) and subsequent bridge linking both (Bigarella et al. 1975, Oliveira et al. 2000, Wang et al. 2004).
This study on the distributional pattern of C. amazoniensis provides additional evidence of the value of fungal herbarium data. In another study Wollan et al. (2008) also predicted that Northern Europe fleshy fungi distribution also can be inferred by herbarium data.
To Dr. M. Cathie Aime for her kind presubmission review, Dr. Leonor C. Maia for providing the specimen of C. amazonensis, to Victor R.M. Coimbra for contributing with the line drawings, and FACEPE (BFP Proc. 0100- 2.03/09) for providing post-doctoral funding.
1. Alves-Araújo, A., D. Araújo, J. Marques, A. Melo, J. R. Maciel, J. Uirapuã, T. Pontes, M. F. A. Lucena, A. L. DuBocage & M. Alves 2008. Diversity of Angiosperms in fragments of Atlantic Forest in the State of Pernambuco, Northeastern Brazil. Bioremed., Biodiv. and Bioavailab. 2: 14-26. [ Links ]
2. Andrade-Lima, D. 1966. Contribuição ao paralelismo da flora Amazônico-Nordestina. Bol. Téc. Inst. Pesq. Agronôm. Pernambuco 19: 1-30. [ Links ]
3. Bigarella, J. J., D. Andrade-Lima & P. J. Riehs. 1975. Considerações a respeito das mudanças paleoambientais na distribuição de algumas espécies vegetais e animais no Brasil. An. Acad. Bras. Ciênc. 47 (Suplemento): 411-467. [ Links ]
4. Corner, E. J. H. 1950. A Monograph of Clavaria and Allied Genera. Oxford University Press, London. [ Links ]
5. Corner, E. J. H. 1970. Supplement to"A monograph of Clavaria and allied genera. Beih. Nova Hedw. 33: 1-299. [ Links ]
6. Costa, L. P. 2003. The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J. Biogeogr. 30: 71-86. [ Links ]
7. Costa-Lima, M. L. F. 1998. A Reserva da Biosfera da Biosfera da Mata Atlântica em Pernambuco: Situação Atual, Ações e Perspectivas. Série Cadernos da Reserva da Biosfera nº 12, São Paulo. [ Links ]
8. Ducke, A. 1953. As leguminosas de Pernambuco e Paraíba. Mem. Inst. Oswaldo Cruz 5: 417-461. [ Links ]
9. Gomes-Silva, A.C. & T. B. Gibertoni. 2009. Revisão do Herbário URM. Novas Ocorrências de Aphyllophorales para a Amazônia brasileira. Rev. Bras. Bot. 32:587-596. [ Links ]
10. Henkel, T. W, M. C. Aime, J. K. Uehling & M.E. Smith. 2011. New species and distribution records of Clavulina (Cantharellales, Basidiomycota) from the Guyana Shield. Mycologia 103: 883-894. [ Links ]
11. Kimmel, T., D. Piechowski & G. Gottsberger 2008. The history of fragmentation of the lowland Atlantic Forest of Pernambuco, Brazil. Bioremed., Biodiv., Bioavailab 2: 1-4. [ Links ]
12. Melo-Santos, A. M., D. R. Cavalcanti, J. M. C. Silva & M. Tabarelli. 2007. Biogeographical reationships in north-eastern Brazil. J. Biogeogr. 34: 437-446. [ Links ]
13. Menolli Jr., N., T. Asai & M. Capelari. 2009. Amanita coacta (Amanitaceae, Agaricales) with a key to Amanita species occuring in Brazil. Mycotaxon 107: 419-430. [ Links ]
14. Moyersoen, B. 2006. Pakaraimea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytol. 172: 753-762. [ Links ]
15. Oliveira, P. E., A. M. Franca- Barreto & K. Suguio. 1999. Late Pleistocene/Holocene climatic and vegetational history of the Brazilian caatinga: the fossil dunes of the middle São Francisco River. Palaeogeogr. Palaeoclimatol. Palaeoecol. 152: 319-337. [ Links ]
16. Online Auction Color. 2004. Online Auction Color Chart. Online Auction Color Chart Co., Stanford [ Links ]
17. Petersen, R.H. 1984. Notes on clavarioid fungi. XVIII. A preliminary outline of Clavulina in southeastern Australia. Nova Hedwigia 37: 19-35. [ Links ]
18. Petersen R.H. 1988. Notes on clavarioid fungi. XXII. Three interesting South American collections. Mycologia 80: 571-576. [ Links ]
19. Santiago, A. C. P. & I. C. L. Barros 2003. Pteridoflora do Refúgio Ecológico Charles Darwin (Igarassu, Pernambuco, Brazil). Acta Bot. Bras. 17: 597-604. [ Links ]
20. Smith, S. E. & D. J. Read. 2008. Mycorrhizal Symbiosis. 3th ed. Academic Press, New York. [ Links ]
21. Tedersoo, L. A. Sadam, M. Zambrano, R. Valencia & M. Bahram. 2010. Low diversity and high host preference of ectomycorrhizal fungi in Wester Amazonia, a neotropical biodiversity hotspot. ISME Journal 4: 465-471. [ Links ]
22. Thaker, J. R. & T. W. Henkel. 2004. New species of Clavulina from Guyana. Mycologia 96: 650-657. [ Links ]
24. Tulloss, R. E., C. L. Ovrebo & R. E. Halling 1992. Studies on Amanita (Amanitaceae) from Andean Colombia. Mem. New York Bot. Gard. 66: 1-46. [ Links ]
25. Vellinga, E. C., B.E. Wolfe & A. Pringle. 2009. Global pattern of ectomycorrhizal introductions. New Phytol. 181: 960-973. [ Links ]
26. Wang, X., A. S. Auler, R. L. Edwards, H. Cheng, P. S. Cristalli, P. L. Smart, D. A. Richards & C.-C. Shen. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climates anomalies. Nature 432: 740-743. [ Links ]
27. Wartchow, F. 2009. Volvariella cubensis: a rare neotropical agaric new to South America. Mycotaxon 107: 181-187. [ Links ]
28. Wartchow, F. 2012. Clavulina incrustata, a new species from Pernambuco, Brazil. Cryptog., Mycol. 33 (in press). [ Links ]
29. Wartchow, F. & L. C. Maia. 2007. The neotropical Amanita crebresulcata Bas: new citation from Northeast Brazil. Hoehnea 34: 131-134. [ Links ]
30. Wollan, A. K., V. Bakkestuen, H. Kauserud, G. Gulden & R. Halvorsen. 2008. Modelling and predicting fungal distribution patterns using herbarium data. J. Biogeogr. 35: 2298-2310. [ Links ]
Original recibido el 29 de Junio de 2011;
primera decisión: 31 de Agosto de 2011;
aceptado el 6 de Septiembre de 2011.
Editor responsable: Carlos Urcelay.