Journal of Nematology 30(2):232-236. 1998. © The Society of Nematologists 1998. Thripenema fuscum n. sp. (: ), a Parasite of the Tobacco , Frankliniella fusca (Thysanoptera) 1

C. TIPPING, 2 K. B. NGUYEN,2 J. E. FUNDERBURK, 3 AND G. C. SMART, JR. 2

Abstract: Thripenemafuscumn. sp., a parasite of the tobacco thrips, Franklinieltafusca, is described and illustrated from material collected from peanut (Arachis hypogaea) in Marianna, Florida. Thripenema fuscura can be distinguished from all other previously described Thripenema spp. by the dorsal curvature of the male and the presence of a stylet in the male. Highest parasitism rates of F. fusca by 7". fuscum in peanuts were 51% in 1995 and 68% in 1996. Key words: biocontrol, description, FranklinieUafusca, parasitic , key, nematode, new species, parasite, peanut, , Thripenemafuscura, Thysanoptera, tobacco thrips.

Nematodes infesting Thysanoptera were Thripenema khrustalevi from two hosts, Thrips first recorded from Europe in Thrips physo- trehernei Prisner and T. physophus L. phus L. (Uzel, 1895). Russell (1912) found a During the summers of 1995 and 1996 we nematode inhabiting the bean thrips, Helio- conducted a survey of the natural enemies thripsfasciatus (L.), in California but did not of tobacco thrips, FranklinieUafusca (Hinds), describe the nematode. Sharga (1932) de- found on 'Florunner' peanut (Arachis hy- scribed a nematode from Aptinothrips rufus pogaea L.) at the North Florida Research and (Gmelin) in England as Tylenchus aptini. Ly- Education Center field station, Marianna, saght (1936) proposed the taxon Anguillu- Florida. Several were discovered lina aptini for this species, and a year later within the abdominal cavity of an adult fe- published an ecological study of the nema- male F. fusca. After collection of additional tode including seasonal abundance and life specimens, we concluded that the nematode cycle (Lysaght, 1937). Wachek (1955) trans- represented a new species in the genus ferred A. aptini to the genus . Thripenema, which we describe herein as Nickle and Wood (1964) reported Howar- Thripenema fuscum. The new species is dula aptini infecting two species of blueberry named after the host, F. fusca. thrips, FranklinieUa vaccinii Morgan and Tae- niothrips vaccinophilus Hood. Reddy et al. MATERIALS AND METHODS (1982) reported Howardula aptini infecting Collection of nematodes: Collections of pea- Megaluriothrips sp. nut flowers began September 1995 until Oc- Siddiqi (1986) created a new genus, Thump- tober peanut harvest and again in 1996 from enema, based on host range and the oval July to October peanut harvest. Percent in- shape of the parasitic female. His revision of fection was estimated by weekly collections the genus included renaming the nema- of 35 randomly selected flowers. Flowers todes described by Sharga (1932), Nickle were gendy opened with larval forceps while and Wood (1964), and Reddy et al. (1982) submerged in a 5% formalin solution. All as T. aptini, T. nickelwoodi, and T. reniraoi, stages of thrips present were dissected. Para- respectively. Chizov et al. (1995) described sitic and unmated reproductive stage fe- males, eggs, adult males, and all juvenile stages were found. Infective stage females Received for publication 16 July 1997. also were obtained by dissecting peanut 1 Florida Agricultural Experiment Station Journal Series No. R-05834. A portion of a Ph.D. dissertation by the first author. flowers in a small dish of distilled water un- 2 Graduate Research Associate, Senior Biological Scientist, der a stereomicroscope at x35. and Professor, respectively, Entomology. and Nematology De- partment, Institute of Food and Agricultural Sciences, Univer- Light microscopy preparation: Nematode life sity of Florida, Gainesville, FL 32611-0620. stages dissected from thrips and collected s Professor, North Florida Research and Education Center, Quincy, FL 32351. from peanut flowers were transferred to E-mail: [email protected]:as.ufl.edu warm lactophenol for 3 days before mount- 232 Th~ipenema fuscum n. sp.: Tipping et al. 233 ing in glycerin on glass slides. Measurements tinuous with body, sometimes slightly offset. are given in micrometers as means +_ standard Lateral fields with two incisures forming a deviations, followed by ranges in parentheses. band occupying up to 40% of body width. Styler about three times as long as head SYSTEMATICS width (Fig. 1B), without knobs but with Thripenema fuscum Tipping and Nguyen, slight basal thickening. Stylet lumen wide. n. sp. Dorso-esophageal gland orifice about one (Figs. 1,2) stylet length posterior to stylet base. Esopha- Description gus long, posterior end reaching beyond Holotype (male): Length = 296 pro; width = mid-body (Fig. 1A). Anterior part of esopha- 13.6 pm; a = 21.6; c = 9.3; stylet length = 10.6 gus thin, less than 40 pm long, then reduced pm; spicule length -- 12.3 pro; gubernacu- posteriorly. Esophageal glands well devel- lum length = 5.5 pro; tail length = 31.8 pm. oped, long, extending to posterior third of Males (n = 11): Length = 302 + 27 (254- body, nuclei usually distinct. Nerve ring lo- 333); greatest width = 14.9 + 1.8 (12.1-16.7); cated near base of anterior part of esopha- a = 20.4 + 2.0 (17.5-23.5); c = 9.3 + 0.7 (8.4- gus. Secretory-excretory pore not observed. 10.2); stylet length = 11.4 + 2.0 (9.0-15.2); Ovary single, prodelphic. Uterus well devel- spicule length = 12.9 + 1.5 (10.3-15.2); gu- oped, containing sperm in mature females bernaculum length = 6.0 + 1 (3.6-7.0); tail (Fig. 1E). Vulva usually one or more tail length = 32.5 + 3.5 (27.3-37.8). lengths anterior to anus. Tail tapering pos- Parasitic females (n = 11): Length = 152 + teriorly to a rounded or conical tip, some- 26.8 (121.0-186.0); width = 72.8 + 9.7 (59.0- times with short hyaline portion. 94.0); a = 2.1 + 0.3 (1.6-2.5). Free-living males: Body curved dorsally Eggs (n = 13): Length = 53.6 + 9.6 (42.4- when relaxed (Fig. 2B). Lateral fields with 71.2); width = 26.8 + 5.8 (16.7-37.9). two incisures forming a smooth band (Fig. aUotype (infective female): Length = 274 pm; 2D) occupying one-fifth to one-fourth of width = 12.1 pm; a = 22.6; b = 1.5; c = 11.9; body width. Lip region usually slightly swol- esophagus length = 178 pm; stylet length = len, occasionally distinctly offset, moderately 12.7 pm; V% = 84; tail length = 23 pm. sclerotized. Stylet present (Fig. 2A), very Infective females (n = 16): Length = 257 + thin, nearly indistinguishable after fixation. 14.6 (227-279); width = 12.2 + 1.1 (10.0- Stylet base slightly thickened. Esophagus de- 13.6); a = 21.4 + 2.2 (17.0-25.5); b -- 1.5 + 0.1 generate, indistinct. Testis well developed, (1.3-1.7); c = 11.6 + 1.0 (10.5-13.0); esopha- usually occupying up to one-half of body cav- gus length = 167 + 13.6 (139-189); stylet ity diameter at mid-body and containing nu- length = 11.5 + 1.3 (9.1-13.6); V% = 81.8 + merous sperm throughout its entire length. 1.7 (78.0-84.0); tail length = 22.4 + 2.2 Spicules paired, thin. Gubernaculum (19.7-24.2). straight or slightly curved with posterior tip Parasitic females: Different stages of para- rounded, somewhat curved dorsally, well cu- sitic females found in thrips, ranging from ticularized. Caudal alae large, rounded, with slightly swollen young females (Fig. 1C) to crenate margins (Fig. 2C). fully swollen older mature females (Fig. Type host and locality 1D,F). Body of mature female oval or ellip- Tobacco thrips, FranklinieUa fusca, col- tical. Styler and esophagus indistinct or not lected from peanut, Jackson County, Marl- observed in mature females but distinct in anna, Florida, USA. younger females. Vulva subterminal. Occa- sionally, part of uterus protruding from Type specimens vulva. Ovary long, convoluted, with two or Holotype (male) and allotype (infective female): three flexures. Uterus large, usually contain- Deposited in the U. S. Department of Agri- ing a single egg (Fig. 1D,F). culture Nematode Collection (USDANC), Infective females: Body nearly straight or Beltsville, Maryland, USA. slightly curved ventrally when relaxed (Fig. Paratypes: Deposited in the USDANC, and 1A). Lip region moderately sclerotized, con- the Florida Department of Agriculture and 234 Journal of Nematology, Volume 30, No. 2, June 1998

:iii

B C

F E

FIG. 1. Thripenemafuscum n. sp., female. A) Infective female. B) Anterior region of infective female. C,D,F) Progressive enlargement of parasitic females. E) Gonad of infective female. Scale bar 26 lain for A, C, D, and F, 12 pm for B and E.

Consumer Services, Division of Plant Industry Relationships: Thripenemafuscum n. sp. can Nematode Collection, Gainesville, FL, USA. be distinguished from all other species of Diagnosis: Male large (averaging 302 pm), Thripenema by the male possessing a stylet body curved dorsally with thin stylet present. and a dorsally curved body. Further, T. fus- Spicule averaging 12.9 pro. Parasitic females cum n. sp. differs from T. reniraoi by the c- oval, averaging 152 x 73 pm. Stylet not ob- ratio (11.6 vs. 9.9) and larger eggs (55 x 27 served. Eggs large, 54 x 27 pro. Infective fe- pm vs. 30 x. 28 pm); from T. nicklewoodi by male averaging 257 pm, stylet base without parasitic female size (152 x 73 pm vs. 210 x knobs but slightly thickened; c = 11.5. 56 pm), ratio a (2.1 vs. 3.8), large eggs (55 x Thripenema fuscum n. sp.: Tipping et al. 235

D ///,

FIG. 2. Thripenemafuscumn. sp., male. A) Anterior region of male. B) Young male exhibiting slight dorsal curve. C) Bursa. D) Lateral field of male. Scale bar 14 pm for A, C, and D, 30 lam for B.

27 lam vs. 35 x 18 ~lm); from T. khrustaleviby males (11.5 vs. 13-15 lam); from T. aptini by parasitic female size (152 x 73 lam vs. 250 x parasitic female size (152 x 73 lam vs. 291 x 120 mm) and stylet length of infective fe- 75 lam) and male tail length (27-38 gm vs. 236 Journal of Nematology, Volume 30, No. 2, June 1998

21-27 pm). The following key will assist in developing in wheat (Triticum aestivum L.) identification of known Th@enema spp. and flowers of wild radish (Raphanus raphanistrum L.) during January through Key to species of Thripenema March. Thripenema fuscum has been found 1. Caudal alae reaching tail tip (pelo- parasitizing tobacco thrips collected from deran) ...... 2 these winter host plants. Caudal alae not reaching tail tip (lep- Western flower thrips, Frankliniella occi&n- toderan) ...... 3 talis (Pergande), occasionally are infected 2. Parasitic female spindle-shaped or with T. fuscum. Thripenema nicklewoodi has bean-shaped with tail ending in a been shown to readily parasitize F. occiden- sharp point; V% about 84 ...... talis (Greene and Parrella, 1995; Wilson and ...... T. nickIewoodi Cooley, 1972). Nickle and Wood (1964) re- Parasitic female oval or spherical, vulva ported that pupae of Frankliniella vaccinii terminal ...... and Taeniothrips vaccinophilus also were para- ...... T. khrustalevi sitized by T. nicklewoodi. 3. Stylet present in male, male body curved dorsally ...... T. fuscum n. sp. LITERATURE CITED Stylet absent in male, male body of curved dorsally ...... 4 Chizov, V. N., S.A. Subbotin, and N. N. Zakharen- 4. Parasitic female small, 150-225 pm kova. 1995. Thripenema khrustalevi sp. n. (Tylenchida: Allantonematidae), a parasite of Thrips (Thysanoptera) long ...... T. reniraoi in Moscow. Russian Journal of Nematology 3:89-94. Parasitic female large, 266-316 pm Greene, I.D., and M.P. Parrella. 1995. Two new long ...... T. aptini natural enemies of western flower thrips in California. Pp. 277-279 in B. L. Parker, M. Skinner, and T. Lewis, Biology eds. Thrips biology and management. Proceedings, 1993 International Conference on Thysanoptera. New Infective stage females of Thripenema fus- York: Plenum Publishing. cum n. sp. can be collected by gently swirling Lysaght, A. M. 1936. A note on the adult female of peanut flowers in a dish of distilled water. Anguillulina aptini (Sharga), a nematode parasitizing Aptinothrips rufus Gmelin. Parasitology 28:290-292. After entering the host thrips by penetration Lysaght, A.M. 1937. An ecological study of thrips through the intersegmental membrane of (Aptinothrips rufus) and its nematode parasite (Anguil- the coxal cavities, females change into the lulina aptini) Journal of Ecology 6:169-192. characteristic swollen shape for the genus. Nickle, W. R., and G. W. Wood. 1964. Howardula ap- tini (Sharga 1932) parasitic in blueberry thrips in New The ovary increases in length with several Brunswick. Canadian Journal of Zoology 42:843-846. flexures. Adult thrips and, rarely, second in- Reddy, I. N., W. R. Nickle, and P. N. Rao. 1982. Stud- stars were parasitized. Pupae were not hosts ies on Howardula aptini (Nematoda: Spaerulariidae) for T. fuscum. The ovaries of the parasitized parasitic in Megaluriothrips sp. in India. Indian Journal of Nematology 12:1-5. thrips were reduced and eggs were absent. Russell, H. M. 1912. The bean thrips (Heliothripsfas- Generally, only one parasitic female per host ciatus Pergande). U.S. Department of Agriculture En- was present, but occasionally two or three tomology Bulletin 118:1-45. were observed. Although up to 175 imma- Sharga, U. S. 1932. A new nematode, Tylenchus aptini sp. n., a parasite of Thysanoptera (Insecta: Aptinothrips ture nematodes were dissected from one in- rufus Gmelin). Parasitology 24:268-279. sect, usually only 40 to 50 were present. Af- Siddiqi, M.R. 1986. Tylenchida: Parasites of plants ter development within the host, free-living and . St. Albans, UK: Commonwealth Institute of males and females exited thrips via the anus Parasitology. as reported by Lysaght (1937) for T. aptini Uzel, H. 1895. Monographie der Ordnung Thysa- noptera. K6niggr/ttz, Germany: Tolman. and Nickle and Wood (1964) for T. nickle- Wachek, F. 1955. System und Biologie der entopara- woodi. Mating of T. fuscum probably occurs sitischen Tylenchida. Parasitologische Schriftenreihe 3: in the peanut flowers. 1-119. Highest rates of parasitism of F. fusca in Wilson, T. H., and T. A. Cooley. 1972. A chalcidoid planidium and an entomophilic nematode associated peanut by T. fuscum was 51% in 1995 and with the western flower thrips. Annals of the Entomo- 68% in 1996. In Florida, F. fusca is found logical Society of America 65:414-418.