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 , its two subfamilies Heteroderinae and Meloidogyninae and the nominal genera of Heteroderinae ( 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 , 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 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. with a short stylet and large phasmids in the TYPE GENUS: Meloidogyne Goeldi, 1892 female in common with the Meloidogyninae. Syn. Caconema Cobb, 1924 It also has the excretory pore posterior to Heterodera in part of Miiller, 1884 and Goodey, the median bulb and the marking around 1932 Hypsoperine Sledge and Golden, 1964 the vulva as in the Heteroderinae. Therefore it does not appear to fit in either subfamily. DIFFERENTIAL DIAGNOSIS: The subfamily The illustrations and the description indicate Meloidogyninae can be recognized by the that it is closest to Cryphodera. Since type anterior position of the excretory pore and material or specimens were not available to the irregular perineal pattern of the body confirm this, and the original description and annulation of the female; the large lateral illustrations are not considered adequate, lips of the lip region; the weakly developed Meloidoderita is placed in genus inquirenda. 132 Journal o/ Nematology, Vol. 3, No. 2, April 1971

DIFFERENTIAL DIAGNOSIS: The subfamily fenestration around the vulva in the famale; Heteroderinae can be distinguished from the and the absence of a lens-like structure subfamily Meloidogyninae by the more pos- under the phasmids of the juveniles. terior position of the excretory pore and the absence of irregular body annules around Genus Meloidodera Chitwood, Hannon the perineum of the female; the small lateral and Esser, 1956 lips of the lip region, well developed labial (Fig. 3 A-G) framework and the longer (over 20 t~) Meloidodera Chitwood, Hannon and Esser, 1956: 264-266; Hopper, 1960:939-947. robust stylet of the second-stage juvenile; the presence of a stylet in the third- and fourth- DIAGNOSIS EMENDED: Subfamily Heter- stage juvenile; and the absence of a cap cell oderinae. Female.--No cyst stage. Cuticle terminus in the testis. annulated. Anus terminal. Vulva equatorial. Area immediately anterior and posterior to Genus Heterodera Schmidt, 1871 vulva not annulated; enclosed by regular (Fig. 3 P-W) body annules. Second-stage juvenile.- Heterodera Schmidt, 1871:1-19; Franklin, 1951: Labial disc indistinct. Stylet 25-35 tz. 1-113; Goodey, 1963:54. Esophageal glands fill body width. Phas- DIAGNOS~S EMENDED: Subfamily Heter- mids with lens-like structure in muscle oderinae. Female.--Cyst formed after death. layer. Male.---Less than 1 mm. Region Cuticle with lace-like pattern. Anus dorsal, immediately behind lip region constricted. not on vulva lip. Vulva terminal, usually on Labial disc prominent. Longitudinal stria- prominence. Cyst with clear areas around tions on basal lip annule. Tail present. vulva (fenestration). Second-stage juvenile. Spicules less than 30 ~. --Labial disc absent. Stylet less than 30 ~. TYPE SPECIES: Meloidodera floridensis Esophageal glands fill body width. Phasmids Chitwood, Hannon and Esser, 1956. without lens-like structure in muscle layer. Nominal species included: M. charis Hopper, Male.--To 1.5 mm in length. Region im- 1960. mediately behind lip region not constricted. Species inquirendae: Labial disc absent. Longitudinal striation present or absent on basal annule of lip M. armeniaca Pogosyan, 1960 region. Tail present. Spicules more than M. tadshikistanica Kirjanova and Ivanova, 30t~. 1966 TYPE SPECIES: Heterodera schachtii M. armeniaca is based on one female (31 ) Schmidt, 1871 of which the head is missing. M. tadshiki- Syn. Tylenchus schachtii (Schmidt, 1871) Oerly, stanica has characters typical for the sub- 1880 family Meloidogyninae (26), but was placed Heterodera schachtii minor O. Schmidt, 1930 in the genus Meloidodera because of the Over 40 species have been described in equatorial position of the vulva. Both of this genus. Twenty nominal species and at these species are considered inadequately de- least six species which appear to be unde- scribed and, as material was not available scribed from the nematode collection of the for study, they are considered species in- University of California, Riverside, were ex- quirendae. amined for this study. DIFFERENTIAL DIAGNOSIS: The genus The genus Heterodera can be identified Meloidodera can be distinguished from the by the cyst stage, the dorsal anus and genus Heterodera by the absence of a cyst GENERA OF SUBFAMILY HETERODERINAE • Wouts, Sher 133

stage, the subequatorial position of the vulva ond-stage juvenile.--Labial disc absent. and the annulated cuticle of the female; the Stylet less than 30 ~. Esophageal glands lens-like structure under the phasmids of do not fill body width. Phasmids with lens- the juvenile; and the small male (under 1 like structure in muscle layer. Male.--To mm), with distinct labial disc and short 1.5 mm. Region immediately behind lip spicules (less than 30/~). region not constricted. Labial disc promi- Specimens of both nominal species were nent. No longitudinal striations on basal lip available for study and in addition at least annule. Tail present. Spicules more than one undescribed species was examined. 30 ~. TYPE SPECIES: A talodera ucri new species. Genus Cryphodera Colbran, 1966 DIFFERENTIAL DIAGNOSIS: The genus (Fig. 3 H-I) Atalodera is closest to the genera Heterodera Cryphodera Colbran, 1966:41--47. and Cryphodera. It can be distinguished DIAONOSIS EMENDEO: Subfamily Heter- from Heterodera by the absence of a cyst oderinae. Female.--No cyst stage. Cuticle and the terminal anus of the female; the lens- annulated. Anus terminal. Vulva sub- like structure associated with the phasmids terminal. Area immediately anterior and and the narrow esophageal glands of the posterior to vulva not annulated; enclosed by juvenile; and the prominent labial disc of regular body annules. Second-stage juvenile. the male. It differs from the genus Cry- --Labial disc indistinct. Stylet 25-35 ~. phodera in that the cuticle of the adult female Esophageal glands fill body width. Phasmids is not annulated, and the vulva and anus are with lens-like structure in muscle layer. terminal; the narrow esophageal glands in Male.--Less than 1 mm. Region immedi- the juvenile; and the larger males with longer ately behind lip region constricted. Labial spicules. disc prominent. Longitudinal striations on The name Atalodera is derived from the basal lip annule. Tail present. Spicules less Greek atalos = "tender" and deros = "skin," than 30 ~. as modified into a Latin feminine by Schmidt TYPE SPECIES: Cryphodera eucalypti (35) for Heterodera. Colbran, 1966. Juveniles identified as Atalodera have DIFFERENTIAL DIAGNOSIS; The genus been collected from soil or roots from the Cryphodera is most closely related to the following habitats and localities in southern genus Meloidodera from which it differs only California: Haplopappus palmari Gray, in the subterminal position of the vulva. University of California campus, Riverside; The type and only named species in the Adenostoma Jasciculatum Hooker and genus was available for study. In addition, Arnott, from a hill east of the University of at least two undescribed species were ex- California, Riverside campus; Salvia sp., amined, one from Australia and one inter- Arabis pulchra Jones, Eriodictyon tricho- cepted in a sample from Oregon, U.S.A. calyx Heller and Haplopappus cooperi (Gray) Hall from several localities in the Genus Atalodera new genus Mojave Desert south of Victorville; Salvia (Fig. 1 and Fig. 3 J--O) sp. one mile northwest of Gilman Hot DIAGNOSIS: Subfamily Heteroderinae. Fe- Springs, Riverside County; oak (Quercus male.---No cyst stage. Cuticle with lace-like sp.) and Salvia sp. from Bishop Ranch, pattern. Anus and vulva terminal, on promi- Santa Barbara County; and Styrax oJficinalis nence. No fenestration around vulva. Sec- L. var. cali]ornica (Torr.) Rehd. from 134 Journal o[ Nematology, Vol. 3, No. 2, April 1971

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Fro. 1. Atalodera ucri n. gen., n. sp. (A-E, juvenile) A. Face view; B. Anterior end; C, Esophagus; D. Posterior end, lateral; E. Posterior end, dorso-ventral: (F-I, male) F. Face view; G. Anterior end; H. Posterior end, lateral; I. Posterior end, dorso-ventral: (J-L, female) J. Face view; K. Anterior end; L. Female, entire: M. Male, entire. GENERA OF SUBFAMILY HETERODERINAE ° Wouts, Sher 135

Mount Palomar, San Diego County. Some length median bulb = 23 ~; width median of these juveniles appear to represent the bulb = 23 ~; length valve in median bulb same species, but they differ from the type = 8.5 t~; width valve in median bulb = species. 6.5 ~; excretory pore from anterior end A talodera ucri n. sp. --- 102 ~ (21 ~ posterior to median bulb); (Fig. 1 and Fig. 3 J--O) vulva-anus distance = 22.5 ~; height vulva MEASUREMENTS (207 9 paratypes): L = cone = 67 t~; width cone at base = 82 t~; 501 /~ (360--680); width = 354 ~ (275- cuticle thickness at mid-body = 10 t~- Fe- 439); a = 1.5 (1.0--2.2); stylet = 29 ~ (26- male, young. Body asymmetrically swollen, 32); length styler knobs (11) = 2.4 t, (2.0- contains approximately 30 eggs; egg size 2.8); width stylet knobs (11) = 4.9 ~ (4.1- (6) 29 to 33 × 70 to 83 ~. Cuticle of head 5.5); O = 22 (13-30); length median bulb annulated from anterior end to middle of = 28 /~ (26-36); width median bulb-29 stylet, rest of cuticle with lace-like pattern. /~ (24-36); length/width ratio median bulb Lip region with distinct labial disc; first lip =0.97 (0.9-1.2); length valve in median annule prominently set off. Stylet well de- bulb= 8.5 t~ (7.2-10.0); width valve in veloped, knobs rounded. Median bulb, median bulb ---- 6.7 t~ (5.0-7.5); height vulva spherical. Dorsal esophageal gland along cone (10) = 70 ~ (56-85) ; width cone base ventral side of body; ventral glands looped (10) = 92 t~ (83-110); vulva-anus distance laterally below dorsal gland. (9) = 17.7 ~ (12-24); length vulva slit ( 7 paratypes) : Young females elongate, (11) =34 t~ (28-39); anus-phasmid dis- ovaries do not fill body, increase gradually tance (7) = 17 tz (12-21). in size to a fully swollen, spherical, old (20~ ~ paratypes): L= 1296 ~ (1036- female filled with eggs. Maximum number of 1420); a= 53 (47-63); b = 10.5 (9.4- eggs observed per female approximately 300. 12.8); b'=5.4 (4.2-7.0); c (6)=280 Vulva cone distinct, flattened posteriorly. (276-468); stylet = 27 t~ (24-29); length Body pearly white, covered with distinct sub- stylet knobs = 2.3 t' (2.0-2.6); width stylet crystalline layer. Neck bends dorsally, ven- knobs = 4.7 t' (4.0-5.5); O = 24 (15-34); trally or laterally. Labial disc in enface view hemizonid from anterior end (14) -- 142 tetraradiate, narrow lateral lips difficult to (123-178); gubernaculum = 11 ~ (10-13); see. Dorsal gland in fully swollen females spicules = 35 t~ (34-37). greatly expanded with large vacuole below (25 second-stage juvenile paratypes): L nucleus. Ventral glands appear as small ap- = 503 ~ (450-555); a=29 (25-34); b pendix below the dorsal gland. =5.3 (4.7-5.7); b'=2.3 (2.0-2.6); c= ( ~ allotype) : L = 1220 ~; a = 50.1; b = 13.4 (12.3-15.5); stylet= 24 ~t (23-25); 11.0; b'= 5.5; stylet = 28 ~; length stylet length stylet knobs = 1.7 t~ (1.5-2.0); width knobs = 2.5 t~; width stylet knobs = 5 t~; stylet knobs = 4.1 ~ (3.5-5.0);0 = 27 (21- O = 16; hemizonid from anterior end = 111 33); hemizonid from anterior end = 103 e; excretory pore--hemizonid = 9.0 t,; gu- (98-116); tail=39 ~ (29-42); H6=21 bernaculum = 11 t~; spicules = 35 t~. Lip t~ (15-24); phasmid from tail terminus = region with pronounced labial disc, four lip 31 t~ (25-36). annules. Stylet knobs sloping. Median bulb ( 7 holotype) : L = 490 t~; width = 215 16/~ long, 9 t~ wide; valve obscure. Esopha- t,; a = 2.3; stylet = 27 t~; length stylet knobs geal glands overlap five times body width, = 2 ~; width styler knobs = 4.5 t'; 0 = 20; fill ventral half of body; nuclei obscure.

~H =length of hyaline zone of the tail. Lateral field with four incisures, approxi- 136 Journal o] Nematology, Vol. 3, No. 2, April 1971

mately 1A body width wide, outer incisures juveniles, Nematology Department, Rotham- crenate. Excretory pore 4 annules anterior sted Experimental Station, Harpenden, En- to hemizonid. Body protruding around distal gland; 6 9 9, 6 ~ ~, 10 juveniles, Nema- end of spicules. Gubernaculum bow-shaped. tode Collection Agricultural University, ( ~ paratypes) : Lip region with 3-6 Wageningen, the Netherlands; 4 2 2, 6 ~ ~, annules. Excretory pore anterior, posterior 8 juveniles, Nematode Collection, Entomol- or at position of hemizonid. Esophageal ogy Research Institute, Central Experimental glands narrow, middle of overlap usually fills Farm, Ottawa, Canada; and 10 2 2, 6 ~ d, ventral half of body. All males were isolated 10 juveniles, Entomology Laboratory, De- from soil. partment of Primary Industries, Brisbane, SECOND-STAGE JUVENILES (paratypes): Queensland, Australia. Lip region with 4 annules, basal annule TYPE HABITAT AND LOCALITY: Soil and slightly wider than anterior ones. Anterior roots of Haplopappus palmari Gray in the cephalid two annules below the lip region, uncultivated eastern part of University of posterior cephalid at middle of stylet. Stylet California campus, Riverside, California. knobs round or anteriorly flattened. Pro- DIAGNOSIS: Atalodera ucri can be dis- corpus constricted immediately anterior to tinguished from the two undescribed species median bulb. Median bulb ovate. Esopha- examined by the well-developed stylet and geal glands fill about the ventral half of the the large vacuole in the dorsal esophageal body; nucleus of dorsal gland larger than gland of the fully developed female; also the nuclei of ventral glands. Hemizonid at posi- low dorsal esophageal gland opening, the tion of or one annule anterior to excretory three lateral incisures, the asymmetrical lens- pore. Lateral field with three incisures; outer like structure under the phasmid, and rela- incisures smooth; near phasmids crenate. tively short tail of the second-stage juvenile. Phasmids with asymmetrical lens-like struc- Specimens of Atalodera ucri have been ture immediately under muscle layer. collected only from the type locality. All HOLOTYPE" Female collected by W. M. stages were collected only during April, Wouts, April 14, 1969, catalog number 16 males during March and April and juveniles University of California Nematode Collec- were obtainable all year. tion, Riverside, California. ALLOTYPE: Male, same data except col- Genus Sarisodera new genus lected March 26, 1969, catalog number 17. (Fig. 2 and Fig. 3 X-AA) PARATYPES: 133 2 2, 76 $ ~, 136 ju- DIAGNOSIS: Subfamily Heteroderinae. Fe- venile paratypes from same locality as holo- male.mCyst formed after death. Cuticle type, distributed as follows: 56 e 9, 17 6 6, with lace-like pattern. Vulva sunken into 41 juveniles, Department of Nematology, terminal vulva cone. Anus on upper inside University of California, Riverside; 34 ~ 2, of dorsal vulva lip. No fenestration around 9 6 $, 23 juveniles, Department of Nema- vulva. Second-stage ]uvenile.--Labial disc tology, University of California, Davis, cata- absent. Stylet more than 38 t*. Esophageal log numbers UCNC 175-177; 10 22, 16 glands fill body width. Phasmids with lens- ~, 23 juveniles, Nematode Collection En- like structure in muscle layer. Male.--To tomology Division, DSIR, Nelson, New Zea- 1.5 mm. Region immediately behind lips land; 8 2 9,7 6 6,9 juveniles, USDA Nema- not constricted. Labial disc absent. No tode Collection, Nematology Investigations, longitudinal striation on basal lip annule. Beltsville, Maryland; 5 22, 9 6~, 13 Tail absent. Spicules over 30 t~. GENERA OF SUBFAMILY HETERODERINAE • IVouts, Sher 137

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FIO. 2. Sarisodera hydrophila n. gen., n. sp. (A-E, juvenile) A. Face view; B. Anterior end; C. Esophagus; D. Posterior end; E. Tail near phasmids, ventral view: (F-I, male) F. Anterior end; G. Esophagus; H. Posterior end, lateral; I. Posterior end, dorso-ventral: (J-L, female) J. Face view; K. Anterior end; L. Outline. 138 Journal o/ Nematology, Vol. 3, No. 2, tlpril 1971 OAOPOFN

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, 10/-I 4A,P,F,N,V 401.1 ~ J ,R I .2OO,t.l I G,I,O,W, AA

FIG. 3. Subfamily Heteroderinae. (A-B) Meloidodera [loridensis, juvenile. A. Face view; B. Phas- raids, dorso-ventral: M. charis. C. Phasmids, dorso-ventral, juvenile: (D--F, male) D. Posterior end; E. Anterior end; F. Face view: Meloidodera sp. G, Outline female: (Ill) Cryphodera sp. H. Anterior end, juvenile; I. Outline female: (J-O) Atalodera ucri n. gen., n. sp. J. Esophageal glands, juvenile; K. Phasmids, dorso-ventral, juvenile; L. Posterior end, male; M. Anterior end, GENERA OF SUBFAMILY HETERODERINAE • Wouts, Sher 139

TYPE SPECIES: Sarisodera hydrophila 481); a =- 1.5 (1.2-1.8); stylet = 51 t~ (45- new species 56); length stylet knobs = 3.3 ~ (2.6-4.1); DIFFERENTIAL DIAGNOSIS" The genus width stylet knobs = 7.3 t~ (6.0-9.0); O (6) Sarisodera is closest to the genus Heterodera = 9.0 (6.5-12.3); length median bulb = 28 with which it shares the ability to form a t~ (23-35); width median bulb = 25 ~ (19- cyst. It can be distinguished from all the 32); length/width ratio median bulb = 1.1 genera in the subfamily Heteroderinae by (0.9-1.4); length valve in median bulb = the vulva sunken into the vulva cone, the 6.4 t~ (5.1-8.5); width valve in median bulb anus located on the upper inside of the = 4.9 t~ (4.4-9.8); length vulva slit = 72 t~ dorsal vulva lip, the long stylet and the ab- (62-85). sence of the male tail. It can further be dis- (20 8 ~ paratypes): L= 1053 t~ (597- tinguished from Heterodera by the lens-like 1405); a=46 (33-55); b --- 7.3 (5.0-9.4); structure associated with the phasmids in b' -- 5.3 (4.0-6.5); stylet = 43 t~ (38-46); the juvenile. length stylet knobs = 2.7/z (2.3-3.6); width The name Sarisodera is derived from the stylet knobs = 6.5 t~ (5.0-7.0) ; O = 9.6 Greek sarisa --- "long Macedonian pike" and (7.0-12.6); hemizonid from anterior end deros = "skin," as modified into a Latin (15) = 155 tz (112-203); gubernaculum feminine by Schmidt (35) for Heterodera. (10) = 14 t~ (12-18); spicules (10) = 39 Specimens of the genus Sarisodera have t~ (33-46). been collected from soil or roots from the (25 second-stage juvenile paratypes): L following habitats and localities in Cali- -- 579 t~ (466-558); a = 26 (24-28); b = fornia: willow (Salix lasiolepis Benth.), 12 3.6 (3.3-3.9); b'= 2.2 (1.9-2.4); c=9.7 miles east of Temecula, Riverside County; (9.0-10.6); stylet = 40 ~ (39-43); length fern and Laurel sp., University of California, stylet knobs = 3.4 t~ (3.0-3.8); width stylet Berkeley; fern, Humboldt County; Lyono- knobs = 7.4 t~ (6.9-8.0); 0 = 11 (8-14); thamnus floribundus Gray, Santa Cruz Is- hemizonid from anterior end -- 122 ¢t (113- land; Pinus sp., Monterey; and Quercus sp., 131); tail = 54 t~ (44-61); H = 31 ~ (26- Santa Barbara. Specimens reported as 36) ; phasmid from tail terminus -- 46 t~ (37- Heterodera sp. by Nickle (28) from white 50). pine (Pinus monticola Dougl. ) in Idaho have ( Q holotype) : L = 610 t~; width = 385 been identified as belonging to the genus ~; a = 1.6; stylet --- 50 t~; length median bulb Sarisodera. These collections appear to --35 t,; width median bulb = 29 t~; length represent at least five species. Sufficient valve in the median bulb = 7.7 ~; width valve specimens of only the following species were in median bulb = 4.5 t~; excretory pore from available for an adequate description. the anterior end = 162 t~; thickness of cuticle at mid-body = 19 ~,. Body fully swollen, Sarisodera hydrophila n. sp. head asymmetrically placed. Cuticle with (Fig. 2 and Fig. 3 X-AA) lace-like pattern. Stylet distinctly visible. MEASUREMENTS: ( 19 2 ~ paratypes): L Median bulb oval, valve distinct. Dorsal = 565 ~ (359-688); width = 385 ~ (238- esophageal gland approximately size of <-- male; N. Face view, male; O. Outline posterior end, female: (P-W) Heterodera schachtii. P. Face view, juvenile; Q. Anterior end, juvenile; R. Esophageal glands, juvenile; S. Phasmids, dorso-ven- tral, juvenile; T. Posterior end, male; U. Anterior end, male; V. Face view, male; W. Outline posterior end, female: (X-Z, AA) Sarisodera hydrophila n. gen., n. sp. X. Phasmids, juvenile; Y. Posterior end, male; Z. Anterior end, male; AA. Outline posterior end, female. 140 Journal of Nematology, l/ol. 3, No. 2, April 1971

median bulb, ventral glands obscure. Body ( ~ paratypes) : Lip region with 5-8 with approximately 70 eggs, size of eggs (3) annules. Stylet knobs sloping. Excretory 38 to 42 x 110 ~. Vulva lips broadly pore 1-7 annules posterior to hemizonid. rounded, anus on ventral side of dorsal Esophageal glands usually fill body width. vulva lip. Males were extracted primarily from the ( 2 paratypes) : Young females oval, roots in a mist chamber. ovaries do not fill body, increase in size SECOND-STAGE JUVENILES: (paratypes) during development to old female. Fully Lip region with 4 annules. Stylet knobs flat- swollen females longer than wide. Maximum tened. Procorpus constricted immediately number of eggs per female approximately anterior to median bulb. Median bulb oval. 400. Posterior end characterized by distinct Esophageal glands fill the body width, over- vulva lips without distinct cone. Cyst yellow lap intestine ventrally and laterally; nucleus to reddish-brown. Lip region with distinct of dorsal gland larger than nuclei of ventral labial disc and prominently set off first lip glands. Lateral field with 4 ineisures. Phas- annule. Body cuticle at anterior end annu- mids with symmetrical lens-like structure lated, annulation not extending posterior to immediately under the muscle layer. middle of stylet. Median bulb usually dis- HOLOTYPE: Female collected by W. M. tinctly longer than wide. Wouts, July 19, 1969, catalog number 18 (allotype) L= 1240 ~; a = 51.7; b--- University of California Nematode Collec- 8.5; b'= 6.0; stylet--44 ~; length stylet tion, Riverside, California. knobs-- 3.5 ~; width stylet knobs = 7.5 v; ALLOTYPE: Male same data except col- O--16; length median bulb---19 ~, width lected June 26, 1969, catalog number 19. median bulb = 10 ~; length valve -- 4 ~, PARATYPES: 187 2 2, 152 6 6, 153 ju- width valve = 2 ~; hemizonid from anterior veniles distributed as follows: 98 9 2, 55 end-- 161 ~; excretory pore from anterior 6 ~, 63 juveniles, Department of Nematol- end = 177 ~; gubernaculum -- 16.5 ~; spic- ogy, University of California, Riverside; ules---45 ~. Lip region slightly set off, 6 34 9 Q, 12 6 6, 12 juveniles, Department of lip annules. Stylet knobs slightly sloping. Nematology, University of California, Davis, Lateral field with 4 incisures, approximately catalog numbers UCNC 178-181; 29 2 2, ~/~ of body width wide, outer incisures 29~ 6, 15 juveniles, Nematode Collection, crenate. Excretory pore 5 annules posterior Entomology Division, DSIR, Nelson, New to the hemizonid. Hemizonid almost 2 an- Zealand; 3 2 2, 6 ~ 6, 15 juveniles, USDA nules long. Esophageal glands overlap in- Nematode Collection, Nematology Investi- testine ventrally two times body width; an- gations, Beltsville, Maryland; 8 2 2, 13 ~ ~, terior half fills body width, posterior half 11 juveniles, Nematology Department Roth- fills % of body width; esophageal nuclei dis- amsted Experimental Station, Harpenden, tinct, of equal size, two located in anterior England; 3 2 2, 15 6 6, 12 juveniles, half, one in posterior half of overlap. Tail Agricultural University, Wageningen, the absent. Spicules almost straight, protruding Netherlands; 3 2 ~, 13 $ 6, 14 juveniles, from ventral side of body terminus in a Nematode Collection, Entomology Research conical extension of the cuticle (spicular Institute, Central Experimental Farm, Ot- sheath); spicular sheath opening with fine, tawa, Canada; and 9 92, 9 66, 11 ju- dorsal and ventral micro-spines. Gubernacu- veniles, Entomology Laboratory, Depart- lum slightly curved, anterior half wider than ment of Primary Industries, Brisbane, posterior half. Queensland, Australia. GENERA OF SUBFAMILY HETERODERINAE • Wouts, Sher 141

TYPE HABITAT AND LOCALITY: Soil and the juvenile (stylet absent in third and roots of willow (Salix lasiolepis Benth.) in fourth stage Meloidogyne juveniles); testis Arroyo River, 12 miles east of Temecula, morphology; host parasite relationships; host Riverside County, California. range; habitat; chromosome morphology, DIAGNOSIS: Sarisodera hydrophila can be number, and composition (45); and symp- distinguished from the five undescribed toms and signs of disease. On the basis of species examined, by the long stylet in all these differences Heteroderidae is considered stages, the lace-like pattern of the cuticle to contain two subdivisions as proposed by and the oval shape of the female; the four Paramonov (30). lateral incisures, the stylet with anteriorly The main features distinguishing the genera flattened knobs and the short tail of the of the subfamily Heteroderinae are listed in second-stage juvenile. Table 1 and illustrated in Fig. 3. The genera Specimens of Sarisodera hydophila have are first grouped on the basis of annulated been collected only from the type locality. and non-annulated female cuticle, then the All stages of the life cycle could be obtained latter are subdivided into cyst-forming and at any time of the year. non-cyst-forming. Several characters in the female and the male separate the non-an- KEY TO THE GENERA OF THE nulated and annulated forms. The annulated SUBFAMILY HETERODERINAE genera include MeloModera and Cryphodera. 1. Female cuticle not annulated, juveniles They differ from each other only in the without labial disc, spicules more than 30~ position of the vulva; thus the female is es- long ...... 2 Female cuticle annulated, juveniles with sential for separation of these genera. Within indistinct labial disc, spicules less than the genera with non-annulated females the 30 # long ...... 4 differences between the females, males and 2. Females not forming a cyst, esophageal glands of the juveniles do not fill the width juveniles of the non-cyst-forming, A talodera, of the body, males with labial disc ...... and the cyst-forming, Heterodera and Sari- ...... A talodera n. gen. sodera, are very pronounced. Sarisodera Females forming a cyst, esophageal glands in the juveniles fill the width of the body, is unique in having a long stylet, the sunken males without labial disc ...... 3 vulva and the anus on the inside of the 3. Vulva not sunken into a terminal cone, dorsal vulva lip. anus not on vulva lip, juvenile stylet less Within Heterodera, the largest and best than 30/~ long, males with tail ___ Heterodera Vulva sunken into a terminal cone, anus known genus, many different forms are on vulva lip, styler juvenile more than 38/z represented. Several workers have tried to long, males without tail Sarisodera n. gen. combine these. Cooper (12) used the bullae 4. Vulva close to anus (subterminal) ...... Cryphodera and number of fenestrae in the vulva cone Vulva some distance away from anus (sub- of the cyst; Decker ( 13 ), Skarbilovich (39), equatorial) ...... Meloidodera Taylor (42) and Triantaphyllou (46) used DISCUSSION the shape of the cyst to define the groups they proposed. Intensive comparative study Well defined morphological, biological of all stages of is needed for an and cytogenetic differences separate the sub- Heterodera families Heteroderinae and Meloidogyninae. understanding of the speciation and phy- These include: size of the lateral lips in the logeny within this group. lip region; position of the excretory pore and The Heteroderinae are considered to have type of cuticle in the female; length and de- evolved from slender didelphic plant-para- velopment of stylet and labial framework in sitic nematodes with annulated cuticle, short 142 Journal of Nematology, Vol. 3, No. 2, April 1971

TABLE 1. Genera-differentiating characters within subfamily Heteroderinae.

Females not annulated Females annulated non-cyst cyst-forming Comparison feature Meloidodera Cryphodera A talodera Heterodera Sarisodera

Adult size small small large large large Stylet short short short short long Vulva subequatorial subterminal subterm, subterm, subterm. Annulation, cuticle present present absent absent absent Cyst absent absent absent present present Labial disc, juvenile present present absent absent absent Longit. ann., present lip present present absent & absent absent Labial disc, present present present absent absent Constricted neck, $ present present absent absent absent Spicules short short long long long Tail, ~ present present present present absent Esoph. gland, juvenile wide wide narrow wide wide Phasmid lens, juvenile present present present absent present tail, large phasmids, longitudinally striated identical in all other characters (Fig. 3). lip annules and four lateral incisures; a form Atalodera is considered to have evolved from equal or close to the Hoplolaiminae. Sup- Cryphodera through cuticular changes which porting this theory, Heteroderinae juveniles permitted the adult to grow larger, but dis- closely resemble the recently described torted the annulation. The considerable dif- second-stage juveniles of Hoplolaimus con- ferences between Atalodera and Cryphodera, caudajuvencus, Golden and Minton, 1970 most probably indicate that several non-cyst (19) and juveniles and males of Meloidodera forming non-annulated forms developed at and Cryphodera have longitudinally striated this level of evolution of which three genera lip annules as in Hoplolaimus (37). Since are probably present in southern California. Meloidodera has a subequatorial vulva in From these, Heterodera and Sarisodera could common with species in Hoplolaiminae, that have evolved by acquiring the ability to form genus is considered most primitive. Crypho- a cyst. Heterodera developed a dorsal anus dera is considered to have evolved from in the female, lost the large phasmid in the Meloidodera via a shift of the vulva, to a juvenile, but retained the shorter stylet and more efficient posterior position which en- the short male tail of its ancestors. Simul- ables the female to lay eggs outside the taneously, Sarisodera retained the terminal roots, even when her body is still partially anus and the large phasmid in the juvenile embedded in the root. The two genera are but developed a sunken vulva in the female, GENERA OF SUBFAMILY HETERODERINAE • Wouts, Sher 143

a long stylet in all stages and lost the tail soil and plant tissue. Proc. Helminthol. Soc. in the male. These changes can be best Wash. 22:87-89. 6. C-Mix'WOOD, B. G. 1949. Root-knot nema- understood by assuming that Sarisodera and todes-Part I. A revision of the genus Heterodera evolved along two different evo- Meloidogyne Goeldi 1887. Proc. Helmin- lutionary lines, Sarisodera from a short thol. Soc. Wash. 16:90-104. 7. CHITWOOD, B. G. AND M. B. CrirrwooD. styleted, non-annulated, non-cyst forming 1950. An Introduction to Nematology. genus with a sunken vulva, as has been seen Monumental Printing Co., Baltimore. 213 in an undescribed genus from southern Cali- PP. 8. CmTWOOD, B. G., C. J. H~NON AND R. P. fornia and Heterodera from a form with a ESSER. 1956. A new nematode genus terminal vulva close to Atalodera. Meloidodera, linking the genera Heterodera The subfamily Heteroderinae is considered and Meloidogyne. Phytopathology 46:264- 266. to be a large well-defined group widely 9. COBB, N. A. 1918. Estimating the nema separated from Meloidogyninae. With the population of soil. U. S. Department of increasing number of genera it may become Agriculture, Agr. Tech. Circ. 1. 47 pp. 10. COBB, N. A. 1924. The amphids of Ca- necessary to subdivide it into groups of conema (nora. nov.) and other nemas. J. genera, probably based on the annulated Parasitol. 1I: 118-120. cuticle and the ability to form a cyst, each 11. COLBRAN, R.C. 1966. Studies of plant and soil nematodes. 12. The eucalypt cystoid group of genera representing a subfamily in nematode Cryphodera eucalypti n. g., n. sp. the family Heteroderidae. None of these, (Nematoda:Heteroderidae) a parasite of however, resemble Meloidogyninae, which Eucalypts in Queensland. Queensland J. Agr. Anim. Set. 23:41-47. would, therefore, be removed from Heter- 12. COOPER, B. A. 1955. A preliminary key oderidae. The unique characters of Meloi- to British species of Heterodera for use in dogyninae make inclusion in other families of soil examination. Soil Zoology. Proc. Univ. Nottingham Sec. Easter Sch. Agr. Sci.: the Tylenchoidea impossible and separation 269-280. of Meloidogyninae from Heteroderidae will 13. DECKER, H. 1969. Phytonematologie. Bio- therefore most probably result in elevation logie und Bek~rnpfung pflanzenparasitiirer of this subfamily to family rank. At this Nematoden. VEB Deutsch Landwirtschafts- verlag Berlin. 526 pp. time, however, such decisions are not justi- 14. DUNN, R.A. 1969. Extraction of cysts of fied. Heterodera species from soils by centrifuga- tion in high density solution. J. Nematol. LITERATURE CITED 1:7 (Abstr.). 1. ALLEN, M. W. AND S. A. SHER. 1967. Tax- 15. FILIPJEV, I.N. 1934. Nematody vrednye i onomic problems concerning the phyto- poliznye v serskom khozyaistve. Moscow parasitic nematodes. Annu. Rev. Phyto- and Lenigrad, Ogiz Selkhozgiz, 440 pp. pathol. 5:247-264. (In Russian). 2. BAINES, R. C., F. J. FOOTE, L. H. STOLZY, 16. FILIPJEV, 1. N. AND J. H. SCHULIRMANS STEK- R. H. SMALL AND M. J. GARBER. 1959. HOVEN. 1941. A Manual of Agricultural Factors influencing control of the citrus Helminthology. E. J. Brill, Leiden. 878 pp. nematode in the field with DD. Hilgardia 17. FRANKLIN, M. T. 1951. The Cyst-forming 29:359-381. Species of Heterodera. CAB publication. 3. BAKER, A. D. 1953. Rapid method for Wilding & Son, Ltd., Shrewsbury, England. mounting nematodes in glycerin. Can. 147 pp. Entomol. 85:77-78. 18. GOELDI, E. A. 1892. Relatoria sobre a 4, BAKER,A. D. 1962. Cheek Lists of the Nema- molestia do cafeiro na provincia da cafeiro tode Superfamilies Dorylaimoidea, Rhabdi- na provincia da Rio de Janeiro. Arch. Mus. toidea, Tylenchoidea and Aphelenchoidea. Nac. Rio de J. 8:7-112. E. J. Brill, Leiden. 261 pp. 19. GOLDEN, A. M. AND N. A. M1NTON. 1970. 5. CAVENESS, F. E. ANn H. J. JENSEN. 1955. Description and larval heteromorphism Modification of the centrifugal flotation of Hoplolaimus concaudajuvencus n. sp. technique for the isolation and concen- (Nematoda:Hoplolaimidae). J. Nematol. tration of nematodes and their eggs from 2:161-166. 144 Journal of Nematology, Vol. 3, No. 2, April 1971

20. GOODEY, J. B. 1963. Laboratory Methods (ed.) Trait6 de Zoologie; Classe des N6ma- for Work with Plant and Soil Nematodes. todes, Sous classe des (= Gt. Brit. Min. Agr. Fish. Food, Tech. Bull. Phasmidia Auct.). Tome IV, Fascicule III. No. 2. 72 pp. Masson et Cie., Paris. 21. GOODEY, J. B. 1963. Soil and Freshwater 35. SCHM1DT, A. 1871. t3ber den Riibennema- Nematodes. Sec. ed. Methuen & Co. Ltd., toden (Heterodera schachtii A.S.). Z. London. 544 pp. Vergl. Riibenzuckerind. Zollver. 21:1-19. 22. GOODEY, T. 1932. On the nomenclature of 36. SCHMIDT, O. 1930. Sind Riiben- und Hafer- the root-gall nematodes. J. Helminthol. 10: Nematoden identisch? Arch. Pflanzenbau. 21-28. 3: 420-464. 23. GOODEY, T. 1937. Two methods of stain- 37. SHER, S.A. 1963. Revision of the Hoplo- ing nematodes in plant tissue. J. Helminthol. laiminae (Nematoda) II. Hoplolaimus 15:137-144. Daday, 1905 and Aorolaimus n. gen. Nema- 24. GOODEY, T. 1951. Soil and Freshwater tologica 9: 267-295. Nematodes. Methuen, London. 390 pp. 38. SKARBILOVICH, T. S. 1947. K perestroikie 25. HOPPER, B. E. 1960. Contributions to the sistemtiki nematod siemiejstva Anguil- knowledge of the genus Meloidodera lulinidae Baylis and Daubney, 1962. Dokl. (Nematoda:) with a description Akad. Nauk. SSR LVII:307-308. (In of M. charis n. sp. Can. J. Zool. 38:939- Russian). 947. 39. SKARmLOVICH, T.S. 1959. On the structure 26. KIRJANOVA, E. S. AND T. S. IVANOVA. 1966. of systematics of the nematode Order First finds of root nematodes of the genus Tylenchida Thorne, 1949. Acta Parasitol. Heterodera and Meloidodera (Nematoda: Pol. 7:117-132. Heteroderidae) in Tadshikistan. Fauna and 40. SLEDGE, E. C. AND A. M. GOLDEN. 1964. zoogeography of insects in Central Asia. Hypsoperine graminis (Nematoda:Heter- Inst. Zoo1. Akad. Nauk. Tadzk. SSR. oderidae) a new genus and species of plant Dushanbe:253-260. (In Russian). parasitic nematode. Proc. Helminthol. Soc. 27. M/.JLLER, C. 1884. Mitteilungen iiber die Wash. 31:83-88. unseren Kulturpflanzen sch/idlichen, das 41. SMALL, R. H. AND R. J. MINTEER. 1969. Geschlecht Heterodera bildenden Wiirmer. Mist chamber for recovery of nematodes Landwirt. Jahrb. Schweiz 13: 1-42. from plant roots. Mimeograph, Nematology 28. NICKEL, W.R. 1960. Nematodes associated Department, Univ. of California, River- with the rootlets of western white pine in side. Northern Idaho. Plant Dis. Rep. 44:470- 42. TAYLOR, A.L. 1957. Heterodera taxonomy. 471. p. (H. taxon.) 1-12. In: E. J. Cairns (ed.) 29. OERLEY, L. 1880. Monographie der Anguil- Proceedings of the S-19 Workshop in luliden. Eine von der k. und natur- Phytonematology, 1957. (Held at the Uni- historischen Gesellschaft gekr6nte Preis- versity of Tennessee July 1-6, 1957). schrift. Termeszet. Fiizetek 4:16-177. Technical Committee of the Southern Re- 30. PARAMANOV, A. A. 1967. Critical survey gional Nematology Project (S-19), U.S. of the Suborder Tylenchina (Filipjev, Department of Agriculture. 1934) Nematoda:Secernentea. Proc. Acad. 43. THORNE, G. 1949. On the classification of Sci. SSR 18:78-101. (In Russian). the Tylenchida, new Order (Nematoda, 31. POGOSYAN, E. E. 1960. A new nematode Phasmidia). Proc. Helminthol. Soc. Wash. species Meloidodera armeniaca n. sp. 16:37-73. (Nematoda:Heteroderidae) in Armenian 44. THORNE, G. 1961. Principles of Nematol- SSR. Dokl. Akad. Nauk. Arm. SSR 31: ogy. McGraw-Hill Book Co. Inc., New 311-313. (In Russian with Armenian sum- York, Toronto, London, 553 pp. mary). 45. TRIANTAPHYLLOU, A. C. 1969. Cytogenetic 32. POGOSYAN, E. E. 1966. A new nematode evolution of the phylogeny in the family genus and species of the family Heteroderi- Heteroderidae. Proc. Syrup. Tropic. Nema- dae (Nematoda) in the Armenian SSR. tol., Univ. P. R., Rio Piedras, Puerto Rico: Dokl. Akad. Nauk. Arm. SSR 42:117-123. 11-17. (In Russian with Armenian summary). 46. TRIANTAPHYLLOU, A. C. 1970. Cytogenetic 33. RAILLIET, A. 1896. Quelques rectifications aspects of evolution of the family Heter- /i la nomenclature de parasites. Rec. Med. oderidae. J. Nematol. 2:26-32. Vet. Ecole Alfort 73:157-161. 47. WHITEHEAD, A. G. 1968. Taxonomy of 34. RITTER, M. AND J. THEODORIDES. 1965. Meloidogyne (Nematodea: Heteroderidae) Ordre des Tylenchides (= Tylenchida with descriptions of four new species. Thorne, 1949). p. 803-866. In: P. Grass6 Trans. Zool. Soc. London 31:263-401.