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, Siesmayerstr. 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, Urediniomycetes.

Introduction Species of Septobasidium are characterized by resupinate basidiomata, production of auricularioid basidia, and association with scale insects (Couch, 1938). According to ultrastructural and molecular data, Septobasidiales are placed close to Pucciniales (former Uredinales) within the Puccioniomycotina clade (former Urediniomycetes clade) (Bauer et al., 2006). Our knowledge about the distribution, substrates, morphology, and taxonomy of Septobasidiales species is still mostly based on the monograph by Couch (1938). The nature of the ∗

Corresponding author.

insect-fungus association can be considered insect-farming by the fungus according to the life-cycle descriptions given by Couch (1938). In contrast to parasitic fungi on scale insects (hypocrealean ascomycetes and their anamorphs), which kill their host, Septobasidium species are always associated with uninfected living insects as well as infected ones. The uninfected scale insects are protected by the fungal covering and reproduce, whereas only some individuals of the insect population covered by the fungus are infected by haustorial hyphae, killed and digested. Six species of Septbasidium are known for Taiwan (Chen, 1967; Chen,

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2003; Couch, 1938; Sawada, 1931, 1959), mainly based on collections by Sawada: S. acaciae Sawada, S. albidum Pat., S. bogoriense Pat., S. citricolum Sawada, S. parlatoriae Sawada, and S. tanakae (Miyabe) Boedijn & B.A. Steinm. These species grow on stems and branches, only S. citricolum extends from branches to the leaves (Couch, 1938). Hypophyllous species of Septobasidium have hitherto not been reported from Taiwan.

Materials and Methods Specimens were collected at the Fushan Botanical Garden, Taipei and Yilan Counties in March 17, 2006. Microscopic measurements and drawings of the fungal structures were based on specimens stained with 1% aqueous phloxine and mounted in 5–10% KOH. Fungi were identified with the monograph by Couch (1938). Areas of the basidiomata were peeled off in order to discover the scale insects below. Scale insects were transferred to approx. 10% KOH and heated, washed with water and transferred to Aquatex® (Merck) in order to make permanent slides for light microscopy. For identification of the scale insects the online tools of ScaleNet (http://www.sel.barc.usda.gov/scalenet/ scalenet.htm) for family identification, and McKenzie (1945), Miller and Davidson (2005), and Takagi (1969, 1970) for identification of genera and species were used. Specimens are deposited at the herbarium of National Museum of Natural Science, R.O.C. (TNM).

Taxonomy Septobasidium humile Racib. (Figs. 1 & 3A, B)

Basidioma on abaxial side of leaf, max. 70 × 30 mm, consisting of arachnoid, white subiculum with irregular, indistinct margin up to approx. 80 µm broad, scattered ochre pillars, each pillar approx. 60 µm high and 20–30 µm wide, supporting an ochre, flat disc composed of radial hyphae, 200–400 µm diam., discs separate at the margin, becoming a continuous upper layer towards the center, layer approx. 100 µm thick, composed of interwoven, brown, 2–3 µm wide, smooth hyphae with alternate branching. The whole basidioma not exceeding 200 µm thickness, main leaf veins still visible as elevations of the basidioma, additional, inconspicuous elevations housing scale insects, some of them colonized by coiled, 2–3 µm wide hyphae. Most upper layer of the basidioma containing more strongly branched and densely septate, subhyaline or hyaline hyphae supporting probasidia. Probasidia thin-walled, globose, hyaline or subhyaline, 8–9 µm diam. Basidia arising from probasidia, strongly curved, approx. 22–28 µm long (along the curvature of the basidium), 5–6 µm wide, with 3 transversal septa and up to 12 µm long sterigmata. Basidiospores allantoid, smooth, thin-walled, 10–19 × 3–4.5 µm, aseptate, becoming 1–3-septate during germination, producing secondary spores. Material examined. Taiwan, Taipei County: Fushan Botanical Garden, ca. 600 m, on Aulacaspis tubercularis Newstead (Diaspididae) on lower surface of leaf of unidentified Lauraceae, March 17, 2006, R. Kirschner 2655 (TNM). Known habitats. Unidentified scale insects on lower surface of leaves of Tetranthera (now Litsea) sp. (Lauraceae) (Couch, 1938; Raciborski, 1909) and Aulacaspis tubercularis Newstead (Diaspididae) (new host) on unidentified Lauraceae.

Septobasidium Known distribution. Java (Couch, 1938; Raciborski, 1909) and Taiwan (new record). Septobasidium petchii Couch ex L.D. Gómez & Henk (Figs. 2 & 3C, D) Basidioma on abaxial side of leaf, max. 16 × 12 mm, without separate layers or pillars, consisting of arachnoid, white subiculum with irregular, indistinct margin and circular, flat, brown plates 0.5–1.5 mm diam. and 200 thick in some cases covering a scale insect, some of

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them colonized by branched chains of fusiform, 8–12 µm long and 3–4 µm wide cells connected by 1–2 × 0.5 µm ends. Hyphae smooth, thinwalled and hyaline or with wall up to 1 µm thick and brown, cells approx. 7–13 µm long, 2–4 µm wide, often with opposite, rectangular branching and constricted at the septa. Cells of hyphae between the plates gove rise to 1–2 lateral or terminal basidia. Basidia without probasidia, strongly helicoid or sigmoid, approx. 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.

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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 sterigmata. Basidiospores smooth, thin-walled, 8–12(–15) × 2–3.5 µm, aseptate, becoming 1septate during germination, producing secondary spores on 1–2 sterigmata. Anamorphic yeast stage. Material examined. Taiwan, Taipei County: Fushan Botanical Garden, ca. 600 m, on Parlatoria sp. (Diaspididae) on lower surface of leaf of Machilus thunbergii (Sieb. & Zucc.) Kos-

termans (Lauraceae), March 17, 2006, R. Kirschner T2677 (TNM). Known habitats. Unidentified scale insects and Parlatoria sp. (Diaspididae) (new host) on lower surface of leaves of Lasianthus sp., Machilus thunbergii, and Murraya exotica (Couch, 1938). Known distribution. Sri Lanka (Couch, 1938) and Taiwan (new record).

Septobasidium

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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 Both species of Septobasidium having hypophyllous basidiomata and curved basidia can be separated from species with corticolous habitats and/or straight basidia. Additionally, very thin basidiomata with short, knot-like pillars supporting umbrella-like disks at the margin are diagnostic characteristics of S. humile (Couch, 1938). The probasidia, however, were smaller than in the measurements by Couch (1938) and Raciborski (1909). Basidioma composition of plates without pillars, opposite rectangular hyphal branching, small spores, and lack of probasidia are diagnostic characteristics of S. petchii (Couch, 1938). The name of Sep-

tobasidium petchii was validated by Gómez & Henk (2004). Both species, previously known only from tropical Southeast Asia, were found in subtropical Taiwan. For the first time, the host insects were identified for S. humile and S. petchii. Both host species belong to the Diaspididae within the Coccoidea. The identification of Aulacaspsis tubercularis was mainly based on the divergent median lobes with serrate inner margin and the body shape with quadrate prosoma having protruding tubercles (Takagi, 1970). This species occurs on leaves and other parts of many species of several plant families, including Lauraceae, in tropical and subtropical countries, where it is a serious pest of mango (Mangifera

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indica L.) (Millar and Davidson, 2005). Parlatoria sp. could not be identified with one of the species of Parlatoria known for Taiwan (Takagi, 1969). The lobes appeared more elongate and their notches more pointed than in the otherwise similar species, P. cinerea and P. fluggeae (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-

Septobasidium Sin. 8: 130–148. Chen, M.M. 2003. Forest Fungi Phytogeography: Forest Fungi Phytogeography of China, North America, and Siberia and International Quarantine of Tree Pathogens. Pacific Mushroom Research & Education Center, Sacramento, U.S.A. Couch, J.N. 1938. The Genus Septobasidium. University of North Carolina Press, Chapel Hill. Gómez, L.D. and D.A. Henk. 2004. Validation of the species of Septobasidium described by John N. Couch. Lankesteriana 4: 75–96. n.v. Gómez, L.D. and L. Kisimova-Horovitz. 2001. A new species of Septobasidium from Costa Rica. Mycotaxon 80: 255–259. Koroch, A., H. Juliani, J. Bischoff, E. Lewis, G. Bills, J. Simon, and J. White. 2004. Examination of plant biotrophy in the scale insect parasitizing fungus Dussiella tuberiformis. Symbiosis 37: 267–280. McKenzie, H.L. 1945. A revision of Parlatoria and closely allied genera (Homoptera: Coccoidea: Diaspididae). Microentomology 10: 47–121 + figs. 27–60. Miller, D.R. and J.A. Davidson. 2005. Armored scale insect pests of trees and shrubs. (Hemiptera: Diaspididae). Cornell University Press, New York.

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Mueller, U.G. and N. Gerardo. 2002. Fungusfarming insects: multiple origins and diverse evolutionary histories. PNAS 99: 15247– 15249. Raciborski, M. 1909. Parasitische und epiphytische Pilze Javas. Bull. Acad. Scie. Cracovie 1: 346–394. Sawada, K. 1931. Descriptive catalogue of the Formosan fungi. V. Rep. Dept. Agric. Gov. Res. Inst. Formosa 51: 1–131 + 5 plates Sawada, K. 1959. Descriptive catalogue of Taiwan (Formosan) fungi. XI. Special Publ. Coll. Agric. Natl. Taiwan Univ. 8: 1–268. Schmutterer, H. 1959. Schildläuse oder Coccoidea I. Deckelschildläuse oder Diaspididae. In: F. Dahl, Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und ihrer Lebensweise. 45. Teil. Fischer, Jena, Germany. Takagi, S. 1969. Diaspididae of Taiwan based on material collected in connection with the Japan-US co-operative science programme, 1965. (Homoptera: Coccoidea). Part 1. Insecta Matsumurana 32: 1–110. Takagi, S. 1970. Diaspididae of Taiwan based on material collected in connection with the Japan-US co-operative science programme, 1965. (Homoptera: Coccoidea). Part 2. Insecta Matsumurana 33: 1–146.

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臺灣兩個 Septobasidium 屬新記錄種 羅南德1

陳啟楨2

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 Lauraceae 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 (Coccoidea) 的營養供給的專一性有關。