Fungi Rickiani: The Brazilian Clavarioid Collection at PACA and BPI Herbaria

Seventy-two clavarioid specimens from Johannes Rick's collection at PACA and BPI were revised. Eleven taxa are presented. Illustrations of the microstructures are provided for nine taxa. The description of Scytinopogon robustus includes information from recently collected specimens and SEM photographs of the basidiospores. A new combination, Clavulina ridleyi, is proposed.


Introduction
Johannes Rick (1869Rick ( −1946 was an Austrian Jesuit who first came to Brazil in 1903 to finish his studies as a Jesuit priest and in parallel to study the mycobiota from Rio Grande do Sul (Rabuske & Rambo 2004). One year after his arrival he published the first paper on Brazilian fungi (Fidalgo 1968, but no figures were provided and the descriptions were incomplete for an adequate taxonomic identification (Rick 1928(Rick , 1931(Rick , 1959. Most of Rick's collections can be found at PACA (Brazil), BPI, FH (USA), K (England) and S (Sweden) herbaria (Rick 1928;Fidalgo 1962).
Rick's clavarioid collection at PACA and BPI combined consists of 108 exsiccates. Many of the species names used by Rick in the identifications have been observed to be misidentifications. He frequently used measurements or characteristics of European specimens to determine Brazilian collections. Even though Rick was a particularly careful and attentive mycologist, it has been noted by some recent authors that his spore measurements were not entirely reliable, due to the low quality of the equipment used at the time (Dennis 1960;Corner 1950Corner , 1970, therefore almost all simple club-shaped, yellow taxa of Clavariaceae were mixed due to insufficient microscopic observation (Petersen 1965).
The Herbarium Anchieta -PACA, considered one of the largest in the state, very well-represented in Brazil and housing the largest collection made by Rick, was founded in 1932 in Porto Alegre. Currently, the collection may be found at Instituto Anchietano de Pesquisas/Unisinos, in São Leopoldo, Brazil. The data of the collections are all computerized, and all images of nomenclatural types are available at http://www.anchietano.unisinos.br, at Specieslink (http://www.splink.org.br) and through INCT Herbário Virtual da Flora e Fungos do Brasil (http://inct.florabrasil.net/). The herbarium maintains exchanges with other national and international herbaria through loans, exchanges and donations integrated with research. But mainly, the herbarium receives visits from researchers from different educational and research institutions.
Considering that Rick's collections are some of the most important records of clavarioid fungi from Brazil and their revisions are important to better know the diversity from Southern Brazil, the aim of this work was to review the clavarioid fungi collected and studied by Rick, including the type collections deposited at PACA and BPI.
For the microscopical analysis, portions of the basidiomes were mounted in Melzer and 5% KOH solution and were observed with Olympus CX21 microscope using immersion oil lens at 1000× magnification. The use of descriptive terms followed Corner (1947), Largent et al. (1977) and Vellinga & Noordeloos (2001). The spore measurements excluded the ornamentation (Corner 1947). Twenty-five of each microstructures studied were measured for each collection. Q refers to the quotient average length/width ration range of basidiospores (Largent et al. 1977). All microscopic illustrations were traced with the aid of digital photographs.
The scanning electronic microscopy (SEM) was conducted at Laboratório Central de Microscopia Eletrônica (LCME/UFSC). Fragments of the hymenophore were removed from dried basidiomes, mounted directly on aluminum stubs using carbon adhesive tabs, and coated with 30 nm of gold. The fragments were examined with an SEM operating at 10 keV.
Voucher material of recent collections was deposited at herbarium FLOR at Universidade Federal de Santa Catarina.
In the following notes the species are described in alphabetical order by family and within family by genus. For each taxon the original diagnosis written by Rick (1959) is presented. Nomenclature of the fungi was updated according to CABI and CBS databases. The herbaria acronyms follow Thiers (2015).

Results
Many of the clavarioid specimens from the Fungi Rickiani collection could not be found or traced. Several of the packets do not contain the specimens that correspond to the description provided in the literature, and in others the hymenium was completely eaten by insects or covered by mold. Eleven taxa were associated with all collections recovered. Of the two Brazilian types presented, one was not found in any herbarium consulted, and now we regard it as nomen dubium (TABLE 1). Rick's classification for Clavariaceae included two genera: Clavaria and Lachnocladium.

Clavaria albipes
Habitat and distribution:-Growing on dead wood, on branches of coniferous trees. Brazil (Corner, 1970;Rick 1959), Malaysia, Guatemala (Corner, 1970), India (Thind 1961), Europe, Japan (Corner 1950) and USA (Petersen 1967 Remarks:-The reason why Rick (1931) identified these collections as Clavaria albipes Mont. is unknown, once Rick's collections are completely different from C. albipes especially when it is considered the color of the basidiomes and the spore morphology (smooth in C. albipes).
Based on Rick's description and the data results from our microscopic analysis these collections refer to Ramaria stricta. This species has straight and ascending branches, dull yellowish buff with yellow tips, and the surface of the basidiomes discolor to purplish brown when damaged (Petersen 1975). The thick-walled hyphae, clamped and indistinctly roughned basidiospores are diagnostic characters (Thind 1961;Petersen 1975). The yellowish color of the hymenium and the subhymenium is caused by the guttula of the basidia (Corner 1950).
Clamps present in all tissues.
Habitat and distribution:-Growing on the ground among grass in the forest. Bolivia, Australia, Japan (Corner 1970), Canada (Coker 1923) and USA (Coker, 1923;Corner 1970;Petersen 1964 Remarks:- Rick (1931) published this collection as Clavaria guarapiensis Speg. based on the macroscopical description published in the protologue, but with no microstrutural comparison. The material consists of three basidiomes in good conditions macro and microscopically. Superficially it looks like a small and delicate Clavulinopsis corniculata (Schaeff.) Corner, but it has basidiospores echinulate like the ones found in Ramariopsis crocea.
Habitat and distribution:-Growing on grassy fields or on the ground in the forest. Brazil (Rick 1928, Corner 1970, Argentina, Austria, Bolivia, Chile, Costa Rica, Jamaica, Panama, Peru, Sweden and Malaysia (Corner 1970, as Clavulinopsis pulchra), USA (Petersen 1968), (Corner 1970 Remarks:-It is possible that the macroscopic aspect of the basidiome led Rick to identify the specimen PACA 12443 as Clavaria inaequalis O.F. Müll. However, C. inaequalis can be distinguinshed by the subglobose to broadly ellipsoid basidiospores, sharply angular to echinulate-warted (Corner 1966a), 5.5−7.2 × 4.5−5.7 µm (Petersen 1968). The specimen collected by Rick is actually C. laeticolor, a species diagnosed by the color change from chrome yellow to deep green in ferrous salts (presence of pistillarin) (Petersen 1968), gregarious to fasciculate basidiomes, and a distinct stipe that becomes finely subtomentose when dried (Petersen 1965). Although some microstructures are collapsed, the hyphae of the context and the basidiospores confirm the redetermination as C. laeticolor.
Habitat and distribution:-Growing on roadside soil banks and on termite nestes. The species is known only from Brazil (Sulzbacher et al. 2012 Remarks:- Rick (1931) published this collection as Clavaria paludicola Lib. based on the morphology and yellowish orange color of the basidiomes and probably he did not noticed the presence of a green symbiont at the substrate. The specimen collected by Rick is a lichenized clavarioid fungus, Sulzbacheromyces caatingae. Sulzbacheromyces B.P. Hodk. & Lücking is a recently erected genus in Lepidostromales with a tropical distribution, with an entirely crustrose, undifferentiated thallus lacking cortex and medullary structures (Sulzbacher et al. 2015). Despite S. caatingae being originally described from the Caatinga biome in Brazil (Sulzbacher et al. 2012, as Lepidostroma), the species has had its distribution expanded in several other localities that belong to different biomes, such as the Atlantic Forest (Sulzbacher et al. 2016).
Sulzbacheromyces and Multiclavula R.H. Petersen, another genus of lichenized fungi, exhibit strong morphological similarities even though they belong to distantly related clades within the subclass Agaricomycetidae (Hodkinson et al. 2014). The number of sterigmata and characteristics from the thallus can possibly partially separate both genera, although there are some exceptions and not all species of Multiclavula have been well-documented regarding thallus morphology.
Materials examined:-BRAZIL. Rio Grande do Sul, 1925, J.E. Rick (BPI 295379, 333159, 333160, 333162, 333164, 723389, as Clavaria pteruloides);ibid., 1907, J.E. Rick (PACA 17243 Remarks:-The basidiospore characteristics described by Rick were not observed in the collections identified by him as Clavaria pteruloides. The basidiospores in these specimens are echinulate and smaller than any of the species known in Clavaria. These specimens correspond instead to Scytinopogon pallescens. Corner (1970) lists many brazilian collections under the name Scytinopogon angulisporus (Pat.) Corner, including several specimens from Rio Grande do Sul and also the type of Lachnocladium chartaceum Pat.. The epithet angulisporus has been removed from Scytinopogon since its type represents a Clavulina J. Schröt. species (Petersen 1988). Thus, the genus is left with the original type pointed out by Singer (1945), Scytinopogon pallescens.
Habitat and distribution:-Growing on soil. Brazil (Rick 1959) and Malaysia (Massee 1899 Remarks:- Lloyd (1923) identified some of Rick's collections as Clavulina cinerea, and even though Rick (1959) recognized the similarity he pointed out the grayish color of the basidiomes of C. cinerea. Furthermore, C. cinerea has blunt tips; basidiospores ranging from 6.5−11 × 6.0−10 µm; bigger basidia (40−70 µm long) with a fuscous cytoplasm that corresponds to the gray color of the basidiome (Olariaga et al. 2009) that is not observed in the specimen collected by Rick. The characteristics observed in Rick's collections at PACA and the type of Clavaria ridleyi include ramifications with cristate tips, basidia bispored and secondarily septate with one or more septa after spore-discharge and subglobose basidiospores. This combination places the specimens in Clavulina J. Schröt, and therefore we are proposing the new combination.
Habitat and distribution:-Growing in forest and pastures, mostly terrestrial, occasionally on decayed wood. Brazil, Jamaica, Cuba (Corner 1950), Guadaloupe, Costa Rica, Panama, Colombia, Ceylon, Java, Borneo, Phillipines, New Zealand, Tibet, Solomons Island (Corner 1970 Remarks:- Rick (1959) published these collections as Lachnocladium cartilagineum Berk & M.A. Curtis based on the whitish color of the basidiomes and on the spores dimensions. Even though the published description of this specimen and the description by Rick within the package have the dimensions of the basidiospores as being 5.0−7.0 µm, the basidiospores from all collections are actually smaller (3.5−4.5 × 3.0−4.0 µm), they are not smooth and apiculate as in L. cartilagineum and therefore the specimens were identified as R. kunzei. This species is very variable in size, shape and basidiospores size, however the stipe is always villous or tomentose and the dried basidiomes darken with potash (Corner 1950(Corner , 1970. Ramariopsis kunzei is widespread in tropical forests (Corner 1967).