Comparative morphology of Globodera, Cactodera, and Punctodera spp. () with scanning electron rnicroscopy@) Abubaker A. OTHMAN”,James G. BALDWIN**and Manuel MUNDO-~CAMPO** * Departwent of Plant Protection, University of Gayounis, Facztlty of Agriculture, PO. Box 919, El Beida, Libya and ** Department of Nematology, University of California, Riverside, c4 92521, USA.

SUMMARY

Second-stage juveniles (J2), males,and females of , G. solanacearunl, G. virginiae, G. tabacum, G. pallida, , C. eremica, C. weissi, C. betulae, Punctodera punctata and P. chalcoensis were examined with the scanning electron microscope (SEM) to discover and clarify characters which may be useful for phylogenetic analysis of Heteroderidae. Certain features of lip patterns are useful for defining al1 three genera. However, intraspecific variation may have resulted in previous misrepresentation of lip charactersfor some taxa. Monophyly ofGlobodera, Cactodera, and Punctodera is supported by the relatively small labial discand trend toward fusionof al1 lips in males. Monophyly ofGlobodera may be supported by protuberances on the female head region, Cactodera by reduced lateral lips in 52, and Punctodera by fusion of submedial lips with the labial disc and adjacent head annules. The unique en face pattern of J2 of C. betulae may indicate a transformation series between Cactodera or Punctodera, and . The position of phasmids in J2 and posterior termination of lateral lines in J2 and males indicate differencesamong heteroderid species, but maynot be useful for defining genera or phylogenetic analysis of the family. Comparative morphological-developmental investigations of overall cuticular and perineal patterns of females and cysts include promising characters for interpreting phylogeny but will best be evaluated with insight into changes with age.

RESUME

Morphologie compareé d’espèces des genres Globodera, Cactodera et Punctodera au wicroscope e7ectronique à balayage

Des juvéniles de deuxième stade (J2), des mâles et des femelles de Globodera rostochiensis, G. solanacearum, G. uirginiae, G. tabacum, G. pallida, Cactodera cacti, C. eremica, C. weissi, C. betulae, Punctodera punctata et P. chalcoensis ont été examinés au microscopeélectronique à balayagepour découvrir et préciserles caractères qui pourraient&Ire utilisés pour une analyse phylogénique des Heteroderidae. Certains caractères de la figure Iabiale H (en vue de face) sont utilisables pour la définition de chacun de ces trois genres. Toutefois, la variation intraspécifique a parfois antérieurement conduit à une représentation erronée des caractères labiaux chez certains taxa. La monophylie de Globodera, Cactodera et Punctodera est suggérée par un disque labial relativement petit et une tendance à la fusion des lèvres, chez le mâle. La monophylie de Globodera peut s’appuyer sur les protubérances de la région céphalique des femelles; celle deCactodera sur la réduction des lèvres latérales chez les52; et celle de Punctodera sur la fusion des lèvres submédianes avec le disque labialet les anneaux céphaliques adjacents. La (( figure labiale n, unique, des J2 de C. betulae pourrait indiquer une variation en chaîne entre Cactodera, ou Punctodera, et Heterodera. La position des phasmides chez lesJ2, et la terminaison postérieure des lignes latérales chez lesJ2 et les mâles sont révélatrices de différences parmi les espèces d’Heteroderidae, mais ne peuvent être utilisées, ni pour la définition des genres, ni pour une analyse phylogénique de la famille. Des observations comparatives sur la morphologieet le développement de la cuticule et des caractères périnéaux des femelles et des kystes a révélé des Caractères prometteurs pour l’interprétation de la phylogénie, mais qui seront mieux évalues à la lumière des changements liés à l’âge.

(1) This research supportedin part by the Libyan people, theUS National Science Foundation Grant 84-157627, and California Department of Food and Agriculture.

Revue Néinatol. Il (1) :53-63 (1988) 53 A. A. Othman, J. G:Baldwin & M. Mundo-Campo

Globodera Skarbilovich, 1959 (Behrens,1975) was The stages were processed for SEM by glycerin infil- introduced to accommodate cyst-forming heteroderids tration(Sher & Bell, 1975) and criticalpoint drying with females that are spherical, lack a terminal protru- (Othman & Baldwin, 1985); figures 1-5 are al1 of speci- sion, and lack an egg matrix. Subsequently, Punctodera mens prepared by glycerin. Mulvey and Stone, 1976 was erected to accommodate specieswith anal and vulval fenestrae inthe cysts, Results followed by Cactodera Krall & Krall, 1978 with only vulval circumfenestrae. HEADMORPHOLOGY Severalphylogenetic relationships have beenpro- posed among thesegenera but only a littleprogress En face patterns of J2, males, and females of Globo- has been made sinceLuc, Taylor and Cadet (1978) dera,Cactodera, and Pzmctodera arevariable among suggested that Heteroderidae classification is artificial species and stages; however, in al1 species, the pattern and inconsistent, partially because it is based on insuf- is based on a labial disc surrounded by six lips (two ficient data including morphology. There are limited com- lateral and four submedial).En face patterns of 52 of al1 parative SEM morphologicalobservations of Globodera, three genera have on ovoid labial disc and lateral lips Punctodera and Cactodera (Green, 1971; 1975; Mulvey, may fuse with the labial disc. Globodera rostochiensis, G. 1973a,b; Stone, 1975) andsome studies restricted to solanacearum, G. virginiae, G. tabacum, and G. pallida description of a single species (Wouts, 1984; Baldwin each include variable J2s with en face patterns having & Bell, 1985); however, use of these findings for in- both separated and fused lips (Fig. 1 A-1). However, al1 terpretingphylogeny is limited by incompleteness. six lips are typically separate in J2 of G. rostochiensis For example,details may be obscured by poorquality (Fig. 1 A), whereas most commonly submedial lips are of preparation, and often toofew specimens have been fusedin J2 ofG. solanacearum, G. virginiae and G. examined to discuss variability. In this study we report tabacum and G. pallida (Fig. 1 DyF, H, 1). detailed SEM morphological comparison of characters In J2 of C. cacti, C. weissi, and C. eremica al1 lips are including en face patterns, lateral fields, tails, and sen- generally separate and lateral lips are reduced in size sory openings of second-stage juveniles (J2) and males (Fig. 1 K-M). Rare individual J2 of C. cucti existhow- as well as en facepatterns of females. These characters, ever, in which submedial lips are fused on one side of which may be useful for phylogenetic analysis (Stone, the labial disc (Fig. 1 10. Llp patterns of J2 of C. betulae 1975, 1979; Ferris, 1979, 1985; Wouts, 1985), are are similar to those of P. punctata and P. chalcoensis. describedfor eleven species representing Globodera, These consist of adjacentsubmedial lips that fuse Cactodera, and Punctodera. Cuticular and perineal pat- completely with each other and partiallywith the labial terns of females andcysts are excluded fromthe present disc; lateral lips are distinct and may also partially fuse report because preliminary observations indicated de- with the labial disc (Fig. 1 N-P). Typically, fusion also tailedcomparisons among taxawere confounded by occurs between submedial lips and the adjacent head changes with development and age of individuals (0th- annule in C. betztlae, but not in Punctodera spp. man, 1985). Terminology for en face patterns and charac- En face patterns of males of Globodera,Cactodera, ter States is as previously described (Baldwin, 1986). and Punctodera also vary among species. Unlike 32, how- men these new observations are considered with pre- ever, the labial disc is circular (v~elongate) and typi- vious studiesof cyst and noncyst-forming Heteroderidae cally separated from lips(Fig. 2). In malesof G. rosto- (Green, 1971; Mulvey, 1973a,b; Stone, 1975; Momota chiemis adjacent submedial lipspartially or completely _- & Oshima, 1976; Baldwin, Mundo-Ocampo & Othman, fuse with each other and with lateral lips tending to form 1983; Baldwin & Bell, 1985; Othman & Baldwin, 1985, a continuous annule (Fig. 2 A). Individuals exist, ho- 1986; Othman, Baldwin & Bell, 1986) thecombined wever, in which adjacent submedial lips are separate (Fig. data can be used for furthertesting and refining hypo- 2 B). The lateral lips, whichencircle clearly marked theses of phylogeny of the family. amphid openings, arealso clearly demarcated (Fig. 2 A). In males of G. solanacearum, G. virginiae, and G. Materials and methods tabacum adjacent submedial lips are either separate or fused on oneor both sides of the labial disc. The lateral Second-stage juveniles, males, and females of Globo- lipsare typically separate from submedial lips (Fig. dera rostochiensis, G. solanacearum: G. virginiae: G. 2 C-H), and there may be sometendency for lateral lips tabacum: G. pallida,Cactodera cacti, C. eremica, C. to fuse with the labial disc in G. virginiae (Fig. 2 E, F). weissi, C. betulae, Punctodera punctata,and P. chalcoen- Males of G. pallida typically have fused adjacent sub- sis were collected from the sources indicated (Tab. 1). medial lipswith separate lateral lips (Fig.2 1). Cactodera cacti and C. zoeissi have adjacent submedial lips separate * AIthough Stone(1983) proposed these as subspeciesof G. from each other,but in C. weissi they are partially fused rostochiensis, the recommendation has not yet been widely with lateral lips (Fig.2 J-K). Cactodera betulaeis unique adopted. among the three genera examined with partial to com-

54 Revue Nérnatol. 11 (1) : 53-63 (1988) Morphology of Globodera, Cactodera and Punctoderi with SEM

Table 1 Species and number of Globodera spp., Cactodera spp., and Punctodera spp. examined and their source.

~~ ~ Host SourceExamined Nuniber Globodera rostochiensis Corne11 University 50 juveniles (Wollenweber, 1923) Solanuni tuberosum L. Ithaca, NY 19 males Behrens, 1975 18 females G. solanacearum Horse nettle North Carolina State 100 juveniles (Miller & Gray, 1972) Solanum carolinense L. University, Raleigh, NC; 10 males Behrens, 1975 Virginia Polytechnical 100 females Institute, Blacksburg, VA G. virginiae Horse nettle North Carolina State 100 juveniles (Miller & Gray, 1968) Solanum carolinense L. University, Raleigh, NC; 1O males Behrens, 1975 Virginia Polytechnical 80 females Institute, Blacksburg, VA G. tabacunz Tobacco Virginia Polytechnical 50 males (Lownsbery & Lownsbery, 1954) Nicotiana tabacunz L. Institute, Blacksburg, VA 20 juveniles Behrens, 1975 150 females G. pallida Potato Virginia Polytechnical 40 males (Stone, 1973) Solanunl dulcamara L. Institute, Blacksburg, VA; 45 juveniles Behrens, 1975 S. tuberosum L. Rothamsted Experimental Station, 25 females England; International Potato Center, Lima, Peru Cactodera cacti Division of Plant Industry, 350 juveniles (Filipjev & Schuurmans Cereus speciosissi~nusDC. Gainesville, FL 1 male Stekhoven, 1941) (UC Riverside greenhouse culture) 20 females Krall & Krall, 1978 C. eremica Shadscale Cedar Valley, Utah 60 juveniles Baldwin & Bell, 1985 Atriplex confertifolia (UC Riverside greenhouse culture) 1O males (Torr. & Frem.) Wats 2 females C. weissi Polygonunz hydropiperoides BARC-W 60 juveniles (Steiner, 1949) Miclur. Beltsville, MD 8 males Kra11 & Krall, 1978 20 females C. betulae Betulae pubescens Ehrh. University of Arkansas 320 juveniles (Hirschmann & Riggs, 1969) Fayetteville, AR 10 males Krall & Krall, 1978 (UC Riverside greenhouse culture) 40 females Punctodera punctata Annual bluegrass New Jersey 30 juveniles (Thorne, 1928) Poa annua L. 8 males Mulvey & Stone, 1976 i5 females P. chalcoensis Maize Michoacan, 30 juveniles Stone, Sosa-Moss & Zea mays L. 9 males Mulvey, 1976 60 females

plete fusion of nearly al1 lip parts with each other and surrounded by a circular plate formedby fusion of lips adjacent head annules (Fig. 2 L-M). In en face patterns (Fig. 3 A, B). Lateral lips however, are clearly demar- of males of P. punctata and P. chalcoensis adjacent cated in G. solana.ceamm, G. virginiae, G. tabacum, and submedial lips are completely fused with each other as P. chalcoensis (Fig. 3 B). In G. rostochiensis, C. erernica, well as with lateral lips (in most individuals) to form a and P. punctata the lateral lips are not clearly demar- continuousannule surrounding the labial disc cated(Fig. 3 A). In females of al1 GZoboderu spp. (Fig. 2 N-P). transverse rows of protuberances occur posterior to the En face patterns of females of Globodera, Cactodera, lip region (Fig. 3 C, D); these protuberances were not and Punctodera are quitesimilar in al1 species. The labial observed in other genera. disc is oblong to rectangular. It is elevated above and

55 Fig. 1. En face pattern of second-stage juveniles of Globodera spp., Cactodera spp., and Punctodera spp. A : G. rustochiensis, common; B : G. rostochiensis, varient; C : G. solanacearum, common; D : G. solanacearunz, varient; E : G. virginiae common; F : G. virginiae, varient; G : G. tabacunl, common; H : G. tabacum, varient; 1 : G. pallida; J : C. cactc common; K : C. cacti varient; L : C. eremica; M : C. weissi; N : C. betulae; O : P. punctata; P : P. chalcoensis.

56 Revue Néynatol. 11 (1) : 53-63 (19881 Fig. 2. En face pattern of males of Globodera spp., and Punctodera spp. A : G. rostochiensis, common; B : G. rostochiensis, varient; C : G. solanacearuw, common; D : G. solanacearunl, varient; E : G. virginiae, common; F : G. virginiae, varient; G : G. tabacum, common; H : G. tabacum, varient; 1 : G. pallida; J : C. cacti; K : C. weissi; L : C. betulae, common; M : C. betulae, varient; N : P. punctata; O :P. chalcoensis, common; P : P. chalcoensis, varient. Revue Neinatol. Il (1) :53-63 (1988) 57 A. A. Othman, J. G. Baldwin & M. Mundo-Canzpo

LATERALFIELD AND PHASMIDS (Fig. 5 H, 1). Phasmid openings were not confirmed in males of any of the six species (Figs 4, 5). The lateral field of J2 of Globodera, Cactodera, and Punctodera species examined originates as one, two, or Discussion three areolated bands, about nine to thirteen annules posterior tothe labial disc. At midbody it consists of four SEM examination of J2 and adults of eleven species incisuresdelineating three longitudinal bands. The of Globodera, Cactodera, and Punctodera revealed new middle band is smooth whereas the outer two bands are characters that can be used in conjunction with other areolated, although in some cases areolations are faint. characters for testing phylogenetic relationships among The lateral field changes little throughout the lengthof Heteroderidae genera. For example, the en face region thenematode except in the area near the phasmid of males of Globodera, Cactodera (including lip patterns openings. In this region the middle band ends about of C. eremica as described in Baldwin and Bell, 1985), twelve totwenty annules anterior tothe tail end and Punctodera are variable within and among species (Fig. 3 E-O); in C. cacti, C. eremica and C. weissi the and genera and yet they share some tendencies which middle band tends to persist very near to the terminus make their patterns distinctive among Heteroderidae. of the lateral field (Fig. 3 J-L). Phasmid openings typi- These tendencies include arelatively small labial disc (e. cally are about five toseven annules anterior to the end g. vs males of Sarisoderahydrophila and Rhizonema of the lateral field (Fig. 3 E-O). Where the phasmid sequoiae, discussed in Othman andBaldwin, 1986), and opening occurs with three bands in the lateral field, it a trendtoward fusion of al1 lips to forma relatively thick typically is asymmetricbetween bands (Fig. 3 J-K), continuous lip annule, as expressed in G. rostochiensis whereaswith two bandsit is more likely tooccur and most completely in C. betulae. These derived pat- centrally in the lateral field on the incisure (Fig. 3 E, F, terns are unlike the highly specialized patterns of the M). The tail tip is narrower and more attenuated in J2 other cyst-forming genus, Heterodera, and noncyst form- of Punctodera than in Cactodera (Fig. 3 J-N). ing heteroderids (Othman, 1985; Othman & Baldwin, The lateral fieldin males of Globodera, Cactodera, and 1985, 1986; Othman, Baldwin, & Bell, 1986) with the possible exception of Verutus volvingentis, a genus of Punctodera is similaramong species and typically consists of three longitudinal bands. The middle band uncertaintaxonomic position (Othman & Baldwin, 1985). Characters of the male lip patterns alone, may is smooth, whereas theouter two bandsare faintly areolated; there is little change throughout the lengthof only offer weak support for monophyly of Globodera, the nematode. The lateral field endsnear the tail Cactodera, and Punctodera; however, in combination terminus and in this region variation in details occur, with other derived characters, such as circumfenestrae the hypothesis is strengthened. even withinpopulations; however, sometendencies Lip patterns of J2 of Globodera and Cactodera are seem to be taxon specific (Figs 4, 5). interpreted as relatlvely primitive, sometimes having six In Globodera the incisures of the lateral field usually separate lips, or moreoften with fusion of adjacent converge immediately anteriorto thelevel of the cloaca1 submedial lips and fusion of lateral lips with the labial openingand the pattern is roundedin lateral view disc. The similarity of these features withJZ of Atalodera (Fig. 4 B-H, J). The end view pattern between the two and Thecavenniculatus is striking (Othman, Baldwin & lateral fields is typically V-shaped lines in G. Bell, 1986), and must be considered in light of other rostochiensis and G. solanacearum, whereas irregular possible shared derived features. These include the D tuberclesoccur in G. virginiae, G. tabacum, and G. layer of the female body wall'in Globodera-Cactodera- pallida (Fig. 4 A-Gy1). In Cactodera and Punctodera the Punctodera, as well as Atalodera-Thecavernziculatus terminus of the lateral field often fades or continues (Cliff & Baldwin, 1985), and certainaspects of the around the terminus by merging with lines of the end syncytial host response. Although Mundo and Baldwin view pattern (Fig. 5 B, DyF, 1, K; MJ. Cactodera cacti, (1984) report evidence that the syncytial host response C. weissi, and C. betulae tend to have lines in end view, evolved independently in thetwo groups, thishypothesis whereas C. erenzica and P.chalcoensis are relatively must be further testedby a phylogenetic analysis of the smooth (Fig. 5 A-G, J, L). The terminus of the lateral family which considers additional characters including field of P. punctata is unusual by its modification to lip patterns. many fine tubercles which continue around the end of Cliff and Baldwin (1985) noted that the taxonomic the tail; connecting the two fields (Big: 5 J, K).- position of C. betulae is uncertain with several charac- The tail end view of al1 species is triangular in shape ters, including absence of a D layer, inconsistent with extending to include the smooth spicule sheath; how- other species of the genus. Similarly, the lip pattern of ever, the sheath is greatlyreduced or absent in G. J2 of C. berulae is distinct from other Cactodera spp. by rostochiensis, G. pallida, C. eremica, C. bettdae and P. the fusion of the labial disc with submedial lips; this punctata (Figs 4 A, 1; 5 C, G, J). Spicule tips are bifid character is shared with Punctodera spp. In addition, in al1 Cactodera spp. but notin Globodera or Punctodera submedial lips are fused with adjacent head annules;

586 Revue Nématol. 11 (1) :53-63 (1988) Fig. 3. Head region of females and tails of second-stage juveniles of GZobodera spp., Cactodera spp., and Punctodera spp. A : En face pattern of c. ere??zicawithout distinct lateral lips; B : En face pattern of G. solanaceamln with distinct lateral lip. Scale asin A; C : Dorsal view of G. rostochiensis with tubercles; D : G. rostochiensis with tubercles; E : Tail of G. rostochiensis; F : Tail of G. solanaceam?; G : Tail of G. virginiae; H : Tail of G. tabacum; 1 : Tail of G. palZidu; J : Tail of C. cacti; K : Tail of C. erenzicu; L : Tail of C. weissi; M : Tail of C. betulue; N : Tail of P. punctata; O : Tail of P. chalcoensis (* = lateral; arrowhead = phasmid opening). Revue Nénmtol. 11 (1) :53-63 (1988) 59 A. A. Othman, J. G. Baldwin & M. Mundo-Campo

Fig. 4. Tai1 region of males ofGlobodera spp. A : G. rostochiensis, end view; B : G. rosrochiensis, lateral view; C : G. so2anaceanW . end view; D : G.-solanaceamm, lateral view; E : G. virginiae, _end vjew; F : G, virginiae, lateral view; G : G. taba_cgm,end view; H : G. ta&cum-zview; Ïy-G. pallida, end view; J : G. palliaai lateral view. Scale in end view (A-G, J) as show%ï for A; scale in lateral view (B-F, 1, K, M) as shown for B.

60 Revue Nénlatol. 11 (1) :53-63 (19881 Molphulogy of Globodera, Cactodera and Punctodera with SEM

Fig. 5. Tai1 region of males of Cactodera and Punctodera. A : C. cacti, end view; B : C. cacti, lateral view; C : C. eremica, end view; D : C. eremicu, lateral view; E : C. weissi, end view; F : C. weissi, lateral view; G : C. betulae, end view; H : C. betulae, enlargement of bifid spicule tip from 1; 1 : C. betulae, lateral view; J : P. punctata, end view; IZ : P. punctata, lateral view; L : P. chakoensis, end view; M : P. chahensis, lateral view. Scale in l-G, J, L as shown for A; B-F, 1, K, M as shown for B.

Revue Nérnatol. 11 (1) :53-63 (1988) 61 A. A.Othman, J. G. Baldwin & M. Mundo-Campo

among cyst-forming genera this feature is only shared genus. Stone recognized variationin Globodera spp. with with Heterodera spp. (Othman, 1985). These findings respect to fusion or lack of fusion between submedial may indicate the en face pattern of J2 of C. betulae is lips. However, six separatelips were illustratedand intermediate in a transformation series between Cacto- designated the type 1 pattern to which Globodera was dera or Punctodera, and Heterodera. Bifid spicule tips are ascribed; Our observations indicate that, with the ex- shared by Cactodera including C. betulae and Heterodera ception of G. rostochiensis, the typical Globodera pattern but do notoccur in Punctodera or othercyst , has fused submedial lips, as has been also demonstrated perhaps, further supporting a link between Cactodera for G. zelandica (Wouts, 1984). and Heterodera. The position of phasmids in J2and posterior termin- Monophyly of Globodera may be supported by the ation of lateral lines in J2 and males indicate interesting presence of protuberances on the head region, but it is differences, but thesecharacters have only limited not known whether or notthese are homologous with the promise for defining genera andare apparently too fewer protuberances of Sarisodera, Rhizonema, or Hylo- mosiac indistribution to be useful in phylogenetic nema (Luc, Taylor & Cadet, 1978; Othman & Baldwin, analysis of the family. Phasmids are probably absent in 1985). males of mostspecies of cyst-forminggenera; this Lip patterns of J2 of Punctodera are distinctive from contrasts with their presence inMeIoidoderu (Othman 8.1 Globodera and Cactodera (excluding C. betulae) by Baldwin, 1985). The presence or absence of phasmids partial fusion of the adjacent submedial lips with the in males has been confirmedby TEM in several hetero- labial disc, supportingmonophyly of thisgenus. In derids (Carta & Baldwin, unpubl. observ.), and rnay be addition, the charactersof fused adjacent submedial lips useful charactersin interpreting phylogenyof Heterode- and fusion of the large lateral lips (verszu small lateral ridae. lips in Cactodera) with the labial disc are shared with Our investigation indicates characters which can be most Globodera and could support a hypothesis that usefulin identification and phylogenetic analysis of these two genera are sister groups. The hypothesis of Heteroderidae, but such hypotheses of phylogeny are Globodera and Punctodera as sister group is also suppor- subject to further testing through use of larger samples ted by the shared charactersof a smallvulva and circular as well as additionalpopulations and species. For area lackingthe body surface pattern around thevulva, example, we noted that lip patterns of J2 and males are reduction or absence of a cone in females, and details often highly variable, even within a population. Vari- of the development of fenestrae which apparently differ ation ofsome structures includingcertain features of from Cactodera (Othman, 1985). This is in partial overall cuticular and perineal patterns of females and contrast to Stone's view(1975, 1979) that Cactodera cysts apparently Vary with age (Othman, 1985); while evolved from Globodera, and Punctodera developed these show promise as charactersfor further testing from an independentline; it also slightly varies from the phylogenies, theirmost effective use must follow phylogeny suggested by Wouts (1985) which considers thomugh comparative morphological-developmental in- Cactodera and Punctodera sister groups which collec- vestigations. tively share a common ancestor with Globodera. Stone (1975) reported SEM of en face patterns of J2 ACKNOWLEDGEMENTS of Globodera,Cactodera, and Punctodera"; however previous SEM techniques resulted in collapsed speci- The authorsthank B. B. Brodî, A. M. Golden, M. B. mens and results were inadequate to interpret many Harrison, H. Hirschmann Triantaphyllou, L. 1. Miller, E. M. details. Misinterpretation of en face patterns may have Noffsinger, A. D. Radice, and R. T. Robbins for supplying influenced phylogenetic schemes proposedby Stone and specimens, as well as A. H. Bell for technical assistance. The subsequentinvestigators (Ferris, 1979; Wouts, 1985). authors arealso grateful to the late Dr.A. Stone for reviewing Cactodera was considered by Stone (1975) as having the the manuscript and his valuable comments. type 2 pattern in which submedial lips are fused with adjacent head annules. This character occurs only in C. REFERENCES betulae, the three other species examined typically have six separate lips. Stone designates a type 6 pattern as BALDWIN,J. G. & BELL,A. H. (1985). Cactodera erenzican. sp., applying to Punctodera. This patternis characterized by Afenestrata ajî-icana (Luc et aL 1973) n. gen.,n. comb., and fused submedial lips, -one which Sould not have been an emended diagnosis of Sarisodera Wouts and Sher, 1971 distinctive from manj;-GZ2odefa.-We -have noted that (Heteroderidae). _cf. Ivematol., 17 : i87-201. -- -- - another feature of Punctodera, fusion of the labial disc BALDWIN,J. G., MUNDO-OCAMPO,M. & OTHMAN,A. A. withsubmedial lips, is apparentlydistinctive for the (1983). Cryphodera utahensis n. sp. (Heteroderidae), a new species from wild rose in Utah. J. NemutoZ., 15 : 182-191. BALDWIN,J. G. (1986). Testing hypotheses of phylogeny of * At the time of Stone's description these genera were not Heteroderidae. In Lamberti, F. & Taylor, C.E. (Eds). Cyst recognized as distinct from Heterodera. Nematodes. New York, Plenim Press : 75-99.

62 Revue Némarol. Il (1) :53-63 (1988) Morphology of Globodera, Cactodera and Punctodera with SEM

BEHRENS,E. (1975). Globodera Skarbilovich,1959, eine MUNDO~CAMIJO,M. & BALDWIN, J. G. (1984). Comparison selbstandigeGattung in derUnterfamilie of host responseof Cryphodera utahensiswith other Hetero- Skarbilovich, 1947 (.Nematoda : Heteroderidae). In : Vor- deridae and a discussion of phylogeny. Proc. kelminth. Soc. tragstagung (1) zu aktuellen Problemen der Phytonematologie Wash., 5 : 25-31. am 29.5.1975 in Rostock. Manuskriptdruck der Vonrage OTHMAN,A. A. (1985). Comparison of characters with SEM, for Rostock, DDR (1975) : 12-26. systematics and phylogeny of Heteroderidae (Nematoda : CLIP, G. M. & BALDWIN,J. G. (1985). Fine structure of body ). Ph.D. Thesis, Univ. California, Riverside, wall cuticle of females of eight genera of Heteroderidae. J. 168 p. Nematol., 17 : 286-296. OTHMAN,A. A. & BALDWIN,J. G. (1985). Comparative mor- FERRIS, V. R. (1979). Cladistic approaches in the study of soi1 phology of Meloidodera spp. and Verutus sp. (Heteroderi- and plant parasitic nematodes.Amer. Zool., 19 : 1195-1215. dae) with scanning electron microscopy. J. Nematol., 17 : FERRIS, V. R. (1985). Evolution and biogeography of cyst- 297-309. forming nematodes. OEPP/EPPO Bulletin, 15 : 123-129. w,A. A. & BALDWIN,J. G. (1986). Comparative mor- GREEN,C. D. (1971). The morphology of the terminal areaof phology of Sarisodera hydrophila, Rhizonema sequoiae, and the round-cyst nematodes,S. g. Heterodera rostochiensis and Afenestrata aficana withscanning electron microscopy. allied species. Nematologica, 17 : 34-46. Proc. helminth. Soc. Wash., 53 : 69-79. GREEN, C. D. (1975). The vulval cone and associated struc- OTHMAN,A. A., BALDWIN,J. G. &BELL, A.H. (1986). Compa- tures of some cyst nematodes (Genus Heterodera). Nema- rative morphology of Atalodera spp. and Thecavemziculatus tologica, 21 : 134-144. spp. (Heteroderidae) with scanning electron microscopy.J. KRALL’,E. L. & KRALL’, H. A, (1978). [Systematic changes of Nematol., 18 : 275-287. phytonematodesof the familyHeteroderidae based on SKARBILOVICH,T. S. (1959). On the structureof systematics of trophic specialization of these parasites and their evolutio- the nematodes of the order Tylenchida Thorne,1949, Acta nary connection with agriculture plants.] Moskva, Fitogell. parasitol. polon., 15 : 117-132. minotolog.Issledov. Akad.Nuuk SSSR. Vsesokiluznoe SHER,S.A. & BELL, A. H. (1975). Scanning electron micro- Obschchestvo :39-56. graphs of the anterior region of some species of Tylen- Lyc, M., TAYLOR,D. P. & CADET,P. (1978). Description of choidea (Tylenchida : Nematoda). J. Nematol., 7 : 69-83. a new tropical Heteroderidae,Hylonema ivorense n. gen., n. sp., and a new outlook on the family Heteroderidae (Ne- STONE,A. R. (1975). Head morphology of second-stage juveni- matoda :Tylenchida). Revue Nématol., 1 : 73-86. les of some Heteroderidae (Nematoda: ). Ne- matologica, 21 : 81-88. MOMOTA,Y. & OHSHIMA,Y. (1976).[Scanning electron microscopy of some cyst nematodes.]Japan J. Nematol., 6 : STONE,A. R. (1979). Co-evolution of nematodes and plants. 14-23. Symbol. Bot. Upsal., 22 : 46-61. MULVEY, R. H.(1973~). Morphology of the terminal areas of STONE,A. R. (1983). Three approaches to the status of a whitefemales andcysts of thegenus Heterodera (S. g. species complex, with a revision of some species of Globo- Globodera). J. Nematol., 5 : 303-311. dera (Nematoda : Heteroderidae). In : Stone, A. R., Platt, MULVEY, R.H. (1973b). Cone-top morphology of the white H. M. & Khalil, L. F. (Eds).Concepts in Nematode Systelna- females and cysts of the genus Heterodera (Subgenus He- tics. New York, Academic Press : 221-233. terodera), a cyst-forming nematode. CanJ. Zool., 52 :77-81. Wom-s, W. M. (1984). Globodera zelandica n. sp. (Nematoda: MULVEY, R. &H. STONE, A. R. (1976). Description ofPuncto- Heteroderidae) fromNew Zealand, with a keyto the species dera matadorensisn. gen., n. sp. (Nematoda:Heteroderidae) of the genus Globodera. N. Z. J. Zoology, 11 : 129-135. from Saskatchewan with listsof species and generic diagno- WOUTS, W.M. (1985). Phylogenetic classification of the family ses of Globodera (n. rank), Heterodera, and Sarisoderu. Can. Heteroderidae (Nematoda: Tylenchida). Syst. Parasitol., 7 : J. Zool., 54 ; 772-785. 295-328.

Accepté pour publication le 5 juin 1987.

Revue Nématol. 11 (1) :53-63 (1988) 63