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New Trichomycetes from Western China Author(s): D. B. Strongman, Juan Wang and Shengquan Xu Source: Mycologia, Vol. 102, No. 1 (Jan. - Feb., 2010), pp. 174-184 Published by: Mycological Society of America Stable URL: http://www.jstor.org/stable/20619280 Accessed: 17-06-2015 12:14 UTC

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This content downloaded from 140.184.72.92 on Wed, 17 Jun 2015 12:14:02 UTC All use subject to JSTOR Terms and Conditions Mycologia, 102(1), 2010, pp. 174-184. DOI: 10.3852/09-029 ? 2010 by The Mycological Society of America, Lawrence, KS 66044-8897

New trichomycetes from western China

D.B. continued for Strongman1 surveying trichomycetes will add Saint 's to our Department of Biology, Mary University, substantially knowledge of this group. Nova Scotia, Canada B3H 3C3 Halifax, In this paper we add to the global trichomycete in a small of China Juan Wang inventory region by describing four new Shengquan Xu species, Legeriomyces grandis, Legeriosimilis Paramoebidium bacillare and Smittium shaan Normal elegans, College of Life Science, Shaanxi University, and new records for four Xi 'an, PR China xiense, recording geographic species of from China.

Abstract: Data on trichomycete biodiversity in China MATERIALS AND METHODS is with the of three new expanded description fungal were on Immature, aquatic insects collected from 11 sites species, Legeriomyces grandis, Legeriosimilis elegans, the north and south of sides the Qinling Mountains in Smittium and a Paramoebidium shaanxiense, protist, western current China May 2005-Apr 2007. The report bacillare. The distribution for the geographical includes details on the locations, collection dates and site Glotzia Smittium harpellid species, ephemeridarum, characteristics (Table I). culicis and is extended with Insect were nets Stachylina gravicaudata, specimens collected with aquatic dip their collection in western and five cm mm China, species (30 gape, 0.5 mesh) by disturbing the substrate known from Asia are also here. with the feet and the hosts in the net previously reported capturing dislodged The as well as the Key words: gut fungi, Harpellales, insect endo (kick-sampling). hindgut, peritrophic in were new matrix dipterans, dissected from insect hosts in symbionts, species water on a drops of in Petri plates the stage of stereomi a source. croscope equipped with transmitted light Tricho INTRODUCTION thalli were out of mycete teased the gut with fine-tip forceps and insect pins mounted in pin vises (Grobet USA). Thalli Symbiotic, gut-inhabiting fungi and protists (tricho were transferred to water on a slide (wet are wherever their microscope mycetes) ubiquitous aquatic a mounted) and examined with compound microscope invertebrate hosts have been examined (Lichtwardt either contrast or (with phase differential interference 1986, Lichtwardt et al 2001). However vast contrast geograph illumination) for spores and other taxonomically ical areas with suitable habitat and hosts for et potential significant characteristics (Lichtwardt al 2001). have not been were trichomycetes yet extensively surveyed Digital photomicrographs taken after semipermanent most were a (e.g. of Asia, including China). voucher slides made by infiltrating specimens with cotton cotton In China there have been few reports of trichomy drop of lactophenol blue (200 g phenol, 0.5 g 400 mL 200 mL lactic acid and 200 mL cete fungi, with Harpella melusinae L?ger & Deboscq blue, glycerol, distilled water) on the of the cover then, being the first reported trichomycete (Adler et al placed edge slip, after excess stain, the of the cover 1996). Three new Smittium spp. and five other gut removing sealing edges slip with clear et al All were recorded from the Mountains in fingernail polish (Lichtwardt 2001). fungi Qinling measurements in the below were western China and Xu et al given species descriptions (Strongman 2006). Wang cotton made from material stained with lactophenol blue. (2010) described a new genus and species, Sinotri Where possible species were identified with the LUCID chium chironomidarum S. Xu & at J.Wang, Strongman, keys for trichomycetes available the University of Kansas as well as another new et of new species, Stachylina tianensis]. Website (Lichtwardt al 2004). Voucher specimens S. Xu & both from chironomid were in Wang, Strongman, species deposited the herbarium (SANU), College larvae. Records are from of trichomycetes sparse of Life Science, Shaanxi Normal University, Xi'an, 710062, of other parts of Asia with collections in India (Misra Shaanxi, People's Republic China. 2002, Misra and Tiwari 2008) and an extensive survey in Japan by Lichtwardt et al (1987). Chien and Hsieh RESULTS (2001) documented trichomycetes from marine We recorded four new of habitats in Taiwan. Diversity of trichomycetes is species trichomycetes, eight described and four that were undoubtedly immense in China given the abundance previously species to to of habitats and suitable hosts in such a vast area, so identified only genus due either insufficient material available or to inadequate morphological data to them to a Details on Submitted 24 Feb 2009; accepted for publication 29 Jun 2009. assign species (Table II). 1 E-mail: new are below as well as the Corresponding author. [email protected] the species provided

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Table I. Collection coordinates and of sites for in dates, descriptions survey of trichomycetes Qinling Mountains, western China

Site Collection Year name number Site date Coordinates Site description

2007 Qing5 18 Apr 33?48'42"N South side Qinling Mountains, 1000 m, Hao 108?59'53"E River, Nui Bei Liang Conservation Area, shallow, rocky stream, boulders and cobblestone, pH 7.6, 15 C 18 33?48'41"N Downstream of shallow 14 Qing6 Apr Qing5, pool, pH 7.7, C 108?59'53"E of Qing7 20 Apr 33?48'47"N Upstream Qing5, shallow, rocky stream, and 108?59'49"E boulders cobblestone, pH 7.6, 13 C QingS 24 Apr 33?55'40"N North sideQinling Mountains, 1000 m, Feng Yu Forest Yu 108?50'37"E Park, Feng river, shallow, rocky stream, boulders and cobblestone, pH 8.0, 12 C

33?33'14"N side near 2006 Qingll 18 Apr South Qinling Mountains, Yue River town of shallow 108?32'25"E Xunyangba, rocky stream, boulders and cobblestone, pH 8.1, 14 C 18 South side Qingl2 Apr 33?26'01"N Qinling Mountains, Chang'an River in front of research 108?26'47"E station, Huoditang, shallow small rock and no or stream, cobble, pH temperature recorded. Qingl3 18 Apr 33?26'07"N South side Qinling Mountains, 1500 m, small stream beside research 108?26'49"E station, Huoditang, into stream m flowing Chang'an River, about 2 no or wide, shallow, cobble substrate, pH temperature recorded. QinlNl 21-Apr 33?56'42"N North side Qinling Mountains, 1000 m, Hao 108?55'33"E River, Nui Bei Liang conservation area, shallow, rocky stream, boulders and no or cobblestone, pH temperature recorded. 9 No coordinates recorded 1.5 km from QinlN2 21 Apr upstream QinlNl 10 QinlN3 21 Apr No coordinates recorded 1.5 km downstream from QinlNl as 8 Qing4 31 Dec Same site QinlNl 2005 11 Haopingsi 25Jul 34?04'87"N North side Qinling Mountains, 1300 m, shallow 107?41'64"E rocky stream, boulders and cobblestone, near research no or station, Haopingsi, pH temperature recorded. QinlNl 28 May Same site as QinlNl

names of previously described species found in these 11-12.5 um, strongly obpyriform, tapering to 6.5-8 urn collections from western China. wide distally (Figs. 1, 3) with two long, thin appendages (Fig. 3) that are not coiled within the sporogenous cell before no collar. not TAXONOMY trichospore release, Zygospores seen. In the hindgut of mayfly nymphs (Baetidae). & Legeriomyces grandis Juan Wang, Strongman S.Q. Etymology. From the Latin grandis referring to the nov. Figs. 1-3 Xu, sp. large trichospores of this species. MB 513331 Mycobank Specimens examined. CHINA. SHAANXI PROVINCE: Hao Thallus near on sparse ramosus, haptero compacto digitato River Nui Bei Liang Conservation Area the north X exoriens. Trichosporae magnae, 52-55 11-12.5 um, valde side of theQinling Mountains (site 8, Table I). Lactophenol distaliter 6.5-8 urn latae cotton blue-stained slide from the of a obpyriformes, usque attenuatae, prepared hindgut duas non helicoides intra appendices cellulam genitalem mayfly nymph (Baetidae) collected 31 Dec 2006 (HOLO ante liberationem sporarum ferentes, sine collo. Zygosporae TYPE SANU). non observatae. In Baetidarum. proctodaeo nympharum Commentary. Trichospores in Legeriomyces grandis a Thallus sparsely branched, arising from compact are longer and wider than those in any of the six holdfast X are digitate (Fig. 2). Trichospores large, 52-55 described species in the genus and strongly

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Table II. List of western trichomycete species, their hosts and collection dates from 11 sites in China

Sitea Date Species Host collected

4 Caudomyces japonicus Antocha sp. (Tipulidae) 24 Apr 2007 3 Antocha sp. 20 Apr 2007 2 Antocha sp. 18 Apr 2007 5 Antocha sp. 18 Apr 2006 11 Antocha sp. 11 July 2005; 12 Sept 2005 Gauthieromyces indiens 2 mayflies (Ephemeroptera) 18 Apr 2007 4 mayflies 24 Mar 2007 5 mayflies 18 Apr 2006 8 mayflies 28 May 2005 4 Glotzia ephemeridarumh mayflies 24 Apr 2007; 24 Mar 2007 3 mayflies 20 Apr 2007 2 mayflies 18 Apr 2007 5 mayflies 18 Apr 2006 mayflies 21Apr 2006 mayflies 31 Dec 2006 11 Legeriomyces sp. mayflies 11 July 2005 Legeriomyces grandis? mayflies 31 Dec 2006 Legeriomyces ramosus^ mayflies 31 Dec 2006 Legeriosimilis elegans 7 mayflies 18 Apr 2006 Paramoebidium bacillare 2 stonefly (Leuctridae) 18Apr 2007 Paramoebidium spp. all sites mayflies, stoneflies, midges all dates (Chironomidae) Smittium culici^ 5 midges 18Apr 2006 Smittium shaanxiense 4 midges 24 Mar 2007 6 midges 18 Apr 2006 3 midges 20 Apr 2007 Smittium simulii 4 midges 24 Apr 2007 Smittium sp. 1 6 midges 18 Apr 2006 Smittium sp. 2 11 Antocha sp. 11 July 2005 4 Stachylina gravicaudatah midges 24 Apr 2007 6 Stachylina penetralis midges 18 Apr 2006 4 midges 24 Apr 2007

aSite numbers are those in Table I. b in First records of these species China. c in are in this Species boldface newly described report.

as ramosus Thallus ramis obpyriform is the type species, Legeriomyces sparsus, 2-3 haptero cupulato quod materiam in interiore secernit exorienti Pouzar (Lichtwardt 2004). Baetimyces ancorae L.G. pariete proctodaei bus. in ramorum Valle 8c Santam. is found in mayfly hosts and Trichosporae (2-4) apicibus brevium, leniter 54-56 X 7-8 [im, 3 latas trichospores are in the same size range (Valle and obpyriformes, appendices non ferentes, sine collo. Zygosporae observatae. Ad procto Santamar?a 2002). However B. ancorae trichospores affixus. daeum nympharum Baetidarum are subcylindrical, with a small collar and have two Thallus sparse with 2-3 branches (Fig. 4) arising appendages with characteristic conspicuous coiling from a cup-shape holdfast that secretes material onto within the sporogenous cell that differ from L. grandis. the on Two Genistelloides helicoides M.C. Williams 8c hindgut lining (FlGS. 6, 7). Trichospores (2-4) species, X tips of short branches slightly obpyriform, 54-56 7 Lichtw. and Genistelloides amplispora MM. White 8c 8 with three broad no collar as well as nemouridarum um, appendages, Lichtw., Lancisporomyces (Fig. 5). Zygospores not seen. Attached to hindgut Strongman 8c MM. White, have trichospores in this of mayfly nymphs (Baetidae). size range but they are not obpyriform and inhabit the From the Latin in reference to Etymology. elegans, gut of stonefly hosts (Lichtwardt 2004). the elegant shape of the trichospores. Specimens examined: CHINA. SHAANXI PROVINCE: 8c Table blue Legeriosimilis elegans Strongman, Juan Wang S.Q. Huoditang (site 7, I). Lactophenol-cotton nov. Figs. 4-7 of a Xu, sp. stained slide prepared from the hindgut mayfly nymph 18 from a small stream Mycobank MB 513332 (Baetidae) collected Apr 2006

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to of thallus. Holdfast branched FIGS. 1-3. Legeriomyces grandis. 1. Trichospores attached fertile branches 2. (arrow) a two Bars = urn. imparting digitate appearance. 3. Released trichospore with long fine appendages (arrows). 20

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4. attached to fertile branches on the thallus. 5. Three attached and Figs. 4-7. Legeriosimilis elegans. Trichospores (arrows) one from three broad 6. Base of a thallus with holdfast trichospore detaching thallus, exposing appendages (arrow). cup-shape to Bars = (arrow). 7. Holdfast with secreted material (arrow) attaching it the hindgut lining. 20 jim.

on the running into Chang'an River, Ningshan County, come from baetid mayfly hosts but are easily distin south side of the Mountains Qinling (HOLOTYPE SANU). guished from one another by the number and of Commentary. Trichospores Legeriosimilis elegans appearance three broad appendages in L. elegans are than those in the other four longer species and two fine appendages in L. grandis. described: Legeriosimilis tricaudata M.C. Williams & Lichtw. X [(33-)47(-52) (7-)9.5(-ll) urn]; Legeriosi Paramoebidium bacillare 8c X Strongman, Juan Wang milis europaeus M.M. WHiite 8c Lichtw. (33-40 6 Xu, nov. Figs. 8-10 8 8cM.M. WHiite S.Q. sp. um); Legerisimilis leptocerciStrongman MB 513333 X 5.5-6 and Mycobank (24-28 urn) Legeriosimilis whitneyi Strong Thallus intra laterali bulboso et man 8cM.M. White X 4.5-6 proctodaeum haptero (20-26.5 urn) (Lichtwardt materia fibrosa secreta affixus. Thallus ad valde are hapteron 2004). of L. also than ex crescens brachio Trichospores elegans longer constrictus, haptero inaequaliter pro an unnamed with 30-32 X et brachio minore Legeriosimilis trichospores majore antico distaliter angustato postico 6-8 urn collected from USA et al The brachii antici Alii (White 2006). quod post extenionem partialem augescit. of L. those of status auctus non observati. Proctodaeum length elegans trichospores overlap nympharum Legeriomyces grandis described above, and both species Leuctridarum incolens.

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Thallus attached to the hindgut lining by a lateral oval, 9-12 X 4.5-7 jim, with a collar (11-14 urn) bulbous holdfast and fibrous secreted material (Fig. 16) and single appendage. Zygospores (Type X (Figs. 8, 10). Thallus strongly constricted at the II) are biconical, 56.5-67 7.5-11.5 urn (Figs. 13 on a holdfast, developing unequally from the holdfast into 15), borne zygosporophore arising directly from arm a a a larger anterior tapered distally and smaller conjugated hyphae. Zygospores have collar (15.5 arm X one posterior arm that develops after the anterior has 19.5 3-4 urn) and long, thin appendage partially extended (FlGS. 8, 9). No other developmen (Fig. 15). Attached to hindgut of midge larvae tal stages were seen. Attached to hindgut of Leuc (Chironomidae). tridae nymphs. Etymology. Derived from the location where the or Etymology. From the Latin bacillum meaning rod species was discovered, Shaanxi Province, in China. staff, in reference to the shape of the thallus. Specimens examined. CHINA. SHAANXI PROVINCE: near on Specimens examined: CHINA. SHAANXI PROVINCE: Feng Yu River Nui Bei Liang Conservation Area near Area on the the north side of the Mountains Table Hao River Nui Bei Liang Conservation Qinling (site 4, I). south side of the Qinling Mountains (site 2, Table I). Lactophenol-cotton blue-stained slide prepared from the from the of a larva collected 24 Mar Lactophenol-cotton blue-stained slide prepared hindgut midge (Chironomidae) The slide contains both hindgut of a stoneflynymph (Leuctridae) collected 18 Apr 2007 (HOLOTYPE SANU). holotype as as 2007 from a small pool in the Hao River (HOLOTYPE large and small trichospores well zygospores. Lacto blue-stained slide contains tricho SANU). phenol-cotton mostly on thalli Also Commentary. No other species of Paramoebidium spores (both types) (ISOTYPE SANU). seen collected at site 6 River 8 have vegetative thallus characteristics like those in (Qingl2), Huoditang, Chang'an 2006 and at site 3 (Table I) inHao River 20 2007, P. bacillare (Lichtwardt 2004). The bulbous Apr Apr large, on both the south side of the Qinling Mountains. holdfast and the constriction of the thallus forming Commentary. Smittium naiadis Strongman & S.Q. two unequal sections in P. bacillare distinguishes this Xu and Smittium nodifixum Strongman 8c S.Q. Xu species from Paramoebidium stipula Strongman 8c were described from chironomids, as well as Smittium MM. White from nemourid stonefly nymphs, which chinliense Strongman & S.Q. Xu from tipulid hosts, also have prominent lateral holdfast near the base of collected from the same area in western China as the thallus (Strongman and White 2006). Paramoebi Smittium shaanxiense and Xu The dium bibrachium M.C. Williams & Lichtw. and Para (Strongman 2006). other from in are species China differ trichospore moebidium papillatum Lichtw. 8c M.C. Williams dimensions and thallus characteristics, so they are found in mayfly guts and both have lateral holdfasts easily distinguished from S. shaanxiense. Several (Lichtwardt 2004), but neither have the conspicuous, Smittium are two stalked, bulbous holdfast like P. bacillare. spp. dimorphic, producing morpho logically different trichospores (Lichtwardt 2004). Of these Smittium biformeM.M. White 8cLichtw., Smittium Smittium shaanxiense 8c Juan Wang, Strongman S.Q. dimorphum Lichtw. 8cM.C. Williams, Smittium ditricho nov. Figs. 11-16 Xu, sp. sporum Strongman, Smittium esteparum Ferrington, MB 513334 Mycobank: Lichtw. & L?pez-Lastra and Smittium orthocladii Thallus densus ramificatione abunda, intra proctodaeum Manier (Lichtw.) share some characteristics with S. affixus. haptero inconspicuo Trichosporae dimorphae: shaanxiense (Lichtwardt 2004). The large trichospore magnae in medio leviter tumidae, 33.5-46 X trichosporae dimensions for S. biforme (34-42 X 9-12 um), S. 8.5-14 (xm, eolio (11-18 jim) et ?nica longo appendice (32-48.5 X (5-) 6.5-11 urn) and S. in ditrichosporum longa gracilique instructae; trichosporae parvae, quae X esteparum (31-38 4.5-6.5 urn) overlap S. shaan isdem ramis ac sporae adesse ovales, 9-12 magnae possunt, however the dimensions of the smaller tricho X et xiense, 4.5-7 (xm, collo (11-14 urn) appendice ?nica instruc tae. X spores and the zygospores differ and the Zygosporae (Typus II) biconicae, 56.5-67 7.5 trichospore in ex collars are much shorter in S. and S. 11.5 pm, zygosporophoro hyphis conjugatis directe biforme esteparum Both and small orienti portatae. Zygosporae ubi liberatae collo (15.5-19.5 (Lichtwardt 2004). large trichospores X 3-4 et ?nica tenui instructae. Ad in Smittium X 5.5-6.5 X urn) appendice dimorphum (38-50 urn, 10-12 proctodaeum larvarum Chironomidarum affixus. 5.5-6.5 jim) and 5. orthocladii [(25-) 30(-40) X (6-) X Thallus dense with prolific branching, attached to 7(-8) urn, 8-10 5-6 um)] overlap somewhat S. are the hindgut lining by an inconspicuous holdfast shaanxiense, but both large and small trichospores (Fig. 11). Trichospores dimorphic (Figs. 12, 16) narrower and the zygospores are longer in both with large trichospores slightly swollen medially, species (Lichtwardt 2004) compared to S. shaanxiense. X 33.5-46 8.5-14 urn, possessing a long (11 Several other species in this large and variable genus one 18 urn) collar and long, thin appendage have dimensions overlapping either the large or small can occur on or so accurate identification (Fig. 14). Small trichospores, which trichospore zygospore, the same branches as larger trichospores (Fig. 12), will necessitate careful examination of thallus features,

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V*

Figs. 8-10. Paramoebidium bacillare. 8. Immature thallus with bulbous holdfast (arrow) and secreted material. Note the not unequal division of the main axis of the thallus apparent in the young thallus (arrowhead). 9. Young thallus. 10. Details of = bulbous holdfast and secreted material (arrow). Bars 20 urn.

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:Vv-:.^-;v'--^

....?i#t'"'W '^ggggf^&tita F^

Figs. 11-16. Smittium shaanxiense. 11. a Basal section of thallus with inconspicuous holdfasts (arrows). 12. Fertile branch of thallus with both an at large (arrowhead) and small trichospores (arrows). Part of attached, terminal zygospore the top of the 13. Released 14. The of a a figure. zygospore. larger the dimorphic trichospores (arrow) and zygospore, both released from thallus. Note the collar on each 15. a long spore type. Released zygospore with single, fine appendage. 16. Large (arrowhead) and small both with = urn. trichospores, long collars. Note the considerable size dimorphism. Bars 20

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Figs. 17-22. Glotzia ephemeridarum. 17. Fertile thallus branchlet with five attached trichospores. 18. Released trichospore with three appendages (arrows). 19. A trichospore (arrowhead) and zygospore (arrow). 20-22. Holdfast development. 20. Bulbous basal cell with a large basal protrusion (arrow). 21. Older thallus and basal cell with three protrusions (arrows), mature = urn. presumably branches forming. 22. Swollen basal cell (arrow) of thallus with well developed branches. Bars 20

in addition to size ranges for both trichospores and 22). Two species of Smittium and several Paramoebi zygospores. dium spp. were unidentifiable due to insufficient on Other species. Four species of harpellid fungi, characteristics being available the voucher slides Caudomyces japonicus Lichtw., Kobayasi & Indoh, (Table II). Gauthieromyces indiens Misra & Tiwara, Smittium simulii Lichtw., Stachylina penetralis Lichtw., and discussion protistans (Paramoebidium spp.) all were reported Smittium simulii and Paramoebi from western China by Strongman and Xu (2006). Stachylina penetralis, dium were collected in western China Glotzia ephemeridarum Lichtw., Smittium culicis Manier spp. (Strong man and Xu and these with and Stachylina gravicaudata Siri, M.M. White & Lichtw. 2006) species along are Glotzia ramosus and reported for the first time in Asia extending the ephemeridarum, Legeriomyces Smittium which are here for the first range of these species (Table II). In Asia Legeriomyces culids, reported ramosus is known from India (Misra and Tiwari 2008) time, are all globally distributed (Lichtwardt et al but this is a first report of it from China. The 2001). Caudomyces japonicus is known only from Asia a specimens of Glotzia ephemeridarum (FlGS. 17-22) (Lichtwardt et al 1987) with second species, C had trichospore dimensions and appendages as well longicollis, found in eastern Canada (Strongman as zygospore features that were characteristic of the 2007). Gauthieromyces indiens also is known only from species (Lichtwardt 1972), but some young thalli had Asia (Misra and Tiwari 2008) and there are two other a strongly bulbous basal cell and holdfast (Figs. 20 species, the type, G. microspora Lichtw. from France

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no (Lichtwardt 1983), and G. viviparous L.G. Valle, M.M. features doubt will continue to yield many new White & Cafaro Mexico and of as are recently described from (Valle interesting species trichomycetes surveys et al conducted on a as 2008). Therefore the members of these genera larger scale, including many appear to be distributed widely. Similarly Stachylina habitats and suitable hosts as possible. gravicaudata was described only recently from USA (White et al 2006) but be distributed more might ACKNOWLEDGMENTS widely, given our collection of this species in China. We thank Most morphological features in the collection of Carolyn Bird, Chester Basin, Nova Scotia, for the Latin and for Glotzia ephemeridarum from China fit the species providing diagnoses making suggestions that the versions of the description (Figs. 17-19), however the bulbous basal helped improve English descriptions. Dr RW Lichtwardt read a draft of the and offered cell (Figs. 20, 21) on the thallus is unusual for G. paper was helpful suggestions. Financial support for the field work ephemeridarum (Lichtwardt 1972). The basal cell of provided by the College of Life Science, Shaanxi Normal the holdfast in G. ephemeridarum is branched and at University (SNNU), and both SNNU and Saint has a series of secreted holdfasts Mary's maturity peg-like to University provided money for travel DBS. Mr Yi Bai (Lichtwardt 1972), but there is considerable variation assisted us in the field and with some of the dissections. in the holdfast and associated basal cell among the Glotzia spp. (Lichtwardt 2004). For instance Glotzia a LITERATURE CITED incilis Strongman has prominent bulbous basal cell and Glotzia Gauthier ex Manier 8c Licht centroptili Adler PH, Wang Z, Beard CE. 1996. First records of natural wardt has a swollen basal cell with a lateral holdfast enemies fromChinese blackflies (Diptera: Simuliidae). 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