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The Genera of the Subfamily Heteroderinae (Nematoda: Tylenchoidea) with a Description of Two New Genera 1

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The Genera of the Subfamily Heteroderinae (Nematoda: Tylenchoidea) with a Description of Two New Genera 1 The Genera of the Subfamily Heteroderinae (Nematoda: Tylenchoidea) with a Description of Two New Genera 1 W. M. WOUTS2 AND S. A. SHERa Abstract: The family Heteroderidae, its two subfamilies Heteroderinae and Meloidogyninae and the nominal genera of Heteroderinae (Heterodera Schmidt, 1871; Meloidodera Chitwood, Hannon & Esser, 1956; and Cryphodera Colbran, 1966) are rediagnosed. Meloidoderita Pogosyan, 1966 is considered a genus inquirenda. Two new genera from southern California are described in the subfamily Heteroderinae. A key to the genera, illustrations and a phylogeny of the Heteroderinae are proposed. Key Words: Heteroderidae, Heteroderinae, Meloidogyninae, Heterodera, Meloidodera, Cryphodera, Meloidoderita, Sarisodera n. gen., Atalodera n. gen., Taxonomy, Phylogeny, Key. The subfamily Heteroderinae Filipjev and It was Thorne's 1949 classification of the Schuurmans Stekhoven, 19414 (16) was in- family Heteroderidae that became generally troduced for the genera Heterodera Schmidt, accepted (1, 21, 24, 34). 1871 (35), Paratylenchus Micoletzky, 1922 Thorne (43) included in the subfamily and Tylenchulus Cobb, 1913. In 1947 Skar- Heteroderinae the genera Heterodera and bilovich (38), on the basis of sexual dimor- Meloidogyne Goeldi, 18925 (18), thereby phism (swollen females), proposed the fam- accepting the genus Meloidogyne for the ily Heteroderidae for Heteroderinae and the root-knot nematodes, as proposed by Chit- new subfamily Tylenchulinae. In 1949 wood (6) that same year. Thorne (43), independently, also proposed The genus Meloidodera Chitwood, Han- Heteroderidae. Basing it on the shape of non and Esser, 1956 (8) was described with the female body, the short rounded male tail juveniles similar to Heterodera but with an- and the absence of caudal alae, he included nulated females and no cyst formation. It only the subfamily Heteroderinae. Chitwood was, therefore, considered the link between Heterodera and Meloidogyne. Skarbilovich and Chitwood (7) included Hoplolaiminae (39) placed Meloidodera in the subfamily Filipjev, 1934 and the new subfamily Nacob- Heteroderinae, most other workers (1, 8, binae in this family and Skarbilovich (39) 21 ), however, did not recognize this sub- added Sphaeronematinae Raski and Sher, family and placed Meloidodera in Heter- 1952 and the new subfamily Meloidogyninae. oderidae. Paramonov (30) included only two sub- Since 1956 the genera Cryphodera Col- families, Heteroderinae and Meloidogyninae. bran, 1966 (11), from Australia; Meloido- derita Pogosyan, 1966 (32), from Russia; Received for publication 16 July 1970. and Hypsoperine Sledge & Golden, 1964 t Portion of a Ph.D. thesis submitted by the senior author at the University of California, Riverside. (40) from the U.S.A. have been described. Graduate Research Assistant, Department of Nematology, Hypsoperine was synonymized with Meloi- University of California, Riverside 92502. Now at Ento- mology Division DSIR, Nelson, New Zealand. dogyne by Whitehead (47). a Nematologist, Department of Nematology, University of California, Riverside 92502. The following persons A survey of the nematode collection of the kindly supplied specimens for this study: M. W. Allen, University of California, Riverside, revealed R. C. Colbrau, A. M. Golden, O. J. Raski, D. W. Ricker and A. C. Weiner. Baker's (4) assignation of this subfamily is considered The name Meloidogyne was not published until 1892 correct. and this date is considered correct. 129 130 Journal of Nematology, Vol. 3, No. 2, April 1971 many specimens closely related to Heter- roots were fixed by adding 5 ml of boiling odera, Meloidodera, Cryphodera and Meloi- 4% formalin to approximately 5 ml of an doderita which seemed to form a natural aqueous nematode suspension. After at least group (Heteroderinae) within the family four days in this fixative they were processed Heteroderidae. Although many new forms to glycerine, either through the "Baker rapid (genera and species) were recognized after method" (3) or a modified "slow glycerin a comparative study, only two new species method" (44) in which the cuticles were representing two new genera are being de- punctured with a fine needle to allow the scribed in this study because of insufficient glycerin to enter. The nematodes were and/or poorly preserved material for the mounted in dehydrated glycerin between remaining new forms. cover glasses held in aluminum slides. The anterior end of the female specimen MATERIALS AND METHODS was studied after it had been severed with a This study was primarily based on pre- surgical blade under the dissecting micro- served specimens in the nematode collection scope and mounted as described above. of the Department of Nematology, University When structures to be measured and studied of California, at Riverside. Additional pre- required a particular orientation, specimens served specimens were obtained from the were mounted in glycerin jelly (20). nematode collections of the University of California, Davis; the USDA Plant Industry SYSTEMATICS Station, Beltsville, Maryland; the Queens- Family Heteroderidae (Filipjev & Schuur- land Department of Primary Industries, Bris- mans Stekhoven, 1941 ) Skarbilovich, bane, Australia; and the California State De- 1947 partment of Agriculture, Sacramento. Fresh Heteroderidae: Filipjev & Schuurmans Stekhoven, specimens of the proposed new genera were 1941:159; Thorne, 1949:40; Chitwood & Chit- collected from soil and root samples from wood, 1950:14; Skarbilovich, 1959:120-129; Baker, 1962:172; Goodey, 1963:54. their type localities; from the University of California, Berkeley; and from Santa Cruz DIAGNOSIS EMENDED: Superfamily Ty- Island, off the coast of southern California. lenchoidea (Filipjev, 1934) Chitwood and Over 1400 females and cysts, 600 males and Chitwood, 1937. Female.--Swollen to sub- 2600 juveniles, representing three nominal spherical, sedentary, didelphic. Excretory genera, 23 nominal species, two new genera pore in anterior part of body. Tail absent. and species, two undescribed genera and 12 Anus located terminally or dorsally. Pro- undescribed species in the subfamily Heter- corpus and median bulb not amalgamated. oderinae were examined during this study. Median bulb ovate to spherical, with well Material was isolated from soil by a developed musculature and crescentic valve modified combination of Cobb's (2, 9) sift- plates. Esophageal glands overlap the in- ing method and sugar flotation (5, 14). The testine ventrally. Second-stage juvenile.- stages attached to roots were obtained by Vermiform; infective, migratory stage. boiling infected roots for 30 sec in acid- Third-stage juvenile.---Swollen with short, fuchsin-lactophenol, clearing overnight in blunt tail. Fourth-stage juvenile.--Swollen lactophenol and dissecting the roots for with terminal anus. Male.---Vermiform, nematodes (23). Males were extracted from migratory. Body twisted as much as half a soil or from infected roots in a mist chamber turn (180 ° ) in passing from head to tail. (41). All stages extracted from soil and Tail very short or absent. Caudal alae ab- GENERA OF SUBFAMILY HETERODERINAE ' Wouts, Sher 131 sent. Stylet and cephalic framework well labial framework and short, moderately de- developed. veloped stylet in the second-stage juvenile TYPE GENUS: Heterodera Schmidt, 1871 (under 20 ~); and the cap cell terminus of the testis in the male. Syn. Heterobulbus Railliet, 1896 (Heterodera) Skarbilovich, 1959 (Globodera) Skarbilovich, 1959 Subfamily Heteroderinae Filipjev & Nominal subfamilies included: Heteroderinae Schuurmans Stekhoven, 1941 Filipjev & Schuurmans Stekhoven, 1941. Heteroderinae Filipiev & Schuurmans Stekhoven, Meloidogyninae Skarbilovich, 1959. 1941:159; Skarbilovich, 1959:120-129; Para- The family Heteroderidae can be distin- monov, 1967:79. guished from the other families in the Tylen- DIAGNOSIS EMENDED: Family Heterod- choidea by the swollen to subspherical eridae. Female.---No irregular body annules didelphic female without a tail; the swollen around perineum. Excretory pore posterior third- and fourth-stage juvenile; the twisted to median bulb. Lip region with two lateral body of the male with very short or absent lips narrower than four sublateral. Stylet tail lacking the caudal alae. more than 20 ~. Second-stage juvenile.- Lips of labial region similar to female with Subfamily Meloidogyninae well developed framework. Stylet robust, Skarbilovich, 1959 more than 20 t~. Third- and fourth-stage Meloidogyninae Skarbilovich, 1959:122, 127; Para- juvenile.--Stylet well developed, more than monov, 1967:74. 20 ~. Male.--Lips and labial region similar DIAGNOSIS EMENDED: Family Heterod- to female. Testis single, with blunt anterior eridae. Female. Cuticle annulated, annules end. irregular and discontinuous around per- TYPE GENUS: Heterodera Schmidt, 1871 ineum. Excretory pore opposite or anterior Syn. Heterobulbus Railliet, 1896 to medium bulb. Lip region with two lateral (Heterodera) Skarbilovich, 1959 lips wider than four sublateral. Stylet less (Globodera) Skarbilovich, 1959 than 25 ~. Second-stage ]uvenile.--Lips of Nominal genera included: labial region similar to female. Stylet moder- Meloidodera Chitwood, Hannon and Esser, 1956 Cryphodera Colbran, 1966 ately developed, less than 20 t~. Third- and Atalodera, new genus fourth-stage juvenile.--Stylet absent. Male. Sarisodera, new genus --Lips of labial region similar to female. Genus inquirenda: Meloidoderita Pogosyan, 1966 Testis 1 or 2, anterior end with cap cell The genus Meloidoderita was described terminus.
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