Morphometrical Variability in Helicotylenchus Steiner, 1945. 4 : Study of Field Populations of H

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1984

Morphometrical Variability in Helicotylenchus Steiner, 1945. 4 : Study of Field Populations of H. pseudorobustus and Related Species

Renaud Fortuner California Department of Food and Agriculture

Armand R. Maggenti University of California - Davis

Laurel M. Whittaker California Department of Food and Agriculture

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Fortuner, Renaud; Maggenti, Armand R.; and Whittaker, Laurel M., "Morphometrical Variability in Helicotylenchus Steiner, 1945. 4 : Study of Field Populations of H. pseudorobustus and Related Species" (1984). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 110. https://digitalcommons.unl.edu/parasitologyfacpubs/110

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Morphometrical variability in Helicotylenclzus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus and related species

Renaud FORTUNER*- Armand R. MAGGENTI** and Laurel M. WHITTAKER* * CaliforniaDepartment of Foodand Agriculture, Nematology Lab, Room 340, 1220 N Street, Sacramento,Ca 95814, U.S.A. * * Department of Nematology, University of California, Dauis, Ca 95616, U.S.A.

SUMMARY Multivariateanalyses were made on 28 populations of Helicotylenchuspseudorobustus, eleven populations of H. dihystera, and type populations of H. microlobus, H. bradys, H. phalerus, 13. egyptiensis, and H. africanus. Some morphological differences wereobserved among the populations of H.pseudorobustus, mostlybetwecn samples from North America and from Western Europe. The differences were most apparent in the pattern of junction of the inner lines of lateral field on tail, the position of the phasmids and of the dorsal gland opening. However, these characters Vary within some of the populations studied. Most populations originally identified as H. pseudorobusfus were conspecific with the type population.H. microlobus was confirmed,as synonymof H. pseudorobustus; H. bradys and H. phalerus were proposed as new synonyms of this species. A few samples originally proposed as H. pseudorobustus were in fact closer to H. dihystera or may represent other, unidentified species. Paratypes of H. egyptiensis and H. africanus were described.

RÉSUMÉ Variabilité morphomitrique chez Helicotylenchus Steiner, 1945. 4 : Etude de populations naturelles de H. pseudorobustus et d’espèces voisines Des analyses multifactorielles furent effectuées sur 28 populations de Helicotylenchus pseudorobustus, onze populations de W. dihystera, et des populations types de H. microlobus, H. bradys, H. phalerus, H. egyptiensis et H. africanus. Quelques différences morphologiques furent observées entre les populations de H. pseudorobustus, principa- lement entre les échantillons provenant d’Amérique du Nord et d’Europe Occidentale. Les différences concernent surtout l’aspect du raccordement des lignes internes du champ latéral sur la queue, la position des phasmides et celle du débouché de la glande oesophagienne dorsale. Cependant ces caracteres varient à l’intérieur de certaines des populations étudiées. La plupart des populations identifiées à l’origine comme H. pseudorobustus sont bien conspécifiques de la population type. H. microlobus est confirmé comme synonyme de H. pseudorobustus; H. bradys et H. phalerus sont proposés comme nouveaux synonymes de cette espece. Quelques-unes des populations originel- lement proposées commeH. pseudorobustus sont en faitplus proches de H. dihystera ou peuvent appartenir à d’autres especes, qui n’ont pas étéidentifiées. Les paratypes de H. egyptiensis et de H. africanus inclus dans la présente étude sont décrits.

Thevariability of thetaxonomic characters has thenature of thehost-plant or thegeographical been studied in Helicotylenchus dihystera (Cobb,1893) origin of the sample. Sher, 1961 and published in three previous articles : It is tempting to considerthese observations as Fortuner (1979)considered thevariability in the valid for the entire genus Helicotylenclzus, and to use progeny of a single parthenogenetic female ; Fortuner themto decidewhich characteristics are constant and Quénéhervé (1980) observedthe additional varia- enough within a given species to be used as differen- bility in such a progeny when cultivated under sev- tiating criteria in taxonomic studies. However,it was eral different host-plants ; and Fortuner, Merny and consideredbest tomake similar observations on Roux (1981) reported the variability in field popula- anotherspecies to ascertain that the conclusions tions of a species of Helicotylerzchus which was iden- obtained from H. dihystera were also valid for other tified as H. dihystera as aresult of multivariate members of the genus Helicotylenchus. analyses. H. pseudorobustus (Steiner,1914) Golden, 1956 Thesestudies show thatmany characteristics in wasselected for thepresent study. It is,with H. H. dihystera Vary under external conditions, such as multicinctus and after H. dihystera, the second most

Revue Nèmatol. 7 (2) : 121-135 (1984) 121 R. Fortuner, A.R. Maggenti & L.M. Whittaker reported species of Helicotylenchus inthe world Material and methods literature. Since Sher (1966) redescribed H. pseudorobustus fromtopotypes, several populations of this Forty-threesamples, of one to thirtyspecimens specjes have been described from various countries : each, representing field populations identified as H. SouthDakota (Thorne & Malek,1968), Zaire (Ali pseudorobustus, werereceived fromtwenty-five Geraert & Coomans, 1973), Canada (Anderson, 1974), countries or States (Tab. 1).Paratypes of the related Turkey (Geraert, Zepp & Borazanci, 1975), Malaysia species H. microlobus, H. phalerus and H. bradys were (Sauer & Winoto, 1975), SouthAfrica (Van den Berg included in the study. The eleven field populations & Heyns, 1975, Italy (Mancini & Moretti, 1976) and of H. dihystera studied in Fortuner, Merny & Roux FijiIslands (Van den Berg & Kirby, 1979).These 1981,and paratypes of H. africanus (Micoletzky, various populat>ionsof H. pseudorobustus show great 1916) Andrassy, 1958 and of H. egyptiensis Tarjan, variabilityin several characteristics : theaverage 1964 were also included in the analyses for purposes length of the stylet, which was the most constant of comparison.The specimens used forthe study characteristic in H. dihystera, varies from 23.5 (Van were returned ta their respective owners except for den Berg & Heyns, 1975) to 30 Pm (Thorne & Malek, the specimensfrom Germany, Portugal, Iowa (in 1968) ; thetail is generallydescribed with a large part), California, St Lucia, Nigeria (inpart), and ventralprojection, but some illustrations show a NewZealand which weredeposited in theCDFA rather small process (i.e., Fig. 36 of Van den Berg & Permanent Slide Reference Collection (Nematology). Iiirby, 1979 ; Fig. 3 A of Ali, Geraert & Coomans, 396 specimens of nematodes from the H. Pseudo- 1973 ; Fig. 1 O of Siddiqi, 1972) ; this projection is robustus material and 38 specimens belonging to the often described as annulated but is not annulated in other species (Tab. 1) wereobserved under a Leitz some illustrations (Fig. 1 P of Sher, 1966 ; Fig. 25 D Ortholux II microscopewith an interference con- of Thorne & Malek, 1968 ; Fig. 3 Dl E of Ali, Geraert trast device of Nomarsky, at 450 x and 1000 x & Coomans, 1973) ; the phasmids are observed from magnifications. Drawings were made using a camera two to seven annules anterior to the anus level by lucida or a drawing tube at900 x (total body length Sher (1966), but from four annules posterior to eleven and position of vulva) and 2000 x (al1 other obser- annules anterior to the anus level by Van den Berg vat>ions). and Heyns (1975) ; the fusion of the inner linesof the Themeasurements of the eleven populations of lateral field is generally not described, it is shown as H. dihystera previously recorded by Fortuner, Merny U-shaped in Sher (1966), but other shapes occur in & Roux, (1981), were addedta the gathered data and Siddiqi (1972, Fig. 1 O-P), Ali, Geraert & Coomans included in the analyses. For every specimen, fifteen (1973, Fig. 3 E) andAnderson (1974, Fig. 6 B, C, E). quantitative characters were recorded : These variations may be interpreted as the result of - LON : body length a greater intraspecific variability, or may be seen as - STY : stylet length the proof that there exist several species within H. - STA : length of anterior part of stylet pseudorobustus. - DG0 : distance betweendorsal gland opening As a consequence of this great variability, it was and stylet base diffkulttodifferentiate H. pseudorobustus from - OVI : distance head to esophago-intestinal severalother nominal species of Helicotylenchus : junction - OGO : distance head to end of esophageal glands H. bradys Thorne & Malek,1968, H. microlobus - PEX : distance head to excretory pore Golden, 1956, H. phalerus Anderson, 1974, and also - QUE : tail length H. dihystera. Thelatter specieswas differentiated - DAN : body diameter at anus from H. pseudorobustus byFortuner, Merny and - DIV : distance head to vulva Roux (1981)because of a shorterstylet, a higher - DVU : body diameter at vulva coefficient V, anddifferently shaped fusion of the - ANQ : number of tail annules innerlines of thelateral field, but the taxonomic - ANP : number of annules from phasmid t.o anus position of the other nominal species remains to be level clarified. -- ANW : widt.h of one body annule PRO : length of terminal process on tail The study of field populations tentatively ident- - ified inthe literature as H. pseudorobustus was Body length and distance from head to vulva were initiated to : i) verify their identity ; ii) record the replaced by their ratio RAV = DTV x 100 /LON. intraspecificvariability of H. pseudorobustus and Eleven qualitfative characters were also observed : include it in a redescription of the species ; iii) gather - HAB : habitus additionalinformation on thevariability of taxo- - LIP : shape of lip region nomic characters ; and iv) clarify the status of some - DIS : presence of a labial disc related species. - ANL : lip annulation

122 Revue Nématol. 7 (2) :121-135 (1984) Morphometrical uariability in Helicotylenchus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus

- ICBT : shape of stylet knobs iii) only the samples from Nigeria (Cl, C2), Natal - AR0 : presence of transverse lines on lateral fields (Dl, D2), Cape province (Da. D4, DG) and Transvaal - INC : shape of the junction of the inner lines of (D7) are well separated from the other samplesof H. the lateral field pseudorobustus, and are more related to the samples - TSH : shape of the tail of H.dihystera. Samples from Zaire St.Lucia - ANT : shape of the dorsal tail annules (C4), - ANV : shape of the ventral tail annules (F2),Malaysia (Hl),Korea (H4),Cape Province (D5), - APR : annulation of the terminal process Turkey (BI), Florida (Fl),and California (Gl) are at the edge of the Cloud of points representing the other Data analysisconsisted of stepwisediscriminant samples of H. pseudorobustus ; analysis (Jennrick & Sampson, 1979) for the quanti- iv) H. microlobus, H. bradys, H. phalerus, and H. tative characters. Only 31 samples were used for the egyptiensis are well inside the Cloud of samples of H. definition of thecanonical variables : seventeen pseudorobustus. H. afrîcanus is fardistant from al1 samples of H. pseudorobustus with ten or more speci- other samples ; mens per sample ; six samples of H. dihystera ; and u) the eleven samples of H. dihystera (bottom left six samples of the other species. Then, the position shadedarea) are well separatedfrom the Cloudof of the restof samples was calculated in relationto the points representing typical samples of H. pseudoro- axes so defined. Mahalanobisdistances were cal- bustus. The groupings observed in Fortuner, Merny culated for each pair of samples. A correspondence andRoux (1981) are again recognized here : A-C, analysis(Benzecri & Renzecri,1980) was made for D-E, B-K-J, and F-H-G-1 ; selected quantitative and qualitative characters. The vi) the position of H. pseudorobustus in relation to quantitativecharacters were recoded into classes, axes 1 and 2 is related to the higher valuesof lengths generallyfour classes percharacter, and several of stylet, tail, and tail process, while the position of correspondenceanalyses including both kinds of H. dihystera depends on greater ratio V and distance characters were performed. from the dorsal gland opening to the stylet.

Results ANALYSISOF THE QUALITATIVE AND QUANTITATIVE CHARACTERS ANALYSISOF THE QUANTITATIVE CHARACTERS A first analysis was done with al1 the variables in The positions of the 52 samples (Tab. 1) are shown al1 51 samples, bra 1 and bra 2 were grouped into a onthe graph of Fig. 1, inrelation to axes 1 and single sample (brad), butfailed to differentiate groups 2 which proved to be the more effective for discrimi- of samples.Several other analyses were done with nating between the samples. For every sample, the reduced lists of variables. Of the eleven qualitative Mahalanobis distance to the nearest sample was noted characters recorded, four (HAB, LIP, DIS, and ANL) on the graph of Fig. 1 as a solid line if there was no were discardedbecause they presented the same significantdifference (1% level)between the two aspect in every specimen in al1 the samples except samples, and as a dotted line if there was a differ- afriand egyp. Four other characi.ers (KBT, ANT, ence. ANV, and APR)were discarded because of their vari- Axis 1 is positivelycorrelated mostly with variability, greater within sample than between samples. ablesOGO, PRO,STY, and QUE. Sampleswith The quantitative characters LON (body length) and highervalues in these variables will belocated QUE (tail length) were introduced as the ratio QUL= towards the right of the graph. QUE /LON. Eventually, a good separation between Axis 2 is negatively correlated mostly with vari- the H. dihystera samples and some of the H. pseudo- ables DGO, QUE, RAV, OGO (samples with higher robustus samples was observed when using only five values for these variables to the bottom) and posi- quantitativecharacters : DTL,STY, QUL, ANQ, tively correlated mostly with STA and DAN (higher PRO, and two qualitative characters: AR0 and INC. values on top of graph). AR0 is the presence (1) or the absence (O) of trans- 66.7% of the specimenswere correctly classified verse striae in the lateral field on the body and /or into their owngroup by the analysis. Fig.1 shows that : tail. INC is the junction patternof the two inner lines i) the topotype sample of H. pseudorobustus (Al) is of the lateral field on the tail. This pattern is typi- closest to some of theother Europeans samples : cally y and v shaped in H. dilzystera (see. Fig. 4 of Germany (A2), Italy(A3), and France (A4) ; Fortuner, Merny & Roux, 1981). In the samples of ii) however,there is noseparation between : a) H. pseudorobustus other patterns were aIso observed these four samples ; and b) mostof the samples which (u, F, m, v : see description and Fig. 4 below). The y were identified a priori as H. pseudorobustus (upper andv patterns are here coded : INC 1 ; the other rightshaded area in Fig. 1) ; . patterns are coded : INC 2.

Revue Nématol. 7 (2) :121-135 (2984) 123 Table 1 Description of the samples studied

Sample n Origin Observations Code ??

1. H. pseudoro bustus AI 20 MOSS, Altmatt, Switzerland Topotypes-Sher (1966) A2 24 Pine, Hünxe, Germany A3 11 Chestnut, Torino, Italy Mancini & Moretti (1976) A4 28 Apple, Bergerac, France A5 17 Tomato, Carpentras, France A6 5 Leek and Millet, Soure, Portugal B1 1 Turkey Geraert et aZ,. (1975) B2 15 Kikuyu Grass, Israel Sher (1966) B3 3 Orange, Shahsarar, Iran Cl 14 Citrus, Ibadan, Nigeria Sher (1966) - tentative identification C-2 18 Plantain, Ibadan, Nigeria Sent by Caveness c3 8 Sugarcane, Kumasi, Ghana Sher (1966) - tentative identification c4 2 Tobacco, Nioka, Zaire Ali et al. (1973) Dl 2 Fern, Harding, Natal Van den Berg & Heyns (1975) D2 1 Rubus sp., Ixopo, Natal Van den Berg & Heyns (1975) D3 1 Peach, Upington, Cape Province Van den Berg & Heyns (1975) D4 1 Cotton, Longlands, Cape Province Van den Berg & Heyns (1975) D5 1 Grass, Kokstad, Cape Province Van den Berg & Heyns (1975) D6 9 Cape Province Van den Berg & Heyns (1975) D7 1 Agave, Potgietersrus, Transvaal Van den Berg & Heyns (1975) El 27 Blue Grass, West Point, New York E2 7 Blue Grass, College Park & Beltsville, Maryland E3 25 Corn, Near LaFayette, Indiana E4 17 Corn, Boone County, Iowa F1 16 Homestead, Florida F2 30 Itchgrass, Sulfur Springs, St. Lucia F3 4 Sugarcane, Venezuela Gl 30 Philodendron, San Francisco, California II 1 11 Sweet Potato, Segamat & Labis, Malaysia Sauer & Winoto (1975) H2 6 Pine, Jung Pyung, Korea H3 10 Cedar, Kyungpook, Korea H4 2 Hardy orange, Bosung, Korea H5 3 Persimmon, Taegu, Korea H6 2 Amorpha, Kyungpook, Korea Il 24 Pasture, Kaitoke, New Zealand 2. Paratypes of related species micr 5 Poa pratensis, Madison, Wisconsin Paratypes H. microlobus bradl 7 Soybean, near Viborg, South Dakota Paratypes H. bradys brad2 7 brad2 Soybean, near Ames, Iowa Population H. bradys P 4 Sugarcane, 4 WabourP el Barabra,Egypt Paratypes H. egyptiensis phal 9 Grass,Lethbridge, 9 phal Atta, Canada Paratypes H. phalerus afri 6 VictoriaRhodesiaNorthFalls, 6 afri Topotypes H. africanus 3. Populations of H. dihystera (see Fortuner et al., 1981) HdA 19 Cocoa, Madagascar Pop. A in Fortuner et al. (1981) HdB 20 Banana, Canary Island Pop. B in Fortuner et al. (1981) HdC 17 Forest, Senegal Pop. C in Fortuner et al. (1981) HdD 16 Millet, Senegal Pop. D in Fortuner et al. (1981) HdE 17 Rice, Senegal Pop. E in Fortuner et al. (1981) HdF 19 Peanut, Gambia Pop. P in Fortuner et al. (1981) HdG 17 Corn, Gambia Pop. G in Fortuner et al. (1981) HdH 18 Tobacco, Senegal Pop. H in Fortuner et al. (1981) HdI 16 Peanut, Senegal Pop. 1 in Fortuner et al. (1981) HdJ 16 Papaya, Mauretania Pop. J in Fortuner et al. (1981) H dK 15 HdK Potato, California Pop. Kin Fortuner et al. (1981)

124 Nématol. Revue 7 (2) : 121-135 (1984) Morphometrical variability in Helicotylenchus Steiner, 1945. 4 : Stucly of field populations of H. pseudorobustus

Fig. 1. Stepwise discriminant analysis. Position of 52 samples (Al, etc. : see Tab. 1) in relation to axes 1 and 2, with indication of the lowest distances in solid lines (no significant difference)or dotted lines (difference significant at 1% level).

Revue Nématol. 7 (2) : 121-135 (1984) 125 OUL3 D4 oH2

PR04 oHdK 0g1 0f2 HdEo *Hdl -1 oH4 .'. obrad .WYP ANO~ oH6 oE4 ,Hd F oHdD 082 phalo *FI qly~ AN04

0 B1 STYi 083 D$~~~, mvoE2 oD5 5ty3 H34 oD3 O Il SXIS I - .A6 ANQ2

oHdA af ri.

ANQ~ 0 Cl QUL2 OHdJ .C2 0c4 *Dl 1nc2

AR01 0 Al 0HdB

5TY4

PRO1

0d7

Fig. 2. Correspondance analysis. Position of 51 samples (Al, etc. : see Tab. 1) in relation to axes 1 and 2, with indication of the modalities of quantitative (DTL, STY, QUL, ANQ, and PRO) and qualitative (AR0 and INC) criteria.

126 Revue Némaiol. 7 (2) :121-135 (1984) Morphometrical variability in Helicotylenchus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus

Tai1 shape (TSH)was also considered for the analy- H. pseudorobustus sarnplesare placed between the sis but this character is redundant with PRO : tails two extremes but closer to the European H. pseudo- rounded or with dorsal and ventral sides joining at a robustus than to H. dihystera. Only samples Cl and straight angle have no ventral projection: PRO = O. C2 are among the H. dihystera samples. The samples Tailswith a ventralprojection have PRO = 1 of H. microlobus, H. bradys, and H. phalerus are not to 5 Pm. It was found unnecessary to use both TSH differentiatedfrom the non-European H. pseudo- and PRO. PRO was preferred because, it discrimi- robustus. nates between short and long projections. Fig. 2 shows the position of 51 samples in relation DISCUSSION to axes 1 and 2, found to be the most discriminant to differentiate the samples. Axis 1 is positively corre- Identity of the samples studied latedwith INC 2,and negatively correlated with Theanalyses separated three groups of samples PRO 1 and STY 1. Axis 2 isnegatively correlated among the samples studied. with QUL 1 andPRO 1. - Thegroup “pseudorobustus” : Thisgroup is Fig. 3 shows a classification tree(dendrogram) organizedaround thetopotype sample Al. It in- madebetween some samples chosen among those cludes most European samples (A2,A3, A4), samples with the highest numberof specimens. The topotypes C3 and C4 fromAfrica, andsample Il from New (Al) andsome samples from Europe (A2,A3, A4) are Zealand. It is characterized by stylet length 26-27pm, grouped because of the characters INC 2 and STY 4. ratio V = 61 %, L = 700-750 Km, DG0 at 9 Km, At the oppositeend thedendrogram, H. dihystera phasmids seven to eight annules above anus, inner samples are characterized by INC 1 and STY 1. Other lines of lateral field joining mostly in u pattern (but

200

* B

100

10 1 Ir O Al A2 A3 A4 F2 FI egyp G1 A5 micr El E3 E4 phalbrad 62 HdA Cl HdJ G2 HdlHdK HdF HdH. HdC

Fig. 3. Classification tree (dendrogram) OP some characteristic samples, with indication of the distances between constellations.

R evue Nhnatol. Revue 7 (2) : 121-135 (1984) 127 R. Forluner, A.R. Maggenti CE L.M. Whittaker somey patterns are present), and areolations on In H. dihystera it was observed (Fortuner, 1979 ; body /tail in some specimens. The tail always ends Fortuner & Quénéhervé,1980 ; Fortuner,Merny & in a ventral projection of variable length. Roux, 1981) that the lines join toget.her in a pattern - Thegroup “microlobus” : Thisgroup includes which looks like a y ,or more rarely like a v. In they theparatypes of H. microlobus, H. bradys, H. pattern, the leg of.the y canreach the outer lines or phalerus, and theNorth American samples of H. stop short of them. pseudorobustus El, E2, E3, and E4. It differs from Inthe topotypes of H. pseudorobustus, several the first group mostly in the phasmids being closer different patterns were observed. Generally the inner to theanus (four annules), DG0 farther from the lines join together without a sharp angle, but in a stylet (11 Pm), and the junction of theinner lines rounded pattern resembling the letter u (Fig. 4,H,I). always in the y pattern. Sometimes there is a short leg posterior to the u, Some samples of H. pseudorobustus are intermedi- and the pattern resembles‘the greek letter p (Fig. ate between thetwo groups f A5from France is 4, J) or a diapason (Fig. 4, K). This leg can reach the closer to the group “microlobus” but has phasmids outer lines (Fig. 4, RI) or stop short of them. In one at sixannules above anus ; B3 from Iranand F1 specimen the u pattern is at the level of the outer from Florida arecloser ta the group,“pseudorobustus” lines and the end of the lateral field lookslike an but have phasmids at 4 annules. Gl from California upside-down m with an extra leg (Fig. 4, L). and F3 from Venezuela probably belong to the group Fortuner, Merny and Roux (1981) proposed to use “pseudorobustus” but.have a vulva slightly more these junction patterns to differentiate H. dihystera posterior(V = 62.2and 62.4%). Because of the with y and v patterns, from H. pseudorobustus with generalvariability of thesecharacters, it was con- u, p, or mpatterns. However, in every sample of sidered best not to propose the group LLmicrolobus” H. pseudorobustus, includingthe topotypes, some as a valid species, but to accept it as a geographical specimens present the y/v pattern (Fig. 4, N, O). In variant of H. pseudorobustus, characterized by the North American samples El to E4,al1 the speci: morphologicaldifferences too slight to warrant the mens have a y /v pattern. The charact.er can be used creation of a subspecies. to differentiate species but, as is generally the case for taxonomic criteria in Helicotylenchus, it will not -The samples of H. dihystera : Thesesamples permit a clear dichotomy of the genus. Some species, form a third group clearly separated from the first like H. dihystera have a y /v pattern, other species, twoby shorter stylet, 24-26.5Pm, moreposterior like H. paracanalis (seeFortuner, Merny & Roux, vulva,62.5-65%, often shorter body, 600-750Pm, 1981) have a u/m pattern, but many species, like H. DG0 sometimesmore posterior, 10-15 Pm. The pseudorobustus, include individuals with one or the junction of the inner linesof the lateralfield is always ot,her pattern. of the y pattern. The tail may or may not have a ventralprojection. The samples Cl and C2 from - Tai1 shape Nigeria belong to this group. Al1 specimens of H. pseudorobustus, withthe Samples A6 fromPortugal and B2 from Israel exception of some individuals in samples A6 andB2, include some specimens without ventral tail projec- have a ventraltail projection. The length of this tion. However, al1 other characters correspond to the projectionwas very variable, from 1 to 5 Pm. description of B. pseudorobustus andthey can be Thischaracter has been used inseveral identifica- accepted as membersof this species. tion keys (Sher, 1966 ; Siddiqi, 1972), but its varia- Sample F2 from St. Lucia has some characteristics bilityin H. pseudorobustus and H. dikystera casts of H. pseudorobustus (stylet27 Pm long,tail with serious doubt on the validity of the species so differ- long projection, inner linesof the lateralfield of the u entiated. pattern),and somecharacteristics of H. dikystera (V = 63.4%, DG0 = 13 Pm).This and its longer Descriptions of the species tail (20 Pm) and esophageal glands (165 Pm) explain the position of sample F2 in Fig. 1. It may belong to a different unidentified species. Helicotylenchus pseudorobustus Samples from Turkey (Bl), Malaysia (Hl), Korea (Steiner, 1914) Golden, 1956 (H2 to H6) and SouthAfrica (Dl toD7) aretno small (Fig. 4) ta be identified. Syn. = H. microlobus Perry,in Perry, Darling Infra-specificuariability of somecharaciers & Thorne, 1959 -The junction of the inner lines of the lateral H. bradys Thorne & Malek, 1968 (new syn.) field. H. phalerus Anderson, 1974 (new syn.)

128 Revue Nèmatol. 7 (2) : 121-135 (1984) Morphometrical variability in Helicotylenchus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus

Description * Thestandard deviation of the mean is given between parentheses for every mean. The range in the Fernales : body spiral, body annules 1-2.5 pm wide sample is given. The range in the population cari at mid-body. Lip region hemispherical, with four to be estimated for 95% of the individu& as mean -+ five annules,sometimes difficult to see ; labialdisc 2 s ; or for 99% of the individuals as mean f 3 S. not visible in transverse view. Basal ring of cephalic

Fig. 4. Helicotylenchus pseudorobustus, topotypes (Al).A : whole fernale ; B-D : spermathecae ; E and F : heads ; G : anterior end ; H-O : tails.

Revue Nématol. 7 (2) : 121-135 (1984) 129 R. Fortuner, A.R. Maggenti & L.M. Whittaker

framework 1-3 pm wide, anterior cephalid not seen ; to D7,F2, Hl to H6 whichmay belong to other posterior cephalid seen in five specimens, 15-16 pm species. A species is the sum of al1 the populations from anterior end. Stylet knobs flattened in sixteen whichbelong to it. Wecan consider the accepted specimens, rarely rounded (Fig. 4E) or indented (Fig. samples of H. pseudorobustus as successive draws 4F). Excretory pore at. about the level of esophago- taken at random from the ensemble of populations intestinaljunction, sometimes slightly anterior or constitutingthe species. The mean of thesample posterior to it. Hemizonid often diffkultto see ; when means for a measurement is an estimate of the value seen, level with to two annules anterior to, excretory of this measurement for the species. The means of pore.Hemizonion not seen.Fasciculi absent. Sper- the different measurements and t>heir standard errors matheca empty, offset (Fig. 4 B, C) but sometimes were calculated(in pm) from the sample with appears in line (Fig. 4 D) with the genital tract. Lat- n > 10 : (Alto A5,B2, El,E3, E4, FI, G1, eral field 5-7 pm wide, with transverse lines in the and Il). esophagealregion (al1 specimens) andoften in the Body = 715 (38.5) ; stylet = 26.9 (0.73) ; eso- tail region (thirteen specimens) ; one specimen with phagus = 116 (6) ; esophagealglands = 146 (8) ; a few lines in the vulval region ; longitudinal inner dorsal gland opening = 10.4 (1.3) ; excretory pore = lines join together on tail in a u-shaped pattern ; in 111 (5) ; body diameter = 26.4 (1.9), tail length = fifteen specimens the u junction isfollowed by a short 17.5 (1.1) ; anal body diameter = 15.2 (0.8). Ratios : line bissecting the outer bandof the lateralfield as in a = 27.4 (2.1) ; c = 41.5 (3.7) ; c’ ~1.2(0.1) ; m = the Greek letter “p” ; one of these specimens pres- 48 (1.1) ; V = 61.1% (0.8). ents a m-shaped pattern on one sideof the body (Fig. 4 L) and a u pattern on the other side ; two other The description is identicalto thatof the topotypes specimenspresent thetypical u shape(,Fig. 4 H) except for the following characters : t2he first labial without an additionalline. In the last three specimens, annule is sometimes elevated above the general lip thejunction israther v-shaped (Fig. 4 N,O) but outline (E2 : Fig. 5P ; E3 ; E4) ; the lateral field is different from the long tailedy pattern of H. dihystera mostoften not areolated on body /tail or some (Fig. 4 in Fortuner Merny & ROUX,1981). Phasmids transverse striae are present in only a few specimens are three to eleven annules anterior to anus (mean : (A2 ; A4 : Fig. 5C ; E2 : Fig. 5s ; E3 ; E4 : Fig. 555 ; 7.8, s = 1.9), easy to see or indistinct, in the center F3 ; Gl : Fig. 50 ; Il : Fig.51). In somesamples of the lateral field or closer to the ventral line. Tail (A2 ; A4 : Fig. 5 GG-JJ ; etc.), al1 the specimens with seven to eleven annules (mean : 9.1 , s = 1.2), possess au pattern ; inother samples (A5 : Fig. with or withouta nonannulated ventral section ; 5E-H;A6;Bl;B2;El;E2:Fig.5R,S; E3;E4: dorsal terminal tail annules smaller than the other Fig. 5 GG-JJ ; etc.), al1 the specimenspossess a y tail annules, rarelyof the samesize. Tail more curved pattern ; and in the restof the samples (A3; F1 ; G1 : dorsally with a rounded terminal projection, 1-4 pm Fig. 5 L-O ; II : Fig. 5 I-K ; etc.) both patterns are long (mean : 2.2 Pm), annulated in seventeen speci- present. The tail shape is always typicalof H.pseudo- mens. robustus with a long projection, but the projection is more pointed in some specimens of A3 ; F1 ; Il : Males : unknown. Fig. 5 1. The relative size of the tail annules and the Discussion presence of a non-annulated ventral section at the tailend is extremely variable within each sample. The present observations and measurements gen- California (G1 : Fig. 5 L-O) specimensoften have erally agree with the descriptionof Sher (1966) except irregular mucros at theend of the projection. Mucros for a slightly shorter stylet. The range in 95% of the were also seen in some individuals of A4 (Fig. 5 D) populationcan be estimated as 27.1 f 2 x 0.6 = and A5 (Fig.5 F). 25.9-28.3 pm against 26-30 pm inSher, 1966. The bodyis always spiral (“usually in spiral shape” according to Sher) ; the stylet knobs may be rarely DIAGNOSIS rounded (“flattened or slightly indented anteriorly” -Sher) ; thetail projection is sometimes short Helicolenchus with spiral body, hemispherical lips, (“pronouncedventral projection”-Sher) ; and is stylet of about 27 pm (mean values : 25.5-28 km), always terminally rounded (“usually hemispherical” mediumbody length (mean values : 650-775 Pm)> -Sher). vulva not too far posterior (meanV values : 59-62%), phasmids anterior to anus, inner lines of the lateral field joining on tail in variable patterns, tail about as GENERALVARIABILITY OF THE SPECIES (Fig. 5) long as wide, more curved dorsally and with rounded Thesamples Al to Il (Tab.1)are considered to mediumlength projection, no males and empty belong to H. pseudorobustus excepted B1, Cl, C2, Dl spermatheca.

. 130 Revue Nématol. 7 (2) : 121-135 (1984) Morphometrical variability in Helicotylenchus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus

SYNONYM SPECIES ments of H. pseudorobustus. H. bradys is herepro- posed as a juniorsynonym of H. pseudorobustus. Helicotylenchus microlobus Perry, in Perry, Darling & Thorne 1959* Helicotylenchus phalerus Anderson, 1974 (Fig. 5 T-X) (Fig. 5 CC-FF) Sher(1966) synonymized H. microlobus with H. This species was originally differentiated from H. pseudorobustus because he could not distinguish the pseudorobustus and H. microlobus (consideredby paratypes of the two species.Siddiqi (1972) recog- Anderson as a valid species) by a combination of five nizedboth species as validand proposed several characters, al1 of which were observed in the present characteristicstodifferentiate them. Sauer and studyto be quite variable among samples of H. Winoto (,1975), considering the variability in popu- pseudorobustus : lations of H. pseudorobustus from Malaysiarefused - Presence of a “prominent labial disc with elev- to follow the conclusions of Siddiqi 11972) and ac- atedmargins” in H. phalerus. Thisstructure is cepted the synonymization of Sher (,1966). noticeableonly in some paratypes of H. phalerus Thedifferentiating characters proposed by Sid- (Fig. 5 FF).Other specimens(Fig. 5 EE)are not diqi, 1972 (presenceof transverse striae in the lateral distinguishable from topotypes of H. pseudorobustus. field, distinctness of the phasmids, their position in - Terminal tail process marked by transverse and the central band of the lateral field, shape of the tail lateral striae. This annulation is not always visible projection,relative size of the dorsaltail annules, in specimens of H. phalerus and exists sometimes in ventral tail annulation) are too variable, both in H. specimens or H. pseudorobustus. microlobus andin H. pseudorobustus tohave any - Phasmids easier to see and always in the center taxonomic value. The pattern of the fusion of the of the lateral field. These characters are quite vari- innerlines of thelateral field on the tail, said by able in types of H. pseudorobustus. Siddiqi (1972)to be different between the twospecies, - Shorter distance DG0 - stylet. The differences is y-or rarelyv-shaped in H. microlobus, y-, u-, or between H. microlobus (8.4 Pm, s = 1.9), H. phalerus m-shaped in different samples of H. pseudorobustus. (10.4 Pm, s = 0.7), and the different samples of H. Because of the variability of these characters in the pseudorobustus (from8.8 to 13 Pm) cannot be ac- samples studied, H. microlobus is here accepted as a cepted as diagnostic in view of the great variability junior synonym of H. pseudorobustus. observedamong samples of H. pseudorobustus. - Tai1 with“a smaller and less conspicuously Helicotylenchus bradys Thorne & Malek, 1968 scultured ventral projection.” This structure is small (Fig. 5 Y-BB) in the paratypes examined, but no smaller than in many specimens of H. pseudorobustus. Theannu- This species was originally distinguished from H. lation of the tail projection is quite variable in H. pseudorobustus by“the coarsely annulated lip pseudorobustus. region,long spear andtail form.” Siddiqi (1972) The inner lines of the lateral field join together in used the position of the DG0(less or more than 1/3the y or v pattern, as in H. microlobus and many speci- spear length from the base of the spear) to separate mens of H. pseudorobustus. the two species at line 63 of his key. In lateral view, H. phalerus is here proposed as a junior synonym the lip annulesof paratypes of H. bradys are no wider of H. pseudorobustus. norcoarser than those of somespecimens of H. pseudorobustus. The mean stylet length is 26.4 (s = 0.8) Pm, shorter than indicated in the description (29- Helicotylenchus egyptiensis Tarjan, 1964 33 Pm). The tail terminus “slightly upturned, bluntly (Fig. 6 A-E) rounded” is no different from shapes observed in H. pseudorobustus. The DG0 is 10 (s = 1.3) Pm from the Measurements (in Pm) base of stylet, which is also consistant with measure- Paratypes (n = 4). L = 719 (s = 49) ; stylet = 26 (s = 0.4) ; esophagus = 121 (s = 1.3) ; esophageal glands = 150 (s = 5) ; dorsal gland opening = 10.75 (s = 0.96) ; excretorypore = 118 (s = 4) ; body * H. microlobus and three other species were frrst proposed by Perry in a thesis. Thisis in contravention diameter = 25.6 (s = 1.7) ; taillength = 22.4 with the Code of Nomenclature as noted in Helmintho- (s = 3.9) ; analbody diameter = 15.9 (s = 1.8). Zogical Abstracts 28 (1959), no. 3Sa. The descriptions Ratios : a = 28 (s = 2.7)’; c = 32.5 (s = 3.5) ; c‘ = of the fourspecies were laterincorporated into a 1.4 (s = 2.2) ; m = 49.5 (s = 1.3) ; V = 60.0% published article which maae their names available. (s = 1.2).

RevueNèmatol. 7 (2) : 121-135 (1984) . 131 R. Fortuner, AR. Maggenti h L.M. Whittaker

Fig. 5. Helicotylenchus pseudorobustus, other populations. A-MM : heads or tails ; A-D : sample A4, France, apple ; E-H : sample A5, France, tomato ; I-K : sample Il, New Zealand ; L-O : sample G1, California, Philodendron ; P-S : sample E2, Maryland, Blue grass ; T-X : paratypes of H. microlobus; Y-BB : paratypes of H. bradys; CC-FF : paratypes of H. phalerus; GG-JJ : sample E4, Iowa, corn ; KK-MM : sample H3, Korea, orange.

132 Nématol. Revue 7 (2) : 121-135 (1984) Morphometrical variability in Helicotylenchus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus

Description 720 ; 780 inoriginal description), vulva anterior (mean V value 60 phasmids level wiih anus (from Fernales : Body spiral, body annules 1.5-2 pm wide %) at mid-body. Lip region flattened to slightly rounded, one or two annules posterior to five annules anterior to anus according to Tarjan’s (1964), Sher’s (1966) with four tofive annules, well marked ; labial disc not and Van den Berg and Kirby’s (1979) descriptions), visible in transverse view. Basal ring of the cephalic inner lines of the lateralfield joining on tail in aUlm- framework 2 pm deep. Anterior cephalid difflcult to shapedjunction, tail about as long as wide, with see, 2 pm below the basal ring ; posterior cephalid greater dorsal curvature, with variable terminal pro- 14-15pm from the anterior end. Stylet knobs flat- jection, no males and empty spermatheca. tened to slightly roundedor indented. Excretory pore H. egyptiensis is very close to H. pseudorobustus. level toanterior to esophago-intestinal junction. Hemizonid 1-2 annules anterior to the escretory pore; There is no difference between the measurements of hemizonionsix annules posterior to the excretory thetwo species (Fig. 1). Infact the only marked pore. Fasciculi absent. Spermatheca offset, roundish, differenceis the shape of lips, flattened to slightly rounded in H. egyptiensis, markedly rounded in H. without sperms. Lateral field4-6 pm wide without pseudorobustus. Also the ventral projection is often transverse striae on body or tail ; longitudinal inner smaller and, more pointed in H. egyptiensis. lines join on tail in au- (Fig. 6 B,C, E) or a m-shaped (Fig. 6 D) pattern. Phasmids distinct, level with anus or one annule post,erior, in the center of the lateral Helicotylenchus africanus field ; the punctuations in the lateralfield reported by Tarjan (1964)are artifacts (Sher, 1966). Tail with (Micoletzky, 1916) Andrassy, 1958 eight to fourteen ventral annules with a non-annul- (Fig. 6 F-J) atedterminal ventral section ; dorsalterminal annules similar toor smaller than the other tailannules.. Measurements (in pm) Tail more curved dorsally with a pointed or rounded Topotypes (n-6). L = 856 (s = 70) ; stylet = 29.9 ventralprojection, pm long,annulated or not 1-3 (1.2) ; esophagus = 127(7) ; esophagealglands = annulated. 174 (14) ; dorsal gland opening = 9.5 (1.9) ; excret- Males : absent. orypore = 116(4) ; bodydiameter = 24.3 (3.5) ; Diagnosis tail length = 30.9 (4.3) ; anal body diameter = 15.6 (1.3). Ratios : a = 35.8 (4.3) ; c = 28.2 (3.3) ; c‘ = Helicotylenchus withspiral body, labial region 1.98 (2.5) ; m = 44 (0.6) ; V = 59.0 (1.42). flattened to slightly hemispherical, stylet of medium length(26 Pm), mediumbody length (mean value Description Females : body in C shape ; annules 1.5-2 pm wide at mid-body.Lip region hemispherical, with 415 well-marked annules ; labial disc not visible in lateral view. Basal ringof cephalic framework 2pm deep Anterior cephalid not seen, posterior cephalid 11-16 pm from the anterior end. Stylet lmobs variable in shape,anteriorly indented, flattened, or rounded. Excretory pore anterior to esophago-intestinal junction.Hemizonid just anterior to excretory pore, hemizonion not seen. Fasciculi absent. Spermatheca apparently in-line with the genital tract,full of rounded sperms. Lateral field 4.5-6.5 pm wide with scat- tered transverse striaeon body and tail; longitudinal inner lines join on tail generally in a u-shaped pattern, v-shaped in one specimen (Fig. 6 J). Phasmids 1-8 annules anterior to anus (mean : 3.8, s = 2.7), distinct and in the centerof the lateralfield. Tail with 12-18 annules (mean : 14.8 ann., s = 2.6), about two bodydiameters long, with a short non-annulated ventral section, and dorsal terminal annules smaller Fig. 6. A-E : Helicotylenchusegyptiensis; F-J : than other tail annules. Tail dorsally curved with a Helicotylenchus africanus; A and F : heads ; B-E, rounded terminal projection 2-4 pm long, annulated, G-J : tails. rarely a pointed projection.

Revue Nhatol. 7 (2) : 121-135 (1984) 133 R. Portuner, A.R. 1Maggenti h LM. Whittaker

Males : present butnot included in the present ACKNOWLEDGMENTS study. The authors thank 1. deOliveira Abrantes, R. V. Discussion Anderson, A. Bell, F. E. Caveness,Y. E. Choi, P. Donald, E. Geraert, A. M. Golden, D. J. Hunt, R. Our description agrees with Sher’s (1966) exceptfor McSorley, G. Mancini, R. Mankau, D. C. Norton, theshape of theventral tail projection. Sher de- M. R.Sauer, C. ScottoLa Massese, M. R.Siddiqi, scribed a “distinct pointed ventral projection,” but J. D.Smolik, A. C. Tarjan, E. Vanden Berg, B. illustrated (Fig. 2 B of Sher, 1966) a rounded pro- Weischer,R. Winoto Suatmadji, and G. W. Yeates jection. Of the six topotypes examined here,five have Who suppliedthe specimens ; J. Holmes, G. Merny, a distinctly rounded projection, only one has a more P. Mullon, and P. Schneeman Who helped withthe pointed projection (Fig. 6 J). One specimen presents statistics ; and A. French, J. M. Legay, and J. F. Southey Who reviewed the manuscript. a rounded projection and a short mucro identical to some structures observed in H. pseudorobustus (Fig. 6 1). H. africanus is easily distinguished fromH. pseudorobustus by its C shape, relatively long tail, and presence of males. Its styletis slightly longer and its vulva REFERENCES slightlymore anterior than those of H. pseudorobustus. ALI, S. S., GERAERT,E. & COOMANS,A. (1973). Some spiral nematodesfrom Africa. Biol. Jaarb. Dodonaea, 41 : 53-70. ANDERSON, V.R. (1974). Canadianspecies of the genus Helicotylenchus Steiner,1945 (Nematoda : Hoplo- Conclusions laimidae),their identifying characteristics and descriptions of three new species. Can. J. Zool., 52 : Multivariateanalyses proved once again to be a 1365-1381. valuable taxonomic tool to compare populations of ANDRASSY,1. (1958). Hoplolaimustylenchiformis related species. The present analyses show that sev- Daday, 1905 (syn. H. coronatus Cobb, 1923) und die eral criteria could differentiate Helicotylenchus pseu- Gattungen der Unterfamilie Hoplolaiminae Filipjev, dorobustus from H. dihystera inspite of the high 1936. Nematologica, 3 : 44-56. intzaspecificvariability of al1 charactersin both BENZECRI,J. P. & BENZECRI,F. (1980). Pratiquede species.The analyses also casta new light on ths l‘analysedes données. 1. L’analysedes correspon- relationshipsbetween H. pseudorobustus and H. dances, ezposé élémentaire. Paris, Dunod, 424 p. ’ microlobus, indispute for thelast twenty years. FORTUNER,R.(1979). Morphometrical variabilityin Multivariate analyses have in the past, willand in the Helicotylenchus Steiner, 1945.1. Theprogeny of future, help solve specific problems in taxonomy. It a single female. Revue Nématol. 2 : 197-202. may bepossible to usesimilar techniques at the FORTUNER,R. (1981). Les nématodes associés au riz genericlevel, to clarifythe relationships of taxa pluvial en Côte-d’Ivoire. Agron. trop., Nogent, 36 : withinand between certain genera. However, it is 70-77. doubtful that multivariate analyses can be used for FORTUNER,R. & QUÉNÉHERVÉ,P. (1980). Morpho- specific differentiation and identification in the genus metrical variability inHelicotylenchus Steiner, 1945. Helicotylenchus. There are now about 180 species in 2. Influence of the host on H. dihystera (Cobb, 1893) Sher, 1961. Revue Nématol. : 291-296. the genus,differentiated bytheir originalauthors frommore than forty measurements or qualitative FORTUNER,R., MERNY, G. & Roux, C. (1981). Morpho- characters,most of whichare highly variable. A metrical variability in Helicotylenchus Steiner, 1945. 3 : Observationson African populations of Heli- multivariate analysis including al1 the species and al1 cotylenchusdihystera and considerations on related the characters may or may not show some grouping species. Revue Nimatol. 4 : 235-260. of species inthe genus. Theidentification of the GERAERT,E., ZEPP, A. & BORAZANCI,N. (1975). Some criteriaresponsible for these groupings, and the plantnematodes from Turkey. Meded. Landb- evaluation of the taxonomic value of the groups so Hoogesch. Rijksuniv., Gent, 40 : 511-515. defined,would require a careful studyby both a GOLDEN,A. M. (1956). Taxonomy of the spiral nema- statistician and a taxonomist. For practicalidenti- todes (Rotylenchus and Helicotylenchus) andthe fication of species, other methods, for example the developmental stages and host-parasite relationships evaluation of the similarity between pairs of species, of R. buxophilus n.sp., attacking boxwood. Univ. will have to be investigated. Maryland agric. Exp. Stn Bull. A-85, 28 p.

134 Revue Nématol. 7 (2) :121-135 (1984) Morphometrical uariability in Helicotylenchus Steiner, 1945. 4 : Study of field populations of H. pseudorobustus

JENNRICII,R. 1. & SAMPSON,P. F. (1979).Stepwise SIDDIQUI,M.R. (1972). On the genus Helicotylenchus discriminant analysis. In : Dixon, W. J. & Brown, Steiner, 1945 (Nematoda : Tylenchida),with des- M. B. (Eds) BMDP-79Biomedical Computer Pro- criptions of nine new specics. Nematologica, 18 : gramsP-Series, Berkeley,Univ. California Press : 74-9 1. 711-733. STEINER,G. (1914).Freilebende Nematoden aus der MANCINI, G. & MORETTI, F. (1977). Il genere Helico- Schweiz. Arch. Hydrobiol., 9 : 259-276. lenchus Steiner, 1945 in Piemonte c Valle d’Aosta, TARJAN,A. C. (1964). Two newmucronate-tailed nota 1. Redia, 59 (1976) : 225-228. spiral nematodes (Helicotylenchus : Hoplolaiminae). MICOLETZRY,H. (1916). Ergebnisse einer botanischen Nematologica, 10 : 185-191. Forschungsreise nach Deutsch-Ostafrika und Siida- TIIORNE,G. & MALEK, R. B. (1968).Nematodes of frilca (Kapland, Natal und Rhodesien). Süsswasser- theNorthern Great Plains. Part 1. Tylenchida Nematoden aus Südafrika. Denkschr. Kaiserl. Akad. (Nemata : Secernentea). Bull. S. Dak.agric. Ezp. Wissensch.,Wien, 92 : 149-171. Stn, 31 : 1-111. SAUER,M. R. & WINOTO,R. (1975). The genus Heli- VANDEN BERG,E. & HEYNS,J. (1975). South African cotylencllus Steiner, 1945 in West Malaysia. Nemato- Hoplolaiminae. 4. The genus Helicotylenchus Steiner, logica, 21 : 341-350. 1945. Phytophylactica, 7 : 35-52. SHER, S. A. (1966).Revision of the Hoplolaiminae VAN DEN BERG,E. & KIRBY, M. F. (1979). Some (Nematoda)VI. Helicotylenchus Steiner, 1945. spiralnematodes from the Fiji Islands (Hoplolai- Nematologica, 12 : 1-56. midae : Nematoda). Phytophylactica, 11 : 99-109.

Accepté pour publication le 27 mai 1983.

Revue Nématol. 7 (2) : 121-135 (1984) 135