Xiphinema Insigne Loos, 1949, and X

Study of biometrical variability in Xiphinema insigne Loos, 1949, and X. elongatum Schuurmans Stekhoven & Teunissen, 1938 ; description of X. savanicola n. s.p (Nernatoda : Longidoridae) and comments on thelytokous species

Michel Luc * andJohn F. SO,UTHEY Muséum national d’Histoire naturelle, Laboratoire des Vers, associé au CNRS, 43 rue Cuvier, Paris, France and A.D.A.S., Harpenden Laboratory, Hatching Green, Harpenden, Herts, England.

SUMMARY

The taxonomic statusof Xiphinema insigne Loos, 1949, and X. elongatum Schuurmans Stekhoven &. Teunissen, 1938 is briefly reviewed and results are presented of a study of intraspecific variability of each of these species based on material from twelve populations (including type material) of X. insigne and twenty-two populations of X. elongatum. It is concluded that X. insigne, as at present understood, comprises several morphological forms wich may have started as geographical variants butwhose distribution has been modified by movements of plants and soi1 in commerce. It is not considered practicable at present to name taxa within thiscomplex, or to redefine X. insigne Lobs sensu stricto, because of the surprising degree of variability shown among the few available type specimens. X. elongatum presents a different picture. It shows a ‘more continuous pattern of variation than X. insigne, though there is evidence of a geographically based division into two groupsof populations. The first group, characterized by shorter tail andlonger stylet, al1 originate from West Africa whereas the second, having longer tail and shorter stylet, are mainly from East Africa or South East Asia/Pacific areas. “On the spot” differentiation was noted in Mauritiuswhere two clearly distinguishable populationswere mixed at the samelocation. Xiphinema savanicola n. sp., from Ivory Coast, Nigeria, Malawi, Gambia and Senegal, is described and figured. It seems to be associated mainly with’ Savannahgrasses. The new species has a shorter stylet than anyof the three most similar species : X. insigne, X. elongatum and X. elitum Khan, Chawla &. Sahaj 1978. In tail lengthit is inter- mediate between X. elongatum and X. insigne ; it differs from X. elitum in having a smaller V value. Canonical variate analysis and single-linkage cluster analysis of morphometric data from eight populations of X. insigne, twenty of X. elongatum and two of X. savanicola have strikingly supported the main conclusions, narnely the difference in nature of variability between X. insigne and X. elongatum and the validity of the three species. In the three species studied, as in about 75% of described Xiphinema species, males are rare or unknown so parthenogenesis is assumed to be the rule. The problems for the taxonomist in thelytokous (constantly parthenogenetic) species are discussed in detail. Since the ‘biological‘ species concept is not applicable one is dependent on arbitrary criteria to distinguish morphospecies. It is concluded that Cronquist’s (1977) definition, “species are the smallest groups that are consistently and persistently distinct, and distinguishable by ordinary means”, can be applied with suitable qualification. Therefore thelytoltous species which can be distinguished by morphological features only should be accepted as valid. It is in anycase desirable, and usual, to describe and name taxa initially on morphological criteria, accepting that later biological worlt may lead to revision.

Nematologist of the Office de la Recherche Scientifique et Technique Outre-Mer (ORSTOM).

Revue Nématol. 3 (2) : 243-269 (1980) 243 M. Luc & J. F. Southey

RÉSUMÉ

Etude bionzétrique de la variabilité chez Xiphinema insigne Loos, 1949 e€ X. elongatum Schuurmans Stekhoven h Teunissen, 1938: description de X. savanicola n. sp. (Nematoda : Longidoridae) et commentaires sur les espèces thelytoques ef commentaires sur les espèces thelytoques

Le statut taxonomique de Xiphinema insigne Loos, 1949 et de X. elongatum Schuurmans Stekhoven & Teunissen, 1939, brièvement évoqué, est suivi d’une étude de la variabilité int,raspécifique chez chacune des deux espèces, étude portant sur douze populations (dont le matériel type) pour X. insigne et 2.2 populations pour A’. elongafum. En conclusion des observations faites, X. insigne, tel qu’actuellement défini,comprend plusieurs types morphologiques qui ont pu diverger en tant que formes géographiques, mais dont la répartition a dû,être modifiée par les transports de plantes et de sol. Les auteurs considerent qu’il n’est pas possibIe actuellement de définir des taxa . à l’intérieur de ce complexe, ou de redéfinir X. insigne Loos sensu stricto, par suite du surprenantdegré de variabilité observé chez les spécimens types eux-mêmes. X. elongatum présente des caractéristiques différentes ; le mode de variation y est beaucoup plus continu que chez X. insigne encore que des indices existent d’une division géographique des populations en deux groupes ; le premier, caractérisé par une queue plus courte et un stylet plus long, ne comprend que des populations provenant de l’Afrique de l’Ouest, tandis que les populations formant le second proviennent dans leur majorité d’Afrique de l’Est ou d’Extrême-Orient. en un cas (Ile Maurice) il a été observé deux populations clairement distinctes ayant. la même localisation. Xiphinema sauanicola n. sp., récolté en Afrique (Sénégal, Gambie, Côte d’Ivoire, Nigeria et Malawi), est décrit et illustré. Cetate espèce, essentiellement associéesaux graminées de savane, est proche de A’. insigne, X. elongafum et X. elitum Khan, Chawla & Saha, 1978, espèces dont elle diffère par son stylet plus court ; la queue de A-.sauanicola n. sp. a une longueur intermédiaire entre X. elongatum et X. insigne, et, la valeur de V est inférieure à celle observée chez X. elitum. Il a été procédé à une analyse factorielle discriminante, et à une agrégation suivant le saut minimum, l’une et l’autre fondées sur huit populations de X. insigne, vingt de X. elongatum et deux de X:sauanicola. Leursrésultats ont nettement confirmé les principales observations, en particulier les différences dans le type de variabilité chez X. insigne et S. elongatum, de même que la validité des trois espèces. Chez ces trois espèces, de même que chez 75% des espèces du genre Xiphinema, les mâles sont rares ou inconnus et la. parthénogenèse apparaît être larègle. Les problèmes posés autaxonomiste parces espèces thélytoques, c’est-à- dire à parthénogenèse constante, sont discutés en détail. Etant donné qu’un concept (( biologique )) de l’espèce ne peut s’appliquerici, la définition de telles “ espèces morphologiques ‘’ nepeut reposerque sur descritères arbitraires. Il .est conclu que la définition plus générale de l’espèce donnée par Cronquist (1977), a l’espèce est. le plus petit groupe montrant de façon consistante et persistante des caradères distincts appréciables par des techniques normales )), peut s’appliquer ici sans grande difficulté. 11 en résulte que les espdces thélytoques, qui ne peuvent être distinguées que par des caractères morphologiques, doivent être considérées comme valables. 11 est en tout état de cause désirable, et utile, de décrire et nommer, dans une première phase, les différents taxa sur des critères uniquement morphologiques, quitte à ce que, par la suite, des travaux portant sur leur biologie amènent à certaines révisions.

Thepresent study began in 1968 when one X. insigne which included X. indicum Siddiqi, of theauthors (J.F.S.) and Dr. J.J.M. Flegg 1959,these two populations could be distin- provisionally identified Xiphinema’ insigne Loos, guished from one another and from “indicum-the 1949 from soi1 associated with dwarf ornamental like” populations by several constant features, (“bonsai”) trees imported from Japan and with such that withoutreference to Tarjan and Luc’s sugarcaneroots from the Philippines ; inthe paper, they might have been regarded as separ- latter case X.elongatunz Schuurmans Stekhoven ate species. Theseobservations led to the ini- & Teunissen, 1938 was present also. These two tiation of a detailed study of the morphological populations of X. insigne were fvrther compared variabilityinrelation tothe geographical with specimens from various other populations distribution of X. Insigne. of this species, includingtype specimens. The senior author, in thecourse of determina- Although a11 thepopulations observed corre- tion of various Xiphinema populations mainly

~ ...... ~ ._ . sponded to Tarjan and Luc’s (1963)- concept of-- collected inWest Africa,referred several.. of 244 Revue Nématol. 3 (2) : 243-269 (1980) Variability of Xiphinema insigne and X. elongatum ; X. savanicola 72. sp.

them to X. elongatum. Although these popula- thereafter the remaining syntypes became para- tions differed slightly from each other in several lectotypes (rather than paratypes as stated by characters, al1 of them could be included without Tarjan and Luc) which have no forma1 “type” major difficulty in the species X.elongatum as status for nomenclatural purposes. Tarjan and redefined by Tarjan and Luc (1963), but five of Luc’s paralectotypes also included a fourth . thepopulations appeared to form a distinct topotypespecimen from Loos’s collection, not group‘which could represent a separate,and used by him in his description. new,species. Furthermore during a survey of Tarjanand Luc (1963) found a surprising Xiphinema speciesassociated with sugarcane degree of variabilityamong Loos’s syntypes, in Mauritius (Williams & Luc, 1977) two easily consideringtheir small number, as illustrated distinguishable“forms” of’ X. elongatum were especially bythe drawings of tailsin their recognized,although both of them fit within Figure 1. This led them to synonymizewith the known limits of X.elongatum. Consequently X. insigne the klosely related species X. indicum the study of A’. elongatum has been extended to Siddiqi,1959. Siddiqi had basedhis diagnosis includebiometrical and morphological varia- of X. indicum chiefly on reduction in size and tions, and geographical distribution. function of theanterior ovary as compared , The computer facilities at Rothamsted Exper- withpopulations which he had attributed to imental Station have been used, with the help X. insigne proper, butunfortunately neither of colleagues in the Statistics Department there, Loos (1949) norTarjan and Luc(1963) described to apply canonical variate analysis to biometric in detail, or illustrated, the genital tract of the I data (Tab. 1, 3 & 6) fromthe populations under typematerial, so thestatus of X. indicum is study. noteasy to determine by reference totheir Results ofOur jointwork are given in this papers. paper and include an analysis of the variability of biometricalcharacters in X. insigne and Cohn andSher (1972) accepted Tarjan and X. elongatum, the description of X. savanicola Luc’s concept of X. insigne, gave measurements n. sp. (correspondingto the five African popula- of severalpopulations which they attributed tions close to X. elongatum citedabove), and to thisspecies and noted its similarity toX. elon- comments on the problem of identifying thely- gatum; they said that the two species differed tokous (= constantly parthenogenetic) species. essentially in only two characters, the V value and the tail length. Southey (1973)also accepted Tarjan and Luc’s and Cohn and Sher’s conclusions regarding X. insigne but recognized two Xiphinema insigne Loos, 1949 morphologicalforms of this specieswhich he (Figs. 1, 2, 3) designated ‘long-tail type’ and ‘ indicum type’. Bajaj and Jairajpuri (1977) have made a detailed Loos (1949) described and illustrated X’iphi- study of X.insigne populations in India. They nema insigne from soi1 about the rootsof soursop too recognized the two forms mentioned above, (Anona muricata L.), coconut (Cocos nucifera L.) five of iheir populations belonging to the former and grass (unidentified) at Kurunegala, Ceylon and eighteen to the latter type, but they were (nowSri Lanka). He based hisdescription on unable to justify reinstatement of X. indicurn three adult females (syntypes), andhis drawings as a valid species by reference to the original on one of them, butdid not designate a holotype. descriptions of typematerial of X. insigne Tarjanand Luc (1963) redescribed X. insigne (Loos, 1949 ; Tarjan & Luc, 1963) andtype anddesignated a lectotypewith the following specimens of X. indicum. measurements : L = 2.243 mm ; a = 55 ; b = In a recent study, Jairajpuri and Bajaj (1978) 7.1 ; c = 20; V = 8308 ; stylet (total)= 161Pm. observed in a population designatedas X.insigne Untilthe designation of alectotype, Loos’s and originating from the type localityof X. indi- type-series(syntypes) were of equalvalidity cum (Aligarh,India) that the anterior ovary in nomenclature (Article 73 of the International is constantly and consistently shorter than the Code of Zoological Nomenclature,1964), but posterior one ; however the two entire genital

Revue Nématol. 3 (2) : 243-269 (1980) 245 M. Luc di. J. P. Southey

branchesare approximately equal in length, information about the structure of the genital except during the breeding season. The anterior tract. Loos (1949) indicated thatthe two ovaryis not sterileb’ut its eggproduction appears brancheswere approximately equal (“about to be only about 1/60 of that of the posterior 14% of the body length”) while Tarjan and Luc ovary. These observations are very interesting (1963)gave 8-1 1% and 8-13 %, respectively, because theyprobably explain the apparent for relativelengths of anteriorand posterior contradictionbetween the report by some genitalbranches of fourspecimens (lectotype authors of “gonads [= genitalbranches] of andthree paralectotypes) with a mean of 9% approximately the same length” and the report foreach branch ; it isnot known whether or byothers of “anteriorovary much reduced”. not length of the reflexed ovaries was taken into account.Fig. 1 A, B shows details of these POPULATIONS AND SPECIMENS STUDIED structuresin the two paralectotype specimens in which they could be discerned. A is from .the 1. Sri Lanka (Ceylon), four paralectotypes (courtesy short-tailed specimen (Fig. 1, E) (c‘ = 3.8) C. A. Loos, A. C. Tarjan and S.A. Sher) from theFlorida collectioncorresponding to 2. Sri Lanka, Udopussellawa, from virgin jungle, host ; unknown (courtesy S. A. Sher) Fig. 1 (b) of Tarjan and Luc (1963) it seems 3. Japan,source 1ocalit.y unknown ; Brit.ish quar- to be the only gravid female among the original antine interception fromsoil associated with ‘bon- syntype material. Although only the posterior sai’ trees (Juniperus sp.) uteruscontains an ovum, t,hê anteriorovary 4. U.S.A., Raleigh,North Carolina ; hosttomato showsoocytes atan advancedstage and is

(courtesy R. T. Robbins) clearlyfunctional. B fromis the long-tailed 1

5. U.S.A., Fresno, California ; hostpurple plum spec.imen (c‘ = 5.1) corresponding to Fig. 1 (e) , (courtesy R. T. Robbins) of Tarjan and Luc (1963) ; the ovaries are much 6. Philippines,Salngan area, Iloilo Province, Panay less developed but about equal in size. Island ; soil around roots of sugar-cane (courtesy Tate & Lyle Techn. Serv.,,London) A specimen, originally from Loos’ collection, ‘7. Mauritius, Bel Ombre ; associated with sugar- now in the collection of the University of Cali- cane (courtesy 3. R. Williams) fornia, Riverside, was lent for study by the late 8. Malawi, BvumbweExperiment Station, Limbe ; Prof.Sher (Fig. 1, C, D). Thisseems to be associated with napier grass (Penniseturn purpu- reurn) (cpurtesy M. R. Siddiqi) additionalto the three syntypes described by 9. Thailand, Thonburi ; associated with Citrus sinen- Loos(1949) and the fourth specimen referred sis (courtesy S. A. Sher) to by Tarjan and Luc (1963) It has the typical 10. India,Aligarh ; associated with Grewia asiatica long tail (c’ = 5.1) shown by al1 the type series (paratypes of X. indicurn Siddiqi, 1959) exceptthe Florida specimen. This “Riverside” 11. Pakistan,Haripur ; soil aroundroots of loquat specimen,although remounted: carries Loos’ (Eriobotrya japonica) (courtesy M. R. Siddiqi) originallabels, withthe words “Xiphinenza 12. Israel, Raanana ;host unlrnown (courtesy E. Cohn) insignis Loos TYPE Glyc.7/44.”. Alt>hough labelled in this way, it cannot be considered as holotype because Loos (1949) did not designate BRIEF CHARACTERISTICS OF THE POPULATIONS atype specimen in his publication [Internat. STUDIED (for measurements see Table 1) Code zool. Nomencl., Art 73 (b) Csr. (c)].The Several good descriptions of X.insigne having Riverside specimen is clearly not the lectotype been published, it appeared unnecessary to the (compare Fig. 1, D with Tarjan and Luc’s (1963) authorsto give a complete and forma1rede- Fig. 1, j and Loos‘ (1949)Fig. 3, A. Repeated scription of this species. Thus,only the more attempts to trace the lectotype specimen have importantcharacteristics of thepopulations failed so it is presumed lost. studied will be given below. Presentlocation of paralectotypes : (i) One

Pop. l.,X. insigne paralectotypes (Fig. 1, A-E). female innematode collection, University of , Generalmorphology is in agreement with the Florida, Gainesville, (A.C. Tarjan) (= Tarjan description of Loos (1949) and Tarjan and Luc & Luc (1963), Fig. 1, b). (ii)Two females origin- , (1963).However these authors gave scant ally in the.persona1 collection of C.A. Loos, now ... . . -. .~ - .-. ~ _- .- ...... 246 Revue Nématol. 3 (2) : 243-269 (1980) Variabilifyof Xiphinema insigne and -Y. elongatum ; X. savanicola n. sp.

Revue Nématol. 3 (2) : 243-269 (1980) 247 M. Luc & J. F. Southey

Fig. 1. Xiphinemainsigne, females.Specimens from Sri Lanka. A-E : paralectotypes. A : genital tract [specimen corresponding to Tarjan and Luc (1963), Fig. 1, b]. B : genital tract [specimen sub- sequently damaged, corresponding to Tarjan andLuc (1963),Fig. 1, el. C & D : specimen from Riverside collection ; C : details of anterior end ; D : tail region. Tarjan's paralectotype. E : tail region. Specimens from Udopussellawa (Tab. 1, population 2). F : anterior genital branch. G. H : tails. (C-H : after Siddiqi, unpublished drawings). -. - .~ . . -. -. -

248 ' Revue Nématol. 3 (2): 243-269 (1980j Variability of Xiphinema insigne cmcl X, elongatum ; X. savanicola II. sp. depositedinthe collection of Nematology tostylefound generally in their second(long- Department, Rothamsted Experimental Station tailed) groupof populations. (= Tarjan & Luc, 1963 ; Fig. 1, a & e, the latter damaged and almost useless). (iii)One female, Pop. 6, Philippines, sugar-cane (Fig. 2, D-L). originally in the persona1 collection of C.A. Loos Thispopulation came close tothe Japanese and labelled “TYPE” but not described either population, e.g. in body length, V value and tail by Loos (1949) or by Tarjan and Luc (1963), now lengthbut differed inthe shorter odontostyle in the collection,of Department of Nematology, (mean = 93pm). Measurenlents of juveniles University of California, Riverside. are given in Table 2 and their tail shapes illustrated in Fig. 2, I-L. This population was mixed Pop. 2, Sri Lanlca, Udopusselawa (Fig. 1,F-H). with a S.longatrrnz population, no. 20 (page 254 These two specimens, botli of long-tailed type, Table 3) ; measurements of thesetwo popula- seem close to the paralectotypes apart from the tions wereremarlcably similar apart fromtail greater lengthof their tails (cf. populations3 & 4 length and V value (cf. comnlents of Cohn and below). Sher, 1972). In fact the difference in V value is probably related to the difference in tail length Pop. 3, Japan, irnportedbonsai trees (Fig.2, so thatthe latter may be theonly primary A-C). Thesespecimens comprise a well defined difference between the L,wo species in this case. form characterized by relatively largesize (mean body length = 2,74 mm), high V value (mean = Pop. 7, Maurifius, sugar-cane.This population 35.4), long tail (mean length= 127 pm, c’ = 5.0), was described briefly and illustrated by Williams long odontostyle (103 pm) and equally developed and Luc (1977). Measurements and morphology genitalbranches. They agree well withthe correspond closely with those of the Philippines descriptionand measurements of X. insigne population associated with the same host plant. from Japan given by Saigusaand Yamamoto Inthe short odontostyle and long tail these (1971) Who also described and figured one male twopopulations resemble those in the second specimen. Measurements of first, third and fourth group of populations (19-23) reported by Bajaj juvenile stages are given in Table 2. and Jairajpuri (1977) frorn India. Pop. 4 & 5, U.S.A., North Carolina (tomato) Pop. 8, Malawi, napier grass (Fig. 3, A-C). Of andCalifornia (plum). These two American the populations studied this one has the longest populationsmost closely resemble that from tail (mean length = 148 pm ; c’ = 6.4) and the Japan (no. 3). Thesample from Fresno, Calif. greatest V value(mean = 38). Otherfeatures included one male : L = 2.78 mm ; a = 71.2 ; that appear to distinguish it from other popula- tail=64pm;c=43;~’=2.9;OST=102pm; tions are the low and flattish lip region, practic- OPH = 66 pm (?) * ; total stylet = 168 pm (?)* ; allycontinuous with the body contour (not hyalinetail tip = 17 pm ; spicule(chord) = or scarcely offset) and the muscular structures 49 pm, (arc) = 53 pm. [*odontophore obscure]. surrounding the inner part of the vagina which Thesemeasurements are in reasonable agree- form a larger and more conspicuous sub-globular ment with those of the few males of X. insigne mass in lateral view. reported by other authors (Cohn, 1969 ; Saigusa & Yamamoto, 1971 ; Bajaj & Jairajpuri, 1977) Pop.9, Thailand,Thonburi (Fig. 3, D-H). but the body length, tail length andc‘ value are These specimens are similar to Loos’ type mate- greater than in any of them ; in these features rial of X. insigne in most respects, apart from theyare nearest to Saigusa andYamamoto’s thegreater V value(mean = 34.6)in which Japanese specimen. In tail shape and structure they resemble theJapanese and Philippine the Californianspecimen also mostresembles populations. The tail length is even more vari- that figured by Saigusa and Yamamoto. In the able than in the type population and much more relatively long odontostyle and stylet the Cali- so thanin the remaining populations studiecl fornianspecimen agrees with al1 exceptthe (Fig. 3, F-H). (tail length = 81-149Pm, c’ = malefound by Bajajand Jairajpuri (1977) in 3.6-7.1 amongonly 8 specimens.)Compared their population 22 which had the shorter odon- withthe Malawi population (6) thevaginal

Revue Nématol. 3 (Z),: 243-269 (1980) 249 M.Luc & J. F. Southey

Fig. 2. Xiphinema insigne. A-C : female associated with bonsai trees from Japan (Tab. 1, population 3). A, B : details of ant.erior and posterior genital branches. C : tail. D-L : specimens associated with sugar-cane from the Philippines (Tab. 1, population 6). D : details of anterior end of female. E-H : female tails. 1-L :

-~ .~first- to-_ fourth-stage tail shapes. ~-(D-H -: afterSiddiqi, unpublished drawings). .-. -. ... -- 250 Revue Nématol. 3 (2) : 243-269 (1980) Variability of Xiphinema insigne and ,Y. elongatum ; X. sevanicola n. sp.

Table 2 , Measurements of juvenile stages (51-54)of some X. insigne populations (Standard deviation ( f) is given where n 3 10) Philippines Japan India Japan Philippines Pakistan (Population 6) (Population 3) (Population 10) (Population II) 13 1 O 2 0.85 f 0.04 0.81 0.81, 0.85 (0.79-0.94) 6.40.8 6.0 5.4, 5.3 (5.5-8.1) Odontostyle (Pm) 38 f 2.5 48 42, 39 (34-44) Replacement od. 49 f 2.5 (Pm) (46-56) c 57, 54 Ondotophore 32 5 1.4 30 - (Pm) (30-35)

9 O O 4 1.O4 1 .O2 (0.93-1.15) (0.98-1.07) 6.9 5.4 (6.0-8,0) (4.9-6.0) Odontostyle 50 56 (Pm) (47-52) (54-57) Replacement od. 67 70 (Pm) (63-69) (69-72) Odontophore 40 35 (Pm) (38-41) (33-36)

53 n 8 11 4 7 1, (mm) 1.37 1.61 f 0.10 . 1.17 1.37 (1.19-1.60) (1.46-1.77) (1.14-1.20) (1.26-1.48) 6.6 5.9 f 0.8 5.1 5.0 (6.0-7.5) (5.2-7.5) (4.9-5.5). (4.3-5.5) Odontostyle 66 72 f 1.8 74 72 (Pm) (63-68) (69-75) (72-75) (69-75) Replacement od. 79 86 f 2.4 86 86 (Pm) (75-83) (82-89) (84-87) (84-90) Odontophore 46 49 f 3.2 39, 42 45 (Pm) (44-47) (44-54) [n = 23 (44-45)

13 9 5 7 1.90 f 0.17 2.14 1.65 1.86 (1.66-2.21) (1.87-2.26) (1.51-1.76) (1.77-1.98) 6.0 f 0.6 ' 5.5 4.7 4.3 (5.2-7.2) (4.2-6.3) (4.5-5.0) (3.9-5.1) Odontostyle 78 f 2.4 88 88 86 (P.ml . (75-83) (83-91 ) (84-90) (80-90) Replacement od. 92 f 2.9 104 105 105 (Pm) (86-97) (99-107) ( 102-1 08) (101-111) Odontophore 53 f 2.4 58 51, 51, 51 53 (Pm) (50-56) (54-63) [n = 31 (51-57)

, Revue Nématol. 3 (2) : 243-269 (1980) 251 M. Luc LE J. F. Southey /

Fig. 3. Xiphinerna insigne, females. A-C : specimens from'Malawi (Tab. 1, population 8). A : details of anterior end. B : anterior genital branch. C : tail. D-H : specimens from Thonburi, Thailand (Tab. 1, population 9). D & E.: anterior and posterior genital branches. F-H : tails. (al1 after Siddiqi, unpublished drawings).

~~ - -. , ~,..

252 Revue'Némafol. 3 (2) : 243-269 (1980) Variability of Xiphinema insigne and X. elongatum ; X. savanicola 11. sp.

muscles,form flattera more saucer-shaped first species and for the secondspecies, of a structure in lateral view (Fig. 3, D & E). Brazilianpopulation sampled in the vicinity of thetype locality, the type specimens not Pop. 10,11, 12, c indic un^' populations. The having been preserved. paratypes of X. indicurn Siddiqi, 1959 and the specimens from West Pakistan, originally deter- Cohn and Sher (1973) consideredX. truncafum mined by Siddiqi as S. indicum, tallied well Thorne, 1939, tobe a junior synonym.of X. elon- withhis descx-iption (Siddiqi,1959) andwith gatum; but Luc and Dalmasso (1975) rejected the description and data of Bajaj and Jairajpuri this synonymy and treated X. truncafum as a (1977) ; Our studies of this material add nothing speciesinquirenda., givingdetailed arguments , to their findings. Specimens from Israel appear for this opinion. also to correspond with the ilzdicum form. Since its description, X. elongatum Bas been recorded by a number of authors in association DISCUSSION withdifferent .plants and crops. The original descriptionwas rather limited, but redescrip- Themorphological and biometrical observations or data from additional populations have tionsdescribed above strongly suggest that been published by Loos (1949), Lordello (1951), Xiphinemainsigne as at presentunderstood Williams (1959), Siddiqi (1961), Carvalho (1962), comprises several more or less distinct morpho- Tarjanand Luc (1963), Timm (1965), Cohn logical formswhich are perhaps primarily and Sher (1972), Loof and Maas (1972), Heyns geographic,al variantswhose original distribution (1974),Williams andLuc (1977), Loof and has been somewhat confounded by movenlents Sharma(1979). Thus this species can be con- of host-plant material in commerce. sideredsuEciently ltnown to render forma1 The results of canonical variate analysis (see redescription unnecessary. p. 2.62 and Figs. 7-10) suggest a similar subdivi- The type specimen is preserved in the collec- sion and morphological featuresother than tion of theInstitut des ParcsNationaux du biometric ones could be used to assist in their C.ongo, 1 rue Defacz, Brussels, Belgium. separation.However, a major dificulty about assigning morphospecific status to subdivisions ' of X. insigne Loos sensu lato is thesurprising POPULATIONSAND SPECIMENS STUDIED variabilityamong the few availableand de- 1. Ïsrael,Kubeiba ; associatedwith avocado tree scribed topotype specimens (Tab. l and Fig. l, (courtesy E. Cohn and S. A. Sher) A-E). The problem might be resolved if a fresh O,. Senegal, Bambey ; clean soil, after tomato (cour- collection could be made from the type locality, tesy C. Netscher) enabling X. insigne to be redefined with refer- 3. Senegal, Sor ; associated with Citrus sp. (courtesy ence to both t.he lectotype description .and an D. P. Taylor) accurate characterization of the type population. 4. Ivory Coast, Bouaké; associated with upland rice cv. Moroberekan (courtesy A. Ravisé) 5. Upper-Volta, locality not known ; associated with peanut (courtesy G. Germani) Xiphinema elongatum 6. Togoland, Ganavé ; associated with cassava (cour- Schuurmans Stelchoven cf2 Teunissen, 1038 tesy G. de Guiran) (F,igs. 4 & 5) 7. Benin (Dahomey), Sokohoué; associated with cot- ton (courtesy G. Germani) 8. Nigeria, Ibadan ; associatedwith various plants Originally described by Schuurmans Stelcho- (courtesy F. E. Caveness) ven and Teunissen (1938) from a single female 9. Rhodesia, Triangle ; associatedwith sugar-cane fromRutshuru (Zaire), Xiphirzernaelolzgatum (courtesy G. C. Martin) was redescribed, from the type, by Tarjan and 10. Rhodesia,Hippo Valley ; associatedwith Citrus Luc(1963) and synonymised by these authors sp. (Courtesy G. C. Martin) with X. pratense Loos, 1949 and X. campinense 11. Rhodesia, Chirundu ; associated with sugar-cane Lorclello, 1951,after study of syntypes of the (courtesy G. C. Martin)

Revue Nématol. 3 (2) : 243-269 (1980) 253 M.Luc & J. F. Southey

254 Variability of Xiphinema insigne and X. elongat um ; X. savanicola n. sp.

12. Zambia, Mtondwe ; associated with tobacco (cour- - Zambia (courtesy D. C. M. Corbett) : sugar-cane, tesy D. C. M. Corbett) Upper Bua River and Zomba Experiment Station ; 13. Mozambique, Porto-Bello ;associated with coconut napier grass, Tuchila ; Paspalum notatum (= P. dis- trees and Pueraria sp. (courtesy Y. Frémond) fichum), Zomba;peach-tree, Chitede Experiment Station ; maize, Chititi Dambo 14. Madagascar,Antalaha ; associated withvanilla and Gliricidia sp. (courtesy G. de Guiran) - Madagascar(courtesy G. de Guiran) : Vetiveria zizanoides, Nossi-Bé ; vanilla,Antalaha ; sugar- 15. Mauritius, Pamplemousse ; associated with sugar- cane, Brickaville and Nossi-Bé cane (courtesy J. R. Williams) 16. & 17. Mauritius, Réduit ; associated withsugar- cane (courtesy J. R. Williams) VARIATIONSBETWEEN POPULATIONS 18. Thailand,Sattahip ; associatedwith asparagus Compared to X.insigne, X.elongatum appears (courtesy E. Cohn and S. A. Sher) to constitute a more homogeneous species with 19. Thailand,Sattahip ; associatedwith carnation amore continuous pattern of variation, as (courtesy E. Cohn and S. A. Sher) reflected in Fig. 7 for measurable data and in 20. Philippines, Salngan area, Iloilo Province, Panay Fig. 4 for the shape of the tail. Island ; soi1 around roots of sugar-cane (courtesy Tate & Lyle Techn. Serv., London) Considering theprincipal numerical data separately : 21. Cabo Verde Islands ; uocality unknown (courtesy G. Germani) - the mean value of body length (L) varies 22. Fiji Islands ; locality unknown (courtesy P. A. A. from 2.01 mm(pop. 4) to 2.50 mm(pop. lO), Loof) without gap between; the extremesfor al1 populations studied are 1.82 mm (pop. 6) and 2.77 Twenty other populations have been determined (POP. 10) ; as X.elongaturn but not studied in detail. They - the mean value of the coefficient V varies, are the following : without gap, from37.2 (pop. 1)to 45.2 (pop. lO), theoverall extremes being 34.5 (pop. 1) and - Ivory Coast : Acalypha sp., Abidjan ; Alternalz- fhera sp., Sanchezia parvibracteata, Adiopodoumé 48.9 (pop. 6) ; ' - Nigeria (courtesy F. E. Caveness) : Imperata cylin- - themean value of totalstylet Iength drica (= 1. arundinacea), Ojo-Eoje, Oyo Prov. ; varies,without gap, from 141 pm (pop. 10) to bush cover,mile 55, Igbeti-KishiRoad ; maize, 171 pm (pop. 4 & 5) ; the overall extremes are mile 3, Ibadan-IfeRoad ; bushand tree cover, mile 4, Ehoro Auchi Road 134 pm (pop. 10) and 178 pm (pop. 5 & 6) ; - Rhodesia (courtesy G. C. Martin) : flower garden, - the mean values for tail length and coeffi- Gwelo ; tobacco, Bulawayo. cient c' show a slight gap between two groups - Kenya (courtesy D. C. M. Corbett) : Themeda sp., of populations. Populations 2, 3, 4, 5, 6, 7 and 21 Nairobi have shorter tails. In this group of populations,

Table 4 Measurements of juvenile stages of Xiphinema elongatum population 20 (Philippines)

JI J2 53 J4

11 9 13 15 10 L (mm) L 0.66 f 0.06 0.87 f 0.04 1.29 f 0.11 1.79 & '0.26 (0.53-0.72) (0.81-0.94) (1.19-1.64) (1.32-2.17) c' . 4.4 f 0.1 4.4 f 0.6 3.6 f 0.3 3.5 f 0.3 (4.2-4.5) (3.5-5.0) (3.1-4.1) (3.1-4.0) Odontostyle(Pm) 34 f 1.9 46 1.3 62 f'l.9 74 f 2.8 (31-37) (44-47) (59-65) (71-78) Replacement od. (Pm) 46 f 1.4 fi3 f 2.4 79 f 2.3 93 f 3.7 (44-47) (59-68) (75-83) (86-97) Odontophore(Pm) 29 f 2.2 37 f 1.5 44 & 1.6 51 f 2.3 (25-31) (35-40) (41-47) (47-53)

Revue Nématol. 3 (2) : 243-269 (1980) 255 M. Luc & J. F. Southey

Fig. 4. Xiphinerna elongatum. A-J : tail of females of various populations (see Tab. 3). A : population 4, Ivory Coast. B : population 6, Togoland. C, D : population 8, Nigeria. E : population 11, Chirundu, Rhodesia. F-G : population 12, Zambia. 1-1-1 : population 15,Pamplemousse, Mauritius. J : population 17, Réduit, Mauritius. K-T : tail of larval and adult female stages, population20, Philippines, K & L : first-stage larvae ; M-N : second-stage larvae ; O, P : third-stage larvae ; Q-R : fourth-stage larvae ; S, T : females...... - . ~ ~.,- . . - - - _-- -- - 256 Reoue Nématol. 3 (2) : 243-269 (1980) Variability of Xiphinema insigne and X. elongatum ; X. savanic,ola n. sp. the mean values for tail length and c’ coefficient related to a given population. The length of the vary, respectively, from 48 pm (pop. 3) and 2.0 hyalineterminal part of thetail (II), as well (pop. 2 & 3) to 54 pm (pop. 5,G & 21) ancl 2.3 as its valueas a percentage of the total tail length (pop. 4 & 6). The second group of populations (11%) havebeen calculated for some of the has longer tail and higher c’ coefficient ; their observedpopulations (Tab. 5). Amongthese meanvalues vary respectively from 59 pm populationsonly no 17appears t,o be slightly and 2.5 (pop. 14) to 67 pm and 2.9 (pop. 12). But different in having a meanh and h% values muchoverlapping exists if oneconsiders the higher than others. individualdata, as for theother numerical Correlating tail length and total stylet length, characters mentioned above. thegrouping of “short-tailed”populations Incontrast to X. irzsigrze, thetail shape appearsclearer because al1 thesepopulations appears surprisingly constant in al1 populations have a lneantotal stylet length eyual to or of X. elongalum (Fig. 4). Where the tail is longer, exeeding 164 pm ; whereas al1 the others (with itsventral curve is morepronounced and the the exception of no 17) have a mean total stylet extremity may be slightly subdigitate, but this length eyual or under 161 pm. Canonical variate appears to be more linkedwit.11 individuals than analysis(see p. 262)based on five biometric

I I I I I l l I I l I

Fig. 5. Xiphinema elongafzzm. A-C : Details of anterior end of females in three populations (see Tab. 3). A : population 14, Madagascar. B : population 15, Pample- mousse, Mauritius. C : population 17, Réduit, Mauritius.

Table 5 Xiphinema elongatum: mean and range of the hyaline terminal part of the tail expressed in Fm (h) and in percentage of the total tail length (h%) for some populations

Populations h’ h%

2 (Senegal) 15 (13-17 31 (28-33) 3 (Senegal) 16.5 (14-19) 34(30-39) 7 (Benin) 15 (13-18) 30 (24-37) 14 (Madagascar) 17.5 (14.5-21.5) 30 (24-39) 15 (Mauritius) 18 (14-25) 28(22-35) 16 (Mauritius) 20 (17-21) 30 (27-36) 17 (Mauritius) (21-30)26 40 (33-45)

Revue Nématol. 3 (2) : 243-269 (1980) 25 7 M. Luc dl- J. F. Southey features (L, c’, V, odontostylelength, odonto- Xiphinema savanicola n. sp. phore length) very neatly supports the grouping (Fig. 6) discussed above, as well as illustrating the other- Wise continuous pattern of variation in X.elongatum. Note. thatthe anomalousposition of Severalpopulations of this newspecies, al1 population 17 is brought out on the third canoni- of them collected intropical or subtropical cal axis (Fig. 8) and, according to this, popula- Africawere observed andmeasured. They tion10 appears rather distinct. It shouldbe are as follows : noted that the group of populations with short Pop. 1. (type population): Soil, Savannah near Dabou, tailand long stylet al1 originatefrom West Ivory Coast : Gramineae(mainly Imperatacylin- Africa(Senegal, Gabo Verde Islands,Ivory drica,Hyparrhenia dissoluta, Schizachyrium semiberbe and Loudetia ambiens). Coast, Upper Volta, Togoland and Benin) ; but Pop. 2 : Soil,Savannah grasses, Abeokuta-Ilaro- population 8 (Nigeria)appears closer toEast Igbogila road, 28.75 miles from Abeokuta, Abeokuta African of Far Eastern populations. Neverthe- Prov., W. Nigeria (leg. F. E. Caveness). less some evidence of, geographical variation is Pop. 3 : Soil, Cynodon magennisii (Gramineae), Blan- discernible here. t.yre Club, Blantyre, Malawi (leg. D. c. M. Corbett). But anotherkind of differentiationexists, Pop. 4 : Soil, tomato, garden near Cap Point, Gambia. which appears clearly ifwe examine the three Pop. 5 : Soil, peanut, I.S.R.A. Station,Bambey, populationsfrom Mauritius. Theseoriginate Senegal. from the same host plant (sugar-cane) from two localities only.At one location,two different Other specimens observed but not measured : populat>ions(16 and 17) were mixed butthey one female from soil, Savannah grasses, Lamto were suficientlydifferent to bedistinguished nearToumodi, Ivory Coast, and one female evenunder a low powerstereomicroscope ; from soil, oil palm nursery established on savan- population 15, from the other locality, is similar nahland, I.R.H.O. Estate, Mopoyem, Ivory to no 16 ; so disregarding the locality, two types Coast. of X. elongatum, slightlydifferent, occur in Mauritius : type 15/16 and type 17. These two DIMENSIONS Mauritian types were called “forms” by Williams and Luc (1977) : “‘form” A corresponds to popu- Pemales (see Table 6) lations 15 and 16 ; “forme” B to population 17. Males (population 2), Nigeria (n = 2) : L = They differ in a number of characteristics : 2.38-2.40 mm ; a = 77.4-79.3 ; b = 7.4-7.7 ; posteriorbody curvature ismore pronounced tail length = 47-50 pm ; c = 47.6-51.1 ; c’ = 1.7- and body, V and total stylet length are higher 2.0 ; odontostyle = 76-83 pm ; odontophore = in population 17. This “on the spot” variation 52-54 pm ; total spear length = 130-135pm ; is dificultto explain. It does not seern to be spicules = 44-48 pm. related to the isolationof Mauritius, for example, because populations 15 and16 are similar to Juueniles : stage4 (type population) : see several populations from very different parts of table 6. the world (forexample Zambia, Philippines, Holotype (female,type population) : L = Thailand). 2.28 mm ; a = 68.1 ; b = 7.2 ; V = 37.7 ; tail Heyns (1974) observed geographical variation length = 83 Pm; c = 27.5;cf = 4.4; odon- in South Africa between populations of X.elon- tostyle = 80.5 pm ; odontophore = 51.5 pm ; gatum originating from Western Cape Province total spear length = 131 pm. andthose from Transvaal or Natal on the Easternside. The characters involved were DESCRIPTION body,stylet and tail lengths. Heyns (1974) describedalso theonly malesknown for the Pendes (type-population) : VVhen heat re- species ; he observed three males, among hun- laxed, body is ventrally curved, having a loose dreds of females,each of themin a different hook-shapedappearance ; bodymore tapered ~.population. posteriorly ; body diameter near vulva 33 pm ~. - .. . ~~ ,- -_ - - -.- - . - . -- -- 258 Revue Nématol. 3 (2) : 243-269 (1980) Variability of Xiphinema insigne and X. elongaturn ; X. savanicola n. sp.

Table 6 Xiphinema savanicola n. sp. : biometrics of females and fourth-stage juveniles (Means and standard deviation (f)are given for fernales of populations 1 and 2) Females Juveniles (J 4) Pop. 1 Pop. 2 Pop. 3 Pop. 4 Pop. 5 Pop. 1 (IvoryCoast,(Nigeria) (Malawi) (Gambia)(Senegal) (IvoryCoast) type. population) n 31 15 3’ 1 1 9 L (mm) 2.23 & 0.12 2.40 ‘f0.11 2.45 2.90 1.70 (1.98-2.47) (2.29-F.68) (2.43-2.68) (1.60-1.85) a 69.1 f 7.3 69.3 & 4.6 96.6 72.1 58.8 (56.0-82.9) (59.8-77.5) (86.0-97.2) (54.3-64.6) b 7.0 f 0.55 7.2 -f 0.5 7.0 - 8.3 5.4 (5.5-8.4) (6.3-7.8) (5.0-6.0) Tai1 length (Pm) 80 & 5.3 84 f 6.6 87 83 76 (69-94) (69-95) (88-91) ( 7 1-82) C 28.0 f 2.3 28.5 f 2.0 28.2 34.9 22.1 (22.9-31.6) (26.1-33.2) (26.7-30.4) (19.7-23.4) C’ 4.1 f 0.4 4.0 -J= 0.3 4.8 3.8 4.3 (3.3-5.0) (3.2-4.5) (5.2-5.7) (3.9-4.8) V 38.4 f 1.5 39.9 f 1.4 36.5 42.0 - (35.4-41.6) (36.2-41.5) (42.4-42.9) Od. style (Pm) 79 & 2.1 77.5 & 2.7 84 77 67 (74-83) (74-84) (69-72) (60-70) Od. phore (Pm) 52 & 1.6 51.5 f 1.7 61 54 44.5 (48-55) (49-56) (45-47) (44-48) Tot. stylet (Pm) 131 f 2.9 129 f 3.4 145 131 111.5 (126-137) (125-134) (114-119) (108-115) Repl. od. st. (Pm) - - - - - 79 (77-82)

(29-38).Cuticle finely transverselystriated, tubular with basal annule situated at 63-74 pm apparently composed -of two layers-; thickness from anterior end. Hemizonid flat (4.5-7 pm) at of the cuticle : 2.5 pm at mid-body, 3-3.5 pm in 147 pm (138-159) from anterior end ; hemizonion the neck part and 4.5-6 pm OR the dorsal side lentiform (2.5 pm) at 186-1.96 pm from anterior of the tail. Lateral chord occupying about 1/5 end.Nerve ring (8-13 pm) at 12-41pm from to 114of thecorresponding diameter, at mid- spearbase. Oesophagus typical of the genus ; body. Cervical pores absent or only one or two basal bulb measuring 95 x 15 pm (79-109 x 13- on the ventral and dorsal lines and two or three 17) ; “mucro” (2-3.5 pm) at 41 pm (24-83) from on thelateral ones ; latero-subdorsalpores spear Sase. Intestinewithout any particular irregularly , and widely spaced ; latero-subven- feature. Vaginamore or less perpendicularto tral pores very rare ; ventral pores present only bodyaxis. Two genitalbranches having the on anterior half of the body. Labial area some- samestructure and approximately the same whatflattened anteriorly, 10.5-11.5 pm in length ; the total length of each branch, mea- diameter, followed by a cylindrical portion, 5.5- sured from vulval slit to apex of the ovary on 6 pm in height, separated from the rest of the 24females (excluding thosewith a developing body by a marked depression. Amphid aperture egg), was for the anterior one, 201 pm (164-272) slit-like,slightly anterior to the depression, or 9.1% (7.3-12.6) of body length and, for the occupying 60-75% of the corresponding diame- posteriorone, 188 pm (159-274) or 8.1% (7.1- ter. Spear typical of the genus ; width of flanges 12.2) of body length ; the difference in the mean 9.5-1 1.5 pm. Guidingapparatus apparently length of the two branches is slight but. it must

Revue Nématol. 3, (2) : 243-269 (1980) 259 M. Luc 22 J. P. Southey

Fig. 6. Xiphinema savanicola n. sp. A-E : population 1 (type), Ivory Coast. A : female, detail of anterior portion. B : detail of anterior genital branch. C, D : female. t,ails. E : fourth-stage juvenile tail. F-J : population 2, Nigeria. F : female tail. G : detail of the tip of female tail. H : posterior portion of male. 1 : position of the ventral supple- ments in thesecond male. J : spicule and accessory piece. Variabilitg of Yiphinema insigne and S. elongatum; S. savanicola n. sp.

be notedthat on the 24 femalesobserved, PARATYPES: Femalesdeposited atthe same 17 possess an anterior branch longer than the placeas the holotype ; two females deposited posteriorone. Vulva and ovejector without ineach of the followingNematology labora- distinctivefeatures ; structure of eachgenital tories : RothamstedEsperimental Station, branch rather simple : oviduct thin, oftencoiled, Harpenden,England ; Plantenzielctenkundige composed of cells apparently fibrillar, not easily Dienst,Wageningen, Netherlands ; lnstituut tlistinguished,without any muscular or other voorDierkunde, Gent, Belgium ; U.S.D.A., differentiation (no Z organ or Z pseudo-organ) ; Nematode Collection,Beltsville, Maryland, pouch of the oviduct and uterus pouch slightly U.S.A. ; University of California, Davis, U.S.A. ;

developed, separatecl byasmall sphinc.ter ; O.R.S.T.O.M., Daljar, Sknkgal. , ovary generally stout. Two eggs observed : 173- 129 x 20-23 pm. Tail regularly elongate-conoid, TYPE HABITAT AND LOCALITY : Soi],, Savannah slightlyventrally curved with rounded end. nearDabou, Ivory Coast ; associatedwith Cuticle mainly dorsally thickened, with interna1 Gramineaemainly Imperda cylindrica,Hypap- layerradially striated ; hyalinebasal part (or rheniadissoluta, Schizachyriurn semiberbe and non-protoplasmicpart) rather short : 12.5 pin Loudetia ambiens. (11.5-14.5) or15.5% (13.3-19.3) of taillength. DIAGNOSIS: S. savanicola n. sp. is characterized ,Extremitywith plain cutide without blind bymoderate body and stylet lengths (under canal. Two or three pairs of caudal pores, rather 3 mm and under 150 pm, respectively) ; female regularlyspaced, the anterior one slightly genital apparatus with two conlplete branches, posterior to the anus level. withoututerine differentiation ; vulvapreme- dian(V = 35.4-42) ; ' tailregularly conoid- Males (populationfrom Nigeria) : Body elongated (tail length : 69-95 pm ; c' = 3.3-5.7) slightly arcuate in the fore half and curved in slightly bent ventrally and with rounded encl. ahook shape in the posterior part ; diameter The most similarspecies are : X.insigne, X.elon- at mid-body 30-31 Pm. Cuticle,labial region, gafum and A'. elitum Khan, Chawla & Saha, spear and oesophagus as in females. Two testes.' 1978. From X. insigne, X. savanicola n. sp. Spicules, stout,curved, rounded at both ends. differs mainly in its shorter stylet and shorter Accessory piece short (8-9 pm). Ventral supple- tail ; from X. elongatum mainly in its shorter ments : adanal double papilla situated 13-15 pm stylet and longer tail; from X.elitum by having anterior to the anus ; 3-4 single ventral papillae a shorter stylet (114-137 pm vs 165-180 pm) and situated at 82, 107, 131 pm in front of the anus more anteriorlysituated vulva (V = 35.4- in one male and83, 102,113,128pm in the other. 42.9 vs 48-50). Tailconoid-digitate, with roundeda dorsal profile and a ventral profile continuing the gene- OBSERVATIONS: Inspite of intensivesurveys ralventral profile of thebody ; digitatepart made over more than twenty years, on various (10-11 pm)rounded at its end ; cuticleplain, crops and natural habitats,X. insigne has never without blind canal. Three,pairsof caudal pores. beenrecorded in tropical West Africa. It is possible that X.savarzicola n.sp. represents a Fourth-stage juverziles (type population): Body vicariantspecies of X. insigne inthat area. onlyslightly curved, but curvature more pro- ..Yiphinema savanicola n.sp. appears to be nouncedposteriorly ; diameter at mid-body mainlyassociated with Gramineae and may 29 pm (25-34). Cuticle, labial region, spear and constitute a species characteristic of the natural oesophagus similar to those of female. Tail simi- Savannah of intertropical Africa ; thisspecies lar in shape to the female tail, but less pointed appearscapable of secondaryadaptation to at the terminus whichis rounded, with plain artifically planted grasses of golf greens (Malawi cuticule.Three caudal pores. . population).Specimens found around peanut (Senegal),tomato (Gambia) or young palm- HOLOTYPE: female,. slide'2518 deposited at the tree(Ivory Coast) may be associated with Laboratoiredes Vers,Muséum national d'His- grasses which were in each case present at the toire naturelle, 43, rue Cuvier, Paris. samplingpoints, and in any case thesecrops

Revue Nématol. 3 (2) : 243-269 (1980) 26 1 M. Luc & .J. F. Southey

AXlS 2

+2 8

insigne

O AXlS 1

-2

-4

-6 savanicola

-6 -4 -2 O +2 +4 +6

1 Fig. 7. Distribution of 30 populations of Xiphinema and three type specimens of X. insigne Loos relative to the first two axes of a canonical variate analysis using population means of five morphometric characters : L, V, c',

odontostyle length, odontophore length. The circles are drawn from 95 % confidence radii (r) where r = n is the sample size. L = lectotype, Pl = Florida paralectotype, P2 = Riverside paralectotype. Variability of Xiphinema insigne and X. elongatum; X. savanicola n. sp.

have been established on typical Savannah soils. thepotential for separation)is accounted for The specific name savanicola for this new species bythe first two axes and 95.2% by the first was suggested by these observations. The diffe- threeaxes, so thereis no advantage in going rent populations m,easured and observedshow further. Spatial positions for the lectotype and close similarities. The Malawi population differs two of theparalectotypes of X. insigne have slightly in its shorter stylet and the Gambian alsobeen plotted ; their wide spacingreflects female is only tentatively ‘referred to the new the observedvariabilit? among the fewspeci- species due to its greater body and spear lengths.mens in relationto that of the other populations. One pointmust beemphazised : despite the Thegraphs clearly accord withseparation position of thevulva, constantly anterior to intothe three species ; they also suggesttwo mid-body(mean value of Vfor al1 females subgroups within X. elongatum (see p. 257) and measured : 39.1),.the anterior genital branch somepossible subdivisions of ,Y. insigne as is nlost often longer than the posteriorone. discussed , on p. 252. Table 7 gives ‘importance values’ for each of the five characters obtained by multiplying the appropriate loading used in Noteon canonical variate analysis (CVA) the analysisby thestandard deviation of the populationmeans for eachcharacter. This This form of multivariate analysis (Seal,1964 ; shows that relative tail length (c’) and odonto- Blackith & Reyment, 1971) has particular value stylelength contributed most to separation in groups in which heavy reliance is placed on onaxes 1 and2, whilebody-Iength (L) and morphometric features in differentiatingspecies, V-value contributed most on axis 3. as is the case in genus Xiphinerna. It provides anobjective means of assessing therelative Table 7 similarity of individuals and populations on the “Importance values” * for five variates used basis of selecteda combination of variates in canonical variate analysis of 30 populations of Xiphinema (characters)but cannot make use of morpho- ,- logical featuresunless they can be expressed (axis)Canonicalvariate 1 2 3 quantitatively. CVA was used to analyse measurement data L 0.11 0.65 1.O3 for 30 X{phinerna populations comprising eight V. 0.74 0.44 1.88 “ 2.50 2.04 0.49 assigned to X. insigne, 20 to X. elongaturn and Odontostyle length 1.58 1.88 0.53 two to the new species X. savanicola. For this Odontophore length 0.67 0.86 0.55 purpose five characters were chosen from those for which data were availxble (Tables 1, 3, 6) as * “Importance value” = CVA loading x SD of variate beinguseful inidentification of Xiphinerna

species, namely L (mm), ’ V, c’, odontostyle Thecomputer program included a single- length (Pm) and odontophore length (Pm). linkagecluster analysis (Gower & Ross,1969) Fig. 7, tracedfrom the computer printout, the results of which were printed out as a den- sho’ws the two-dimensional placing of the 30 po- drogram (Fig. 10). This shows the clustering of pulationsrelative tothe first two axes of the the populations at different levels on a scale of CVA basedon population means for the five similarity.The similarity values, S, between variates.Figure 8 isa similar plot for axes 1 each pair of populations were obtained from the and 3, showing additional separation for a few Mahalanobis’distances, Dl calculatedin the populations when theadditional dimension is canonicalvariate analysis [S = (1 - D/20)x introduced(notably X. insigne populations 4 lOO%]. and 10 and X.elongaturn populations 10 and 17) Thethree species areseparated at the 75% and Figure9 is a plotof the individual nematodes level. At the 80% level theIndian (indicum) on thefirst two axes. Five axes are available population of X. insigne and the Malawi popu- for plotting but the results of analysis showed lationseparate from each other and from the that 85.6% of the variance (and thus most of rest of insigne; at the 85% level the Japanese

Revue Nématol. 3 (2) : 243-269 (1980) 263 M. Luc & J.F. Southey -

AXlS 3

+4 10 17

5 21 11 3 2 22

1E 4 .14 l5 16 13 18 -2

-4

-6

-6 -4 -2 +2 +4 +6

Fig. 8. Distribution of 30 populations-of Xiphinemn and three type. specimens of X. insigne Loos relative to axes 1 and 3 of a canonical variate analysis as in Fig. 7 above. 95 y0 confidences circles have been drawn for X. insigne populations only. Numbers 1 and 2 in a squarerefer to X.savanicola ;numbers without circle refer to X.elongatum. L = lectotype, Pl = Florida paralectotype, P2 = Riverside paralectotype of X. insigne.

264 Variability of Xiphinema insigne and X. elongatum ; X. savanicola 12. sp.

AXlS +1 O 2 insigne

a +8 BB

BB m BB rn B B B'B B B +6 BB BBB BB B

O BB B I B m..

+4 B. @: A m BB B YB A BB AA AA A A AA UB A A AAA A B AAAA AA A 8 +* A AA AA AA AA A A A B AAAA A A A A AAA A A A ,. A AA AAAA A A A AAAA A A A O AAA A AAA AA . AAA AXlS 1 A A A AA A AA A A A AAA AA AAA AAAAA AA AA AA AAA -2 A AAAA AAA AA A A A AA A A AA AA A AA AA -4 A A

elongatum A

AA -6 savanicola

-8

-8 -.6 -4 - O +2 +4 ' +6 +8 +10 Fig. 9. Distribution of individual nematodesof 30 populations of Xiphinema, and three typespecimens of X. insigne Loos, relative to the first two axes of a canonical variate analysis as in Fig. 7 above. L = lectotype, Pl = Florida paralectotype, P2 = Riverside paralectotype.

Revue Nématol. 3 (2) : 243-269 (1980) 265 M. Luc dl- J.F. Southey

ORIGIN OF bearing in mind that some species are described POPULhTlONS SPECIES on the basis of few individualsand, as White 10 111dia 9 Tiiails~~d (1954) has pointed out, a very unequal sex ratio 7 rvl;lur~lills does notnecessarily imply parthenogenesis. G Pl~ilippi~lcs X insigne 4 N.C:trolina However,parthenogenesis certainly occurs in 5 C.lliI‘ornia Xiphinema (Dalmasso, 1970), and is well known 3 Ja1x1,t in other plant nematode genera (Triantaphyllou ------8 Malawi 13 hlor:lnlbiqoc & Hirschmann, 1964, 1978).Inevitably it J5 blaurilios presents diffkulties for the taxonomist because Jh 3lsuritio’j 14 ~lJ,l~~:,sc~lr it isincompatible with the so-calledclassical S Nigcri:, (biological) species concept based on interbreed- ing and gene interchange (White, 1954 ; Mayr, 19 Tll~~il.~l~d 13 2;tnlbi.t 1969 ; Enghoff,1976). To quote White (1954), 9 Rhodcsin “. . . a parthenogenetic speciesis notreally 23 Fiji .Y.rlongaftort 10 Pllilippincs equivalentto a bisexual one since it consists II llllodcsi.1 . of an indefinite number of biotypesbetween IO Rllodcni;r which no exchange of genes is possibleand which 2 sellrgal 21 C;tpe Verde 1s. will continue to diverge in the course of evolu- 3 Senes.ll tion as one mutation after another establishes 5 Uppcr Volln ci Togo1:lnd itself in the different lines of descent.” 4 1rwryCa:tct According toWhite (1954) then, one ‘might ------17 hhuririuc 2 Nlgeria expect to observe in constantly parthenogenetic ____c__,vory Conct 1 x. sasntricu/o 11 sp. (i.e. thelytokous) groups a more or less contin- 70 80 90 lm uous series of slightly differing forms, the kind -Scale of rilnil.lrily of situation in fact that occurs in certain apo- Fig. 10. Dendrogram showing theclustering of 30 micticplant genera such as flieracium and populations of Xiphinema, comprising X. elongatum, Rubus. But this picture does not seem to cor- X. insigne and X. savanicola n. sp. at different levels of similarity as computed by canonicalvariate analysis respond to the case of the three species consi- of five morphometriccharacters. On the scale dered in this paper. These species are certainly. 100 = perfect similarity. close morphologically ; they can al1 be assumed to be thelytokous(in the several populations and Californian populations of X. insigne toge- inwhich rare males have been observed,no ther separate from the ‘North Carolina popula- females contained spermatozoids) ; two of them tion and from a group comprising the Thailand, (A-. insigne and X. elongatum) are well known Philippinesand Mauritius populations, and andpan-tropical in distribution ; thethird, X. elonga.tum dividesinto the two groups X. savanicola, perhapsrepresent a “vicariant” mentioned on p. 257 with population 10 (Rhode- of X. insigne. The three species are suffkiently sia) also separating at this level. clearly distinguishable from one another as to leaveno doubt of their separate identity ‘and results of canonicalvariate analysis (page 262 and Figs. 7-10) support. this view. Thus they appear The problem of thelytokous species to be a small group of close but quite distinct forms rather than a large clusterof clona1 popu- The genus Xiphinema already contains about lations differing slightly, and often marginally, 110nominal species and it isprobable that from one another, as White (1954)would lead many moreremain to bedescribed mainly in us to expect. thetropical and subtropical areas where the genus is most prevalent. In about 75% of the But,in practice, the observed pattern of described species males are very rare or unknown divergence in parthenogenetic groups will pre- suggesting that parthenogenesisis common. sumablydepend on the, rate of mutation and

. . , Caution.is needed-in making. .this assumption, the tjme- scale-over which mutation. occurred. has

266 Nématol. Revue 3 (2): 243-269 (1980) Variability of Xiphinema insigne and X. elongatum; X. savanicola n. sp.

And if one assumes that the three species had a methods forclarifying resemblances or differ- common thelytokous ancestor, one might expect ences. To nematode taxonomists, optical micro- to observe signs of further divergence (in time) sopyis an “ordinary means” (the usual one), within them. In fact, resultsof Our study suggest scanning electron microscopy (S.E.M.) may be that this is takingplace, especially in X. insigne becoming so for some groups, but transmission (seepage 253) where about fivemore or less E.M. for example, is not- as yet. distinct morpl1ological variants seem to be Karyological (chromosomal) analysis is valu- recognizable which might be shown by further able, for example to show where polyploidy has work, to merit morphospecific status. In X. elon- given rise to thelytokous forms, as in the work gatum toothere are signs of divergence into of Cuanyand Dalmasso (1975) and Trianta- ’. perhaps two groups of rather continuously vary- phyllouand Hirschmann (1978) on the Hete- ing populations ; too few populations of X. sava- roderatrifolii complex.Populations identified nicola havebeen studied as yet to assess the as H. trifolii includediploid amphimictic, and situation in this species. triploidand tetraploid parthenogenetic forms, The question now arises, what definition of a the latter types beingclosely related to other species is capable of encompassing thelytokous described and undescribed parthenogenetic spe- forms ? Thatrecently proposed by Cronquist cies. Triantaphyllouand Hirschmann (1978) (1978) seems to us to offer a commonsense solu- conclude that this complex represents “a con- tion : “Speciesare the smallest groups that are glomerate of manyindependently evolving

consistently and persistentlydistinct, and distin- populations” whichneed taxonomicrevision. ’ guishableby ordinary means. “Cronquist reco- Some cytologically different forms appear not to gnizes,of course, that such terms as “consist- bereadiiy distinguishable morphologically, i.e. ently”, “persistently” and “ordinary means”beg are sibling species. questions and need qualification, but, as he says, The sibling species concept, which arose from theyset “the limits.within taxonomists can insistenceon genetic isolation as the prime reasonably disagree”. “Smallest group” implies criterion for species, is regarded by Cronquist as rejection of the subspeciesconcept; butit is “an embarrassment to the system”, though he commonexperience, at least so faras plant- admits that some sibling species may be accept- parasiticnematodes are concerned, thatsub- able (and, among nematodes it may sometimes species end,more or less rapidly,by being be of practicalvalue to name sibling species elevated to species. “Co~zsistently” means that which can be distinguished by markeddifferences “all, or avery large proportion,of the individuals in pathogenicity or host range ; perhaps obser- under consideration clearly belong to one group vation of these differencesshould then be or another,and not somewhere inbetween”. regarded as “ordinary” means). To Say that al1 “Persistently” means that “theremust be a or most species are reproductively isolatedis not reasonable assurance that al1 or a vast majority the sameas saying that al1 reproductively of the offspring of members of a given species isolatedpopulations must be accepted as spe- will alsobelong to this species,for the fore- cies. It remains true that reproductive isolation seeable future”. Cronquist gave as an example, is essential for stable speciation (i.e. to satisfy the brownbear and the black bear : they Cronquist’scondition of persistence),though are b‘consistently’’ distinct,but not “persis- the isolationneed not necessarily be strictly tently”, because they can interbreed and have genetic - cf. certainorchid species (again a fertile progeny, with mixed characters ; thus mentioned by Cronquist, 1978) that are isolated they cannot represent distinct species. Concern- mainlyby adaptation to specificpollinators. ingthelytokous species theirpersistency is Thereis less of aproblem with thelytokous the crucial point. “Ordinary means” will clearly morphospecies once this argument is accepted. Vary with the groupunder consideration, e.g. They are certainly fully isolated genetically, but with bacteria, biochemical and serological crite- the fact that individuals and clones within such riaare standard, whereas with plant-parasitic species are equally isolated does not make these and free-living nematodes such techniques must the truespecies. However, this peculiar situation be regarded as research tools or supplementary whichresults from constant parthenogenesis

Revue Némafol. 3 (2): 243-269 (1980) 26 7 M. Luc LE J.F. Southey

~ ~~

does mean that signs of intraspecific divergence BLACKITH,R. E. Ji: REYMENT,R. A. (1971). Multi- areto be espected,and we havepointed to variatenzorphometrics. London & New York, Aca- evidencefor this in X. insigne particularly. demic Press, 412 p. Thereis of coursescope here as elsewhere for CARVALHO, J. C. (1962). Observaçoes emtorno de duas especies de Xiphinema. Arq. Inst. biol. Sao difference of opinionbetween lumpersand Paulo, 29 : 217-221. splittersamong tasonomists, and it isalways COHN, E.(1969). The occurrence anddistribution of possible thatintermediate populations will be species of Xiphinema and Longidorus in Israel. Ne- discovered, leading to synonymy, but such cases matologica, 15 : 179-192. seem .infrequent ; among more than 75 appar- COHN, E. & SHER,S. A. (1972). ,A contributmionto entlythelytokous species of Xiphinema only .the taxonomy of the genus Xiphinema Cobb, 1913. one recentexample has been traced, viz. the J. Nematol., 4 ; 36-65. synonymization of X. denoudeni Loof & Maas, CRONQUIST,R. (1977). Once again, what is a species? 1972with .lcrugi Lordello,1955 (Lamberti In : Beltsuille Symposia in Agricultural Research. (2) X. Biosystematics in Agriculture., New York, Chichester & Tarjan, 1974 ; Luc & Hunt, 1978). Brisbane & Toronto, John Wiley & Sons : 3-20. To sumup, we conclude that thelyt,okous CUANY, A. & DALMASSO,A. (1975).Caracteres et species which can be clearly defined by morpho- spécificité de deux espèces biologiques d’Heterodera logical and morphometric characters should be se développant sur Dianthus caryophyllus. Nematol. accepted as valid according to Cronquist’s (1978) medit., 3 : 11-21. definition. Inthe examplesdescribed inthis DALMASSO,A. (1970).La gamétogenese des genres paper,canonical variate analysis has proved Xiphinema et Longidorus (Nematoda : Dorylaimida). C. r. hebd. Séanc. Acad. Sci., Paris, Sér. D, 270 : useful in helping to define thelimits of such 824-827. species ; it hasalso been used, for example in the ÈNGHOFF,H. (1976). Taxonomic problems in partheno- genus Globodera (Green, 1971 ; Evans & Franco, genetic animals. Zool. Scripta, 5 : 103-104. 1978) and ‘it might be applied with advantage EVANS,K. & FRANCO,J. (1978). Morphological vari- to other nematode groups. We agree with Loof ation in some populations of potato cyst-nematodes (1970) as to the necessity to describe and name from Europe and South America. Nematologica, 23 morphologically distinct populations or groups (1977) : 417-430. of populations (morphospecies) so as to provide GOWER,J. C. Ji: Ross, G. J. S. (1969). Minimum a basis on which cytologists and other specialists spanningtrees and single-linkage clusteranalysis. can work (see Triantaphyllou and Hirschmann, Appl. Statistics, 18 : 54-64. 1978) and we accept.that revisionwill often GREEN,C. D. (1971). The morphology of the terminal area of the round cyst nematodes, s.g. Heterodera be necessary as a result. rostochiensis and allied species. Nematologica, 17 : 34-46. ACKNOWLEDGEMENTS HEYNS,J. (1974). Thegenus Xiphinema inSouth Forthe loan of type specimens for study we are Africa. II. X. elongatum group (Nematoda : Dory- indebtedto C.A. Loos, A. C. Tarjan, the late S. A. laimida). Phytophylactica, 6 : 249-260. Sher,and M. R.Siddiqi. We also thanknumerous JAIRAJPURI,M. S. & BAJAJ,H. K. (1978). Observations other nematologists, cited in the text, Who have sent on the biology of Xiphinema basiri and X. insigne. nteresting material of the species studied. Thanks are RevueNématol., 1 : 327-239. ’ due to C. F. Banfield, K. Ryder and other colleagues KHAN,E., CHAWLA,M. L. & SAHA,M. (1978). Cm- of theStatistics and Computer Departments at Ro- ments on the classification of t.he Longidoroidea thamsted Experimental Station for canonicil variate (Nematoda) with description of three new species. analysis, otherprocessing of biometric data and advice. Indian J. Nematol., 6 (1976) : 47-62. J. J. M. Flegg’srole atthe outset of thestudy is mentioned on page 244. We are particularly indebted LAMBERTI,F. & TARJAN,A. C. (1974). Xiphinema to M. R. Siddiqi for permission to use some of his costaricense n. sp. (Longidoridae, Nernatoda), a new original drawings of X. insigne. species of dagger nematode from CostaRica. Ne- matol. medit., 2 : 1-11. LOOF,P. A. A. (1970). Morphological variationand the species concept. Zesz. probl. Postep. Nuuk. roln., REFERENCES no 92 : 489-496. BAJAJ,H. K. & JAIRAJPURI,M. S. (1977). Variability LOOF,P. A. A. & MAAS, P. W. Th. (1972). The genus within Xiphinema insigne populations from India. Xiphinema (Dorylaimida) in Surinam.Nematologica,

.~ ~- 18 : 92-119. . -. , .. - __ Nematologica, 23 :,33-46. - ~- - - ~ ~- ._

268 Revue Nématol. 3 (2) : 243-269 (1980) Variability of Xiphinema insigne and X. elongatum ; X. savanicola n. sp.

LOOF,P. A. A. & SHARMA,R. D. (1979). Plant para- SIDDIQI,M. R. (1959).Studies on Xiphinema spp. sitic nematodes from Bahia State, Brazil : the genus (Nematoda ; Dorylaimoidea)from Aligarh (North Xiphinema Cobb, 1913 (Dorylaimoidea). Nemato- India) with cornments on the genus Longidorus Mi- logica, 25 : 111-127. coletzky, 1922. Proc. helminth. Soc. Wash., 26 : 151- Loos, C. A. (1949).Notes onfree-living andplant 163. parasiticnematodes from Ceylon. No 5. J. zool. SOUTIIEY,J. F. (1973).Identification of Xiphinema Soc. India, 1 : 23-29. species. In : The Longidoridae, Harpenden, Rotham- LORDELLO,L. G. E.(1951). Xiphinemacampinense, sted Experimental Station : 37-58. nova especie (Nematoda, Dorylaimidae). Bragantia, TARJAN,A. C. & Luc, M. (1963). Observationson 11 : 313-316. Xiphinema insigne Loos, 1949 and Xiphinema elorz- LORDELLO,L. G. E.(1955). Xiphinemakrugi n. sp. gatum SchuurmansStekhoven & Teunissen, 1938 (Nematoda, Dorylaimidae) from Brazil with a key (Nematoda : Dorylaimidae). Nematologica, 9 : 163- to species of Xiphinema. Proc. helminth. Soc. Was- 172. hington, 22 : 16-21. TIIORNE,G. (1939). A monograph of thenematodes Luc, M. & DALMASSO,A. (1975). Considerations on of the superfamily Dorylaimoidea. Capita Zool., 8 : the genus Xiphinema Cobb, 1913 (Nematoda, Lon- 1-261. gidoridae) and a “lattice” for the identification of species. Cah. ORSTOM, Sér. Biol., 10 : 303-307. TI”, R. W. (1965). A‘preliminary suruey of the plant Luc, M. & HUNT,D. J. (1978).Redescription of parasitic nematodes of Thailand and the philippines. Xiphinemalongicaudatum Luc, 1961 and obser- Bangkok, S.E.A.T.O.,71 p. vations on Xiphine~na krugiLordello, 1955 (Nema- TRIANTAPHYLLOU,A. C. & HIRSCIIMANN,H. (1978). toda : Longidoridae). Nematologica, 24 : 1-18. Cytology of the Heteroderatrifolii parthenogenetic MAYR, E. (1969). Principles of systematic zoology. New species complex. Nematologica, 24 : 418-424. York, McGraw Hill, 428 p. WHITE,M. J. D. (1954). Animal cytology and euolution. SAIGUSA,T. & YAMAMOTO,Y. (1971).[Distribution (2nd Edition). Cambridge Univ. Press, 454 p. and hosts of a dagger nematode, Xiphinema insigne Loos, detected on export lily bulbs.] Res. Bull. Pl. WILLIAMS,J. R. (1959). Studies on the nematode soi1 Protect. Seru. Japan, 9 : 27-38. fauna of sugar-cane fields inMauritius. 3. Dory- SCHUURMANS STEKHOVEN,J. H. & TEUNISSEN,R. J. H. laimidae (Dorylaimoidea, Enoplid,a).Occ. Pap. Mau- (1938). Nématodes libres terrestres. Eql. Parc Natl. ritius. Sugar Ind. Res. Inst., 3 : 1-28. Albert ; Mission G. E. de Witte ; Inst.Parcs Nat. WILLIAMS,J. R. & Luc, M. (1977).The species of Congo Belge, Bruxelles, 22 : 1-229. Xiphinema Cobb, 1913 (Nematoda : Longidoridae) SEAL, H. L. (1964). Multiuariatestafistical analysis inthe sugar-cane fields of Mauritius. Occ. Pap. for biologists. London, Methuen & Co., 207 p. Mauritius Sugar Ind. Res. Inst., 30 : 1-19.

Accepté pour publication le 21 mars 1980.

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