New Reports of Two Hypophyllous Septobasidium Species from Taiwan

Fung. Sci. 22(1, 2): 39–46, 2007 New reports of two hypophyllous Septobasidium species from Taiwan

Roland Kirschner1 and Chee-Jen Chen2∗

1. Department of Mycology, Institute for Ecology, Evolution & Diversity, J.W. Goethe-University, Siesmay- erstr. 70–72, Bldg. B, D-60323 Frankfurt, Germany. (Email: [email protected]) 2. Department of Biotechnology, Southern Taiwan University, Nan-Tai Street 1, Yungkang City, Tainan 71043, Taiwan R.O.C. (Email: [email protected]) (Accepted: April 24, 2007)

ABSTRACT

Two resupinate basidiomycetes associated with scale insects, Septobasidium humile and Septobasidium petchii, hitherto only known from Java and Sri Lanka are for the first time reported from Taiwan. Both species were collected on leaves of species of Lauraceae in the Fushan Botanical Garden, described and illustrated with drawings and photographs, and their host insects for the first time identified as members of the Diaspididae (Coccoidea). The specificity of Septobasidium species against diaspidid hosts is discussed with respect to the presumptive modes of nutrition of the Diaspididae known from literature.

Keywords: Aulacaspis tubercularis, Parlatoria, Pucciniomycotina, Septobasidium, symbiosis, Urediniomy- cetes.

Introduction insect-fungus association can be considered insect-farming by the fungus according to the Species of Septobasidium are characterized life-cycle descriptions given by Couch (1938). by resupinate basidiomata, production of auri- In contrast to parasitic fungi on scale insects cularioid basidia, and association with scale in- (hypocrealean ascomycetes and their ana- sects (Couch, 1938). According to ultrastruc- morphs), which kill their host, Septobasidium tural and molecular data, Septobasidiales are species are always associated with uninfected placed close to Pucciniales (former Uredinales) living insects as well as infected ones. The un- within the Puccioniomycotina clade (former infected scale insects are protected by the fun- Urediniomycetes clade) (Bauer et al., 2006). gal covering and reproduce, whereas only some Our knowledge about the distribution, sub- individuals of the insect population covered by strates, morphology, and taxonomy of Septo- the fungus are infected by haustorial hyphae, basidiales species is still mostly based on the killed and digested. Six species of Septbasidium monograph by Couch (1938). The nature of the are known for Taiwan (Chen, 1967; Chen,

∗ Corresponding author. 40 Fung. Sci. 22(1, 2), 2007

2003; Couch, 1938; Sawada, 1931, 1959), Basidioma on abaxial side of leaf, max. 70 × mainly based on collections by Sawada: S. aca- 30 mm, consisting of arachnoid, white subicu- ciae Sawada, S. albidum Pat., S. bogoriense lum with irregular, indistinct margin up to Pat., S. citricolum Sawada, S. parlatoriae Sa- approx. 80 µm broad, scattered ochre pillars, wada, and S. tanakae (Miyabe) Boedijn & B.A. each pillar approx. 60 µm high and 20–30 µm Steinm. These species grow on stems and wide, supporting an ochre, flat disc composed branches, only S. citricolum extends from of radial hyphae, 200–400 µm diam., discs branches to the leaves (Couch, 1938). Hy- separate at the margin, becoming a continuous pophyllous species of Septobasidium have hith- upper layer towards the center, layer approx. erto not been reported from Taiwan. 100 µm thick, composed of interwoven, brown, 2–3 µm wide, smooth hyphae with alternate Materials and Methods branching. The whole basidioma not exceeding 200 µm thickness, main leaf veins still visible Specimens were collected at the Fushan Bo- as elevations of the basidioma, additional, in- tanical Garden, Taipei and Yilan Counties in conspicuous elevations housing scale insects, March 17, 2006. Microscopic measurements some of them colonized by coiled, 2–3 µm wide and drawings of the fungal structures were hyphae. Most upper layer of the basidioma con- based on specimens stained with 1% aqueous taining more strongly branched and densely phloxine and mounted in 5–10% KOH. Fungi septate, subhyaline or hyaline hyphae support- were identified with the monograph by Couch ing probasidia. Probasidia thin-walled, globose, (1938). hyaline or subhyaline, 8–9 µm diam. Basidia Areas of the basidiomata were peeled off in arising from probasidia, strongly curved, order to discover the scale insects below. Scale approx. 22–28 µm long (along the curvature of insects were transferred to approx. 10% KOH the basidium), 5–6 µm wide, with 3 transversal and heated, washed with water and transferred septa and up to 12 µm long sterigmata. Basidio- to Aquatex® (Merck) in order to make perma- spores allantoid, smooth, thin-walled, 10–19 × nent slides for light microscopy. For identifica- 3–4.5 µm, aseptate, becoming 1–3-septate dur- tion of the scale insects the online tools of Sca- ing germination, producing secondary spores. leNet (http://www.sel.barc.usda.gov/scalenet/ Material examined. Taiwan, Taipei County: scalenet.htm) for family identification, and Fushan Botanical Garden, ca. 600 m, on Aula- McKenzie (1945), Miller and Davidson (2005), caspis tubercularis Newstead (Diaspididae) on and Takagi (1969, 1970) for identification of lower surface of leaf of unidentified Lauraceae, genera and species were used. Specimens are March 17, 2006, R. Kirschner 2655 (TNM). deposited at the herbarium of National Museum Known habitats. Unidentified scale insects of Natural Science, R.O.C. (TNM). on lower surface of leaves of Tetranthera (now Litsea) sp. (Lauraceae) (Couch, 1938; Racibor- Taxonomy ski, 1909) and Aulacaspis tubercularis New- stead (Diaspididae) (new host) on unidentified Septobasidium humile Racib. (Figs. 1 & 3A, B) Lauraceae. Septobasidium 41

Known distribution. Java (Couch, 1938; them colonized by branched chains of fusiform, Raciborski, 1909) and Taiwan (new record). 8–12 µm long and 3–4 µm wide cells connected by 1–2 × 0.5 µm ends. Hyphae smooth, thin- Septobasidium petchii Couch ex L.D. Gómez walled and hyaline or with wall up to 1 µm & Henk (Figs. 2 & 3C, D) thick and brown, cells approx. 7–13 µm long, Basidioma on abaxial side of leaf, max. 16 × 2–4 µm wide, often with opposite, rectangular 12 mm, without separate layers or pillars, con- branching and constricted at the septa. Cells of sisting of arachnoid, white subiculum with ir- hyphae between the plates gove rise to 1–2 lat- regular, indistinct margin and circular, flat, eral or terminal basidia. Basidia without pro- brown plates 0.5–1.5 mm diam. and 200 thick basidia, strongly helicoid or sigmoid, approx. in some cases covering a scale insect, some of 15–18 × 3–4 µm (measured along curvature),

Fig. 1. Septobasidium humile. A. Habitus sketch of margin of basidioma showing short-stalked umbrella-like pillars. Scale bar = 100 µm. B. Sketch of a section through a central part of the basidioma. Scale bar = 100 µm. C. Coiled haustorial hyphae. D. Hyphae bearing probasidia. E. Basidiospores. Scale bars in C–E = 10 µm.

42 Fung. Sci. 22(1, 2), 2007

Fig. 2. Septobasidium petchii. A. Habitus sketch of a part of a basidioma showing plates scattered on the subiculum. Scale bar = 1 mm. B. Section through a border of a plate-like thickening of a basidioma. Scale bar = 100 µm. C. Hyphae showing rectangular branching. These hyphae can be hyaline or pigmented. D. Hyphal apex bearing basidia. E. Basidiospores, some of them with sterigmata producing secondary spores. F. Haustorial cells. Scale bars in C–F = 10 µm. with 3 transversal septa and up to 18 µm long termans (Lauraceae), March 17, 2006, R. Kir- sterigmata. Basidiospores smooth, thin-walled, schner T2677 (TNM). 8–12(–15) × 2–3.5 µm, aseptate, becoming 1- Known habitats. Unidentified scale insects septate during germination, producing secon- and Parlatoria sp. (Diaspididae) (new host) on dary spores on 1–2 sterigmata. Anamorphic lower surface of leaves of Lasianthus sp., Ma- yeast stage. chilus thunbergii, and Murraya exotica (Couch, Material examined. Taiwan, Taipei County: 1938). Fushan Botanical Garden, ca. 600 m, on Parla- Known distribution. Sri Lanka (Couch, toria sp. (Diaspididae) on lower surface of leaf 1938) and Taiwan (new record). of Machilus thunbergii (Sieb. & Zucc.) Kos- Septobasidium 43

Fig. 3. Photographs of hypophyllous Septobasidium species and their diaspidid host insects. A. Septobasidium humile. Margin of basidioma showing short-stalked umbrella-like pillars. Scale bar = 1 mm. B. Aulacaspis tubercularis – host of S. humile. Ventral view of pygidial margin of mature female. Scale bar = 25 µm. C. Septobasidium petchii. Complete basidioma. Scale bar = 15 mm. D. Parlatoria sp. – host of S. petchii. Ventral view of pygidial margin of second instar skin. Scale bar = 25 µm.

Discussion tobasidium petchii was validated by Gómez & Henk (2004). Both species, previously known Both species of Septobasidium having hy- only from tropical Southeast Asia, were found pophyllous basidiomata and curved basidia can in subtropical Taiwan. be separated from species with corticolous For the first time, the host insects were iden- habitats and/or straight basidia. Additionally, tified for S. humile and S. petchii. Both host very thin basidiomata with short, knot-like pil- species belong to the Diaspididae within the lars supporting umbrella-like disks at the mar- Coccoidea. The identification of Aulacaspsis gin are diagnostic characteristics of S. humile tubercularis was mainly based on the divergent (Couch, 1938). The probasidia, however, were median lobes with serrate inner margin and the smaller than in the measurements by Couch body shape with quadrate prosoma having pro- (1938) and Raciborski (1909). Basidioma com- truding tubercles (Takagi, 1970). This species position of plates without pillars, opposite rec- occurs on leaves and other parts of many spe- tangular hyphal branching, small spores, and cies of several plant families, including Lau- lack of probasidia are diagnostic characteristics raceae, in tropical and subtropical countries, of S. petchii (Couch, 1938). The name of Sep- where it is a serious pest of mango (Mangifera

44 Fung. Sci. 22(1, 2), 2007 indica L.) (Millar and Davidson, 2005). Parla- toria sp. could not be identified with one of the species of Parlatoria known for Taiwan (Ta- kagi, 1969). The lobes appeared more elongate and their notches more pointed than in the oth- erwise similar species, P. ci n erea and P. flug- geae (McKenzie, 1945). Consulting the hitherto known names of host insects given by Couch (1938), Gómez & Kisimova-Horovitz (2001), and Henk (2006), we found that most of them belong to the Dias- pididae, with only few exceptions fro4& Septobasidium 45

Sin. 8: 130–148. Mueller, U.G. and N. Gerardo. 2002. Fungus- Chen, M.M. 2003. Forest Fungi Phytogeogra- farming insects: multiple origins and diverse phy: Forest Fungi Phytogeography of China, evolutionary histories. PNAS 99: 15247– North America, and Siberia and International 15249. Quarantine of Tree Pathogens. Pacific Mush- Raciborski, M. 1909. Parasitische und epi- room Research & Education Center, Sacra- phytische Pilze Javas. Bull. Acad. Scie. Cra- mento, U.S.A. covie 1: 346–394. Couch, J.N. 1938. The Genus Septobasidium. Sawada, K. 1931. Descriptive catalogue of the University of North Carolina Press, Chapel Formosan fungi. V. Rep. Dept. Agric. Gov. Hill. Res. Inst. Formosa 51: 1–131 + 5 plates Gómez, L.D. and D.A. Henk. 2004. Validation Sawada, K. 1959. Descriptive catalogue of of the species of Septobasidium described by Taiwan (Formosan) fungi. XI. Special Publ. John N. Couch. Lankesteriana 4: 75–96. n.v. Coll. Agric. Natl. Taiwan Univ. 8: 1–268. Gómez, L.D. and L. Kisimova-Horovitz. 2001. Schmutterer, H. 1959. Schildläuse oder Coc- A new species of Septobasidium from Costa coidea I. Deckelschildläuse oder Diaspididae. Rica. Mycotaxon 80: 255–259. In: F. Dahl, Die Tierwelt Deutschlands und Koroch, A., H. Juliani, J. Bischoff, E. Lewis, G. der angrenzenden Meeresteile nach ihren Bills, J. Simon, and J. White. 2004. Examina- Merkmalen und ihrer Lebensweise. 45. Teil. tion of plant biotrophy in the scale insect Fischer, Jena, Germany. parasitizing fungus Dussiella tuberiformis. Takagi, S. 1969. Diaspididae of Taiwan based Symbiosis 37: 267–280. on material collected in connection with the McKenzie, H.L. 1945. A revision of Parlatoria Japan-US co-operative science programme, and closely allied genera (Homoptera: Coc- 1965. (Homoptera: Coccoidea). Part 1. coidea: Diaspididae). Microentomology 10: Insecta Matsumurana 32: 1–110. 47–121 + figs. 27–60. Takagi, S. 1970. Diaspididae of Taiwan based Miller, D.R. and J.A. Davidson. 2005. Armored on material collected in connection with the scale insect pests of trees and shrubs. Japan-US co-operative science programme, (Hemiptera: Diaspididae). Cornell University 1965. (Homoptera: Coccoidea). Part 2. Press, New York. Insecta Matsumurana 33: 1–146.

46 Fung. Sci. 22(1, 2), 2007 臺灣兩個 Septobasidium 屬新記錄種

1 2 羅南德陳啟楨

1. 德國法蘭克福大學真菌系暨生態、演化與多樣性研究所 (email: [email protected]) 2. 南台科技大學生物科技系 (email: [email protected]) 摘要

兩種與鱗翅類昆蟲有關聯性的平貼型子實體之寄生真菌 Septobasidium humile 及 Septobasidium petchii，目前僅知曾在瓜哇及斯理蘭卡發現過，在臺灣為第一次發表。這兩種真菌採集自福山植物園，從 Lau- raceae 植物的葉片上分離，並形態描述、繪圖與照相，從文獻推測這類真菌與其宿主 Diaspididae (Coc- coidea) 的營養供給的專一性有關。