A reappraisal of Tylenchina (Nemata). 6. The family Belonolaimidae Whitehead, 1960 (l)

Renaud FORTUNER* and Michel LUC** California Department of Food & Agriculture, Analysis & Identification, 1220 N Street, Sacramento, CA 95814, USA, and Muséum national d’Histoire naturelle, Laboratoire des Vers, 61, rue de Buffopz, 75005 Paris, Prame.

SUMMARY

The family Belonolaimidae is redefinedto include two subfamilies, Belonolaiminae withBelonolainlus, Carphodorus, Morulaimus, Geocenamus, and Sauertylenchus, andTelotylenchinae with Tylenchorhynchus (= Telotylenchus),Trophurus, Trichotylenchus, Nagelus, Paratrophurus, Merlinius, Triversus, and Anzplinzerlinius.The following synonymizations are proposed : Ibipora = Mo- rulaimus, Hexadoms = Geocenamus, Uliginotylenchus = Trichotylenchus, Meiodorus and Mulveyotus = Triversus, Histotylenchus and Telotylenchoides = Paratrophurus. The synonymy of Tylenchorhynchusincludes nine generic names.Doliclzorhynchus is a junior homonym. Tetylenchus is kept in genera dubia vel incertae sedis. A tabular key is proposed for identification of the genera in the family.

RESUME

Réévaluation des Tylenchina (Nemata). 5. La famille des Belonolainzidae Whitehea4 1960

La famille des Belonolaimidae est redéfinie avec deux sous-familles: Belonolaiminae, comprenant Belonolaimus, Carphodorus, Morulaimus,Geocenanzus et Sauertylenchus etTelotylenchinae, comprenant Tylenchorhynchus (= Telotylenchus), Trophuws, Trichotylenchus,Nagelus, Paratrophurus, Medinius, Triversus et Amnplinlerlinius. Lessynonymies suivantes sont proposées : Ibipora = Mondaimus, Hexadorus = Geocenamus,Uliginotylenchus = Trichotylenchus,Meiodorus et Mulveyotus = Triversus, Histotylenchus et Telotylenchoides = Paratrophurus. La synonymie deTylenchorhynchuscomprend neuf noms génériques.Dolichor- hynchus est un homonyme plus récent. Tetylenchtls est classé comme genus dubium. Une clef tabulaire est proposée pour aider à l’identification des genres de la famille.

The family Belonolaimidae is here redefined to in- A few months later, Siddiqi (1960) independently pro- clude two groups of taxa that untilnow were considered posed Telotylenchinae for a new genus, Telotylenchus, to be distinct : the belonolaimids (Belonolaiminae, and for Pseudhalenchus, both with overlapping glands. Telotylenchinae) with overlapping oesophageal glands, The structure of the glandular oesophagus was empha- and the tylenchorhynchids (Tylenchorhynchinae, Mer- sized again by the same author (Siddiqi, 1971~)when liniinae, Trophurinae) withglands abutting and he placed Tylenchorhynchinae and related subfamilies bulb-shaped. with abutting glands in Dolichodoridae, while Telotylen- Belonolaimus was placed by Chitwood (1950) in the chinae was placed in Belonolaimidae. family Dolichodoridae. Thorne (1949) did not include It is Our opinion that there is no structural difference this genus inhis revision of Tylenchida, but Loof (1958), betweenforms with abutting glands(the so-called using the system of Thorne and its emphasis on the “ bulb ”), and forms with glands overlapping the an- aspect of the glandular partof the oesophagus, separated terior part of the intestine. These forms differ only in Belonolaimus from Dolichodorus byclassifying, them the lengthof the glands, and in theposition of the oeso- into two different subfamilies (Hoplolaiminaeand phageal lumen relative to the glands (Seinhorst, 1971). Tylenchinae, respectively). The twokinds of arrangementsmay Co-exist in the When Whitehead (1960) proposed a new subfamily, same family(for example, Pararotylenchus is a Hoplolai- Belonolaiminae, heincluded init only generawith midae with abutting glands), in the same genus (Pmyletz- glandularoverlap (Belonolaimus and Trichotylenchus). choides magnicauda has abutting glands, while P. ritteri

(1) This article is part of a study on the classification of Tylenchina by the present authors and D. J. Raski, A. R. Maggenti (University of California, Davis) and E. Geraert (Rijksuniversiteit, Gent). * Associate in the Division of Nematology, University of California, Davis, USA. ** Nematologist fiom ORSTOM.

Revue Nénzatol. 10 (2) : 183-202 (1987) 183 t R. Fortuner & M. Luc has a longoverlapping lobe) andeven inthe same biology of the various genera in the family are best species, for example Ditylenchus myceliophagus as dis- treated at subfamily level. Telotylenchinae are surface cussed by Fortuner (1982). grazers feeding on the epidermal cells of plant roots. Once admitted that morphology, size, and location of Belonolaiminae have a long stylet that enables them to oesophageal glands mayVary within anytaxa, including reach deeper into the root while the rest of their body families, it becomes evident that belonolaimids, tylen- remains outside of the plant. chorhynchids, and related groups belong to the same family. The subfamily Telotylenchinae Telotylenchinae Siddiqi, 1960 The family Belonolaimidae = Tylenchorhynchinae Eliava, 1964 (n. syn.) Belonolaimidae Whitehead, 1960 = Trophurinae Paramonov, 1967 (n. syn.) = = Telotylenchidae Siddiqi, 1960 Tetylenchinae Siddiqi, 1970 = Tylenchorhynchidae Eliava, 1974 = Merliniinae Siddiqi, 1971 = Meiodorinae Siddiqi, 1971 (n. syn.) DIAGNOSIS DIAGNOSIS Tylenchoidea. Medium to large sized nematodes, with tail cylindroid to conoid, more than twice as long Belonolaimidae. Cephalicframework with weak to medium sclerotization. Stylet 15 to 40 pm long, with as wide but never elongate filiform (typically c' = 2-5). Phasmids always on posterior half of tail,never en- cone about as long as shaft. Corpus not enlarged and larged into scutella. Deirids presentor absent. Face view metacorporal valveof mediumdevelopment. Labial as seenwith SEM either ancestral (first lip annulus regioncontinuous or with slight indentation, never six-sectored) or with lateral sectors regressed and face bulbous. SEM face viewwith six lip sectors or with viewevolving towards either agrossly quadrangular lateral lip sectors regressed. Labial disc lemon shapedor shape ora four leaf clover shape. Females typically with variously fused with lip sectors. Disc and lip sectors two genital branches (except Trophurus). Columned sometimesfused together. Sensillae openings often uterus with three rows of cells. Males with peloderan visible on the sub-median lip sectors. caudal alae, rarelylobed or stopping just short of the tail tip. Spicules with or without pronounced velum. TYPE GENUS Belonolaimidae are migratory ectoparasites of plant Tylenchorhynchus Cobb, 1913 roots. A few species are endoparasitic. = Bitylenchus Filip'ev, 1934 = Telotylenchus Siddiqi, 1960 (n. syn.) TYPESUBFAMILY = Quinisulcius Siddiqi, 1971 (n. syn.) = "Dolichorhynchus "(primary homonym; n: syn.) Belonolaiminae Whitehead, 1960 = Trilineellus Lewis & Golden, 1981 (n. syn.) = Divittus Jairajpuri, 1984 OTHERSUBFAMILY = Morasinema Javed, 1984 Telotylenchinae Siddiqi, 1960 = Tessellus Jairajpuri & Hunt, 1984 = Neodolichorhynchus Jairajpuri & Hunt, 1984 (n. COMMENTS SYn.1

The family Belonolaimidae occupiesan intennediate OTHER GENERA position between Tylenchidae and Hoplolaimidae. It is Trophurus Loof, 1956 differentiated from Tylenchidae and Dolichodoridae by = Clavaurotylenchus Caveness, 1958 its columned uterus with three rows of cells (four rows Trichotylenchus Whitehead, 1960 in the othertwo families). It differs from Hoplolaimidae = Uliginotylenchzu Siddiqi, 1971 (n. syn.) by having a longer tail, and by having phasmids always Nagelus Thorne & Malek, 1968 on tail. Paratrophurus Arias, 1970 Telotylenchinae is accepted only as a subfamily in = Histotylenchus Siddiqi, 1971 (n. syn.) Beionoiaimidaebecause of themany similarities be- = Telotylenchoides Siddiqi, 1971 tween belonolaimidsand tylenchorhynchids. Faceviews Merlinius Siddiqi, 1970 areoften similar amongst various members of both = Scutylenchus Jairajpuri, 1971 groups (for example, Momlaimus is similar to Merlinius Triversus Sher, 1974 for this character); the cylindroid tail of belonolaimids = Meiodonls Siddiqi, 1976 (n. syn.) is similar to that of Paratrophurus and Amplimerlinius. = Mulveyotus Anderson & Ebsary, 1982 The few differences that exist in morphology and Amplimerlinius Siddiqi, 1976

184 Revue Nématol. 10 (2) : 183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae

GENUSDUBIUM The genera in Telotylenchinae Tetylenchus Filip’ev, 1936 Triversus Sher, 1974 DIAGNOSIS COMMENTSON REJECTED SUBFAMILIES Telotylenchinae. Body about 1 mm long. Lip region Tetylenchinae must berejected after the placement of low, flattened. SEM face view with labial disc and first its type genus in genus dubium (see below). labial annulus fused together; rounded amphid aper- Tylenchorhynchinae is rejected because of the syn- tures often conspicuous. Stylet 11-25 pm long, robust ‘ onymization of Tylenchorhynchus and Telotylenchus. Ty- or with needle-like cone. Labial frameworkthin, weakly lenchorhynchus is the senior synonymat generic level, but sclerotized, with wide basal ring. Metacorporal bulb Telotylenchinae is the senior subfamily and it should be fusiform. Lateral field with four or three lines. Female accepted in accordance withArticle 40 (a) of the Inter- tail conoid, pointed, medium to long(c’ = 3-8). Deirids national Code of Zoological Nomenclature. absent. Male caudal alae sometimes trilobed. Merlinius, the typegenus of Merliniinae, is here accepted as a valid taxon. Merliniinae was differentiated TYPESPECIES by Siddiqi (1971a, 1979) as having six lines in lateral Triversus annulatus (Merny, 1964) Sher, 1974 field, spicules cylindroid with distal end rounded and = Tetylenchus annulatus Merny, 1964 devoid of velum, gubernaculumsimple, not protruding from cloaca, medianbulb not distinctly offset from OTHERSPECIES procorpus, spermatheca offset, usually with two lobes, T. festonatus (Doucet, 1985) n. comb. and vulva opening small,with distinct epitygma and = Meiodorus festonatus Doucet, 1985 reduced lateral membranes. Morphologyof lateral field T. hollisi (Siddiqi, 1976) n. comb. is not a primary differentiating character and is at best = M. hollisi Siddiqi, 1976 accepted only as an identification character; shapes of T. hyalacus (Anderson & Ebsary, 1982) n, comb. spicules andgubernaculum are accepted as generic = Mulveyotus hyalacus Anderson L? Ebsary, 1982 characters only; the exact appearance of corpus, vulva, and spermatheca are not well defined in most species in COMMENTS the taxa considered. They cannot be usedthis at time for definition of systematic relationships. In opposition to This genusfits the subfamilyTelotylenchinae be- these smalldifferences, the close similitude of genera in cause of the shape of the oesophagus, the two-branched .Telotylenchinae and Merliniinaeshould be noted. genital system with three rows in columned uterus, and Merlinius resembles Tylenchorhynchus, Amplimerlinius the tail more than three times as long as wide. The tail resembles Paratrophurus. There are no differences in the is pointed, but pointedtails have been reported in other biology of al1 the taxa concerned. It seems best to group genera in Belonolaimidae (e.g. Tylenchorhynchus tenui- them al1 into a single subfamily. cauda, Merlinius joctus, M. loojï, M. processus, etc.). Trophurus is the only genus in Belonolaimidae with Triversus is here accepted as a valid genus in Teloty- only one female genital branch. Also, it has thickened lenchinae, differentiated mostly by conspicuous basal cuticle on distal end oftail. For this reason, it was ring of the labial framework, low labial region, charac- grouped withMacrotrophurus and Paratrophurus in the teristic SEM face view and malecaudal alae often subfamily Trophurinae.Macrotrophurus has been recog- trilobed. T. annulatus was said by Sher (1974a) tohave nized as a Tylenchidae (Geraert & Raski, 1987). The three lines in the lateral field but, according to Merny definition of Paratrophurus is here enlarged to include (1964), and confirmed by examination of paratypes, the species without any thickening of tail cuticle (see below). two ridges that make up the lateral field can be seen as There exists many species in the family with thickened four lines if the ridges are slightly separated. tail end cuticle, in the genera cited above, but also in Meiodorus was proposed by Siddiqi (1976) in Doli- Tylenchorhynchus, Trichotylenchus, Merlinius, and Nage- chodoridae, Meiodorinae becauseof pointed femaletail lus. The thickening is particularly well marked in Tro- and trilobed caudal alae. Siddiqi (1976) commentedthat phurus, but it cannotbe used as a family criterion. the genuswas intermediate between Dolichodoridae and Regression of the posterior genital branch remains the Tylenchorhynchinae (here given as synonym of Teloty- only character that separates Trophurus from the rest of lenchinae). the genera in Belonolaimidae. The regression of a single Meiodorus is quite similar with the genera in the latter structure is not found to be relevant at subfamily level subfamily, and particularly with Triversus. Both genera and Trophurinae is here rejected. have lip area with labial disc and first labial annulus Meiodorinae is rejected after the synonymization of fused together; labial framework very lightly sclerotized Meiodorus with Triversus. but with wide basal ring; corpusfusiform. Also, Meiodo-

Revue Nématol. 10 (2) : 183-202 (1987) 185 R. Fortuner di M. Luc

~ rus hollisi and M. festonatus both have columned uterus OTHERSPECIES with threerows of cells as in Belonolaimidae, instead of T. acutoides Thorne & Malek, 1968 four rows as in Dolichodoridae (Geraert, pers. comm.). = Quinisulcius acutoides (Thorne & Malek, 1968) Sid- Pointed female tails are found in Meiodorus, Mulveyo- diqi, 1971 tus, Triversus, and someTylenchorhynchus and Merlinius T. acutzrs Allen, 1955 species. Lobed caudal alae exist in some species pre- = Q. acutus (Allen, 1955) Siddiqi, 1971 viouslyplaced in '' Dolichorhynchus " f= Tylenchor- T. aduncus de Guiran, 1967 hynchus). Examination of paratypes of T annulatus T. aerolatus (Baqri & Jairajpuri, 1969) n. comb. proved that the caudalalae issub-trilobed, with a central = Te'lotylenchzcs aerolatusBaqri & Jairajpuri, 1969 lobe thinner and longer than the lateral lobes. In the = Telotylenchus areolatzrs" Fortuner, 1985 original description of the species (Merny, 1964) it was = Trichotylenchus aerolatus (Baqri & Jairajpuri,1969) said that the caudal alae did not quite reach the end of Jairajpuri, 1971 the tail. In fact, the alae are difficult to observe in lateral nec Tylenchorhynchus aerolatus Tobar-Jimenez, 1970 view, but in ventral view it can be seen that the central T. agri Ferris, 1963 ala extends slightly past the tail tip. There is a definite T. ancorastyletus Ivanova, 1983 trend towards lobed caudalalae in Telotylenchinae, and T. annztlatus (Cassidy, 1930) Golden, 1971 this character should not be used sole criterion for the = T. Martini Fielding, 1956 placement of a taxon in Dolichodoridae. Meiodorus is T. anturcticus Wouts & Sher, 1981 here considered in Telotylenchinae. Within this subfam- T. aspericutis Knobloch,1975 , ily, it shows no differences with Triversus. The synony- T. avaricus (Kleynhans, 1975) n. comb. mization of Meiodorus and Mulveyotus proposed by = Telotylenchus avaricus Kleynhans, 1975 T. badliensis Saha & Khan, 1982 Siddiqi (1986) is accepted and both genera are made T. bicatrdatus Khakimov, 1973 junior synonyms of Triversus. T. bohrrensis Gupta & Uma, 1980 T. brassicae Siddiqi, 1961 Tylenchorhynchus Cobb, 1913 T. brevilineatus Williams, 1960 = Bitylenchusbrevilineatus (Williams,1960) Siddiqi, = Bitylenchus Filip'ev, 1934 1986 = Telotylenchus Siddiqi, 1960 (n. syn.) = Tylenchorhynchus indicus Siddiqi, 1961 = Quinisulcius Siddiqi, 1971 (n. syn.) nec T. indicus (Siddiqi, 1960) n. comb. = DoZichorhynchus Mulk & Jairajpuri, 1974 (n. syn.; T. byobius Sturhan, 1966 junior homonym) = Bitylenchus byobius (Sturhan, 1966) Siddiqi, 1986 = Trilineellus Lewis & Golden, 1981 (n.syn.) T. cacti Chawla, Bhamburkar, Khan & Prasad, 1968 = Divittus Jairajpuri, 1984 = Q. cacti (Chawla et al., 1968) Siddiqi, 1986 = Morasinerna Javed, 1984 T. canalis Thorne & Malek, 1968 = Tessellus Jairajpuri & Hunt, 1984 = B. canalis (Thorne & Malek, 1968) Siddiqi, 1986 = Neodolichorhynchus Jairajpuri & Hunt, 1984 T. capitatus Allen, 1955 (n. syn.) = Q. capitatus (Allen, 1955) Siddiqi, 1971 = T. acti Hopper, 1959 DIAGNOSIS = T. nilgiriensis Seshadri, Muthukrisnan& Shunmugan, 1967 Telotylenchinae. Bodymedium sized. Lateral field = T. himalayae (Mahajan, 1974) n. comb. with two, three, four, or fïve lines, sometimes areolated. = Q. himalayae Mahajan, 1974 Longitudinal ridges sometimes present on body.Tai1 conoid to subcylindroid, about three times as long as wide (c' = 2-4), sometimes with thicker cuticle in the distal portion, SEM face view typically with labial disc fused with first lip annulus, and with lateral sectors regressed. The remainingsub-median sectorsgive a * The names Telotylenchusaerolatus Baqri & Jairajpuri, distinctive quadrangular appearance to the face view. 1969, and Tylenchorhynchus aerolatus Tobar-Jimenez, 1970, Papillae often presenton submedian sectors. Head arebased on aerolations '), amisspelling of the word continuous to slightly offset. Stylet. 15-30 pm lo~g~thin cc zreolztions ',. Emendationswere proposed by Fortuner to slender, with cone about as long as shaft, sometimes (1985). However, the Secretaryof the Intemational Commis- needle-like. Deirids often absent. Male with caudalalae sion of Zoological Nomenclature commented that, when an rarely lobed. Spicules with well developed velum. author deliberatelyuses a misspelled wordto derive the name of a taxon, the scientific nameis not in itself a lapsus calami, TYPE SPECIES and it shouldbe accepted as valid (Tubbs, in Zitt.). The emendations proposed by Fortuner (1985) are rejected and T. cylindricus Cobb, 1913 considered as junior objective synonyms.

186 Revue Nekzatol. IO (2) : 183-202 (1987) Reappraisal of Tylenchina. 6. Belonolainzidae

= T. solani (Maqbool, 1982) n. comb. T. haki Fotedar & Mahajan, 1971 = Q. solani Maqbool, 1982 T. hastulatus (Colbran, 1960) n. comb. T. chirchikensis Mavlyanov, 1978 = Belonolainzus hastulatus Colbran, 1960 T. chonai Sethi & Swarup, 1968 = Telotylenchushastulatus (Colbran,1960) Jairajpuri, = Divittus chonai (Sethi & Swarup,1968) Jairajpuri, 1963 1984 T. hordei Khan, 1972 T. clams Allen, 1955 T. huesingi Paetzold, 1958 = T. tener Erzhanova, 1964 = B. huesingi (Paetzold, 1958) Siddiqi, 1986 T. clathrocutis (Lewis & Golden, 1981) n. comb. T. inzpar (Khan & Darekar, 1979) n. comb. = Trilineellus clathrocutis Lewis & Golden, 1981 = Telotylenchus inzpar Khan & Darekar, 1979 T. clavicaudatus Seinhorst, 1963 T. indicus (Siddiqi, 1960) n. comb. = B. clavicaudatus (Seinhorst, 1963) Siddiqi, 1986 = Telotylenchus indicus Siddiqi, 1960 T. claytoni Steiner, 1937 T. intervallatus nom. nov. = Tessellus claytoni (Steiner,1937) Jairajpuri & Hunt, = T. aerolatus Tobar-Jimenez, 1970 1984 = T. areolatus" Fortuner, 1985 T. coffeaeSiddiqi & Basir, 1959 = Bitylenchus aerolatus (Tobar-Jimenez, 1970) Siddiqi, T. contractus Loof, 1964 1986 T. crassicaudatus Williams, 1960 nec T. aerolatus (Baqri & Jairajpuri) n. comb. = Paratrophurus crassicaudatus(Williams, 1960) And& T. irregularis Wu, 1969 ssy, 1973 T. judithae Andrassy, 1962 T. cristatus Ivanova, 1983 = D. (N.)judithae(Andrassy, 1962) Mulk& Siddiqi, 1982 = Dolichorhynchus(Neodolichorhynchus) cristatus (ha- T. kashnzirensis Mahajan, 1974 nova, 1983) Siddiqi, 1986 T. kegenicus Litvinova, 1946 T. curvus Williams, 1960 I: kirjanovae Karapetjan, 1979 = Q. curvus (Williams, 1960) Siddiqi, 1971 T. knoblochi nom. nov. T. cuticaudatus Ray & Das, 1983 = T. tajani (Knobloch, 1975) n. comb. = B. cuticaudatus (Ray & Das, 1983) Siddiqi, 1986 = Q. tarjani Knobloch, 1975 T. dactylurus Das, 1960 nec T. tarjani Andrassy, 1969 T. delhiensis Chawla, Bhamburkar, Khan & Prasad, 1968 T. labiatus (Jairajpuri, 1984) Siddiqi, 1986 T. depressus Jairajpuri, 1982 = Divittus labiatus Jairajpuri, 1984 = T. (Bitylenchus) depressus Jairajpuri, 1982 T. larnelli,ferus(de Man, 1880) Filip'ev, 1936 T. digitatus Das, 1960 = D. (0.)1am.ellifems (de Man, 1880) Mulk & Siddiqi, T. divittatus Siddiqi, 1961 1982 = Trilineellus divittatus (Siddiqi, 1961) Lewis& Golden, T. latus Allen, 1955 1981 T. leviterminalis Siddiqi, Mukherjee & Dasgupta, 1982 = Divittus divittatus (Siddiqi, 1961) Jairajpuri, 1984 = T. paranudus Phukan & Sanwal, 1983 = Morasinenza divittatum (Siddiqi, 1961) Javed, 1984 T. lineatus (Karapetjan, 1979) n. comb. I: dubius (Bütschli, 1873) Filip'ev, 1936 = Q. lineatus Karapetjan, 1979 = B. dubius (Bütschli, 1873) Siddiqi, 1986 T. nzadrasensis Gupta & Uma, 1981 T. ebriensis Seinhorst, 1963 = Divittus nzadrasensis (Gupta & Uma, 1981) Jairajpuri, T. elegans Siddiqi, 1961 1984 = T. goldeni Rashid & Singh, 1982 T. nzanubriatus Litvinova, 1946 T. erenzicolus Allen, 1955 T. nzashhoodi Siddiqi & Basir, 1959 T erevunicus Karapejan, 1979 T maximus Allen, 1955 T. eroshenkoi Siddiqi, 1986 = B. maximus (Allen, 1955) Siddiqi, 1986 T. ewingi Hopper, 1959 T. nzexicanus Knobloch & Laughlin, 1973 T. jlaccidus (Baidulova, 1984) n. comb. T. microconus Siddiqi, Mukherjee & Dasgupta, 1982 = Telotylenchus flaccidus Baidulova, 1984 T. microphasmis Loof, 1960 T. georgiensis Eliashvili, 1971 = D. (N.) microphasmis (Loof, 1960) Mulk & Siddiqi, T. gemzanii nom. nov. 1982 = Dolichorhynchus (Dolichorhynchus) elegansGermani & T. minutus Karapetjan, 1979 Luc, 1984 T. mulki nom. nov. = T. elegans (Germani & Luc, 1984) n. comb. = T. parvus (Mulk & Siddiqi, 1982) n. comb. nec T. elegans Siddiqi, 1961 = D. (D.) parvus Mulk & Siddiqi, 1982 T. gladiolatus Fortuner & Amougou, 1974 nec T. parvus Allen, 1955 = D. (N.)gladiolatus (Fortuner & Amougou, 1974) Mulk T. natalensis IUeynhans, 1984 & Siddiqi, 1982 = B. natalensis (IUeynhans, 1984) Siddiqi, 1986 T. goffarti Sturhan, 1966 T. neoclavicaudatus Mathur & Lal, 1979 = B. goffarti (Sturhan, 1966) Siddiqui, 1986 T. nigericus (Mulk & Jairajpuri, 1974) n. comb. T. gracilifornzis Siddiqi & Siddiqui, 1983 = D. (0.)nigericus Mulk & Jairajpuri, 1974

Revue Nématol. 10 (2) : 183-202 (1987) 187 R. Fortuner & M. LUC

T. nordiensis Khan & Nanjappa, 1974 = Divittzrs sculptus (Seinhorst, 1963) Jairajpuri, 1984 = Tylenchorhynchus aerolatzts Khan & Nanjappa, 1972 = Morasinema sculptum (Seinhorst, 1963) Javed, 1984 nec T. aerolatzts (Baqri & Jairajpuri, 1969) n. comb. T. silvaticus Ferris, 1963 nec T. aerolatus Tobar-Jimenez, 1970 T. solani Gupta & Uma, 1981 T. nudus Allen, 1955 = D. (N..)solani (Gupta & Uma, 1981) Siddiqi, 1986 T. obregonzts (Knobloch & Laughlin, 1973) n. comb. 7: spinaceae Singh, 1976 = Q. obregonus IZnobloch & Laughlin, 1973 T. striatus Allen, 1955 T. obscztrisulcatus Andrassy, 1959 T. sulcatus de Guiran, 1967 = Divittus obscurisulcatus (Andrassy,1959) Jairajpuri, = D. (N.)sulcatus (de Guiran, 1967) Mulk & Siddiqi, 1984 1982 T. obtztsus (Siddiqi, 1978) n. comb. T. swarupi Singh & Khera, 1978 = Telotylenchus obtusus Siddiqi, 1978 = B. swampi (Singh & IUlera, 1978) Siddiqi, 1986 T. oleraceae Gupta & Uma, 1981 T. tarjani Andrassy, 1969 T. paaloofi (Tikyani & Khera, 1970) n. comb. T. teeni Hashim, 1984 = Telotylenchus paaloofi Tikyani & Khera, 1970 = B. teeni (Hashim, 1984) Siddiqi, 1986 = Trichotylenchzls paaloofi (Tikyani & Khera, 1970) Jai- T. tenzticaudatzts Wouts & Sher, 1981 rajpuri, 197 1 T. teres (Khan & Darekar, 1979) Siddiqi, 1986 T. pachys Thorne & Malek, 1968 = Telotylenchzts teres Khan & Darekar, 1979 = Tessellus pachys(Thorne & Malek, 1968) Jairajpuri & T. tobari Sauer & Annells, 1981 Hunt, 1984 = B. tobari (Sauer & Annells, 1981) Siddiqi, 1986 T. paracti (Ray & Das, 1983) n. comb. T. tonkiensis (Mulk & Jairajpuri, 1975) n. comb. = Q.paracti Ray & Das, 1983 = Telotylenchus tonkiensis Mulk & Jairajpuri, 1975 T. parvus Allen, 1955 T. triglyphzts Seinhorst, 1963 = B. parvus (Allen, 1955) Siddiqi, 1986 = Trilineellus triglyphzls (Seinhorst, 1963) Lewis & Gol- T. penniseti Gupta & Uma, 1980 den, 1981 T. phaseoli Sethi & Swarup, 1968 = Divittus triglyphzts (Seinhorst, 1963) Jairajpuri, 1984 = D.ID.) phaseoli (Sethi & Swarup,1968) Mulk & = Morasinema triglyphus (Seinhorst, 1963) Javed, 1984 Jairajpuri, 1974 T. trilineatus Timm, 1963 T. pini Kulinich, 1985 T. tritici Golden, Maqbool & Handoo, 1987 T. prophasmis (Jairajpuri & Hunt, 1984) n. comb. T. tuberosus (Maqbool, Ghazala & Fatima, 1984) n. comb. = D. (0.)prophnsmis Jairajpuri & Hunt, 1984 = D. ID.) tuberosus Maqbool et al., 1984 T. pruni Gupta & Uma, 1981 T. variannzts Mavlyanov, 1978 = Divittus pnmi (Grupta & Uma, 1981) Jairajpuri, 1984 T. varicaztdatzrs Singh, 1971 T. punensis Khan & Darekar, 1979 T. velatzrs Sauer & Annells, 1981 T. punici (Gupta & Uma, 1980) n. comb. T. ventrulis (Loof, 1963) n. comb. = Q.punici Gupta & Uma, 1980 = Telotylenchus ventralis Loof, 1963 T. quaidi Golden, Maqbool & Handoo, 1987 = Trichotylenchzls ventraZis (Loof, 1963) Jairajpuri, 1971 T. queirozi Monteiro & Lordello, 1976 T. ventrosignatus Tobar-Jimenez, 1969 = B. queirozi(Monteir0 & Lordello, 1976) Siddiqi, 1986 = B. ventrosignatus (Tobar-Jimenez, 1969) Siddiqi, 1986 T. rayi nom. nov. T. verutus (Kleynhans, 1975) n. comb. = T. impur Ray & Das, 1983 = Telotylenchus venttus Kleynhans, 1975 nec T. impur (Khan & Darekar, 1979) n. comb. T. vulgaris Upadhyay, Swarup & Sethi, 1972 T. robustus Thorne & Malek, 1968 = B. vulgaris (Upadhyay et al,, 1972) Siddiqi, 1986 = T. robustoides*Thorne& Malek, 1968 T. wilskii Kornobis, 1980 T. sacchari Sivakumar & Muthukrishnan, 1983 = B. wilskii (Kornobis, 1980) Siddiqi, 1986 T. sanwali Kumar, 1982 T. zeae Sethi & Swarup, 1968 T. sculpttts Seinhorst, 1963 = Trilineellus scdptzts (Seinhorst, 1963) Lewis& Golden, 1981 COMMENTS * Thorneand Malek (1968) proposed Tylenchorhynchus robustus. According to some reports (Smolik, in Iitt.; Siddiqi, Tylenchorhynchus is very similar to Merlinius in gen- in litt.) Thorne and Malek later replaced this name with T. eral body shape (shapesof both extremities, oesophagus, robustoides, probably because they thought it was a secondary etc.). It differs fromthis genus by SEM face view homonym of T. robustus (de Man, 1876) Micoletzky, 1922.In (Medinius generally has ancestral six sectors still visible fact, the latter species is the type species of the genus Roty- or it has a characteristic lemon shape withdisc and lenchus since 1936. Since it is not congeneric with the taon lateral sectors fused. This derived shape is unknown in described by Thorne and Malek, the replacement name 'I: Tylenchorhynchus), and by spicule shape (without velum robustoides must be rejected. It becomes a junior objective in Medinius). The numberof lateral field lines(2 to 5 us synonym of T. robustus Thorne & Malek, 1968. 6) permits an easy identification of these two genera.

188 Revue Nématol. 10 (2) :183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae

, Some species in Tylenchorhynchusresemble the genus concluded that these species might be transferred to Tricholylenchus, but this latter taxon is restricted to Telotylenchus if this genus were redefined to include forms withlabial region continuous withbody contours, species with oesophageallumen shifted laterally between stylet slender, and tail long and thin, cylindroid to the dorsal and one subventralgland, accompanied or not broadly rounded or clavate end. by a glandular overlap. He refrained from making this Species in Anzplimerlinius and Paratrophurus have move becauseof the great similarity between thespecies labial region continuouswith body contours, stylet and with abutting glands and those with aslight overlap. labial framework medium tostrong, and tails cylindroid, Because the two characters used (gland overlap and medium to short, thick, with broadly rounded ends. lumen shift) are at best secondary characters, and The species in Tylenchorhynchushave several charac- because the exact glandular structure is not known for teristics that are somewhat unusual amongst Tylenchina most species, Telotylenchus Siddiqi, 1960is here pro- in the sense that they are at the sametime easy to posed as a new junior synonym of Tylenchorhynchus. recognize and reasonablyconstant within anygiven Quinisulcius was proposed by Siddiqi (1971a) for the species. These characters (number oflines in lateral species in Tylenchorhynchuswith five lines in thelateral field, presence of longitudinal ridges,etc.) can easily field. Siddiqi added a few other differentiating charac- isolate groups of species and they are a great help for ters : habitusoften well curved, deirids frequently identification. The temptation was great to give a no- present, small-sized spicule velum, and gubernaculum menclatural status to such groups by naming them as bent backwards. Tarjan (1973) considered thatthe genera. Followingthe action of Siddiqi (1970) Who number of lines was the only distinctive character. He proposed the new genus Merlinius for some species in added two secondary differentiating criteria, i. e. lateral Tylenchorhynchus, several authors have made such no- field generally not areolated, andlip regionusually menclatorial moves. offset. We are opposed to suchactions because thedifferen- From the descriptions of the fourteen species cur- ces observed in cuticular features often mask a deeper rently in the genus (Q. capitatus, type species, Q. acti, similarity, or even identity, in the interna1 organs. Also Q. acutoides, Q. acutus, Q. cacti, Q. curuus, Q. hinza- each cuticular character seems to be evolving indepen- layae, Q.lineatus, Q. nilgiriensis,Q. obregonus, Q. dently from the others. For example, the presence of paracti, Q. punici, Q. solani, Q.tarjani), thebent longitudinal ridges is independant of the number of gubernaculum is the only consistent character, and it has lines in thelateral field, of areolation of these fields, and beenobserved inthe three species where males are of the morphology of the anterior region. Using such known. However, it should be noted that this character characters to create genera result in the multiplication can Vary in other taxa, when it is observed from a good of small groups that do notindicate a clear evolutionary number of specimens (Tylenchorhynchusaerolatus). Dei- trend. In the present article, we will not accept super- rids are described in only two species CQ. acutoides, Q. ficial resemblances as generic differentiating criteria. acutus). The rest of the characters are either variable in This explains the long list of genera proposed as syn- the genus (lip region varies from offset to almost con- onyms of Tylenchorhynchus. tinuous, habitus varies from almost straight to spiral), Telotylenchus, a genus proposed here as a synonym, or theyare not really different fromthe characters is quite different from the genera just discussed in the in Tylenchorhynchus(size of spicule, presence of velum, sense that itwas differentiated on muchfirmer grounds, lateral field areolations). Al1 other characters are quite at least at the time it was proposed (Siddiqi, 1960). It identical in the two genera, including general appear- remained valid, if not unchallenged, for a quarter of'a ance, tail shape in female and males specimens, diges- century. It was considered to be quite separate from tive and reproductive systems, SEM face views also are Tylenchorhynchusbecause of an overlap of the intestine similar (compars Figs 4 B and5 B in Sher& Bell, 1975). by the oesophagealglands. However, Goodey (1963) and The only real difference remains the numberof lines Loof (1963) noted that thetwo genera were in complete in. the lateral field. Siddiqi (1986, page 174) comments agreement except for this one character. Both authors that this number is " a character found to be variable accepted the genus as valid but rejected the subfamily in ... Tylenchorhynchus ". In SEM micrograph pictures Telotylenchinae proposed by Siddiqi together with his of Q. acti (Vovlas, 1983) andin cross section of Q. cacti new genus. This position has recently been reaffirmed (Chawla et al., 1968), the fifth, central line is shallower by Loof (1987). Seinhorst (1971) questioned the value and less marked than the other fourlines. The five-line of glandularoverlap as a criterion forhigher level field of Quinisulcius can be seen as a slight deviation classification. He noted that intermediate forms exist from the basic four-line field of Tylenchorhynchus. The between the two glandular morphologies described as presence of an additional line inthe lateral field is typical in the two genera under discussion. Tylenchor- certainly an interesting feature forspecies identification. hynchus brassicae. T. clams, T. indicus and T. nzashhoodi It has no value for genus differentiation. have glands slightly overlapping, and have the dorsal Quinisulcius is here proposed as a new junior syn- gland nucleus in the posterior half of the gland. He onym of Tylenchorhynchus.

Revue Nérnatol. 10 (2) :183-202 (1987) 189 R. Fortuner & M. Luc

Dolichorhynchus was differentiated by Mulkand proposed as a new junior synonym of Tylenchorhynchus. Jairajpuri (1974) from Tylenchorhynchus by the notched The name Dolichorhynchus is an homonym of Doli- male caudalalae, head bilobed, and body cuticle marked chorhynchus Willey, 1901, a Cephalocordata related to by prominent longitudinal and transverse striae. It in- Amphioxus. It is here rejected and replaced by an avail- cluded only two species (0.phaseoli, type species, and able synonym, Tylenchorhynchus, according to Article D. nigericus). 60 (b) of the International Code ofZoological No- Mulk and Siddiqi (1982) rejected the notched alae as menclature. The specific names of the taxa proposed in a valid generic criterion but they redefined the genusas Dolichorhynchus are available according to Article 11(h) having prominent longitudinal ridges over entire body, (iii) (1). They are accepted here as new combinations. and lateral field with four lines (three ridges). According The use of shape of labial region and structure of to thisnew diagnosis, they transferred five speciesto the lateral field lines in the definition of the genus Dolichor- genus (0.gladiolatus, D.judithae, D. lamell~en~s,D. hynchus prompted several authorsto propose other microphasmis, D. sulcatus). Two more species were later genera defined by various combinations of the charac- described in the genus, D. elegans and D. prophasmis. ters in question (see Tab. 1, summarizing the article of Notched caudal alae have been described for Merli- Jairajpuri and Hunt, 1984). The diagnoses of the four nius brachycephalus and Tylenchorhynchus lamelliferus. Onthe other hand, at least somespecimens of D. Table 1 nigencus have non-notched alae, according to Fig. 1M Differentiation of four genera related to Tylenchorhynchus in Mulk andJairajpuri (1974). We therefore agree with Mulk andSiddiqi (1982) that notched caudalalae is not Gew Lateralfield : Labial regiotl : Cui. annrlli a valid criterion. ojWbilobedlindareal coarse True structure of longitudinal ridges and lateral field can be seenonly in cross section or SEM micrographs. liilineellus Cross sections have been illustrated for a few species in 3x0 no no YeS the genus underdiscussion. Longitudinal ridges are very Dolichorhytxhm 4'pes yes yes-no no Neodolichorhynchus 4 no or yes yes no prominent in D. elegans, D.phuseoli, D. parvz, and D. incomplete sulcatus. However their structure in thefirst two species Tesselllrrs 4,'no no no YeS where the ridges are isolated from each other, is very different from the structure in thelast two, where they are adjacent. In D. gladiolatus, ridges are adjacent and genera here considered (Tab. 1) are not always consist- no more prominent than in Tylenchorhynchus claytoni. ent with the descriptions of the species included. For The lateral fields are composed of three adjacent example, Tessellus cluytoni has the lateral field areolated ridges (forming four lines) in D. sulcatus and D. gladiola- at least partially and thehead offset, Neodolichorhynchus tus; of three ridges forming either four or six lines sulcatus has lateral field completely areolated, Dolichor- depending how far apart they are from each other inD. hynchus parvus and D. elegans only have two lines (one prophasmis; and of only one ridge forming two lines in ridge) in the lateral field, etc. The lateral field of Trili- D. phaseoli, D. parvus and D. elegans. neellus clathrocutis is composed of two ridges that form Because of these widely different structures, and three or four lines depending how close the ridges are because ridges are attested in several genera where they from each other. This is evident on the SEM pictures are associated with lateral fields with two, three, four, of the field published withthe original description of the and six lines, it is concluded that ridges and lateral field type species and in Sauer(1986). Also the generic criteria lines cannot beused to differentiate the genusDolichor- are not consistently used in these related genera. For hynchus. 'example, lip region offset vs continuous is used to Bilobed anterior extremities are described for several differentiate Tessellusfrom Neodolichorhynchus. Lips are species in thegenus, but only SEM micrographs can be offset in Dolichorhynchus except in D. lamelliferus. If the uusted to reveal the true aspect of this character. D. character " lip region offset were accepted in the elegans SEM face view shows a roundlabial disc and six definition of the first two genera, consistency would well-marked labial sectors. A deeper groove separates require creation of another genus for D. lamelliferus. each couplet of submedian sectors. D. prophusmis also Finallyspecies described since the proposa1 of these has grooves between lip sectors, morepronounced genera do not fitwell with any of the generic diagnoses. between submedian sectors. Similar grooves exist in T. D. elegans has caudal alae notched as in Dolichorhynchus, toban (original description) and T. goflarti in Sher and and a non-areolated lateral field as in Neodolichorhyn- Bell (1975). Because the exact morphology of the an- chus. It becomes evident that al1 these characters are at terior end is known for only a few species, and because best specific characters and should not beused to similar shapes exist in Tylenchorhynchus, this character differentiate genera. Consequently Tessellus, Tnlineellus, cannot be used at this time to differentiate the genus. and Neodolichorhynchus are considered as junior syn- Dolichorhynchus Mulk & Jairajpuri, 1974 is here onyms of Tylenchorhynchus.

190 Revue Nirnatol. 10 (2) : 183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae

Siddiqi (1986) treated Neodolichorhynchus as a valid plete discussion for the re-establishment of Bitylenchus subgenus under Dolichorhynchus. He differentiated it was to be published in Nematologia mediterranea; this $rom Dolichorhynchus (Dolichorhynchus) mostly by the article has not appeared in that or any other journal. absence vs presence of minute vulval flaps. Vulval flaps Siddiqi (1986) formally reinstated Bitylenchus as a valid are symmetrical outgrowthsfound on thelateral sides of genus with B. dubius (Bütschli) as type, a speaes remark- the vulva. D. (Dolichorhynchus) phaseoli(type species of ably similar to Tylenchorhynchus in general appearance. the subgenus)was redescribed by Samsoen and Geraert Siddiqi differentiated Bitylenchus by the areolation of (1975) from a local population in Cameroon. The latero- the lateral field outer bands, and the presence of a non ventral ridges (the two longitudinal ridges thatare protrusible gubernaculum.In the diagnosis of the closest to the ventral one) are raised and strengthened genus, he also highlighted the presence of a large post- at the vulva level to form the flaps. The original de- anal intestinal sac, intestinal fasciculi, and he noted that scription of D. (Neodolichorhynchus) sulcatus indicated the female tail tip had a relatively thicker cuticle. These that thelatero-ventral ridges disappear at thevulva level characteristics are absent or doubtful in someof the (deGuiran, 1967). Jairajpuri andHunt (1984) and species placed by Siddiqi (1986) under Bitylenchus. For Siddiqi (1986) failed to indicate what evolutionary sig- example, B. areolatus has lateral fields areolated, but it nificance (ifany) they attach to this difference in hasno post-analsac, no fasciculi, the cuticle at the structure between the two species above. It is easy to female tail tip is not particularly thick, and the guber- define groups of species sharing one or two character- naculum protrudesfrom thecloaca. In B. tobari al1 three istics, but it takes more to show that these forms are bands of the lateral fields are areolated. Post-anal sac is phylogenetically related. Vulval flaps occur in many taxa absent from this species and from B. ventrosignatus. B. throughout Tylenchina andthis character is of doubtful goffartiand B. queirozi have protruding gubernaculum. value as a marker of phylogenetic relationships. Generally speaking, the characters used by Siddiqi to Vulval flaps are mentioned,sometimes withreser- redefine Bitylenchus often were not reported by the vations, in the species grouped by Siddiqi (1986) under authors of original species descriptions. Some may be the subgenus Dolichor/ynchus.In D. (D.) elegans an exam- inferred from the illustrations but with a high risk of ination of paratypes revealed the presence of very faint error when no text backs the figures. vulval flaps, most probably formedby the division ofthe Some of the species left in Tylenchorhynchus by ventral longitudinal groove as described in D. phaseoli Siddiqi (1986) possess some of the criteria he gave as by Samsoen and Geraert(1975). Vulval structures were distinctive of Bitylenchus. For example, the outer bands not described in any of the species placed in the sub- of the lateral fields of T. antarcticus are areolated; T. agri genus Neodolichorhynchus. It is not proper to infer the has a large post-anal sac; T. cylindricus has intestinal absence of a structure ina species because the structure fasciculi; the female tail tip of T. contractus has thicker is not mentioned in its description. cuticle; T. claytoni has a gubernaculum that does not Neodolichorhynchus is again rejected. protrude from the cloaca; etc. Divittus Jairajpuri, 1984 and Morasinema Javed, 1984 Bitylenchus sensu Siddiqi (1986) was defined using were proposed the same day (20 July 1984) with the very secondary characteristics that are not known for same typespecies Tylenchorhynchus divittatus. Jairajpuri many taxa, and that, when hown, do not clearly differ- (1984), acting as first revisor, rejected Morasinema as entiate this genus from Tylenchorhynchus. Bitylenchus is junior objective synonym. again considered as a junior synonym of Tylenchorhyn- Divittus was characterized by three lines in thelateral chus. field, and the absence of longitudinal ridges on body. Consistent with the discussions above, these characters are not accepted as diagnostic at the generic level, and Trichotylenchus Whitehead, 1960 Divittus is here consideredas a junior synonym of Tylen- = Uliginotylenchus Siddiqi, 1971 chorhynchus. Divittus (= Morasinema), and Tessellus were considered to be synonymous with Tylenchorhyn- DIAGNOSIS chus by Siddiqi (1986). Bitylenchus was proposed as a subgenus under Tylen- Telotylenchinae. Lip regioncontinuous with body chus and differentiated from three other related sub- contour. In SEM face views, oral disc lemon-shaped, genera (Tylenchus,Tylenchorhynchus, and Chitinotylen- submedian lobes low and flattened, lateral lobes com- chus) by the absence of a labial framework and the pletelyregressed, amphidsapertures appears as slits presence of two genital branches (Filip’ev, 1934). or pores at lateral edge of labial &SC. Stylet attenuated, Jairajpuri (1982) published a study of Bitylenchus as 15-25 pm long, with needle-like cone (somewhat stron- a subgenus under Tylenchorhynchus, including a short ger in T. palustris). Lateral field areolated, with three description and a key to its species. He failed to provide lines. Deirids absent. Tai1 long, three tosix times as long a differentiating statement to establish its relationships as wide, cylindroid, with a broadly rounded or clavate with other related subgenera. He indicated that a com- end, sometimes with thicker cuticle at tail tip. Males

Revue Nématol. 10 (2) : 183-202 (1987) 191 R. Fortuner di M. Luc

spicules with well developed velum, and bent guber- broadly rounded than shown in the original figure. In naculum. fact tails ofal1 the species under discussion have the same general shape : long, cylindroid, with a broadly TYPESPECIES rounded end. Some are more clavate, others are regu- larly cylindroid, but this should not be considered at Trichotylenchus falcijonnis Whitehead, 1960 generic level. Following the conclusions of Seinhorst (1971), the ~THERSPECIES basic resemblance betweenTrichotylenchus and Uligino- T. astriatzls Khan & Nanjappa, 1971 tylenchus is here recognized. Consequently, Uliginoty- = T. trilokiae Singh, 1971 lenchus Siddiqi, 1971 is proposed as a new junior syn- T. bijasciatus (Andrassy, 1961) n. comb.* onym of Trichotylenchus. = Tylenchorhynchzls bifasciatus Andrassy, 1961 Trichotylenchus is characterized among other Teloty- T. palustris (Merny & Germani, 1968) Seinhorst, 1971 lenchinae by the shape of labial region, which is elevated T. papyrus (Siddiqi, 1970) Seinhorst, 1971 and continuous with the body contour and by the tail T. rectangularis Netscher & Germani, 1969 long, thin, and cylindroid. The slender stylet with T. rhopalocercus (Seinhorst, 1963) Seinhorst, 1968 needle-like cone issimilar to some species in Tylen- T. uliginosus (Siddiqi, 1970) Seinhorst, 1971 chorhynchus. The lemon shaped disc and lateral sectors = Uliginotylenchus uligimus (Siddiqi,1970) Siddiqi, are found also in Merlinius and Morulaimus. 197 1

COMMENTS Paratrophurus Arias, 1970 Trichotylenchus was originally characterized by over- lapping glands and placed under Belonolaiminae, then = Histotylenchus Siddiqi, 1971 Telotylenchinae. Seinhorst (197 1) commented on the = Telotylenchoides Siddiqi, 1971 resemblance between Trichotylenchus and those species in Tylenchorhynchus that were later placed by Siddiqi DIAGNOSIS (1971 a) in the new genus Uliginotylenchus. The only Telotylenchinae. Body medium sized. Anterior ex- difference between the two genera is the absence of a tremity usually bullet shaped, more rarely a little flat- glandularoverlap in Uliginotylenchus. According to tened;continuous withbody contours, veryrarely Seinhorst (1971), in al1 species the oesophageal lumen slightly offset. Face view (SEM) quadrangular. Stylet is asymmetrically shifted between the dorsal and one 20-25 pm long. Lateral field with four lines. Deirids subventral gland. present. Tai1 short (c' = 1.5-2.5), cylindroid with broa- Tarjan (1973) rejected the analysis of Seinhorst (197 1) dly rounded end. Protoplasmic contents of tail often because : regressed. Oesophageal glands abutting or overlapping 1) Glandular overlap is a good classification cri- the intestine. Male : spicules with velum. terion. It has been argued throughout the present re- view that it is not. TYPESPECIES 2) U. palustris does not have a slender stylet with needle-likecone. Paratypes of this specieshave been P. 1003Arias, 1970 examined by the present authors. Stylet is not " rather strong " as indicated in the original description, but of OTHERSPECIES a thickness average for tylenchorhynchids. It is true that P. acristylus Siddiqi & Siddiqui, 1983 its cone is not " needle-like ",but stronger. Nevertheless, P. anornalus Kleynhans & Heyns, 1983 al1 other character fit comfortably withthe generic data. P. baoulensis (Netscher & Germani, 1969) n. comb. 3) T. rectangularis has four lines in thelateral field. = Telotylenchus baoulensis Netscher & Germani, 1969 Our examination of paratypes showedthat there are only P. bursifer (Loof, 1960) Siddiqi, 1971 ' three lines, as indicated in the original description. P. dissitus (Colbran, 1969) Siddiqi, 1971 4) T. rectangularis and T. palustris have cylindrical P. hedys (Kleynhans, 1975) n. comb. tails whereas the rest of the species have tails with clavate = H. hedys Kleynhans, 1975 extremities. Examination of paratypes showed that T. P. histoides (Siddiqi, 1971) n. comb. rectangularis tail ends, while not clavate, are more = H. histoides Siddiqi, 1971 P. historicus (Jairajpuri & Baqri, 1968) n. comb. = Telotylenchus historiczcs Jairajpuri & Baqri, 1968 * Siddiqi (1986) cites Seinhorst, 1971 as the authority for P. hozuei (Raski, Prasad & Swarup, 1964) n. comb. Trichotylenchus bifasciatus. Seinhorst (1971) noted that '' T. = Telotylenchus hovsei Raski, Prasad & Swarup, 1964 bifascians " (sic)probably should be placed inTrichotylenchus, P. hungariczu Andrassy, 1973 but he did not made the transfer. P. Kenuni Decker & El Amin, 1978

192 Revue Nématol. IO (2) :183-202 (6987) Reappraisal of Tylenchina. 6. Belonolaimidae

P. lobatus Loof & Yassin, 1971 shorter (cf less than 2.5 us more than 3 in Trichotylen- P. sudanensis Decker, Yassin & Al Amin, 1975 chus), and by SEM face view, quadrangular instead of P. siddiqii nom. nov. lemonshaped in Trichotylenchus.Amplinzerlinius re- = H. sudanensis Siddiqi, 1977 sembles Paratrophurus in general appearance, but dif- nec P. sudanensis Decker, Yassin & Al Amin, 1975 fers from it by SEM face view, and by male spicules without velum.Also, Amplimerlinius species al1 have six COMMENTS lines in the lateral field. When Siddiqi (197 1b) described Histotylenchus and Telotylenchoides, the former genuswas not compared to Merlinius Siddiqi, 1970 Paratroph.urus, and the latterwas said to differ from this = Scutylenchus Jairajpuri, 1971 genus only by its overlapping glands. Both new genera had overlapping glands, but the overlap in Tetotylen- DIAGNOSIS choides was said to differ from that in Telotylenchus, Trichotylenchus and Histotylenchus in that the dorsal Telotylenchinae.Body medium sized. Lateral field nucleus was close to the oesophago-intestinal junction, with six lines (eight lines in M. koreanus, though only with the subventral nuclei anterior to it. However the six are visible in lateral view). Longitudinal ridges some- same author (Siddiqi, 1977) later described Histotylen- times present (M. koreanus). Deirids, when present, at chus sudanensis with subventral nuclei opposite or an- a level where the lateral field has only four lines. Tai1 terior to the oesophago-intestinal junction. From the medium sized (c' = 2-4), conoid, never with thickened illustrations in Siddiqi (1971 b), the dorsal nucleus lies cuticle in distal portion. Labial region continuous to 5 to 11 pm posterior to thejunction in Telotylenchoides, slightly offset. SEM face view typically with oval labial 20 pm posterior in Telotylenchus, and 36 pm posterior disc surroundedwith six-sectored first lip annulus, in Histotylenchus. This slight difference in measure- submedian sectors somewhat flattened. Labial region ments is not considered diagnostic at the generic level. annuli interruptedby longitudinal striations or grooves. The shape of the anterior end is somewhat more rec- Stylet generally medium sized, 20-25 pm long, some- tangular in Histotylenchus, and more conoid-rounded times shorter (10 Fm) or longer (up to 40-50 pm), cone in Paratrophum and Telotylenchus. This difference seems sometimes needle shaped. Male spicules without well slight and- inconclusive. Lateral fields are said to be developed velum, cylindroid, blunt ended. Gubernacu- areolated over entire body in Histotylenchus, but not lum not protruding from cloaca. areolated in the other two genera. Lateral field areo- lations are at best a specific character as demonstrated TYPESPECIES once again whenSiddiqi (1977) described Histotylenchus M. brevidens (Allen, 1955) Siddiqi, 1970 sudanensis without areolations except in oesophageal = Tylenchorhynckus brevidens Allen, 1955 region and a few lines in outer bandsover rest of body. The lumen of the stylet cone was said to be asym- metrical near its base in Histotylenchus. The stylet lumen OTHERSPECIES is very difficult to observe withthe light microscope. In M. adakensis Bernard, 1984 the absence of special preparation techniques,this struc- M. aflinis (Allen, 1955) Siddiqi, 1970 ture is seen as light refractions that change with focus. = Nagelus afinis (Allen, 1955) Siddiqi, 1979 By contrast with these slight differences in details, M. alboranensis (Tobar-Jimenez, 1970) Tarjan, 1973 there are many features in common among thespecies = N. alboranensis (Tobar-Jimenez, 1970) Siddiqi, 1986 of al1 three genera, including their general appearance, M. alpinus (Allen, 1955) Siddiqi, 1970 SEM face view, etc. Histotylenchus and Telotylenchoides = N. alpinus (Allen, 1955) Siddiqi, 1979 are here proposed as new synonyms of Paratrophurus. M. apricus (Andrassy, 1980) n. comb. The genus differs from Tylenchorhynchus mostly by = S. apricus Andrassy, 1980 M. bavaricus (Sturhan, 1966) Siddiqi, 1970 the shape of the tail, which is short, cylindroid, and has M. bijnorensis Khan, 1971 a broadly rounded end. It is interesting to note that, M. bogdanovikatjkovi (Kir'yanova, 1941) Siddiqi, 1970 while the relative length of tail is well within the range M. capitonis Ivanova, 1983 of values for belonolaimids (cf = 2 to 33, the proto- M. circellus Anderson & Ebsary, 1982 plasmic contents of the tail, in the species with a thick M. conicus (Allen, 1955) Siddiqi, 1970 distal tail cuticle, has a relative length of 1.5 to 2 anal = N. conicus (Allen, 1955) Siddiqi, 1979 body widths, similar to ratio cf inhoplolaimids. Tails in M. curiosus (Wilski, 1965) Sher, 1974 , Paratrophurus seem to be experiencing an axial, sym- = N. curiosus (Wilski, 1965) Siddiqi, 1986 metrical regression that eventually would result in tails M. cylindricaudatus (Ivanova, 1968) Siddiqi, 1970 as short as those in Hoplolaimidae. = S. cylindricaudatus (Ivanova, 1968) Siddiqi, 1979 Paratrophurus differs from Trichotylenchus, a genus M. fakatus Eroshenko, 1981 also with cylindroid tail,by the,tail being relatively = N. fakatus (Eroshenko, 1981) Siddiqi, 1986

Revue Nématol. 10 (2) : 183-202 (1987) 193 R. Fortuner 8 M. Luc

M. gaudialis (Izatullaeva, 1967) Siddiqi, 1986 M. superbus (Allen, 1955) Siddiqi, 1970 M. graminicola (Kir’yanova, 1951) Siddiqi, 1976 = N. superbus (Allen, 1955) Siddiqi, 1979 M. grandis (Allen, 1955) Siddiqi, 1970 M. tartuensis (IGall’, 1959) Siddiqi, 1970 = N. grandis (Allen, 1955) Siddiqi, 1979 = S. tartuensis (JGall’, 1959) Siddiqi, 1979 M. hexagrammus (Sturhan, 1966) Siddiqi, 1970 M. tatrensis (Sabova, 1967) Tarjan, 1973 = N. hexagrammus (Sturhan, 1966) Siddiqi, 1979 = N. tatrensis (Sabova, 1967) Siddiqi, 1986 = M. berberidis (Sethi 81 Swarup, 1968) Siddiqi, 1970 M. tessellatus (Goodey, 1952) Siddiqi, 1970 M. hexincisus (Jairajpuri & Baqri, 1968) Siddiqi, 1970 = S. tessellatus (Goodey, 1952) Siddiqi, 1979 = S. kexincisus (Jairajpuri & Baqri, 1968) Siddiqi, 1979 M. tetylus Anderson & Ebsary, 1982 M. joctus (Thorne, 1949) Sher, 1974 M. tkomasi (Skwiercz, 1984) n. comb. M. koreanus Choi & Geraert, 1971 = S. thomasi Skwiercz, 1984 = S. koreanus (Choi & Geraert, 1971) Siddiqi, 1979 M. tortilis IZazachenko, 1980 M. laminatzrs (Wu, 1969) Siddiqi, 1970 M. tumensis (Skwiercz, 1984) n. comb. = S. lanzinatus (Wu, 1969) Anderson & Ebsary, 1982 = S. tumensis Skwiercz, 1984 M. lenonls (Brown, 1956) Siddiqi, 1970 M. undyfemrs (Haque, 1967) Siddiqi, 1970 = S. lenonrs (Brown, 1956) Siddiqi, 1979 M. variabilis (Ivanova & Shagalina, 1983) n. comb. M. lineutus (Allen, 1955) Siddiqi, 1970 = S. variabilis Ivanova & Shagalina, 1983 = N. lineutus (Allen, 1955) Siddiqi, 1979 M. varians (Thorne & Malek, 1968) Siddiqi, 1970 M. longus (Wu, 1969) Sturhan, 1981 = N. varians (Thorne & Malek, 1968) Siddiqi, 1986 = Geocenamus longus (Wu, 1969) Tarjan, 1973 = S. longus (Wu, 1969) Skwiercz, 1984 COMMENTS M. loofi Siddiqi, 1979 M. macrodens (Allen, 1955) Siddiqi, 1970 Scutylenchus was originally proposed for Tylenchor- = N. macrodens (Allen, 1955) Siddiqi, 1979 hynchus mamillatusTobar-Jimenez, 1966 and differen- M. macrophasmidus Khan & Darekar, 1979 tiated by the large phasmids, sloping stylet knobs, = N. macrophasmidus (Khan & Darekar, 1979) Siddiqi, areolated lateral field, and digitate tail tip. After An- 1986 derson (1977) and Hooper (1978) proposed this genus M. mamillatus (Tobar-Jimenez, 1970) Anderson, 1977 as a junior synonym of Medinius, Siddiqi (1979) revali- = Sczrtylenchusmamillatus (Tobar-Jimenez, 1970) Jai- dated it because of the longitudinal grooves that are rajpuri, 197 1 divided by transverse striae into small blocks, and by the M. microdorus (Geraert, 1966) Siddiqi, 1970 absence of deirids in S. mamillatus. M. nanus (Allen, 1955) Siddiqi, 1970 Because phasmids in S. mamillatus are no larger than M. neohexagrammus Ivanova, 1978 phasmids in Merlinius, because cuticular details are not = N. neohexagrammus (Ivanova, 1978) Siddiqi, 1986 accepted as diagnostic at generic level, and because the M. niazae Maqbool, Fatima & Hashmi, 1983 rest of the characters proposedto differentiate Scutylen- M. notkus (Allen, 1955) Siddiqi, 1970 chus are common in species of Telotylenchinae, Scuty- M. paramonovi Volkova, 1972 lenchus is again considered to be a junior synonym of M. planitierum Eroshenko, 1984 Merlinius. M. plerorbus Anderson & Ebsary, 1982 Merlinius is accepted as a valid genus because of the M. processus Siddiqi,1979 ’ differences in face view, and malespicule structure. The M. productus (Thorne, 1949) Sher, 1974 six-line lateral field makes it easy to identify this genus M. pseudobavaricus Saltukoglu, Geraert & Coomans, 1976 and differentiate its species from those in the related M. quadrzfer (Andrassy, 1954) Siddiqi, 1970 genus Tylenchorhynchus. = S. quadrifer (Andrassy, 1954) Siddiqi, 1979 = S. ornatus (Allen, 1955) Siddiqi, 1979 M. quettensis (Maqbool, Ghazala & Fatima, 1984) n. comb. = S. quettensis Maqbool, Ghazala & Fatima, 1984 Nagelus Thorne & Malek, 1968 M. rugosus (Siddiqi, 1963) Siddiqi, 1970 = S. rugosus (Siddiqi, 1963) Siddiqi, 1979 DIAGNOSIS M. salechardicus Nesterov, 1985 M. semicircularis Luth, 1984 Telotylenchinae. SEM face view broadly oval, and lat- M. siddiqii Mulk, 1978 erally elongated, with labial disc partially or completely = S. siddiqii (Mulk, 1978) Skwiercz, 1984 fused with first lip annulus, lip annulussectors alsopar- M. sobolevi (Mukhina, 1970) Taqan, 1973 tially or completely fused together. Amphids apertures = S. sobolevi (Mukhina, 1970) Siddiqi, 1979 within thestructure made by the firstannulus and M. sphaerocephalus (Ivanova, 1982) n. comb. labial disc.The rest oflabial annuli without longitudinal = S. sphaerocephalzls Ivanova, 1982 grooves or indentations. Deirids present in the lateral M. stegus (Thorne & Malek, 1968) Siddiqi, 1970 field at a level where the field has six lines. Tai1irregu- = S. stegzls (Thorne & Malek, 1968) Siddiqi, 1979 larly conoid, with a distal hyaline part. Male spicules

194 Revue Nématol. 10 (2) :183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae without well developed velum, cylindroid, blunt ended. A. socialis (Andrassy, 1962) Siddiqi, 1976 Gubernaculum not protruding fromcloaca. = Tylenchorhynchus socialis Andrissy, 1962 A. umbonatus Ivanova, 1982 TYPE SPECIES A. viciae (Saltukoglu, 1973) Siddiqi, 1976 = Merlinius viciae Saltukoglu, 1973 N. aberrans Thorne & Malek, 1968 COMMENTS OTHERSPECIES See list in Powers, Baldwin and Bell (1983) Amplimerlinius is somewhat similar to Paratrophurus in the large body size with continuous lip region and COMMENTS cylindroid tail with a hyaline distal part. It differs by SEM face view (Paratrophurus has a somewhat rec- Powers, Baldwin and Bell (1983) recently reviewed tangular SEM face view pattern, similar to Tylenchor- this genus, and differentiated it from Merlinius mostly hynchus) and by thestructure of the male spicules. by the structureof the anterior end, as seen in SEM face The six-lined lateral field permits an easy identification yiew, and by the lack of longitudinal lip striations, of this genus. position of deirids, and hyaline tail extremity. It shares Amplimerlinius also resembles Pratylenchoides, a genus these characters with Amplimerlinius, but Nagelus can in Pratylenchidae. Pratylenchoides hasa lower labial be differentiated from this genus by SEM face view, region than Amplimerlinius, and its labial disc is fused more oval, slightly offset lip region, andfemale tail with the sub-median lip sectors only, but the lateral conoid. sectors are not modified. Pratylenchoides isgenerally smaller and has a smaller stylet than Amplimerlinius. Most of its species have glands overlapping the intes- Amplimerlinius Siddiqi, 1976 tine; somehave only four lines in thelateral fields. The sexual dimorphism visible in Pratylenchoides (with male DIAGNOSIS stylet and median bulb somewhat atrophied) has not been describedin any Anaplinzerlinius. Finally the labial Telotylenchinae. Body mediumto large (1 to 2 mm). framework is different between the MO genera. The Labial region continuous with bodycontour. SEM face basal plate is thinner in Amplimerlinius which also has view similar to that of Nagelus except that it is more a basal ring longer than Pratylenchoides. rounded. Lateral field with six lines over most of body. Deirids present, in the six-line area of lateral field. Tail Trophums Loof, 1956 cylindroid with a broadly rounded terminus,with thick- ened cuticle at distal extremity. Labial framework and DIAGNOSIS stylet robust. Oesophageal glands sometimes overlap- ping the beginning of the intestine for a short distance. Telotylenchinae. Body medium sized to large. Lip Male spicules without welldeveloped velum, blunt region bullet-shaped (conoid-rounded), continuous with ended. Gubernaculum not protruding fromcloaca. body contour. SEM face view appears to be smooth, with the labial disc and labial sectors fused in a single structure (Sher & Bell,1975). Stylet 10-20 pm long. TYPE SPECIES Oesophageal glandsabutting, pyriform. Tail cylindroid, A. amplus Siddiqi, 1976 witha broadly rounded terminus, sometimes rather shortfor the family,with thick cuticle atthe distal OTHERSPECIES extremity. Females with only one genital branch, pos- terior branch atrophied to a post-uterine sac. However Amplimerlinius clavicaudatus (Choi & Geraert, 1975) Sid- the vulva is at mid-body. diqi, 1976 = Merlinius clavicaudatus Choi & Geraert, 1975 A. caroli (Fortuner, 1985) Siddiqi, 1986 TYPESPECIES = Aphelenchus dubius Steiner, 1914 in Goodey, 1932 T. iwzperialis Loof, 1956 A. iearus (Wallace & Greet, 1964) Siddiqi, 1976 = Tylenchorhynchus icarus Wallace & Greet, 1964 OTHER A. intemedius (Bravo, 1976) Siddiqi, 1976 SPECIES = Merlinius intemedius Bravo, 1976 Trophurus inzpar Ganguly & Khan, 1983 A. macrurus (Goodey, 1932) Siddiqi, 1976 T. lomus Saha, Chawla & Khan, 1974 = Aphelenchus dubius Steiner, 1914 T. longimarginatus Roman, 1962 nec Tylenchus dubius Biitschli, 1873 T. marathwadensis Suryawanshi, 1971 A. omentelus IUeynhans & Heyns, 1983 T. nlinnesotensis (Caveness, 1958) Caveness, 1959 A. siddiqii Mancini, Cotroneo & Moretti, 1982 = Clavaurotylenchus nzinnesotensis Caveness, 1958

Revue Nénzatol. 10 (2) :183-202 (1987) 195 R. Fortuner & M. LUC

~ ~~~~~

T. roigi Razhivin, O'Relly & Perez Millan, 1973 (m = 60-80). In forms with elongate stylets, procorpus I: scognarniglii Talamé, 1974 enlargedand separated from the medianbulb by a T. sculptusLoof, 1956 constriction. Median bulb strong, muscular, with large T. similis Khan & Nanjappa, 1971 valve. Labial region often offset, bulbous inlateral view, T. ussuriensis Eroshenko, 1981 sometimes continuous with body contour. SEM face view generally witha well marked, round,labial disc and COMMENTS a first lip annulus with submediansectors well marked Trophurus is unique among Tylenchina in having the and lateral sectorsregressed, almost absent. Rarely, vulva at mid-body while the posterior genital branch is lateral sectorsonly slightly regressed. In onegenus, atrophied. As noted by Loof (1956) the ratio V is equal Moruluivzus, labial disc and lateral sectors are fused into to about 50 in some monodelphic Tylenchidae, but in a lemon-shaped structure. Female tail long, generally those cases, it is the long filiform tail that is responsible cylindroid to broadlyrounded end, sometimes more for this unusual situation. In Trophurus, the tail is short, conoid. Deirids always absent. there is no posterior branch to speak of, and the vulva Belonolaiminae differs from Telotylenchinae by its is nevertheless in the middle of the body. This makes it biology, with a tendancy towards an elongation of the easy to accept Trophurus in Telotylenchinae,a subfamily stylet to reach inside the roots. SEM face views, with where al1 other genera have two genital branches. Tails well marked round labial disc are characteristic for most of Trophurus species are short (cf under 2), but theslim genera. stylets are quite different fromthe robust styletsof Hoplolaimidae, a familycharacterized by its short tails. TYPE GENUS Also, phasmids are located on the tail. As in Parutrophu- Belonolaimus Steiner, 1949 rus and Amplimerlinius, the shorter tails accompanied by = Zbipora Monteiro & Lordello, 1977 (n. syn.) a thick distal cuticle seems to indicate a regression of tail length in an axial, symmetrical manner. Tai1regression OTHERGENERA in Hoplolaimidaeseems to follow either themode asymmetrical (Helicotylenchus)or the modeaxial, lateral Carphodorus Colbran, 1965 (Hoplolairnus). Morulaimus Sauer, 1966 Geocenamus Thorne & Malek, 1968 = Hexadorus Ivanova & Shagalina, 1983 (n. syn.) Genus dubium Sauertylenchus Sher, 1974

Tetylenchus Filip'ev, 1936 The genera in Belonolaiminae

Sher (1974~)reviewed the history and status of this Sauertylenchus Sher, 1974 genus fiist proposed in 1936 by Filip'ev with T. tenuis (Micoletzky, 1921) asthe type species. He found that the type species was not adequately describedor illustrated, DIAGNOSIS' and that the poorly preserved holotype did not retain Belonolaiminae. Body large sized (1.7 mm in the type sufficient characters to make a specific or generic species). SEM face view with six sectors present, lateral diagnosis possible. He placed T. tenuis in species dubiae sectors slightly smaller than submedians. Labial frame- and the genus Tetylenchus in genera dubiu. The rest of work weakly developed. Stylet thin, long (37 pm in the the species in Tetylenchus were transferred by Sher type species). Deirids absent. Glands abutting. Male spic- (1974~) toMerlinius, Leipotylenchus,and Triversus. Sid- ules with flanges. Gubernaculum slightly protruding diqi (1979), after studying thepoorly preserved holotype from cloaca. of T. tenuis agreed with the decision of Sher, and noted that there was a possibility that this species might be a TYPEAND ONLY SPECIES Ditylenchus. In agreement with Sher's (1974~)opinion, Tetylenchus is here considered a genus dubium. S. labiodiscus Sher, 1974

COMMENTS The subfamiiy Belonoiaiminae-iihitehead, 1960 Sher (1974 b) placed Sauertylenchusin Tylenchorhyn- DIAGNOSIS chinae (= Telotylenchinae). However, the bulbous labial region, round labial disc, weakly developed labial Belonolaimidae. Cephalic framework oftenvery weak, framework, strongly valvated median bulb, elongate sometimes heavily sclerotized. Stylet slender, elongate, stylet, link this genus to the belonolaimids. This genus usually 60-150 pm long, with cone longer than shaft from Australia may be seenas a relict of ancestral forms

196 Revue Nematol. 10 (2) : 183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae from which evolved the presentday belonolaimids. (60-130 Pm) overlaps the corresponding rangein Geoce- Because it shares some derived characters with members namus (27-65 p).The male of H. deserticola was of this subfamily (strong valve, elongate stylet), it is now described by Ivanova and Shagalina (1983b). The spicu- transfered to Belonolaiminae. les and gubernaculum correspondwell to thedefinition of Geocenamus. Hexadorus is here proposed as junior synonym of Geocenamus. Geocenamus Thorne & Malek, 1968 Geocenanzus differs from Sauertylenchus by the = Hexadorus Ivanova & Shagalina, 1983 (n. syn.) smaller body lengthand theshape of male spicules.The six lines in lateral fields provide an easy way to differ- DIAGNOSIS entiate the two genera. Belonolaiminae. Body medium sized. Labial region bulbous. SEM face view with well marked round labial disc. First lip annulus divided into six sectors, lateral Morulaimus Sauer, 1966 sectors smaller. Labialframework weaklydeveloped. Lateral field with six lines. Deirids absent (but said to DIAGNOSIS beinconspicuous by Siddiqi,1986). Stylet slender, 25-130 p long, cone longer than shaft. Tail conoid to Belonolaiminae. SEM face view with labial disc le- almost cylindroid. Spicules without velum, blunt ended. mon-shaped; first labial annulus dividedinto six sectors, Gubernaculum not protruding fromcloaca. lateral sectors smaller, submedian sectors somewhat flattened. Labial regionnot marked by deep longitudinal TYPESPECIES indentations. Stylet elongate, 60-100 Pm long. Cone d. tenuidem Thome & Malek, 1968 60-80 O/o of total stylet length. Labial framework always = Tylenchorhynchus polonicus Szczygiel, 1970 weak. Procorpus thickened to accommodate the long = G. polonicus (Szczygiel, 1970) Sturhan, 1981 stylet, and separatedfrom themedian bulb by aconstric- tion; median bulb with strongvalve. Oesophageal glands overlapping beginningof intestine. Tail sometimes short OTHERSPECIES for Belonolaimidae(c' = 2 to 3), tail shape varies from G. arealoferus (Razzhivin, 1971) n. comb. cylindroid with a broadly rounded terminus to almost = Morulaitnus arealoferus Razzhivin, 1971 conoid. G. arcticus (Mulvey, 1969) Tarjan, 1973 G. deserticola (Ivanova & Shagalina) n. comb. = Hexadorus deserticola Ivanova & Shagalina, 1983 TYPESPECIES G. kivjanovae (Sagitov, 1973) n. comb. = Dolichodorus kirjanovae Sagitov, 1973 M. arenicolus Sauer, 1966 = H. kivjanovae (Sagitov, 1973) Siddiqi, 1986 G. longus (Wu, 1969) Tarjan, 1973 , OTHERSPECIES = II: longus Wu, 1969 G. tokobaevi (Sultanalieva, 1983) n. comb. Morulaitnus geniculatus Sauer, 1966 = Morulaimus tokobaevi Sultanalieva, 1983 = Scutellonewza magnum Yeates, 1967 = H. tokobaevi (Sultanalieva, 1983) Siddiqi, 1986 M. sclerus Sauer, 1966 G. uralensis Baidulova, 1983 M. simplex Sauer & Annells, 1981 M. soldus Colbran, 1969 COMMENTS M. whitei (Fisher, 1965) Sauer, 1966 = Telotylenchus whitei Fisher, 1965 Geocenamus was originally proposed in Tylenchor- hynchinae, and said by Siddiqi (1979) to be related to COMMENTS Merlinius. Like Sauertylenchus, its bulbouslabial region, round labial disc, andsometimes elongate stylet are Morulaimus is differentiated from Belonolainzus by derived characters that prompted us to move this small the lemon shaped labial disc. The species in this genus genus to Belonolaiminae. are generally smaller and proportionnally thinner, with Hexadorus was recently proposed in Belonolaiminae a shorter stylet, and with a tail shorter and more co- by Ivanova and Shagalina (1983) for a new species, H. noid than species in Belonolaimus. To date, al1 species deserticola and for Morulaimus arealoferus. Its general described in Morulaimus have a four-Iine lateral field, appearance (labial region, tail shape, lateral field, bi- which helps in their identification. lobedspermatheca, male spicules of M. arealoferus, Morulaimus differs from Sauertylenchus and Geoce- etc.) is quite similar to Geocenamus. Stylet length of H. nanzus by the more regressed lateral lip sectors. It has arealoferus (60-70 Pm) is similar to that of G. longus a longer stylet and the glands overlap the intestine for (56-65Pm). Range of stylet lengths in Hexadorus a longer distance.

Revue Néinatol. 10 (2) :183-202 (1987) 197 R. Fortuner & M. Luc

Belonolaimus Steiner, 1949 with lateral sectors a little smaller than the submedians. Labial region with deepindentations. Labial framework = Ibipora Monteiro & Lordello, 1977 (n. syn.) massive, strongly developed. Stylet elongate, about 95 ym long, with cone about 68 O/o of stylet length. DIAGNOSIS Corpus as in Belonolaimus. Oesophageal glands overlap beginning of intestine. Tai1 relatively short (c’ = 1.7), Belonolaiminae. SEM face view shows a wellmarked cylindroid with a broadlyrounded terminus. Lateral rounded labial disc,and first lip annulusdivided into six field said to be withtwo lines in original description, but sectors, lateral sectors almost completelyregressed, seen SEM pictures show four lines (Sauer, Brzeski & Chap- only as small interruptions of the firstone or two labial man, 1980). annuli. Labialregion marked by deep longitudinal grooves.Stylet very long, 60-150 pm long, its cone TYPE AND ONLY SPECIES 70-80 O/O of total stylet length. Corpus as in Morulaimus. Oesophageal glands overlapping beginningof intestine. C. bilineatzls Colbran, 1966 Female tail cylindroid with a broadly rounded terminus. Lateral field with four lines or less. COMMENTS Carphodorus was originally described in Dolichodori- TYPESPECIES nae, but it is considered to be closer to Belonolaimus B. gracilis Steiner, 1949 because of the overlapping glands, face view, female and male tails, caudal alae, etc. Its massive labial framework OTHERSPECIES is reminiscent of the corresponding structure in Doli- chodoridae, but Sauer, Brzeski and Chapman (1980) B. unuma (Monteiro & Lordello, 1977) n. comb. have shown that only theexternal edges and theinterna1 = Ibipora anama Monteiro & Lordello, 1977 lining of the labial arches are heavily sclerotized, while B. euthychilus Rau, 1963 the basal plate remains thin. This also is observed in B. jaru (Monteiro & Lordello, 1977) n. comb. Morulaimus sclerus and M. whitei. The superficial re- = jura Monteiro & Lordello, 1977 1. semblance of labial framework in Carphodonls. and B. lineatus Roman, 1964 dolichodorids is due to convergent evolution, :but it = 1. lineatus (Roman, 1964) Monteiro & Lordello, 1977 B. Iolii Siviour, 1978 helps identify Carphodorus amongBelonolaiminae. = I. Zolii (Siviour, 1978) Siviour & McLeod, 1979 Carphodonu can be differentiated from the species in B. longicaudatzls Rau, 1958 Morulaimus with a heavily sclerified labialframework by B. maritimzls Rau, 1963 its labial disc thatis rounded as in Belonolaimus and not B. nortoni Rau, 1963 lemon-shaped as in Morulaimus.

COMMENTS Discussion Ibipora was proposed as intermediate between Moru- Belonolaimidae as definedhere isa large family laimus and Belonolaimus because its species have the grouping togethera number of forms thathave followed same face view as the latter and lateral fields with four divergent paths of evolution. lines, as in the former. The numberof lateral field lines When compared to theancestral tylenchid (as defined in not diagnostic at generic level. The species in Ibipora inLuc et al., 1987), or to Tylenchidae and related have a styletranging from 65 to 100 pm thatis somewhat families, the belonolaimids can be seenas having com- shorter than species in Belonolaimus S. str. (90-150 pm). pleted the first step on roadthe to undergroundobligate This small difference does not warrant the recognition parasitism of higher plantroots. Al1 members of Belono- of a separate genus. Ibipora is here proposed as a new laimidae are phytoparasites. The alternate life styles junior synonym of Belonolaimus. such as above ground plant-parasitism and insect asso- Belonolaimus differs from Morulaimus mostly in the ciation well represented in Tylenchidae and Anguinidae, SEM face view. The characters discussed in the para- are unknown among the belonolaimids which also are graph on Morulaimus can help in the identification of unable to survive on a fungal diet. these two genera. Withfew exceptions (e. g. semi-endoparasitism of Tylenchorhynchus acti (= Quinisulcius acti)described by Vovlas, 1983) Belonolaimidae remained migratoryecto- Carphodorus Colbran, 1965 parasites. It will be for the Hoplolaimidae to become DIAGNOSIS migratory or sedentary semi-endoparasites, for the Pra- tylenchidae to developmigratory endoparasitism and Belonolaiminae. SEM face view with well marked semi-endoparasitism, and for Heteroderidae to succeed labial disc; first labial annulus divided into six sectors, fully in sedentary endo-parasitism.

198 Revue Nématol. 10 (2) :183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae

N 01

cc) -r W \O \O w II E

Revue Nématol. 10 (2) : 183-202 11987) 199 R. Fortuner di M. Luc

Morphologically, thepassage to obligate parasitism of in Carphodorus and in some Morulainzus speciesis higher plants is associated withlengthening of the stylet, heavily sclerotized and resembles the structures ob- usually longer than inTylenchidae and Anguinidae. The served in Dolichodoridae. However, in Anzplinzerlinius, reduction of the tail that seems to be associated with Morulairnus and Carphodorus, as in al1 other belonolai- plant parasitism is already well attested in Belonolaimi- mids, the labial plate and thebasal ring remainthin and dae where the filiform tail of the Tylenchidae is un- lightly sclerotized, and quite different from the heavy known. The oesophageal glands beginto increase in size, structures observed in Dolichodoridae andPratylenchi- overlapping the intestine in many species. The colum- dae. There exists a trend towards a reinforcement of the ned uterus has three rows of cells (instead or four rows labial framework in Belonolaimidae, but it follows an in the less derived families). original path, quite distinct from thetrends observed in The belonolaimids still possessmany ancestral, other families. non-derived features, e. g. genital system with two bran- ches (with the exception of Trophurus),absence of sexual TAIL dimorphism, presence of a strong oesophago-intestinal Tails in Belonolaimidaeprobably originated from valve, presence of deirids in many species, and amphi- forms similar to present day Psilenchus. The tail of P. mictic reproduction more, frequent thanparthenogen- aestuanzls (as illustrated by Siddiqi, 1986) might be seen esis. On theother hand, several evolutionarytrends as an intermediate form with a long, thin, hyaline characteristic of Tylenchina (Luc et al., 1987) are visible extremity and a conoid firsthalf. Except for the hyaline in thefamily but, because of multiple parallelisms, they part, the tail is somewhat similar to conoid tails in many are difficult to arrangeinto a coherent phylogenetic Belonolaimidae (Tylenchorhynchus,Merlinius, Moru- picture. These trendswill be discussed for fourrelevant laimus, etc.). Thick terminal cuticle in tails of many features : stylet, labial framework, tail, and face view. species of these genera may be seen as remnants of a similar regression that may have occured in the past. STYLET Tnchotylenchus tails represent what maywell be a Stylets evolved in atleast three directions : i)a gradua1 different path of tail regression. Tails in this genus are lengthening and strengthening of the stylet from the long and thin, but they have a cylindroid shape. They most basic forms (stylet = 20 pm; m = 50; cone and may have originated from filiform tails after an axial shaft slender but notmodified, knobs smalland sloping regression. backwards) to forms close to hoplolaimid stylets (stylei Many belonolaimids have thickset, short tails, with a = 40 Pm;m = 50; cone andshaft robust; knobs cylindroid shape and a broadly rounded end. Such tails anteriorly flattened; example : Amplimerlinius amplus); may have originated from either one of the two forms ii)a great elongationof the stylet and particularly of its above, or they may have evolved independantly fromthe cone but no other modifications (stylet = 100-150 pm, ancestors of the family. It is significant to note that many m = 60-80; example Belonolaimus spp.); iii) a modi- among this third category of tails seem to be in the fication of the cone to a thin, needle-like structure process of an axial regression in which the protoplasmic (many Tylenchorhynchus, Trichotylenchus,and Merlinius contents of the tail regress first, being replaced by an species). extra-thick cuticle at tail tip. A similar regression may The first trend can be used to explain the structure have contributed to the formation of the short, cylin- of the stylets in the more derived families, Pratylenchi- droid to hemispherical-ended tails found in many hoplo- dae, Hoplolaimidae and Heteroderidae.The second one laimids. is associated with an adaptation to " external endopara- ' sitism where the body of the nematode remains outside LABIALREGION the plantwhile the elongate stylet can reach deepinside Many Belonolaimids have a labial region similar to the roots. Conversely the third trend shows an adap- that in Tylenchidae, high, ogival, and continuous with tation to surface grazing, where thethin needle-like the body contour. Two main evolutions seem to have stylet can easily penetrate cells at the periphery of the occured from this ancestral shape; labial region glo- root. il bose, bulbous, which occurs in many species in Belo- nolaimidae; and ii)labial region with smalla indentation LABIALFRAMEWORIZ that resembles the labial region of hoplolaimids. Face In most species in Belonolaimidae, the labial frame- views can only be resolved usingSEM photographs. In workis thin, lightly sclerotized, andthe basal plate the most ancestral shape, a roundishor ovoid labialdisc extends posteriorly in a very thinannular extension is associated with a first lip annulus divided into six (= basal ring) close tothe cuticle. Some speciesof sectors equally developed. In Belonolaimidae, amphids Amplimerlinius have a labial framework more strongly are dorso-ventrally directed slits at theedge of the labial sclerotized, somewhat similar to theframework in Praty- disc; the sub-median sectors are always somewhat flat- lenchidae. Similarly, the anterior part of the framework tened; andthe lateral sectors are smaller. From this

200 Revue Nématol. 10 (2) :183-202 (1987) Reappraisal of Tylenchina. 6. Belonolaimidae

ancestral shape, three lines of evolution can be ident- FORTUNER,R. (1982). On the genusDitylenchus Filipjev, 1936 ified; i) the labial disc and reduced lateral sectors are (Nematoda : Tylenchida). Revue NématoZ., 5 : 17-38. often fused together in a lemon shaped structure(Merli- FORTUNER,R. (1986). English translationsof selected taxononzic nius and Morulaiwzus for example);ii) in many formsin papers in nematology. Volume 3. Califomia Department of Belonolaiminae, the labial disc keeps its identity and Food and Agriculture, Sacramento, USA, 74 p. becomes quite round and prominent, the submedian GERAERT,E. & RASKI, D. J. (1987). A reappraisal of Tylen- sectors enlarge while the lateral sectors regress and china(Nemata). 3. The familyTylenchidae Orley, 1880 almost disappear; the whole structure resembles a four (Tylenchoidea). Revue Névnatol., 10 : 143-161. leaf cloverthat is similar to theface view in Dolichodori- GOODEY,T. (1963). Soil andfreshwater nematodes (2d ed., rev. dae (but with amphids dorso-ventrally directed instead J. B. Goodey). Methuen & Co Ltd, London, XVI -1- 544 p. of lateral slits as in this latter family); iii)in Tylenchor- hynchus, the lateral sectors have completely disappeared, DE GUIRAN,G. (1967). Description de deux espèces nouvelles du genre TylenchorhynchusCobb, 1913 (Nematodr,. Tylen- while the disc and submedian sectors are fused into a chinae) accompagnée d'une cle des femelles, et précisions quadrangularstructure. The amphids remain at the sur T. mamillatus Tobar-Jimenez, 1966. Nematologica, 13 : lateral edges of this quadrangle. In a further evolution, 217-230. the labial disc and first labial annulus are completely fused together, leaving the amphid andoral openings as HOOPER,D. J. (1 978). The identification and biology ofstunt the only structures recognizable in an othenvise plain nematodes (Tylenchorhynchidae) especially thosein Wes- tefn Europe. In : Spiral and stunt nematodes,Association of structure limited by the second labial annulus (Nagelus Applied Biologists, Nematology Group, Rothamsted, En- Triversus forexample; in theamphid openings are gland, 75 p. enlarged). It isrelatively easy to proposehypotheses onthe IVANOVA,T. S. & SHAGALINA,L. M. (1983). [A new genus and evolution of characters within Belonolaimidae. It is species of nematode Hexadorus deserticola gen. n., sp. n. much more difficult to establish phylogenies of the taxa (Tylenchida, Belonolaiminae) thein deserts of Central Asia.] themselves without running the risk to classify charac- Parazitologiya 17 : 318-321. [Translationin Fortuner, 1986.1 ters rather than taxa. IVANOVA,T. S.'& SHAGALINA,L. M. (1983). [Descriptionof the Only two subfamilies are accepted here because they male of Hexadorus deserticola Ivanova & Shagalina, 1983 correspond to clearly distinct biological characteristics. (Nematoda : Belonolaiminae).] bv. Akad. Nuuk turkmen. Monophyly of these subfamilies is questionable. Moru- SSR, 1 : 72-74. luimus because of its conical tails and lemon shaped JAIRAJPURI, M. S. (1982). Some studies on Tylenchorhynchi- SEM face views, probably originated from an ancestor nae : the subgenus Bitylenchus Filipjev, 1934 with descrip- different from that of the other members of Belonolai- tion of Tylenchorhynchus (Bitylenchus) depressusn. sp. and minae with cylindroid tails and four-leaf clover SEM a key to species of Bitylenchus. Meded. Fac. LandbWetens. face view. In Telotylenchinae, at least two paths of Gent, 47 : 765-770. evolution can be recognized. One goes towards genera JAIRAJPURI,M. S. (1984). Morasimema Javed, 1984, synonym closest to Pratylenchidae and Hoplolaimidae(Anzpli?ner- of Divittus Jairajpuri, 1984. Syst. Parasitol., 6 : 256. linius and Paratrophurus); the otherfollowed a divergent JAIRAJPURI, M. S. & HUNT,D. J. (1984). The taxonomy of way towards typical Tylenchorhynchus and Merlinius Tylenchorhynchinae (Nematoda : Tylenchida) with longi- with superficial root-grazing habits. tudinal lines and ridges. Syst. Parasitol., 6 : 261-268. LOOF,P. A.A. (1956). Trophurus, anew tylenchid genus REFERENCES (Nematoda). Versl. Meded. Plziektenk. Diensr. Wageningen, 129 (1955) : 191-195. ANDERSON, V. R. (1977). Additional diagnostic characters and LOOF,P. A. A. (1958). Some remarks on the status of the relationships of Merlinius laminatus (Wu, 1969) Siddiqi, subfamily Dolichodorinae, with description of Macrotro- 1970 (Nematoda, : Merlininae). Can. J. Zool., 55 : phurus arbusticola n. g., n. sp. (Nematoda : Tylenchidae). 1923-1926. Nematologica, 3 : 301-307. CHAWLA, M.L., BHAMBURIWR,L., B. KHAN, E. & PRASAD,S. LOOF,P. A. A. (1963). A new species of Telotylenchus (Ne- K. (,1968). One new genus and seven new species of nema- matoda : Tylenchida). Nenzatologica, 9 : 76-80. todes from India. Labdev J. Sci. Technol,, 6B : 86-100. LOOF,P. A. A.(1987). Tylenchorhynchidae Eliava, 1964 a CHITWOOD,B. G.(1950). An outlineclassification of the junior synonym of Telotylenchidae Siddiqi, 1960 (Nema- nematodes. In : Chitwood, B. G. & Chitwood, M. B. (Eds). roda : Tylenchoidea). Revue Nématol., 10 : 123-124. An introduction to nematology.I. Anatomy. Baltimore, USA, Luc, M., MAGGENTI, A. R., FORTUNER,R., RASKI, D. J. & Monumental Printing Co : 12-27. GERAERT,E. (1987). A reappraisal of Tylenchina (Nemata). FILIPJEV,1. N. (1934). [Harnzfil and usefil nematodes rural 1. For a new approachto the taxonomyof Tylenchina. Revue in Ne'nzatoZ., : 127-134. econonty.] Moscow, Leningrad, USSR, 440 p. [Partial trans- 10 . lationin Fortuner, 1986.1 MERNY, G. (1964).Un nouveau Tylenchida d'Afrique tropi-

Revue Nématol. 10 (2) : 183-202 (1987) 20 1 R. Fortuner & M. Luc

cale : Tetylenchusannulatus nsp. Nematologica, 10 : classification of the families Dolichodoridae and Belonolai- 425-430. rnidae n. rank. Proc. helmintk. Soc. Wash., 37 : 68-77. MULK,M. M. & JAIRAJPURI,M. S. (1974). Proposa1 of a new SIDDIQI,M. R. (1971a). Structure of the oesophagus in the genus Dolichorhynchus and a new species Dolichorhynchus classification of the superfamily Tylenchoidea (Nematoda). nigericus (Nematoda : Dolichodoridae). Indian J. Nématol., Indian J. Nematol., 1 : 25-43. 2 : 15-18. SIDDIQI,M. R. (1971b). Onthe plant-parasitic nematode MULK, M. M.& SIDDIQI, M.R. (1982). Three new species of genera Histotylenchus and Telotylenchoides gen. n. (Teloty- hoplolaimidnematodes from South America. Indian J. lenchinae), with observations on the genus Paratrophurzcs Nematoi., 12 : 124-131. Arias (Trophurinae). Nematologica, 17 : 190-200. POWERS,T. O., BALDWIN,J. G. & BELL,A. H. (1983). SIDDIQI, M.R. (1976). New plant nematode generaPlesiodorus Taxonornic limitsof the genus Nagelus (Thorne and Malek, (Dolichodorinae), Meiodonu (Meiodorinaesub-fam. n.), 1968) Siddiqi, 1979 witha description of Nagelus borealis n. Amplimerlinizu (Merliniinae) andGracilancea (Tylodoridae sp. from Alaska J. Nématol., 15 : 582-593. grad. n.). Nematologica, 22 : 390-416. SAMSOEN,L. & GERAERT,E. (1975). La faune nkmatologique SIDDIQI,M. R. (1978). Telotylenchus obtusussp. n. andHistoty- des rizières du Cameroun. 1. Ordre des Tylenchides. Revue lenchus sudanensis sp. n. (Nematoda : Tylenchida : Teloty- Zool. Bot. afr., 89 : 536-554. lenchinae). Nematol. medit., 5 (1977) : 281-289. SAUER,M. R. (1985). A scanning electron microscope study of SIDDIQI,M. R. (1979).Taxonomy of the plant nematode plant and soi1 nematodes. C.S.I.R.O., Australia, 64 p. subfamily Merliniinae Siddiqi, 1970, with descriptions of SAUER, M.R., BRZESIZI,M. W. & CHAPMAN,R. N. (1980). Merlinius processus n. sp., M. loofin. sp. andAmplimerlinizrs Observationson the morphology of Belonolaiminae. Ne- globigenls n. sp. from Europe. Syst. Parasitol., 1 : 43-59. matol. medit. 8 : 121-129. SIDDIQI,M. R. (1986). Tylenchidaparasites of plantsand SEINHORST, J. W. (1971). On the generaTrichotylenchus and insects. CommonwealthAgricultural Bureaux, Slough, Telotylenchus. Nematologica, 17 : 413-416. Great Britain, IX + 645 p. SEINHORST,J. W. (1971). The structure of the,glandular part TARJAN,A. C. (1973). A synopsis of the genera and species in of theesophagus of Tylenchidae. Nematologica, 17 : Tylenchorhynchinae (Tylenchoidea, Nematoda). Proc. hel- 431-443. minth. Soc. Wash., 40 : 123-144. SHER,S. A. (1974~).The classification of Tetylenchus Filipjev, THORNE,G. (1949). On the classification of the Tylenchida, 1936, Leipotylenchus n. gen. (Leipotylenchinae n. subf.) and< neworder (Nematoda : Phasmidia). Proc. helmintk. Soc. Triversus n. gen. (Nematoda: Tylenchoidea). Nematologica, IVash., 16 : 37-73. 19 (1973) : 318-325. THORNE,G. & MALEK,R. B. (1968).Nematodes of the SHER,S. A. (1974b). Sauertylenchtu labiodiscus n. gen., n. sp. Northern Great Plains. Part 1. Tylenchida (Nemata: Secer- from Australia (Nematoda: Tylenchorhynchinae). J. Nema- nentea). S. Dakota Agn". Exp. Stn Techn. Bull., 31 : 11 1 p. toi., 6 : 37-40. VOVLAS,N. (1983).Observations onthe morphology and SHER,S. A. & BELL, A. H. (1975). Scanning electron micrc- histopathologyof Quinisulcizcs action corn. Revue Nematol., graphs of the anterior region of some species of Tylen- 6 : 79-83. choidea (Tylenchida : Nematoda). J. Nematol., 7 : 69-83. WHITEHEAD, G.A. (1960). Trichotylenchus falciformisn. g., n. SIDDIQI,M. R. (1960). Telotylenchus, a new nematode genus sp. (Belonolaiminae n. subfam. : Tylenchida Thorne, 1949) fromNorth India (Tylenchida : Telotylenchinaen. an associate of grass roots (Hyparrhenia sp.) in Southern sub-fam.). Nernatologica, 5 : 73-77. Tanganika. Nematologica, 4 (1959) : 279-285. SIDDIQI,M. R. (1970). On the plant-parasitic nematode genera WILLEY,A. (1901). Dolichorhynchus indicus, n. g., n. sp. a new Merlinius gen. n.and Tylenchorhynchus Cobband the acraniate. Q. 3. microsc. Sci., 44 : 269-271. Accepté pour publication le 10 mars 1987.

202 Revue Nématol. 10 (2) : 183-202 (1987)