Cryptogamie, Mycologie, 2012, 33 (1): 105-113© 2012 Adac. Tous droits réservés

Clavulina incrustata,a new species from Pernambuco, Brazil

Felipe WARTCHOW*

Universidade Federal da Paraíba, Departamento de Sistemática e Ecologia/CCEN,CEP: 58051-970, João Pessoa, PB, BRAZIL.

E-mail: fwartchow@yahoo.com.br

Abstract – Clavulina incrustata is described from Atlantic Forest of Pernambuco, NortheastBrazil, and is characterized by the branched basidiomata, hymenium pale vinaceous fadingto very pale cream-vinaceous, small subglobose to broadly ellipsoidal basidiospores, andcontext hyphae bearing ferrugineous brown incrusted matter. Illustrations of the holotypeand a key for Neotropical taxa are provided.

Atlantic Forest / Cantharellaceae / Clavulinaceae / neotropics / taxonomy

Résumé – Clavulina incrustata, décrite de la forêt atlantique de Pernambuco, Brésil, estcaractérisé par la ramification typique, la couleur vineuse de l’hyménium devenant ensuitecouleur crème, les basidiospores pétites et subglobuleuses à subellipsoïdes et son contextcontenant des hyphes incrustées de matière brun ferrugineux. La nouvelle espèce estillustrée et une clé aux espèces néotropicales est fournie.

Cantharellaceae / Clavulinaceae / Forêt Atlantique / néotropiques / taxonomie

INTRODUCTION

Clavulina J. Schröt. is a genus in the order Cantharellales (De Kesel et al.2011, Nakasone 2011). It often produces clavarioid basidioma and is distinguished bysmooth basidiospores, basidia with stichic nuclear division that often develop atransversal septum, cornuted sterigmata and the ectomycorrhizal nature (Henkel etal. 2005, 2011). According to the latest version of the Dictionary of the Fungi (Kirk etal. 2008) Clavulina comprises 40 species with a widespread distribution. However, themore recent account by Uehling et al. (2012) reports on 75 taxa described hitherto asmany species have very recently been described, especially from the Neotropics. Inall, 19 taxa of Clavulina (17 of them new species) were discovered in Guyana near tothe frontier with Brazil (Thacker & Henkel 2004, Henkel et al. 2005, 2011, 2012,Uehling et al. 2012) where Clavulina is considered as one of the conspicuous elementsof the ectomycorrhizal connection with the canopy tree Dycimbe corymbosa (Henkelet al. 2002) and as one of the most diverse ECM associations of Guyana and WesternAmazon, that has its center of diversity in tropical South America (Tedersoo et al.2010, Smith et al. 2011). Molecular analysis of the recent taxa described from theneotropics also allowed for an important emendation of the classical concept ofClavulina, which is no longer restricted to typical clavarioid taxa (e.g. Larsson et al.2004, Thacker & Henkel 2004, Uehling et al. 2011).

* Corresponding author.

106 F. Wartchow

From Brazil, Hennings (1904) and Rick (1959) recorded putative Clavulinaspecies from the States of São Paulo and Rio Grande do Sul respectively; Corner(1950, 1970) reported five species, C. amazonica Corner, C. connata (Berk.) Corner,C. delicia (Berk.) Corner, C. panurensis (Berk.) Corner and C. sprucei (Berk.)Corner, from the state of Amazonas, and C. cirrhata (Berk.) Corner from animprecise locality. Other works that cited Clavulina in Brazil are Bononi (1979) andBononi et al. (1981) with C. floridana (Murrill) Corner and C. panurensis from theState of São Paulo; Sobestiansky (2005), with C. coralloides (Fr.: Fr.) J. Schröt.;de Meijer (2006), who reported C. cf. coralloides, C. puigarii (Speg.) Corner andC. aff. rugosa (Bull.: Fr) J. Schröt. from the state of Paraná; and Gomes-Silva &Gibertoni (2009a), reported C. cirrhata from Amazonas. More recently, Baltazar &Gibertoni (2009), in a check-list based exclusively on bibliographic references, citedC. coralloides, C. floridana and C. panurensis from the State of São Paulo, and C.cartilaginea (Berk. & M.A. Curtis) Corner and C. delicia from the state of RioGrande do Sul. In another Brazilian checklist, Gomes-Silva & Gibertoni (2009b)cited all taxa previously reported by Corner (1950) from Amazon, except C.amazonica which was described later (Corner 1970). In the state of Pernambuco,this genus is cited only once, by Wartchow (2012), with C. amazonensis.

The aim of this work is to describe a new species of Clavulina from theAtlantic Forest of the State of Pernambuco, Northeast Brazil.

MATERIAL AND METHODS

The Atlantic Forest has been drastically reduced to several smallfragments since the beginning of the colonization of Brazil in 1500 AD (Kimmelet al. 2008). The “Refúgio Ecológico Charles Darwin” (07º48’37”-07º49’02” S and34º27’25”-34º56’52”W), is a protected private area of about 60 ha located at themunicipality of Igarassu, in the State of Pernambuco, Northeast Brazil (Costa-Lima 1998), corresponding to an Atlantic Forest fragment surrounded byagricultural areas (mainly sugar cane plantations), and has a tree stratum 8-15 mhigh (Santiago & Barros, 2003).

Basidiospores were measured in KOH and measurements are based on25 spores. Abbreviations include L(W) = basidiospore length (width) average,Q gives the length/width ratio range from measured spores with in bold theaverage value. The key presented here is based exclusively on the literature(Corner 1950, Petersen 1964, 1984, 1988, Henkel et al. 2005, 2011, Thacker &Henkel 2004). Color code references follow the Online Auction Color chart(2004). The holotype is deposited at URM (Thiers, continuously updated).

TAXONOMY

Clavulina incrustata Wartchow sp. nov. Figs 1-2

MycoBank: MB 561193Holotypus: BRAZIL. PERNAMBUCO, IGARASSU, REFÚGIO ECOLÓGICO

CHARLES DARWIN, MAY 25, 2010, F. WARTCHOW 22/2010 (URM).Etymology: refers to the extracellular incrustations on the hyphae of the

context.

Clavulina incrustata, a new species from Pernambuco, Brazil 107

Fig. 1. A-B. Clavulina incrustata (holotype). A. Basidiomes after about 20 hours. B. Hyphalsegment from the context of the hymenial portion mounted with water. Scale bar is 10 mm forbasidiome and 10 µm for microstructures.

108 F. Wartchow

BASIDIOMES gregarious, each cluster up to 45 mm high and 18 mm wide,arising from the same stipe or the same point with apparent caespitose habit, butwith separated stipe base; tough after dried. HYMENIUM amphigenous, palevinaceous (OAC 611-613) fading to very pale cream-vinaceous (OAC 676) thencream to dirty white with shades of the vinaceous color; dichotomously branched,

Fig. 2. Clavulina incrustata. A. Basidiospores. B. Basidia, basidioles and subhymenial elements.C. Context hyphae mounted in KOH. Scale bar is 10 µm.

Clavulina incrustata, a new species from Pernambuco, Brazil 109

sometimes trichotomous, appearing spur-like at apices; branches sometimeslaterally flattened, acuminate at apices, branching rank 2-3. STIPE 10-18 ×2-3.5 mm, brown (OAC 747) or dark brown (darker than OAC 733); straight andlaterally compressed three ramifications, smooth, glabrous. ODOR indistinct;TASTE not recorded.

BASIDIOSPORES (6.5-) 6.8-8 (-8.3) × 5.7-6.8 (-7) µm, L = 7.3 µm; W = 6.3 µm,Q = (1.04-) 1.11-1.20 (-1.21), Q = 1.14, subglobose to broadly ellipsoid, veryoccasionally globose, hyaline, thin-walled; contents as one large guttule; hilarappendix sublateral or subapical, rounded obtuse. BASIDIA 43-51 × 6.5-7 µm(width measured at apex), clavate-elongate, 2-spored (very infrequently 1-3);sterigmata cornute up to 5 µm long, slightly thick-walled up to 0.7 µm thick,clamps not observed. BASIDIOLES slender clavate, abundant among basidia.SUBHYMENIUM composed of slender, colorless thin-walled hyphae around 5 µmwide. CONTEXT composed of hyphae 3-8 µm wide, interwoven, hyaline, wall0.5-0.7 µm thick, occasionally trumpet swollen at septa; inflated hyphae 11-13 µmwide, infrequently observed. Ferruginous brown incrusted extracellular matterobserved in water, Melzer’s reagent and KOH 3%, sometimes dissolved intobrown liquid in this latter reagent. CLAMP CONNECTIONS nearly absent to veryrare (only two observed in the context).

Habitat: gregarious and scattered on soil among tropical Atlantic Foresttrees, as for example, Coccoloba sp. (pers. observ.). Alves-Araujo et al. (2008)published a list of tree species from fragments of Atlantic Forest, although notexactly from our type-locality. They reported taxa of Leguminosae (allsubfamilies), Nyctaginaceae (three species of Guapira) and Polygonaceae (sevenCoccoloba spp.), all representing neotropical ectomycorrhizal trees (e.g. Tedersooet al. 2010, Smith et al. 2011).

Remarks: Clavulina incrustata is difficult to overlook in the field due tothe pale vinaceous hymenial surface. After refrigeration for one day, thebasidiome color fades to pale cream-vinaceous then cream to dirty white withshades of the vinaceous color. Microscopically, size and shape of thebasidiospores, ferruginous brown incrusted hyphae and nearly absent clampconnections are diagnostic. The new species could be compared to Clavulinaornatipes (Peck) Corner (Petersen, pers. corresp.), a taxon with northern-hemisphere distribution, from the USA to far-east Asia, but not in Europe. Itdiffers in the dull tan to leaden gray color of the branches, more strigose stipe andlarger basidiospores, of which the smallest mean is 9.2 × 7.7 µm and the largest10.8 × 9.5 µm (Petersen 1964).

Another clampless taxon, C. cartilaginea (Berk. & M.A. Curtis) Cornerfrom Cuba and Malaya shares a vinacecous tint of branches, but differs in itsconcolorous stipe with often strigose base, much more polychotomous branches inone plane (palmate-flabellate), larger basidiomes up to 110 mm high and thepseudoparenchymatous nature of the subhymenium (Corner 1950). In addition,the basidiospores are larger (7-10 × 6-8.5 µm). However, his description is largelybased on Malayan specimens, while the holotype from Cuba is similar to ourspecimens at least in two points: the basidiospores measuring 7-9 × 6-8 µm(according Corner’s 1950 type study), and basidiomes around 40 mm high(11/2 inches, as described by Berkeley & Curtis 1968 for Lachnocladiumcartilagineum Berk. & M.A. Curtis). However, no color is given in the protologue.Coker (1923: 198) also examined the type and reported similar basidiospores toC. incrustata (6.2-8.5 × 5.5-7.5 µm), but reported unilateral instead of anamphigenous hymenium. Later studies by Petersen (1984) also revealed theunilateral hymenium, basidiospores 7.9-8.6 × 6.1-8.3 µm and mostly uninflated

110 F. Wartchow

context hyphae (2.5-4.5 µm diam.). Due the differences mainly in the dispositionof the hymenium, C. cartilaginea is regarded here as distinct from C. incrustata.Lachnocladium cartilagineum sensu Rick (1959) is a misidentification, sincecolored echinulate basidiospores are described for this taxon.

Other neotropical species, such as C. connata (Berk.) Corner, C. delicia(Berk.) Corner and C. sprucei (Berk.) Corner, all clampless, differ in the distinctlyellipsoid basidiospores (7.5-9 × 5.5-6.5 µm in C. connata and 9.5-11 × 5-6 µm inC. delicia), a very unusual trait for the genus. Clavulina sprucei was recentlyrediscovered in the Guiana Shield and has somewhat larger basidiospores 8-10 ×6.5-8 µm in comparison to C. connata and C. delicia, and pale creamish whitebasidiome color (Henkel et al. 2011).

Clavulina amazonensis was fully examined by Petersen (1988) based onVenezuelan collections and examination of the holotype, and also lacks clampconnections. However, it differs from C. incrustata in the thick-walled 2-3(-4)-spored basidia, smaller basidiospores 6.1-7.2 × 5.4-6.5 µm, Q = 1.06-1.24, Q = 1.12and pale orange-tan hyphae in the context (Petersen 1988). It has recently beenfound in Guyana by Henkel et al. (2011) and in the Atlantic forest of NortheastBrazil by Wartchow (2012).

Other species, such as C. humicola T.W. Henkel et al. andC. griseohumicola T.W. Henkel et al. from Dicymbe dominated forests from theGuiana Shield also lack or have very few clamps, but clearly differ in the non- oroccasionally branched habit and color of the basidiomes (Henkel et al. 2005).

The recently described C. tepurumenga T.W. Henkel & Aime from theGuyana Shield has similar basidiospores (7-9 × 6-7 µm, average Q = 1.19), butclearly differs in the higher basidiomes of 40-116 mm, light lilac-gray color,maturing to deeper purplish gray hymenium, smooth, colorless context hyphaeand abundant clamp connections (Henkel et al. 2011).

A very interesting feature was observed in C. incrustata. As the namesuggests, the context hyphae of this new taxon present abundant brownishferruginous incrustations on their wall that are partly dissolved in KOH 3%. Thischaracter has not been described in recent works on Clavulina (e.g. Petersen 1988,Thacker & Henkel 2004, Henkel et al. 2005, 2011). As this morphological featurecould have a taxonomic significance in Clavulina, Petersen (pers. comm.),suggested that related species should also be checked for this character. Untilthen, we consider it to be diagnostic for the recognition of our C. incrustata.

An artificial key to neotropical species of Clavulina

This key includes only Neotropical taxa that where fully described andillustrated (Berkeley & Curtis 1868, Corner 1950, 1970, Petersen 1984, 1988,Thacker & Henkel 2004, Henkel et al. 2005, 2011, Uehling et al. 2012, Wartchow2012). Not included in this key are C. floridana (Bononi 1979), C. cartilaginea(Rick 1961), C. cf. coralloides, C. puiggarii, C. aff. rugosa (de Meijer 2006) due tothe lack of description details or the necessity to re-examine these collections,since they might not occur naturally in Brazil. In addition, the Northernhemisphere C. castaneopsis is also included for a better comparison with our newspecies.

1a. Clamp connections absent or very rare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21b. Clamp connections abundant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

2a. Basidiomes simple or only infrequently united at their base . . . . . . . 32b. Basidiomes in caespitose clusters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

Clavulina incrustata, a new species from Pernambuco, Brazil 111

3a. Basidiomes dull-orange; basidiospores 6.5-8.5 × 6-8 µm . . . . . . . . C. humicola3b. Basidiomes dark bluish gray; basidiospores 8-9.5 × 7-9 µm . . C. griseohumicola

4a. Basidiomes with a resupinate fertile portion. . . . . . . . . . . . . . . . . . . . . 54b. Basidiomes lacking this structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

5a. Basidiomes with erect portion typically coralloid . . . . . . . . . . . . . . . . C. effusa5b. Basidiomes with erect portion rounded . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

6a. Basidiome with erect portion subglobose/subcerebriform, yellow-cream; basidiospores typically subglobose, with spore wall 0.3-0.7 µmthick and a hilar appendix 0.5-0.75 µm long . . . . . . . . . . . . C. cerebriformis6b. Basidiome with erect portion not subglobose/subcerebriform, grayish;basidiospores sublacrymiform, with spore wall 0.8-1 µm thick and a hilarappendix 1-1.3 µm long. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. cinereoglebosa

7a. Hymenium unilateral . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87b. Hymenium amphigenous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

8a. Basidiospores elongate, Q = 1.85 . . . . . . . . . . . . . . . . . . . . . . . . C. delicia8b. Basidiospores subglobose, Q = 1.16 . . . . . . . . . . . . . . . . . . . . C. cartilaginea

9a. Basidiospores mostly ellipsoid, basidiomes whitish. . . . . . . . . . . . . . . . . . . . . 109b. Basidiospores globose to broadly ellipsoid; basidiomes differently colored 11

10a. Basidiomes 40-50 mm high; basidiospore width 5.5-6.5 µm; basidia45-65 µm long; fruiting on soil. . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. connata10b. Basidiomes somewhat shorter, frequently less than 48 mm; basid-iospore width 6.5-8 µm; basidia 29-44 µm long; fruiting of small woody sub-strata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. sprucei

11a. Basidiomes brownish; mean basidiospores size ranging from 9.8 × 8.5 µm(var. castaneopsis) to 10.8 × 9.5 µm (var. lignicola); distribution in NorthernHemisphere. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. castaneopsis11b. Basidiomes with some shade of vinaceous or orange; basidiosporessmaller; neotropical distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

12a. Basidiomes with vinaceous tints; context composed of hyaline hyphaewith extracellular incrustated wall; basidiospores (6.5-) 6.8-8 (-8.3) × 5.7-6.8(-7) µm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. incrustata sp. nov.12b. Basidiomes sordid grayish orange; context with orange-tan hyphae,without extracellular incrustations; basidiospores 6.1-7.2 × 5.5-6.5 µm . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. amazonensis

13a. Basidiomes deeply infundibuliform. . . . . . . . . . . . . . . . . . . . . C. craterelloides13b. Basidiomes typically clavarioid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

14a. Basidiomes simple, only infrequently united at base . . . . . . . . . . . . . 1514b. Basidiomes in caespitose clusters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

15a. Basidiomes grayish blue with purplish overtones; basidiospores 8-9.5 (-11)× (6-) 7-8 µm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. dicymbetorum15b. Basidiomes dull orange tan; basidiospores 6-8 (-9) × 4.5-7 µm . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. monodiminutiva

16a. Basidiomes brownish or blackish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1716b. Basidiomes lilac, purplish, orange, ochraceous or pinkish. . . . . . . . . . . 18

112 F. Wartchow

17a. Basidiomes light gray to blackish; basidiospores 6-8 × 5-6 µm; basidia with4-5 (-6) sterigmata. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. nigricans17b. Basidiomes brown then dirty grayish cream; basidiospores 8.5-10.5 (12) ×7-9.5 µm; basidia with 2 sterigmata. . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. caespitosa

18a. Basidiomes first light lilac gray then deeper purplish gray . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. tepurumenga

18b. Basidiomes showing orange tints. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

19a. Basidiomes whitish to pale ochraceous; branches flattened; basidia36-50 µm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. panurensis19b. Basidiomes light pinkish orange or paler; branches blunt-rounded; basidia47-69 µm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. kunmudlutsa

Acknowledgements. I thank Dr. M. Cathy Aime, Dr. Ron Petersen, Dr. BartBuyck and one anonymous reviewer for kindly reading and improving our manuscript,Maria Aparecida da Silva and Nelson Lima-Junior for helping during collection and Dr.Leonor C. Maia for kindly letting me use the laboratory facilities. FACEPE isacknowledged for a post-doctoral grant (BFP Proc. 0100-2.03/09) to the author.

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