Persoonia 42, 2019: 127–185 ISSN (Online) 1878-9080 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE https://doi.org/10.3767/persoonia.2019.42.06 A phylogenetic and taxonomic revision of sequestrate Russulaceae in Mediterranean and temperate Europe J.M. Vidal1*, P. Alvarado2*, M. Loizides3, G. Konstantinidis4, P. Chachuła5, P. Mleczko6, G. Moreno7, A. Vizzini8, M. Krakhmalnyi9, A. Paz10, J. Cabero11, V. Kaounas12, M. Slavova13, B. Moreno-Arroyo14, J. Llistosella15 Key words Abstract A comprehensive morphological and genetic study of type material and new collections of sequestrate Russulales species formerly belonging to the genera Arcangeliella, Elasmomyces, Gymnomyces, Hydnangium, angiocarpic Hymenogaster, Macowanites, Martellia, Secotium and Zelleromyces is here undertaken, for the purpose of providing Arcangeliella a complete taxonomical revision of sequestrate Russulaceae species in the Mediterranean and temperate regions Elasmomyces of Europe. As a result, seven distinct taxa in the genus Lactarius and 18 in the genus Russula are identified. Six Europe of them are new species: L. populicola, L. subgiennensis, R. bavarica, R. candidissima, R. hobartiae and R. medi­ Gymnomyces terraneensis, and seven represent new combinations: L. josserandii (≡ Zelleromyces josserandii), L. soehneri Lactarius (≡ Hydnangium soehneri), R. candida (≡ Hydnangium candidum), R. cerea (≡ Hydnangium cereum), R. messapica Macowanites var. messapicoides (≡ Macowanites messapicoides), R. meridionalis (≡ Zelleromyces meridionalis) and R. neuhoffii Martellia (≡ Hydnangium neuhoffii). Twenty-two of the 25 taxa are illustrated, while descriptions, microscopy images, as well pseudoangiocarpic as extensive information on the ecology, chorology and phylogeny for all taxa are provided. A key is further included taxonomy to facilitate their identification. Zelleromyces Article info Received: 2 July 2018; Accepted: 4 December 2018; Published: 5 April 2019. INTRODUCTION & Smith 1960, Smith 1963, Miller & Lebel 1999, Fogel & States 2001, Desjardin 2003, Smith et al. 2006). However, several Sequestrate Russulaceae produce pseudoangiocarpic (‘seco- sequestrate species have also been documented in tropical tioid’) basidiomata, where the stipe is external and more or less forests in Africa (Dring & Pegler 1978, Eberhardt & Verbeken reduced, to angiocarpic (‘gasteroid’) basidiomata, where the 2004, Verbeken & Walleyn 2010, Beenken et al. 2016) and Asia stipe is internal, reduced to a columella, or altogether absent. (Corner & Hawker 1953, Heim 1959, Zhang & Yu 1990, Tao Sequestrate Russulaceae seem to be widespread throughout et al. 1993, Verbeken et al. 2014a, b), as well as in temperate the globe, especially in arid and semi-arid regions of Australia Nothofagus forests in Patagonia (Trierveiler-Pereira et al. 2015). and New Zealand (Bougher 1997, Lebel 1998, 2001, 2002, The generic organization of sequestrate taxa within the Rus­ 2003a, b, Lebel & Trappe 2000, Bougher & Lebel 2001, Lebel sulaceae has long been a subject of debate (Singer & Smith & Castellano 2002, Trappe & Claridge 2003, Lebel & Tonkin 1960, Pegler & Young 1979, Beaton et al. 1984, Zhang & Yu 2007) and North America (Zeller & Dodge 1919, 1937, Singer 1990). The subtle differences between Gymnomyces, Martellia, Cystangium, Elasmomyces and Macowanites, as well as the 1 C/ Massaballs 10, E-17118 Sant Sadurní de l’Heura, Girona, Spain. latex-bleeding Arcangeliella and Zelleromyces, led to differ- 2 ALVALAB, La Rochela 47, E-39012 Santander, Spain; ent taxonomic arrangements to accommodate an increasing corresponding author e-mail: [email protected]. 3 P.O. Box 58499, 3734 Limassol, Cyprus. number of emerging species (Lebel & Trappe 2000, Trappe 4 Agiou Kosma 25, 51100 Grevena, Greece. et al. 2002, Vidal 2004a). Early authors hypothesized a single 5 Pieniny National Park, Jagiellońska 107b, PL-34-450 Krościenko nad evolutionary lineage from the gymnocarpic to the angiocarpic Dunajcem, Poland. genera in the Russulales (Malençon 1931, Heim 1938, Singer 6 Institute of Botany, Jagiellonian University in Kraków, Gronostajowa 3, & Smith 1960, Oberwinkler 1977), but genetic studies revealed PL-30-387 Kraków, Poland. 7 Dept. de Ciencias de la Vida (Botánica), Facultad de Biología, Universidad that sequestrate russuloid lineages are polyphyletic and nest de Alcalá, E-28871 Alcalá de Henares, Spain. within the genera Russula and Lactarius (Calonge & Martín 8 Dipt. de Scienze della Vita e Biologia dei Sistemi, Università di Torino, 2000, Miller et al. 2001, Larsson & Larsson 2003, Eberhardt Viale P.A. Mattioli 25, I-10125 Torino, Italy. & Verbeken 2004, Nuytinck et al. 2003, Shimono et al. 2004, 9 Institute of Evolution and Department of Evolutionary and Environmental Biology, University of Haifa, 199 Abba Khoushy Ave, Haifa, 3498838, Smith et al. 2006, Lebel & Tonkin 2007). The split of Lactarius Israel. due to genetic evidence (Buyck et al. 2008, 2010) led to the 10 C/ Vall Ter 791, Urbanització Llac del Cigne, E-17455 Caldes de Malavella, restoration of the old genus Lactifluus and the erection of Multi­ Girona, Spain. furca, although no sequestrate species are yet known to occur 11 C/ El Sol 6, E-49800 Toro, Zamora, Spain. in either of these two lineages. 12 Sokratous 40, TK-19016 Artemis Attika, Greece. 13 Krivolak 4, 1164 Sofia, Bulgaria. The genus Gymnomyces, typified by G. pallidus (Massee 1898), 14 Dept. de Biología Vegetal, Facultad de Biología, Universidad de Córdoba, a species found in myrtaceous forests whose current name is Colonia San José 4, Campus de Rabanales, E-14014 Córdoba, Spain. R. paneeroides (Lebel 2017), was characterized by the absence 15 Dept. de Biologia Evolutiva, Ecologia i Ciències Ambientals, Universitat de Barcelona, Av. Diagonal 643, E-08028 Barcelona, Spain. of a stipe-columella and the presence of sphaerocytes in the * These authors contributed equally. hymenophoral trama. The European species G. xanthosporus © 2019 Naturalis Biodiversity Center & Westerdijk Fungal Biodiversity Institute You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 128 Persoonia – Volume 42, 2019 was originally described by Hawker (1952) as a variety of Hyd­ species that sometimes presents a poorly developed or residual nangium carneum, to accommodate some specimens found in stipe and a percurrent columella, especially in young basidiomata. the UK, and subsequently re-combined into Gymnomyces by Despite these features, Arcangeliella was chosen by Singer & Smith (1962), because of its amyloid spores and sphaerocytes. Smith (1960) to describe several non-European sequestrate Several species were described later from the Mediterranean species with a well-developed stipe-columella, whereas Vidal basin or re-combined into this genus, such as G. ilicis (Llistosel- (2004a) maintained this genus only for angiocarpic, sessile spe- la & Vidal 1995), G. dominguezii (Moreno-Arroyo et al. 1999, cies, keeping Gastrolactarius for pseudoangiocarpic, stipitate and subsequently validated in Calonge 2000), G. sublevis­ species. American mycologists (Dodge 1931, Zeller & Dodge porus (Moreno-Arroyo et al. 2002) and G. meridionalis (Vidal 1935) combined several European taxa into Arcangeliella, 2004a), the latter originally treated in the genus Zelleromyces e.g., A. asterosperma var. asterosperma, A. asterosperma by Moreno-Arroyo et al. (1998b, and subsequently validated var. depauperata, A. asterosperma var. hololeuca, A. laevis in Calonge 2000). or A. stephensii; the first four, however, belonging to the order The genus Martellia, typified by M. mistiformis (Mattirolo 1900), Boletales, have since been transferred to the genus Octaviania was first described from several collections found in Sardinia (Paz et al. 2016). Finally, Mader & Mader (1992) proposed (Italy) under Quercus suber. It was characterized by the absence A. volemoides for a collection made under Picea abies in the of a stipe-columella and lack of sphaerocytes in the hymeno- Austrian Alps, but this species was considered a synonym of phoral trama (Singer & Smith 1960). In the late 20th century, A. borziana by Nuytinck et al. (2003) and Vidal (2004a). new species and combinations were proposed: M. mediterranea The latex-bleeding genus Zelleromyces, typified by Z. cinna­ (Moreno et al. 1991), M. pila (Vidal 1991b), M. monospora (Astier barinus (Singer & Smith 1960), was proposed for angiocarpic & Pacioni 1998), the last two originally described from France species devoid of a stipe-columella. Several Mediterranean in the genus Hydnangium by Patouillard (1910) and Boudier and Central European species were later described or re-com- & Patouillard (1888) respectively, and M. aurantiaca (Astier bined into this genus: Z. josserandii from Morocco and France & Pacioni 1998), originally described from Spain in the genus (Malençon 1975), Z. hispanicus (Calonge & Pegler