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A New Section, Lactifluus Section Neotropicus (Russulaceae), and Two New Lactifluus Species from the Atlantic Forest, Brazil

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A New Section, Lactifluus Section Neotropicus (Russulaceae), and Two New Lactifluus Species from the Atlantic Forest, Brazil Systematics and Biodiversity ISSN: 1477-2000 (Print) 1478-0933 (Online) Journal homepage: https://www.tandfonline.com/loi/tsab20 A new section, Lactifluus section Neotropicus (Russulaceae), and two new Lactifluus species from the Atlantic Forest, Brazil Jaime AndrÉs Duque Barbosa, Lynn Delgat, Samuel Galváo Elias, Annemieke Verbeken, Maria Alice Neves & Aníbal alves de Carvalho Jr. To cite this article: Jaime AndrÉs Duque Barbosa, Lynn Delgat, Samuel Galváo Elias, Annemieke Verbeken, Maria Alice Neves & Aníbal alves de Carvalho Jr. (2020): A new section, Lactifluus section Neotropicus (Russulaceae), and two new Lactifluus species from the Atlantic Forest, Brazil, Systematics and Biodiversity, DOI: 10.1080/14772000.2020.1769221 To link to this article: https://doi.org/10.1080/14772000.2020.1769221 View supplementary material Published online: 16 Jun 2020. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tsab20 Systematics and Biodiversity (2020), 0(0):1–15 Research Article A new section, Lactifluus section Neotropicus (Russulaceae), and two new Lactifluus species from the Atlantic Forest, Brazil JAIME ANDRÉS DUQUE BARBOSA1, LYNN DELGAT2, SAMUEL GALVÁO ELIAS3 , ANNEMIEKE VERBEKEN2 , MARIA ALICE NEVES4 & ANÍBAL ALVES DE CARVALHO, JR.5 1Instituto de Pesquisas Jardim Bot^anico do Rio de Janeiro (JBRJ, Escola Nacional de Bot^anica Tropical (ENBT), Rua Pacheco Le~ao, 2040, Horto, 22460-030, Rio de Janeiro, Rio de Janeiro, Brazil 2Dpt. Biology, Research Group Mycology, Ghent University, K.L. Ledeganckstraat 35, Gent, B-9000, Belgium 3Programa de Pos-Graduac ¸~ao em Biologia Microbiana, Departamento de Biologia Celular, Universidade de Brasılia, Campus Darcy Ribeiro, Brasılia, CEP: 70910-900, Distrito Federal, Brazil 4Programa de Pos-Graduac ¸~ao em Biologia de Fungos, Algas e Plantas, Departamento de Bot^anica, Universidade Federal de Santa Catarina, Campus Universitario Trindade, Florianopolis, CEP: 88040-900, Santa Catarina, Brazil 5Diretoria de Pesquisa Dipeq, Instituto de Pesquisa Jardim Bot^anico do Rio de Janeiro, Rua Pacheco Le~ao, 915 sala 218, Jardim Botanico, Rio de Janeiro, 22460-030, RJ, Brazil (Received 14 June 2019; accepted 18 February 2020) Lactifluus is a monophyletic genus of ectomycorrhizal fungi with about 200 described species classified in four subgenera: L. subg. Gymnocarpus, L. subg. Lactariopsis, L. subg. Lactifluus, and L. subg. Pseudogymnocarpus. Currently L. subg. Lactariopsis is considered monophyletic with approximately 57 species described and classified in four sections: Albati, Edules, Lactariopsis, and Russulopsidei. There are few species of L. subg. Lactariopsis described from the Neotropical region, however local mycologists commonly collect specimens of this subgenus during their mycological surveys. The goals of the present study are to evaluate the phylogenetic and morphological relationships of the species from L. subg. Lactariopsis found in Brazil, to contribute to the knowledge of Lactifluus in Neotropical ecosystems by describing a new section in this subgenus and two new species from Brazil, and to document L. neotropicus as a new record from Brazil. Based on morphological and phylogenetic evidence we propose Lactifluus sect. Neotropicus as a new section and Lactifluus catarinensis and L. marielleae as two new species in this section. We provide a key to the species of L. sect. Neotropicus, which is shown to be a monophyletic group of Neotropical species within L. subg. Lactariopsis. The most striking characteristic of several species in L. subg. Lactariopsis is the secondary angiocarpic development, not present in the other subgenera. Species with a secondary veil can be found in two lineages that diversified more recently than the rest of the genus: L. sect. Lactariopsis and L. sect. Neotropicus. Species that show morphological affinities with the two new species in L. sect. Neotropicus described here are commonly found and we expect a greater diversity to be revealed of this section in the Neotropical region. Key words: ITS, Lactarius, milkcaps, morphology, phylogeny, 28S Introduction phylogeny-based classification of Lactifluus and allied Lactifluus (Pers.) Roussel (Russulaceae, Basidiomycota) genera has been accelerated recently by several molecu- is a genus of ectomycorrhizal fungi with about 200 lar systematic studies of the group (Buyck et al., 2008; accepted species (He et al., 2019) distributed worldwide, De Crop et al., 2017; Verbeken, Stubbe, Van de Putte, which reaches its greatest diversity in the tropics. Eberhardt & Nuytinck, 2014). Lactifluus is monophy- Together with members of the genus Lactarius Pers., letic and classified in four subgenera: L. subg. species are popularly known as milkcaps (Verbeken & Gymnocarpi (R. Heim ex Verbeken) De Crop, L. subg. Nuytinck, 2013). Progress towards generating a Lactariopsis (Henn.) Verbeken, L. subg. Lactifluus and Correspondence to Jaime Andres Duque Barbosa. E-mail: L. subg. Pseudogymnocarpi (Verbeken) De Crop (De [email protected] Crop et al., 2017). ISSN 1477-2000 print / 1478-0933 online # The Trustees of the Natural History Museum, London 2020. All Rights Reserved. https://dx.doi.org/10.1080/14772000.2020.1769221 Published online 16 Jun 2020 2 J. A. Duque Barbosa et al. Lactariopsis (Henn.) Verbeken was erected by surveys. It is also usual to find specimens without a spe- Hennings (1901) as a closely related genus to Lactarius cific name in the herbaria, because of the lack of know- based on the basidiome development with an involute ledge on the genus in the Neotropics. Based on this, the pileus margin connected with the stipe by a membran- goals of the present study are: (1) evaluate the phylo- aceous velum in Lactariopsis zenkeri Henn. The remain- genetic and morphological relationships of the species ing characters described were equal to those found in from L. subg. Lactariopsis found in Brazil, (2) contrib- Lactarius. Heim (1937) proposed the term pseudoangio- ute to the knowledge of the biodiversity of Lactifluus in carpic development to describe the kind of development Neotropical ecosystems by describing a new section in found in species with a velum. Heim (1938) and Singer this subgenus and two new species in this section, and (1942) considered pseudoangiocarpic development as a by documenting L. neotropicus as a new record weak character to define the genus Lactariopsis, and from Brazil. consequently, Heim (1938) considered Lactariopsis as a subgenus in the genus Lactarius. Singer (1942) consid- ered them at sectional level: L. sect. Lactariopsidei.Ina Materials and methods synopsis for L. subgenus Lactariopsis, Verbeken (1998a) adopted the term secondary angiocarpic devel- Collect and morphological studies opment instead of pseudoangiocarpic development (after Specimens were collected in dense ombrophilous forest, Reijnders, 1963) and considered the creation of a sub- Brazilian Atlantic Rain Forest, in Minas Gerais, Rio de genus based on the secondary angiocarpic development Janeiro, Santa Catarina, and Paraiba states (Fig. 1). We as artificial. Hence, Verbeken (1998b) emended and pro- used the opportunistic sampling method in seven collect- posed a larger definition of the subgenus Lactariopsis in ing points: Benjamim Maranh~ao Botanic Garden which species with secondary angiocarpic development (Paraiba State), Mangabeiras City Park (Minas Gerais and other species with close morphological affinities State), Serra dos Org~aos National Park and Tijuca were included. After Lactarius was split into three gen- National Park (Rio de Janeiro State), Lagoa da era (Buyck et al., 2008; Buyck, Hofstetter, Verbeken & Conceic¸~ao, P^antano do Sul to Lagoinha do leste trail Walleyn, 2010), Lactarius, Lactifluus and Multifurca and Santo Amaro da Imperatriz (Santa Catarina State). Buyck & V. Hofst., the subgenus containing species Collection points were georeferenced and mapped with a velum was found to belong within Lactifluus and through a free and open-source software QGIS 3.6 consequently it was recombined to Lactifluus subg. (QGIS Development Team 2019), with standards base- Lactariopsis by Verbeken, Nuytinck and Buyck (2012). map of GADM (Global Administrative Areas [GADM], Currently L. subg. Lactariopsis is considered mono- 2019) and WorldClim 2 (Fick & Hijmans, 2017). The phyletic (De Crop et al., 2017) with 57 species specimens were photographed in the field and macro- described. Four sections have been described, L. sect. scopically described. The collections were examined fol- Albati (Bataille) Verbeken, L. sect. Edules (Verbeken) lowing standard mycological methods (Largent, Johnson Verbeken, L. sect. Lactariopsis and L. sect. & Watling, 1980; Mueller, Bills & Foster, 2004), and Russulopsidei (Verbeken) Verbeken. Seven more mono- later dried in a food dehydrator for 8 h at approximately phyletic clades were recognized by De Crop et al. 40 C. Colour codes follow Kramer (2004; e.g., oac758) (2017). Of these seven, two are entirely Neotropical: or Kornerup and Wanscher (1978; e.g., 6E4) colour Clade 2 and Clade 3. Clade 2 contained L. annulifer guides. Microscopic features were studied from dried (Singer) Nuytinck, L. subiculatus S.L. Mill., Aime & material by mounting free-hand sections of the basidio- T.W. Henkel, L. venezuelanus (Dennis) De Crop and an mata in 5% KOH, Melzer’s reagent, or Congo red. undescribed species from French Guyana. In Clade 3 Cresyl
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