Studies in Fungi 3(1): 39–48 (2018) www.studiesinfungi.org ISSN 2465-4973 Article Doi 10.5943/sif/ 3/1/6 Copyright © Institute of Animal Science, Chinese Academy of Agricultural Sciences Review of the lichen genus Usnea in the Philippines Galinato MGM1*, Baguinon JRC1 and Santiago KAA2 1 2 The Graduate School, University of Santo Tomas, España 1008 Manila, Philippines Monash University Malaysia, Jalan Lagoon Selatan, 47500 Bandar Sunway Selangor Darul Ehsan, Malaysia Galinato MGM, Baguinon JRC, Santiago KAA 2018 – Review of the lichen genus Usnea in the Philippines. Studies in Fungi 3(1), 39–48, Doi 10.5943/sif/3/1/6 Abstract The fruticose lichen Usnea is a cosmopolitan genus also found in the mountains of the Philippines. Despite its abundance, though, this lichen genus is not extensively studied in the country. Since the Philippine Usnea holds great potential in pharmaceutical and agricultural research, the basic knowledge on this lichen is important to establish. Therefore, this paper takes a detailed review of Usnea in the Philippines and summarizes all the literatures that have been conducted on it in all aspects. Further, the provinces that were already reported of the occurrence of this genus are plotted in one figure to also highlight those that have not been explored yet. Currently, 81 species of Usnea were reported in the country. This includes a species that was previously under the genus Usnea but has been arguably reclassified to a different genus in the present (i.e., Eumitria). This review also hopes to direct future studies regarding Usnea. Key words – biodiversity – checklist – distribution – fungal taxonomy – fruticose Introduction The lichen genus Usnea Dill. ex Adans. is one of the most widespread fruticose lichen genera in the world. Within this genus are ~600 species (Hawksworth et al. 1995) which are all distinguished by their beard-like morphology (Randlane et al. 2009) (Fig. 1). However, Clerc (2004) stated that between 700 to 800 taxon names were actually published under the genus– although a reliable approximation is not entirely clear yet. This scenario supports the fact that Usnea is often regarded as taxonomically difficult by lichenologists and hence needs to be revised (Clerc 1998). Despite the lack of published materials, most studies on the genus make use of morphological and biochemical approaches in the identification of specimens up to the species level. This approach on Usnea can be extremely difficult due to the existence of some specimens that may look distinct from one another but are actually the same at the species level. Articus (2004) recognized this situation and stated that some species of Usnea are “extremely variable and ecophenotypes of the same species may look radically different”. Having thalli that can grow up to several feet, the longest lichen species ever recorded is under this genus (Usnea longissima). Likewise, few Usnea species also have distinguishing characteristics. For example, Usnea ceratina has coarse thalli and pink medulla (Fig. 2). In the Philippines, about 32 species of Usnea have been reported (Bawingan et al. 2000, Santiago et al. 2010, Galinato et al. 2017). However, this number is inconsistent because there are existing reports on other species of Usnea in the country that are not properly accounted in literature. Submitted 15 January 2018, Accepted 17 April 2018, Published 23 April 2018 Corresponding Author: Mark Gabriel M. Galinato – e-mail – markgabriel.galinato.gs@ust.edu.ph 39 Fig. 1 – An epiphytic Usnea in Mt. Amuyao in Mountain Province, Philippines. Scale bar = 2 cm. a b Fig. 2 – U. ceratina with its (a) coarse thallus and (b) the pink medulla. Scale bar = 1 mm. Vainio’s preliminary work on Philippine lichens reported 10 species of Usnea in Luzon Island (Vainio 1909), in which the longest lichen, U. longissima, and the species named after the country, U. philippina, were reported. After 28 years, Motyka (1937) continued to explore the country and was able to name a new species believed to have been discovered first in Misamis Occidental, Northern Mindanao (U. misamisensis). Meanwhile, Quisumbing (1951) was the first to 40 report the medicinal use of Philippine Usnea which can cure stomach pain according to his book, “Medicinal Plants of the Philippines” (dela Cruz et al. 2013). A similar study also claimed the pharmacological use of U. barbata in Iloilo as a treatment for wounds (Madulid et al. 1989). This paper is so far the only known paper that reports the presence of the genus in the Visayas region. Moreover, dela Cruz et al. (2013) recognized the work of Herre (1963) as the most extensive enumeration of Usnea spp. in the country. The study listed 25 species of Usnea for the entire Philippines. Presently, there are online catalogues that record the early studies of Sevilla-Santos (1965, 1979) and Sevilla-Santos & Mondragon (1972) on Usnea. Sevilla-Santos’ work in 1965 focused on the antimicrobial activities of U. montagnei and its antibiotic constituents. Following this was the study of several lichens and their thin-layer chromatographic profiles by Sevilla-Santos & Mondragon (1972). This included five species of Usnea. Sevilla-Santos’ work in 1979 is his most credited one, which finally classified the locally-known “lumot niyog” as the lichen Usnea. In 2000, Bawingan et al. carried out an extensive research on the lichen flora of the Cordillera which recorded three Usnea spp. in Benguet. The book of Stevens (2004) reported the occurrence of some Usnea spp. in Laguna and Lanao del Norte, one of which was a new record for the Philippines at that time (U. himantodes). Recent applications of Usnea were studied by Santiago et al. (2010, 2013) who, collectively, demonstrated the antibacterial activities and secondary metabolic profiles of fruticose lichens and 27 Usnea spp., respectively. These studies were credited by many lichenologists all over the world and were used as primary references in studying the genus’ taxonomy and secondary metabolic applications (Kosanić & Ranković 2015, Shukla 2015, Galinato et al. 2017, Timbreza et al. 2017). The same paper also added 14 new records of Usnea for the country, namely: U. articulata, U. baileyi, U. ceratina, U. chaetophora, U. cornuta, U. fragilescens, U. glabrata, U. haumanii, U. hesperina (syn. U. subgracilis), U. hirta, U. intermedia, U. nidulans, U. sorediosula, and U. subcornuta. Furthermore, Sipman et al. (2013) produced a catalogue of 162 lichen species in Palawan which included three Usnea spp. A recent antibacterial study by Timbreza et al. (2017) reported 36 species of Usnea from Bukidnon. Interestingly, 21 of these species are new records for the country, namely: U. aciculifera, U. amabilis, U. bismolliuscula, U. filipendula, U. fragilescens var. mollis, U. grandisora, U. hakonensis, U. himalayana, U. nipparensis, U. orientalis, U. pangiana, U. poliotrix, U. praetervisa, U. pygmoidea, U. scabrata, U. sphacelata, U. subdaseae, U. subfloridana, U. subrubricornuta, U. transitoria, and U. wasmuthii. This paper is, by far, the one that contributed most in the addition of new records of Usnea for the Philippines. The most recent paper focusing on Philippine Usnea was by Galinato et al. (2017) which determined the diversity of the genus in each municipality of the province of Kalinga. According to the study, a total of 25 species were reported in the province including seven new records for the country, namely: U. cavernosa, U. dasaea, U. dasypoga, U. flavocardia, U. glabrescens, U. lapponica, and U. silesiaca. This paper serves as a checklist of all the reported species of Usnea in the Philippines and highlights the provinces where Usnea spp. have already been reported in. Additionally, this collectively summarizes all the studies conducted on Philippine Usnea and updates the national record. All species have been initially verified through suggested online mycological databases such as MycoBank (International Mycological Association, United Kingdom) and Index Fungorum (Royal Botanic Gardens Kew, United Kingdom) to sort out the synonymy. Since there was a recent increase in the number of new records for the country, it is vital to establish an accurate count of species for future studies. The paper can also serve as a reference to track a species, mainly if intended for a study (e.g., allelopathy, bioactivities, biomonitoring, phylogeny, etc.). Discussion Despite the recent progress on lichenological studies in the country, there is barely fundamental research on Philippine Usnea. The taxonomic challenge of the genus is the main contributing factor to this. This led to the lack of published materials focusing on the nature, ecology, and systematics of the genus. Still, it is not surprising that this fruticose lichen is diversely 41 found in the higher portions of the Philippine forests. This claim is evident in the studies of Herre (1963), Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017), wherein a copious number of specimens were collected individually per study. To date, there is only one known paper that reports the occurrence of Usnea in the Visayan Islands which, particularly, describes the ethnopharmacological use of U. barbata in Iloilo (Madulid et al. 1989) (Fig. 3). Species of another fruticose lichen, Ramalina, is reported in some parts of the Visayan region. Hence, it is not impossible that Usnea can also be found in most parts of Visayas. It is worth noting, though, that Ramalina spp. are more capable of growing in lower elevations (~400 masl) than Usnea (~600 masl and above) as observed during fieldworks. In addition to this, the two genera do not often coexist in the field. Ramalina is usually associated with foliose lichens in lower areas whereas Usnea is frequently observed inhabiting the same tree as Cladonia in higher elevations. Therefore, the occurrence of Usnea in a particular site might also be influenced by the elevation. Many of the existing studies did not specifically mention where the Usnea specimens were collected in the country (Quisumbing 1951, Herre 1963, Sevilla-Santos 1965, Sevilla-Santos & Mondragon 1972, Sevilla-Santos 1979). This posed many problems when preparing an accurate map for the localities of Usnea all over the Philippines (Fig. 3). According to Mycobank and Index Fungorum, many species of Usnea had synonymized. This was taken into account alongside papers focusing on the revision of the genus. The names that were discovered synonyms of another taxon (e.g., Usnea arida=U. rubrotincta) were collectively considered as only one count of species and the current accepted name is used in this review. For instance, it was proposed by Truong et al. (2013) that the synonymy of U. hesperina with U. schadenbergiana be rejected and instead U. hesperina be reclassified as U. subgracilis. In the paper of Sevilla-Santos & Mondragon (1972), U. intercalaris was one of the species reported. Its current accepted name was changed to U. nidifica and was used by Timbreza et al. (2017) in their paper. Thus, U. nidifica is registered under both studies in this paper. Meanwhile, U. hossei, U. misamisensis, and U. pectinata were all reclassified as Eumitria pectinata by Articus (2004). Eumitria was a subgenus of Usnea alongside two other subgenera until molecular works gave Eumitria the generic rank (Articus 2004). However, other authors agreed to keep Eumitria as a subgenus “since the backbone of the phylogeny of Usnea s. lat. remained unresolved and phenotypic characters used to circumscribe the lineages were ambiguous” (Truong & Clerc 2013). Eumitria pectinata is currently the accepted name in Index Fungorum despite of this debate but is still considered under Usnea in this review paper (Table 1). Table 1 Reclassified names of some Usnea spp. in the Philippines Current accepted name U. nidificad Previous name(s) used in literature U. hosseib U. misamisensisc U. pectinatad U. intercalarise U. subgracilisf U. hesperinac E. pectinataa Author d Taylor (1847) e Krempelhuber (1874) f Vainio (1915) b Vainio (1921) c Motyka (1937) a Articus (2004) In lieu of these taxonomic changes, this paper used the reclassified taxon names of Usnea spp. that are accepted by the said mycological databases. A total of 81 taxa have been determined for the country from the 19th century up to date. This number includes the previously-named U. hossei, U. misamisensis and U. pectinata, which are now all under the name Eumitria pectinata (although this is still debatable). Therefore, based on literature, 81 species are found in the Philippines following the pronounced contributions by recent studies (Table 2). This number, though, is only a mere estimate since revisions are unavoidable in taxonomic classification. The great increase in number of recorded species in the Philippines may be due to the extensive identification keys and taxonomic studies that became available worldwide (Halonen et al. 1998, Goward et al. 1994, Halonen 2000, McCune 2005, Randlane et al. 2009, Ohmura 2008, 2012, 2014, Ohmura et al. 2010, Truong et al. 2011, Shukla et al. 2014) long after the study on 42 Usnea began in the country. These keys provided better distinction of the specimens that earlier studies may have failed to do which resulted to the clustering of some morphospecies. Chemotaxonomic and molecular methods now also strongly supplement morphological and biochemical data and thus enable a more accurate characterization and identification within the lichen genus. Fig. 3 – Provinces in the Philippines reported with Usnea based on literature. Vector map obtained from Wikipedia Commons. 43 Table 2 Enumeration of Usnea spp. reported in the country and their localities Species Reported location(s) References U. australis Luzon Island Vainio (1909) U. aciculifera Bukidnon Timbreza et al. (2017) U. amabilis Bukidnon Timbreza et al. (2017) U. articulata Ifugao, Kalinga, Mountain Province U. baileyi Benguet, Bukidnon, Ifugao, Kalinga, Palawan U. barbata Bukidnon, Iloilo, Kalinga U. bismolliuscula Bukidnon Santiago et al. (2013), Galinato et al. (2017) Santiago et al. (2010; 2013), Sipman et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Madulid et al. (1989), Timbreza et al. (2017), Galinato et al. (2017) Timbreza et al. (2017) U. cavernosa Kalinga U. ceratina Benguet, Bukidnon, Kalinga U. chaetophora Bukidnon, Ifugao, Kalinga U. chrysopoda Unknown U. ciliata Luzon Island U. cornuta Benguet, Bukidnon, Ifugao, Kalinga U. dasaea Kalinga Vainio (1909) Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Galinato et al. (2017) U. dasypoga Kalinga Galinato et al. (2017) U. dimorpha Benguet Bawingan et al. (2000) U. diplotypus Bukidnon, Kalinga U. elmeri Unknown U. erecta Unknown Timbreza et al. (2017), Galinato et al. (2017) Herre (1963), Sevilla-Santos & Mondragon (1972) Herre (1963) U. esperantiana Bukidnon, Kalinga Timbreza et al. (2017), Galinato et al. (2017) U. eumitroides Unknown Herre (1963) U. filipendula Bukidnon Timbreza et al. (2017) U. flammea Bukidnon, Kalinga Timbreza et al. (2017), Galinato et al. (2017) U. flavocardia Kalinga U. flexilis Palawan U. florida U. fragilescens var. mollis Luzon Island Benguet, Bukidnon, Cavite, Ifugao, Kalinga, Nueva Ecija Bukidnon Galinato et al. (2017) Herre (1963), Sevilla-Santos & Mondragon (1972), Sipman et al. (2013) Vainio (1909) Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Timbreza et al. (2017) U. furcata Luzon Island U. glabrata Benguet, Bukidnon, Ifugao, Kalinga U. glabrescens Kalinga Vainio (1909) Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Galinato et al. (2017) U. grandisora Bukidnon Timbreza et al. (2017) U. hakonensis Bukidnon Timbreza et al. (2017) U. haumanii Ifugao Santiago et al. (2013) U. himalayana Bukidnon Timbreza et al. (2017) U. himantodes Luzon Island Stevens (2004) U. fragilescens Galinato et al. (2017) Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Herre (1963) 44 Table 2 Continued. Species Reported location(s) References U. hirta Benguet, Ifugao, Kalinga Santiago et al. (2013), Galinato et al. (2017) U. humulis Unknown Herre (1963) U. implicata Unknown Herre (1963) U. insignis Unknown Herre (1963) U. intermedia Ifugao Santiago et al. (2013) U. lapponica Kalinga Galinato et al. (2017) U. laevata Unknown U. longgisma Kalinga, Luzon Island U. marivelensis Unknown Herre (1963) Vainio (1909), Herre (1963), Galinato et al. (2017) Herre (1963) U. mearnsii Unknown Herre (1963) U. montagnei Unknown U. nidifica Bukidnon U. nidulans Ifugao, Kalinga Herre (1963), Sevilla-Santos (1965; 1979) Sevilla-Santos & Mondragon (1972), Timbreza et al. (2017) Santiago et al. (2013), Galinato et al. (2017) U. nipparensis Bukidnon Timbreza et al. (2017) U. orientalis Bukidnon Timbreza et al. (2017) U. pangiana Bukidnon Timbreza et al. (2017) U. perplexans Luzon Island U. philippina Luzon Island, Masbate U. poliotrix Bukidnon Vainio (1909) Vainio (1909), Quisumbing (1951), Herre (1963), NDIC Timbreza et al. (2017) U. praetervisa Bukidnon Timbreza et al. (2017) U. pycnoclada Laguna Vainio (1909), Herre (1963), Stevens (2004) U. pygmoidea Bukidnon Timbreza et al. (2017) U. ramosii Unknown Herre (1963) U. roseola Unknown Herre (1963) U. rubrotincta Unknown U. rubicunda Benguet, Bukidnon, Ifugao, Kalinga, Nueva Vizcaya U. rubicunda var. rosea Unknown Herre (1963), Timbreza et al. (2017) Herre (1963), Bawingan et al. (2000), Santiago et al. (2013), Timbreza et al. (2017), Galinato et al. (2017) Herre (1963) U. scabrata Bukidnon U. schadenbergiana Ifugao, Kalinga U. silesiaca Kalinga Timbreza et al. (2017) Herre (1963), Santiago et al. (2013), Galinato et al. (2017) Galinato et al. (2017) U. sorediosula Mountain Province Santiago et al. (2013) U. sphacelata Bukidnon U. squarrosa Luzon Island, Lanao del Norte U. subcornuta Benguet, Ifugao Timbreza et al. (2017) Vainio (1909), Herre (1963), Sevilla-Santos & Mondragon (1972) Santiago et al. (2013) U. subdasaea Bukidnon Timbreza et al. (2017) U. subfloridana Bukidnon Timbreza et al. (2017) U. subgracilis Benguet, Ifugao, Nueva Vizcaya Santiago et al. (2013) U. subrubricornuta Bukidnon Timbreza et al. (2017) 45 Table 2 Continued. Species Reported location(s) U. subscabrosa Benguet, Ifugao, Kalinga U. substerilis Bukidnon, Kalinga References Bawingan et al. (2000), Santiago et al. (2013), Galinato et al. (2017) Timbreza et al. (2017), Galinato et al. (2017) U. transitoria Bukidnon Timbreza et al. (2017) U. trichodea Luzon Island Vainio (1909) U. wasmuthii Bukidnon Eumitria pectinata Bukidnon, Luzon Island Timbreza et al. (2017) Motyka (1937), Herre (1963), Sipman et al. (2013), Timbreza et al. (2017) The number of Usnea species reported in the country is a proof that Philippines indeed harbor a diverse flora and fauna. The big shift in number of reported species in the country (from 32 to 81) supports the fact that Usnea and lichens, in general, are certainly understudied locally. As more places in the country remain unexplored, the more lichens are yet to be discovered. This paper may have established a new piece of information in Philippine Lichenology but it also opened a lot of questions that, hopefully, future studies may answer. It is therefore imperative to keep the series of lichenological studies on-going. Acknowledgements The authors are indebted to Dr. Arvin C. Diesmos and Dr. Cecilia I. Banag for inspiring the production of this paper and their contributions to Philippine Biodiversity and Systematic studies. This paper is especially dedicated to Prof. Dr. Thomas Edison E. dela Cruz who is a mentor to the authors. 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