Description of a new tropical Heteroderidae, Hylolzerna ivorense n. gen., n. sp., and a new outlook on the family Heteroderidae (Nematoda : Ty1enchda)b

Michel Luc, Donald P. TAYLORand Patrice CADET Muséum national d’Histoire naturelle, Laboratoire des Vers, 43 rue Cuvier, Paris, France; Laboratoire de Nématologie, ORSTOM, B.P. 1386 Dakar, Séne‘gal and Laboratoire de Nématologie, ORSTOM, B.P. V51, Abidjan, Côte d’Ivoire.

SUMMARY Hylonema, a new in the Heteroderidae from , is described and illustrated with H. ivorense n. sp. described and designated the type species. The authors suggest that the division of the Heteroderidae into the Heteroderinae, Meloidoderinae and Ataloderinae is highly artificial and servesno useful purpose ; it is proposed to abandon the use of these subfamilies. Zelandodera is considered a junior synonym of Cryphodera resulting in the following nomenclatorial changes : C. podocarpi (Wouts, 1973) n. comb. ; C. nothophagi (Wouts, 1973) n. comb. and C. cozi (Wouts, 1973) n. comb. Sherodera is considered a junior synonym of Atalodera and S. lonicerae becomes A. lonicerae (Wouts, 1973) n. comb. Thus, the family Heteroderidae isconsidered to consist of the following genera : Heterodera Schmidt, 1871 ; Globodera (Skarbilovich, 1959) Mulvey & Stone, 1976 ; Punctodera Mulvey & Stone, 1976 ; Sarisodera Wouts & Sher, 1971 ; Meloidodera Chitwood, Hannon & Esser, 1956 ; Cryplzodera Colbran, 1956 ; Atalodera Wouts & Sher, 1971 and Hylonema n. gen.

RÉSUMÉ I Description d’un nouvel Heteroderidae tropical, Hylonema ivorense n. gen., n. sp., et considérations sur la famille des Heteroderidae (Nematoda : Tylenchida). Les auteurs décrivent un nouveau genre d’Heteroderidae, Hylonelna n. gen., ayant pour type et unique espèce Hylonema ivorense n. gen., n. sp. observé sur de jeune avodirés( africana)en Côte d’Ivoire. Se fondant sur les caractéristiques de ce nouveau genre, les auteurs proposent d’abandonner l’usage des sous-familles généra- lement admises chez les Heteroderidae (Heteroderinae, Mcloidoderinae et Ataloderinae). Le genre Zelandodera est considéré comme synonyme de Cryphodera, entrahant les changèments de nomenclature suivants : C. podocarpi (Wouts, 1973) n. comb., C. notophagi (Wouts, 1973) n. comb., C. cozi (Wouts, 1973) n. comb. De même, Sherodera est considéré comme synonyme d’iltalodera et S. lonicerae devient A. lonicerae (Wouts, 1973) n. comb. La famille des Heteroderidae comprend donc les genres suivants : Heterodera Schmidt, 1871 ; Globodera (Skarbilovich, 1959) Mulvey & Stone, 1976 ; Punctodera Mulvey & Stone, 1976 ; Sarisbdera Wouts & Sher, 1971 ; Meloidodera Chitwood, Hannon & Esser, 1956 ; Cryphodera Colbran, 1956 ; Atalodera Wouts & Sher, 1971 et Hylonema n. gen.

Juveniles and males of a previously unknown Luc, 1978). Detailedmorphological and anato- member of theHeteroderidae were recovered mica1 studies of thenematode were made by one of the authors (P.C.) from soi1 collected resulting in the descriptionof Hylonema ivorense aroundthe roots of “avodiré”, Turraeanfhus n.gen., n. sp. given below. africana Pellegr.,growing in a tropicalrain- Ourinability to include this newgenus in forestreserve at Banco,Ivory Coast. Exam- any of theexisting subfamilies of the Hete- ination and dissection of the roots of this -tree roderidae indicated the importanceof examining revealed the presence of saccate females of an thevalidity of thesesubfamilies and some of undescribedgenus. The description of the the more recently described genera in order to uniquehost-parasite relationship observed is develop a meaningfulorganization of this given in a subsequent article (Taylor, Cadet & family.

Reu. Némafol. 1 (1) : 73 ù 86 (1978) 73 M. Luc, D. P. Taylor dl- P. Cadet

Materials and methods = 36 pm (33-39.5) ; anterior portion of stylet = 18.5 pm (16-21) ; m = 51 (47-55) ; stylet knobs Living males andjuveniles were isolated (h x w) = 3.0 x 6.5 pm (2.5-3.5 x 5.5-8) ; from soi1 bystandard extraction techniques. O (n = 15) = 12.4 (8-16) ; median bulb ( 1 x w) Specimens were killed and fixed with FP 4 : 1 (n = 11) = 11 x 16.5 pm (10-12 x 15-19) ; (Netscher & Seinhorst,1969) and mounted in distance from anterior end to center of median glycerin on Cobb slides according to the rapid bulb = 88.5 pm (85-93) ; hyalineterminal method of Seinhorst (1959). port.ion of tail (“h”) = 70.5 pm (55-88) ; h as % Femaleswere obtained by carefuldissection tail length = 84 (77-92). of infected avodiré roots which had been fixed Holotype (female) : L = 0.42mm ; width = in F.A.A. for 48 hours or longer. Intact females 0.20 mm ; L/w = 2.1 ; stylet = 42 pm ; dist. were mountedin glycerinon Cobb slides as vulva to anus = 19 pm. above. Vulval cones were prepared by dissecting the posterior portion of fixed females, removing the bodycontents in lactic acid (Taylor & Netscher, 1974) and mounting in glycerin jelly DESCRIPTION on Cobb slides. Specimenswere prepared forstereoscan Fernales : Body size andshape variable, electron microscope study (S.E.M.) as described generallyelongated and swollen one wayor bySher and Bell(1975). Conventional optical another ; anterior portion (t( neck P) relatively photomicrographs were madewith Leitza longand distinct from rest of body.Body “Orthomat” photomicroscope. swelling usually progressive withthe largest part of thebody located either anteriorly or posteriorly (apparently depending on its ability ta develop withinhost tissues). Posterior extremity generally rounded in profile, flattened Hylonema ivorense n.gen., n.sp. betweenvulva and anus. Vulva subterminal ; vulval lips not observedin profile. MEASUREMENTS Cuticle ’ thickened, 5 pm anteriorlyand 10-13 pm at centraland posterior portions ; apparently composed of two layers : an interna1 Females : (n = 39) : L = 0.61 mm (0.34-1.01) ; hyaline layer and an external irregularly cracked width = 0.23 mm (0.16-0.34) ; L/w = 2.5 layerproduckg a very rugosesurface (sorne- (1.9-4.6) ; stylet(n = 5) = 41 pm (38-46). what resemblingyounga Heterodera cyst). Males : L (n = 50) = 1.02 mm (0.65-1.42) ; Cuticularsurface with relatively deep, non- a(n = 26) = 39(32-47) ; b(n = 25) = 6.9 oriented striae ; no punctations as in Heterodera (5.4-7.9) ; b‘ (n = 25) = 4.4(3.3-6.2) ; stylet and Sarisodera. (n = 25) = 40.5 pm (38-44) ; anterior portion “Head” conical but of unusualappearance of stylet = 22 pm (19.5-24.5) ; m = 54 (51-56) ; withthe c.uticular structure contrasting with styletknobs (h x w) = 3 x 7 pm (2.5-4.0 that of the restof the body; for thefirst 15-23 pm x 6-10.5) ; O = 8 (5-11) ; spicules (n = 25) = from the anterior end the cuticleis thin (0.6- 32 pm (27-36.5) ; gubernaculum (n = 25) = 1.0 pm) and marked by 15-20 regular transverse 11 pm (9-13) ; medianbulb (1 x w) (n = 13) striae.In lateral view (opticalmicroscope), 13.5 X 9 pm (11.5-18 x 8.5-10.5) ; distance from the first5 or 6 annules appear more distinct and anterior end to center of median bulb (n = 13)= separated, but no distinct labial annules could 94.5 pm (80-110). be discerned. If they correspond to the position Juveniles(2nd stage) : L(n = 50) = 0.64 of t.he cephalic framework, there are 2-3 labial (0.60-0.73) ; a (n = 25) = 30 (25-36) ; b (n = 23) annules. En face view (S.E.M.) shows a roughly = 5.2 (4.1-5.8) ; b’ (m = 25) = 2.5(2.2-2.9) ; quadrangular(rarely triangular) first annule tail length (n = 25) = 83.5 pm (70-96) ; c = (orlabial disc) (Fig. 3, C-D), whichis very 7.9 (7.1-8.9) ; c’ = 6.1 (4.4-6.8) ; stylet (n = 25) distinctand narrower than the next annule.

74 Rev. Nématol. 1 (1) : 73 d 86 (1978) Fig. 1 : Hylonema ivorense n. gen., n. sp. : Female : A-G : outline of body ; 1 : cesophageal portion ; 3, I< : fore part ; L : posterior part (a: muscles ; b : underbridge). Abnormal female : H : outline of the body ; M : postvulval portion. Hylonema ivorense n. gen., n. sp. Femelles : A- G : profils du corps ; I : région œsophagienne ;J, Ii :partie antérieure; L :partie postdrieure (a : muscles; b : pont inprieur). Femelle aberrante : H:profi.! du corps ;iM: partie post-vulvaire.

Rev. Nématol. 1 (1) : 73 & 86 (1978) 75 M. Luc, D.P. Taylor & P. Cadet

Buccal apertureroughly hexagonal ; no elongated and irregularly cyclindrical( length = amphidialapertures observed. The next (2nd) 240 pm ; max.diameter = 60pm). The tail annule,rounded and larger, has irregularly ishemispherical (length = 19 pm ; c' = 0.5) ; scattered rounded protuberances. A hexaradiate no phasmids were observed(Fig. 1, H, M). basalplate is seen in en face view (optical &lales : Bodystraight or weaklycurved, microscope). Stylet long and slender ; anterior elongate,cylindrical, slightly more slender at portionslightly longer than posterior ; stylet theanterior end. A distinct narrowing of the knobsgenerally rounded with flattened or body occurs at the level of the junction of the slightlypointed anterior surfaces. Dorsal oeso- two parts of the stylet giving this part of the phagealgland duct opening approximately body a slightlyconical appearance. Body 5 pm posterior to stylet base. generallytwisted throughout its length ; an- Procorpusmassive, constricted at junction terior and posterior extremes forming an angle with metacorpus whichis enlarged and nearly of 900 with longitudinal axis. spherical(37 x 34pm) with well developed Cuticle distinctlyannulat,ed, average width valveplates (7 x 5 pm).Isthmus short ; of annules 2.5 pm at middle of body.Lateral basal glandular portion containing a very large field with four lines occupying one-fourth body anteriornucleus and two smaller posterior diameter at middle of body.Lines of lateral nuclei. field not fused in posterior portion of body. Excretorypore small, difficult, tolocate. In two females it was located 136 and 184 pm ' Labial region rounded',in relief, separated from t.he anterior end, at the level of the basal fromrest of bodyby a distinctincisure ; bulb of the oesophagus.Nerve ring thin, 5.5 pm (4-6.5)high and10 pm (8-11.5) wide ; surroundingist.hmus. Hemizonid, hemizonion, with 4-5 annules.Anterior annule wider than phasmids, cephalids not observed. others. Labial disc present, difficult to see with Intestine not observed ; anus terminal, pore- optical microscope. En face view with S.E.M. like, 16-20 pmfrom vulva. (Fig. 3, A)shows generallya rectangularly Genitalbranches two, convoluted. Vulva shapedbuccal opening elongated dorso-ven- a slit43 pm (40-46) long,located in a slight trally anda labial discalso generally rectangular, depressionapproximately 8 pm below surface rounded atthe corners, andthinner at the of posterior terminus. No bullae or fenestration center. The long axisof the disc is dorso-ventral. observed.Underbridge conspicuous incertain Amphidial openings are transverse dits located specimens,located 43-54 pm below level of at the edge of the labialdisc. Cephalic sclero- vulva and parallel to it. Length of underSridge tizationstrong. Basal plate convex, angular variable depending on size of female ; average anteriorlyand not extending belowlevel of length 156pm. An expandedcentral area incisure separating lip region from rest of body. present,54 pm longand 36 pm wide, with a Inlateral view the archesare distinct and central opening 9-10 pm in diameter (Fig. 4, C). clearlyvisible bytheir central thickenings. Underbridge innonexpanded portion averages In en face view,basal plate can be seen as a 8 pm in width. wide centralring with six short branches slightly reflexed attheir extremities and ar- Note 1 : One veryfrequently observesone or ranged regularly. even two anterior portions of stylets attached Styletlong, straight, rigid andmoderately tothe cuticle atthe anterior end (Fig. 1, M) thick,with the posterior part very slightly orincluded in a thin residualjuvenile cuticle longer thanthe anterior. Basal knobs wider surroundingthe anterior end of the female thanhigh, anteriorly concave with a short, At least, the last juvenile cuticle becan generally lsluntanteriorly directed point, and convex observedon females, even mature, exfoliating posteriorly. on different places of the body. Cephalidssmall, located at the levels of the third and tenth body annules. Note 2 : An abnormal female was observed in Oesophagus with a t.hin procorpus but thicker which the post'vulval part of thebody is atthe anteriorpart than at the posterior.

76 Rev. Nématol. 1 (1) 73 : à 86 (1978) H I J D

v

Fig. 2 : Hylonema ivorense n. gen., n. sp. Male A : cesophageal region ; B : fore part ; C : posterior part (lateral view) ; D : posterior part (ventralview) ; E : lateral field (at mid-body). 2nd stage juvenile : F : cesophageal region ; G : fore-part ; H : lateral field, intestine ((1 serpentine ))) and genital primordium ; 1, J : tails. Hylonema ivorense n. gen., n. sp. Mâles : A : région œsophagienne ; B : partie antérieure ;C : partie posté- rieure (vue latérale) ;D : partie postérieure (vue ventrale) ;E : champ latéral (à mi-corps). Juvéniles du 2e stade : , F : régionœsophagienne ; G : partieantérieure ; H : champlatéral, intestin (Gserpentin )>) et primordiumgénital ; I, J : queues.

Rev. Nématol. 1 (1) : 73 ù 86 (1978) 77 M. Luc, D.P. Taylor 22 P. Cadet

Median bulbreduced, fusiform, not well de- Labial region rounded,separated from rest limited, with weak musculature ; valves poorly of bodyby a distinct but not deepincisure ; developed.Isthmus thin, short, encircled by a 5 pm (4-5.5) highand 10.5 pm (9.5-11.5) wide nerve ring. Basal bulb elongated, occupying wide. Three annules present, the two posterior most of thebody cavity and overlaping the annules narrower than the anterior. Labial disc intestineventrally or ventro-laterally. Three present, dificult to see with optical microscope. nucleipresent, but diffkult to observe ; an- En face viewwith S.E.M. (Fig. 3, B) shows terior(dorsal) nucleus larger than the others. a short rectangular buccal opening, the longer Intestinewith a single serpentinestructure axis being 1 dorso-ventral ; the labial disc itself (= fasciculi),rarely anastomosing. longer dorso-ventrallywith rounded contour ; Excretorypore situated 140 pm (113-165) sometimesfusing dorsally and ventrally with from anterior end. thefirst labial annule for ashort distance. Hemizonid flat, not causing a bulging on the Amphidialopenings in the form of transverse cuticle,from five annules infront of to one dits locatedwithin the labial disc. Cephalic annulebehind excretory pore, butin general sclerotization pronounced. In lateral view basal one to three annules anterior to excretory pore plateappears slightly convex and rounded andextending for two annules. Hemizonion anteriorly,not extending posteriorly beyond not observed. the incisure separating labial regionfrom rest Testissingle, long, outstretched,occupying of body.Arches clearlyvisible, principally by more than one-third of theposterior portion theircentral reinforcements. In en face view, of thebody. Spermatozoa globular, highly dorsalplate consists of sixbranches, the refractive. sublaterals beingcloser together than the others. Spicules moderatelythick, slightly curved Cephalids not observed. ventrally,dilated at proximal end, thickened Stylet straight, rigid, thin, posterior portion at the median part and bifid at the distal end. longer thananterior ; basalknobs anchor- Gubernaculum thin, short, very slightly curved. shapedwith blunt anteriorly-directed points Spicularsheath short, without process. and convex posterior surface. Tai1 absent to short, rounded, non-annulated Oesophagus with an anteriorly enlarged pro- atextremity or with one or twovery wide corpus,median bulb ovoid with conspicuous annules. Cuticle withan interna1 thickening valveand musculature. Isthmus short, sur- roundedby a wide nervering. Basal portion havingthe form of aband situated ' slightly dorsal in relationto the body axis and extending massive,elongated ; vent>rallyor ventro-late- laterally. Bursa absent. No phasmids observed, rallyoverlapping anterior portion of intestine even with S.E.M. for considerablea distance and occupying almost al1 of body cavity. Three nuclei present ; Juveniles (2nd stage) : Bodystraight or the anterior (dorsal gland) largest and generally veryslight,ly curved ventrally, elongated, cyl- the only one visible. Dorsal gland transparent, indrical,tapering gradually posteriorly and subventral glands granular thus obscuring their slightly anteriorly, with a distinct constric.tion nuclei. at the level of the juncture of the two parts of Intestinewith a single serpentinestructure thestylet giving to anteriorend aslightly (= fasciculi),with no anastomoses. conical appearance. Excretorypore situated 121 pm (110-130) Cuticle markedby distinct transverse an- fromanterior end. Hemizonid flat, extending nulations,annules averaging 2 pm in width one or two annules,and situated at the level at middle of body. Cuticle slightlythicker at of the excretory pore or one or two annules ante- the level of the narrow anterior part of body. rior or posterior to it. Hemizonion not observed. Lateral field withthree straight, parallel in- Genitalprimordium oval, small ; 13.5 pm cisures not crossed by transverse striae, term- (11.5-19) long and 8 pm (6.5-12) wide ; situated inatingposteriorly apprpximately at the level 363 pm (310-410) €rom anterior end ; composed of thephasmids, and occupying .one-fourth of four cells, only thetwo central (germinal) of body diameter at the middle of the body. cells withlarge visible nuclei.

78 Rev. Nématol. 1 (1) : 73 ù 86 (1978) Hylonema ivorense n. gen., n. sp.

Fig. 3 : Hylonema ivorense n. gen., n. sp. SEM photographs (fi en face r) views) A : male ; B : 2nd stage juvenile ; C, D : female (approx. x 10,000). Hylonemaivorense n. gen., n. sp. Photographiesau microscope e'lectronique d balayage. Régions labiales vues de face. A : m≤ B : juvénile de 2e stade; C, D : femelles (approx. X 10 000).

Rev. Ntmatol. 1 (1) : 73 à 86 (1978) 79 M. Luc, D. P. Taylor dt. P. Cadet

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Tai1 elongateand tapering regularly to a sesses al1 the family characteristics (see below). pointed extremity ; hyaline portion very long. However, it is impossible to classify Hylonema Phasmids small, do-like, located 12 pin (8.5-17) inany of thethree recognized subfamilies, posterior to anus, without a lens-like st,ructure. i.e. Heteroderinae, Meloidoderinae, ancl Atalo- Type-host : Roots of “avodiré”, Turraeanthus derinae. In fact, Hylonemaivorense possesses africana Pellegr.(). characters presentin genera belonging to each of these three subfamilies : Type-locality : Forestreserve of the Banco, near Abidjan, Ivory Coast. 1. An underbridge ispresent, in females of Holotype (female) : slide 94-WA-20148, de- H. ivorense, acharacker previously described posited at. theLaboratoire des Vers, Muséum onlyfrom certain species of Heteroderu. and nationald’Histoire naturelle, 43 rue Cuvier, Globodera, both members of the Heteroderinae Paris, Franc,e. (Mulvey & Stone, 1976). Parutypes : 20 females, 30 males and 30 2nd 2. &lales and juveniles of 13. ivorense possess stage juveniles, at the same place. One female, higharches in the basal plate of the cephalic onemale and two juveniles deposited in each framework, a character typic.al of the Meloido- of the following institut-ions : Laboratorium derinae (Wouts, 1973 b). voor Nematologie,voor Landbouwhoogeschool, Wageningen, Netherlands ; Nematology Depart- 3. In H. ivorense t.hereis no cyst stage and ment, Rothamsted Experimental Station, Har- only the anterior portion of the i‘emale cuticle penden,England ; Instituutvoor Zoologie, annulated,is criteria characterist,ic of t.he Rijskuniversiteit,Gent, Belgiunl ; Nematology Ataloderinae (Wouts, 1973c,). The latter charac- Department, University of California, Riverside, ter was verifiecl byexamination of parat,ypes U.S.A. ; NematologyDepartment, University of Atalodera ucri Wouts,1973 and Slzerodera of California, Davis, 1J.S.A. ; Nematology Zonicerae Wouts, 1973, the only two desc.ribed Laboratory, U.S.D.A. Beltsville,U.S.A. ; Bio- species in this subfamily. systematicsResearch Institate, Ot,t,awa, Thepresence of thecombination of these Canada ; Entomology Division, D.S.I.R., Auck- c.haracters in H. ivorense prevented placing this land, New Zealand ; Laboratoire de Nématologie, genusinany of theexisting subfamilies. O.R.S.T.O.M., Dakar, Sénégal ; Laboratoire de Creat.ion of afourth subfamily to accomodate Nématologie,O.R.S.T.O.M., Abidjan, C6t.e only this genus was considered ; however, t,he d’Ivoire. onlyapparent diagnostic character of such a subfmdg wodd bethe lack of egg retention by females.This did not, appear to be of suf- CYTOLOGY fic~ientimportance to c.reate a new subfamily, espec,ially since it is known that in the genus Therelatively few eggs presentin females Nncobbrrs, N. dorsalis Thorne & Allen,1944 dissectedfrom infected roots andthe infre- retains eggs in the female whereas N.aberrans quency of metaphase figures precluded a detailed (Thorne,1935) Thorne Sc Allen,1944 does not cytological study of the species.However, on (Sher, 1970). t.he basis of the few figures observed we believe Another possibilit,y was to exclude Hylonema that n = 7 or 8. fromt,he Heteroderinaeby the absence of a cyststage and from the Meloidoderinae by restridion of annulationson females tothe anteriorend. However, the diagnosis of the Taxonornicposition of Hylonema n.gen. Ataloderinae would have to have been amended withinthe Heteroderidae and consid- to accomodate Hylonema. eration of the validity of its snbfamilies. Thisapproach was also unacceptable tous sincemany characters of Hylonema differ Hylonema n. gen. can be accomodated easily from the two species of this subfamily : absence withinthe family Heteroderidae since it pos- of terminal cone bearingvulva and anus ;

80 Rev. Némabol. 1 (1) : 73 à 86 (1978) Fig. 4 : Hylonema ivorense n. gen., n: sp. Female A, B, C : end on view. A : surface view; B : focus below showing the muscles ; C : underbridge ; D : lateral view of the vulval region. Hylonema ivorense n. gen., n. sp. Femelle : A, B, C : région vulvaire, vue apicale; A : vue ensurface; B: mise au point inférieure montrant les muscles dilateurs ;C : pont inférieur; D : région vulvaire en vue latérale. M. Luc, D.P. Taylor & P. Cadet presence of an underbridge ; higharch of the pointeddistally, and morphologically more basal plate of juveniles and labial dise visible similar to those of Sherodera, andthe cloaca1 in males only by S.E.M. Such a heterogeneous openingisnearly terminal. Thus,although subfamily would be too artificial. these four genera share some common characters, Thissituation has raised the question as to e.g. presenceof a cyst and a basic chromosome whether the division of the Heleroderidae into number of 9, Sarisodera differs from the other subfamilies is accurate and if it serves any real genera in important genital structures in both purpose.We believe thatthis division into sexesmaking the subfamily Heteroderinae a subfamilies is neitheraccurate nor useful ; heterogeneous group. therefore,for the present t.ime we prefer ta Infact, presence of a cystis the major abandon the use of subfamilies in the Hetero- morphological charxter of the Heteroderinae ; dericlae. Our reasoning is detailed below. however,cysts have recently been described The family Heteroderidae at present consists in generabelonging to groupsoutside the of ten genera classified as follows : Heteroderidae. For example, cysts are found in .&leloidoderella Khan,1972, a member of the Subfamilies Genera Meloidogynidae, andin Meloidoderita Poghos- Heteroderinae sian,1966, a member of the Criconematoidea. Filipjev & Sc,h. In the latter, the cystis formed from the uterus Stek., 1941 Heterodera Schmidt,1871 and not from theentire body (Kirjanova & Glo bodera (Skarbilovich, 1959) Poghossian,1973). Since cyst-forming species Mulvey & Stone, 1976 occur in differenttaxonomic lines, relation- Punctodera Mulvey & Stone, ships between the group Heferodera- Glo bodern- 1976 Punctodera and Sarisodera may be the result of Sarisoderinae Sarisodera Wouts & Sher, convergencerather than similar ancestry, a Husain, 1976 1971 statementin agreement with those of Wouts Meloidoderinae Illeloidodera Chit., andSher (1971), Wout8s(1973 a) andHusain Golden, 1971 Hannon & Esser, 1956 (1976),this later author ereating the sub- Cryphodera Colbran, 1966 familySarisoderinae to makethe separation Zelandodera Wouts, 1973 more marked. At.aloderinae Afalodera Wouts, 1973 The Meloidoderinae is also a heteregenous Wouts, 1973 Sherodera Wouts, 1973 grouping. Adeloidodera differs great.ly from Cry- ? Hylonema n. gen. phodera and Zelandodera bythe equatorial ?Vitilin thesubîamily iieleroderinae, the position of theyulva, unique in the Hetero- genera Heterodera,Globodera and Punctodera deridae.This character appears so important, are closely relatedmorphologically, whereas thatWouts (1973 b)stated that '5t may be thefourth genus, Sarisodua, differs from this justified to raise Meloidoderu tao subfamily group in many import.ant charact.ers: in females rank on the basis of t.his unique position of the there is a terminal coneformed bythe pro- vulva". Cryphodera, consisting of onespecies, truding vulval lips and at, the cone extremity and Zelandodera, possessing three, are so closely the cuticleis thic,kened ; whereas inthe first related that we consider them to be synonymous three genera mentioned, the vulva and anus are (see below). situat.ed in a shallowdepression wit,h a thin Thesubfamily Ataloderinae consist#s of two cuticle(vulval basin) and the terminal cone, monospecificgenera, Afalodera and Sherodera, whenexisting (Heterodera), constitutes a part having so few dishguishingcharacters that of the body proper ; in addit.ion the vulva and we consider them as synonymous (see below). sometimes the anus are surrouncled by thinner Talringsplitting to its extreme, we might cuticle(fenestrAe). The cone stxucture of Sari- havebeen justified in recognizing thesub- sodera, infact, is similar to thatpresent in familySarisoderinae Husain, 1976 and in cre- Afalodera and Sherodera.Sarisodera malesare atinganother suhfamily to accomodatte Sari- also quite different from malesof the other three sodera, removing it fromthe Heteroderinae ; genera : theirspicules are straight, thin and another to accomodate Cryphodera-Zelandodera

82 Reu. Némafol. L (1) : 2'3 ù 86 (1978) Hylonema ivorense 12. gen., n. sp. while retaining Meloidodera inthe Meloido- Genus Heterodera Schmidt, 1871 derinae ; and a third to include only Hylonema. Thusthe Heteroderidae wouldconsist of six = Heferobolbm Railliet, 1896 subfamilies,five of whichwould containonly = (Heferodera) Skarbilovich, 1959 a single genus! We believe that such a system is completelyundesirable and unnecessary. At DIAGNOSIS: Heteroderidae. Female : Cyst the present time we prefer to abandon the use formedafter death. Body with posterior pro- of subfamilies in the Heteroderidae and consider tuberance (the vulval cone), more orless lemon- it as a family containing the genera Heterodera, shaped. Cuticle with lacelike pattern of ridges. Globodera,Punctodera, Sarisodera, Meloidodera, Vulvalslit short to long(10-60 Pm) sited at Cryphodera (= Zelandodera), Afalodera(= Shero- apex of vulval cone ; underbridgeand bullae dera) and Hylonema n. gen. present or absent.Perineal tubercles (Mulvey, In the future whennew genera and species 1973) absent. Vulval cone bi-,circum- or ambi- are described and when additional anatomical, fenestrate.Anus dorsal, not on vulval lip. morphologieal,cytological and physiological Juvenile(2nd stage) : Labial disc present but data are available, it may be possible to arrange with low profile, seen clearly only under S.E.M. theHeteroderidae into meaningful groupings. Cuticle of labial region of eventhickness. At the gresent we do not consider this possible. Phasmids without lens-like structure in muscle layer. Male : Up to 1.5 mm inlength. Labial disc present but with low profile. Tail present, length less than half bodywidth. Family Heteroderidae TYPE SPECIES : Heferoderasckachtii Schmidt, (Filipjev & SchuurmansStekhowen, 1941) 1871 Skarbilovich, 1947. = H. (H.) schaclztii Schmidt, 1871 (Skarbilovich, 1959) DIAGNOSISEMENDED (afterWouts, 1973 a) : SuperfamilyTylenchoidea (Orley, 1880) Chit- Wood & Chitwood,1937. Fenzale : Swollen to subspherical,sedentary, didelphic.Cuticle an- Genus Globodera (Skarbilovich, 1959) nulated or non-annulated.Tail absent. Anus Mulvey & Stone, 1976 locatedterminally ordorsally subterminal. Excretorypore posterior to level of valvein = Heterodera(Globodera) Schmidt, 1871 median bulb. Basal plate subdivides head into (Skarbilovi-ch, 1959). six sectors, withthe two lateral sectors narrower than the other four. Stylet longer than 1.7 Fm. DIAGNOSIS: Heteroderidae. Fernale : Cyst Procorpus and median bulb not amalgamated. formedafter death. Body without posterior Medianbulb ovate to spherical,with well protuberance,spherical shape. Cuticle with developed musculatureand crescentic valve lacelike pattern of ridges.Vulva terminal. plates.Oesophageal glands overlap intestine Vulval slit short ( < 15 Fm). Underbridge and ventrally. Juvenile(2nd stage) : Vermiform ; bullae rarely present. Perineal tubercles present. infective migratory stage. Basal plate subdivides Vulval area circumfenestrate ; no anal fenestra. headas in female. Stylet robust, longer than Anus dorsal, not on vulval lip.2nd stage juvenile: 16 Fm. Male : Vermiform,migratory. Body Labial discpresent butwith low profile,seen twisted as much as 1800 fromhead totail. clearlyonly under S.E.M. Cuticle of labial Tailshort orabsent. Caudal alae absent. region of eventhickness. Phasmids without Stylet and cephalic framework well developed. lens-like structurein muscle layer. Male : Testis single. Up to 1.5 mm long. Labial disc presentbut with low profile. Tail present, length less than TYPEGENUS : Heterodera Schmidt, 1871. half body width.

Rev. Nématol. 1 (1) : 73 à 86 (1978) 83 M. Luc, D. P. Taylor & P. Cadet

TYPE SPECIES : Globoderaroslochiensis (Wol- TYPE SPECIES : Sarisoderalzydrophila Wouts LE lenweber,1923) Mulvey LE Stone, 1976. Sher, 1971. = H. (G.) rostochiensis Wollenweber,1923 (Skarbilovich,1959). Genus Meloidodera Chitwood, Hannon & Esser, 1956 Genus Punctodera Mulvey & Stone, 1976 DIAGNOSIS: Heteroderidae. Female : No cysl stage. Cuticle annulatedon entire body. Ma- DIAGNOSIS: Heteroderidae. PelnUle : Cyst jority of eggs retainedwithin body. Vulva formedafter death. Body wit,hout posterior subequatorial ; anus ventrally subterminal, not protuberance,spherical, ovoid orpear-shaped. protrudinpout of bodycontour. Phasmids Cuticle with lacelilce pattern of ridges and terminal. 2nd stage juvenile : Labial disc easily subsurfacepattern of punctations.Vulva ter- visible. Cuticle of labial region distinctly wider minal.Vulva slit very short, underbridge nearbasal plate thannear labial disc.Dorsal absent.Bullae present orabsent. Perjneal andventral parts of basalplate a high arch. tubercles absent. Areas around vulva and anus Four lines inlateral field. Male : Labial disc each circumfenestrateand of similarsize. prominent.Basal plate divides head into six Anus offset towardventral margin of anal sectors of approximately equal size. Not devel- fenestra. 2nd stage juvenile : Labial disc present opingthrough saccate stage. No longitudinal butwith low profile, seenclearly only under striae on basal lip annule. Four lines in lateral S.E.M. Cuticle of labial region of even thickness. field. Tail present. Phasmids without lens-like structure in muscle layer. Male : Up ta 1.5 mm long. Labialdisc TYPESPECIES : Meloidodera floridensis Chitwood, presentbut with low profile. Tailpresent, Hannon & Esser, 1956 length less than half bodywidth.

TYPE SPECIES : Puncfoderapunctata (Thorne, 1928)Mulvey & Stone, 1976. Genus Cryphodera Colbran, 1956 = H. (Globodera)punctata Thorne,1928 (Skarbilovich, 1959). = Zelandodera Wouts, 1973 ; new synonymy.

DIAGNGSIS: Eetemderidae. Femtlle : KG c.yst stage. Cuticle annulatedon entire body. Ma- Genus Sarisodera Wouts & Slier, 1971 jority of eggs retainedwithin body. Vulva terminal ; vulvallips protrude beyond body DIAGNOSIS: Heteroderidae. Female : Cyst contour. No lenestrationaround vulva. Anus formed after death. Cuticle with lacelike pattern subterminal. 2ndstage juvenile : Labial disc of ridges. Vulva sunken in a terminal cone. No conspicuous to very flattened. Cuticle of labial fenestrationaround vulva or anus. 2ndstage region distinctlywider near basal plate than juvenile .- Labial disc present but wit.h low nearlabial disc. Dorsal andventral parts of profile,seen clearlyonly uncler S.E.M. (1). basalplate a high arch. Male .- Labial disc Cuticle of labialregion of eventhickness. prominent.Stylet as long or longer than that 'Phasmidswith or without lens-like structure of 2ndstage juvenile. Longitudinal striae on inmuscle layer. Male : Up to1.5 mm long. basal lip annule. Labial disc present but with lowprofile, only clearlyseen under S.E.M. (l). Tailabsent. TYPE SPECIES : Cryphoderaeucalypti Colbran, 1956

(l) Observedon paratypes of S. hydrophila Wouts & Sher, 1971 and S. africana Luc, Germani & Nets- OTHER SPECIES : C. podocarpi (Wouts,1973) cher, 1973. n. comb.

84 Rev. Nématol. 1 (1) : 73 à 86 (1978) Hylonema ivorcnse n. yen., n. sp.

= Zelandodera podocarpi Wouts, 1973 Since thesefour characters appear to be C. notlzophagi (Wouts, 1973) n. comb. specific in nature and since al1 other characters = Zelandodera noilzophagi Wouts, 1973 areidentical, we consider Zelandodera asa C. coxi (Wouts, 1973) n. comb. juniorsynonym of Cryphodera. = Zelandodera coxi Wouts, 1973.

DISCUSSION: Genus Atalodera Wouts & Sher, 1971

Synonymisation of thesegenera was neces- = Sherodera Wouts, 1973; new synonymy. sary for the reasons listed below. According to Wouts (1973 b) four characters mày be used to DIAGNOSIS: Heteroderidae. Fernale : No cyst separate Cryphodera from Zelandodera. stage. Cuticle annulatedonly in the anterior

’ 1. In Cryphodera the anus is separated from portion of the body. Eggs retained within the the vulva by a slight concave depression which body.Anus andvulva terminal on protu- is absentin Zelarzdodera. However,as seen in berance. No fenestration around vulva or anus. Figure 4 D-H (Wouts, 1973 b) there is a tran- 2ndstage juvenile : Labial disc presentbut sition in the distinctness of this character from with low profile ; onlyclearly seen under C.eucalypfi to Cryphodera sp.to the three S.E.M. (l). Arches low. Stylet less than 30 pm species of Zela.ndodera. In addition, the vulva- long. Oesophageal glands fil1 less than half the anusdistance forms an overlapping series : bodywidth. Phasmids with distinct lens-like Z. coxi = 38-70 pm ; C. eucalypfi = 40-51 pm ; structure in muscle layer. Male : Up to 1.5 mm Z. nothophagi = 41-57 pm and Z. podocarpi = inlength. Labial disc prominent (a). Stylet 58-70 pm. Greater clifferences than these exist longer than that of 2nd stage juvenile. Spicules between the two described species of Sarisodera ; more than 30 pm long. Tai1 short or absent. therefore we consider such differences atthe specific and not the generic level. TYPE SPECIES : Ataloderaucri Wouts & Sher, 1971. 2. In Cryphodera the vulval lips are described as “pronounced, protruding terminally”, whereas OTHER SPECIES : A. lonicerae (Wouts,1973) in Zelandodera thevulval lips aredescribed n. comb. n. l as“protruding slightly out of bodycontour”. = Sheroderalonicerae Wouts, 1973. Again Figure 4 D-H IWouts, 1973 b) shows the transition of thischaracter from C.eucalypti DISCUSSION: Wouts(1973 c) used only two to Cryphodera sp. to 2. podocarpi to Z. nofho- characters to separate these genera : location of phagi and Z. coxi. Z. podocarpi definitely has the anus in females and structure of the basal protruding vulval lips. Thus, we consider that labialannule in males. In Atalodera, the anus these are specific differences but not generic. is“located on transformed, flattened dorsal 3. It is stated that the “numberof lip annules vulvallip” ; in Sherodera it is“located on is usuallyhigher in Zelarzdodera juveniles”. rounded dorsal vulval lip”. Study of specimens That is, C. eucalypti = 3, Z. coxi and Z. notizo- of A. ucri and S. lonicerae has convinced us phagi = 4,and Z. podocarpi = 5. Similar that these differences are slight and are at the variation is found within the genus Heterodera, specieslevel. More striking differences inthis where it isuseful only as supplementala characterexist between the twodescribed characterin species separation.Thus, we species of Sarisodera. In fact, there appears to consider suchminor differences at the species be a parallelisln regardingthis character between and not the generic level. 4. Males of Zelandodera have four lines in the lateral field,whereas thereare three in Cry- (l) Observed on juvenile paratypes of A. lonicerae. (2) S.E.M. observations on maleparatypes of phodera. Again,males of certain species of A. lonicerae showed that only the central part (about Heterodara have four lines, others have three. half the diameter) of the labial disc is elevated.

Rev. Nénzatol. 1 (1) : 73 à 86 (1978) 85 M. Luc, D. P. Taylor & P. Cadet

Sheroderalonicerae and ?Sarisoderaafricana. KHAN, A. M. (1972). Studies on plant parasitic nema- We havealready noted the resemblance in todes associated with vegetable crops in Uttar Pradesh. Finaltechn. Rept, Aligarh Muslim Univ., vulval cone structure among these three genera. Dep., 238 pp. Similarly, we consider the presence or absence KIRJANOVA,E. S. & POGHOSSIAN,E. E.(1973). of longitudinallabial striae in the male as [Redescription of Meloidoderitakirjanovae Poghos- insuffkientto separate genera. The striking sian, 1966 (Nematoda : Meloidoderitidae, fam. n.)]. sindarityoridentity of "other characters Parazitologiya, 7 : 280-285. convince us that Sherodera'is a junior synonym MULVEY, R.H. (1973). Morphology of theterminal of Atalodera. areas of white females and cysts of the genus Hete- rodera (s.g. Globodera). J. Nematol., 5 : 303-311. MULVEY, R. W. & STONE,A. R. (1976): Description Hylonerna n.gen. of Punctoderamatadorensis n. gen., n.sp. (Nema- Genus toda : Heteroderidae)from Saskatchewan with lists of species and genericdiagnoses of Globodera DIAGNOSIS: Heteroderidae. Pemale : No cyst (n. rank), Heterodera, and Sarisodera. Can. J. Zool., stage. Cuticle annulated only in anterior portion 54 : 772-785. of body. Eggs not retained within body. Anus NETSCHER,C. & SEINHORST,J. W. (1969). Propionic and vulva subterminal, in a hollow depression. acid better than acetic acid for killing nematodes. Vulvallips notprotruding. No fenestration Nematologica, 15 : 286. SEINHORST,J. W. (1959). Arapid method for the aroundvulva or anus. Underbridge present. transfer of nematodesfrom fixative to anhydrous 2nd stagejuvenile :. Labial disclow, visible glycerin. Nematologica, 4 : 67-69. onlyon S.E.M.Arch medium. Tail long, fili- SHER, S. A. (1970). Revision of thegenus Naccobus form ; hyaline portion of tail very long. Male : Thorne and Allen, 1944 (Nematoda : Tylenchoidea). Labial disc and arch as in 2nd stage juvenile. J. Nematol., 2 : 228-2,35. Tailshort or absent. No phasmidsobserved, SHER,S. A. & BELL,A. H. (1975). Scanning electron even on S.E.M. micrographs of the anterior region of some species of Tylenchoidea. (Tylenchida : Nematoda). J. Nema- TYPESPECIES : Hylonema ivorense n. gen., n. sp. tol., 7 : 69-83. No other species. TAYLOR,D. P., CADET, P. & Luc, M. (1978).An uniquehost-parasite relationship between Hylo- Diagnosis of H. ivorensen. sp. : having nemaivorense (Nematoda : Heteroderidae) and the characters of the genus. roots of a tropical tree. Rev. Nematol., 1 :

l 99-108 TAYLOR,D. P. & NETSCHER,C. (1974). An improved ACKNOWLEDGEMENTS technique for preparing perineal patterns of Meloi- The authors express their appreciation to B. Sou- dogyne spp. Nematologica, 20 : 268-269. chaud ORSTOM, Dakar, for preparation of al1 speci- WOUTS,W. M. (1973 a).A revision of thefamily mens for study by optical microscopy, and for photo- Heteroderidae(Nematoda : Tylcnchoidea) 1. The graphie assistance ; to Dr S. D. VanGundy of the familyHeteroderidae and its subfamilies. Nema- University of California, Riverside, for making avai- tologica, 18 (1972) : 439-446. lable specimens in their nematology slidecollection, WOUTS,W. M. (1973 b).A revision of thefamily andto A. H. Bell of theUniversity of California, Heteroderidae(Nematoda : Tylenchoidea) II. The Riverside, for assistance in measuring nematodes and subfamily Meloidoderinae. Nematologica, 19 : 218- in processing them for S.E.M. 235. WOUTS,W. M. (1973 c).A revision of thefamily Heteroderidae (Nematoda : Tylenchoidea) III. The REFERENCES subfamily Ataloderinae. Nematologica, 19 : 279-284. WOUTS, W.M. & SHER,S. A. (1971). The generaof the HUSAIN,S. 1. (1976). Phylogeny and inter-relationship subfamily Heteroderinae (Nematoda: Tylenchoidea) of thesuperfamily Heteroderoidea (Skarbilovich, with a description of two new genera. J. Nematol., 1947) Golden, 1971. Geobios, 3 : 9-12. 3 : 129-144.

Accepté pour publication le 21 octobre 1977.

86 Rev. Nématol. 1 (1) : 73 ù 86 (1978)