Enchodelus, THORNE, 1939

MAQSOOD AHMAD & M. SHAMIM JAIRAJPURI, 1980, A REVIEW OF THE GENUS ENCHODELUS THORNE, 1939 WITH DESCRIPTIONS - OF SPECIES FROM INDIA, Records of the Zoological Survey of India 15, pp. 1-42 : 2-12

THE GENUS ENCHODELUS THORNE, 1939

Systematic position ofEnchodelus:

Class Nematoda Subclass Adenophorea (Von Linstow, 1905) Chitwood, 1958 Order Dorylaimida (de Man, 1876) Pearse, 1942 Suborder Dorylaimina (de Man, 1876) Pearse, 1942 Superfamily Dorylaimoidea (de Man, 1876) Thorne, 1934 Family Nordiidae (Jairajpuri & Siddiqi, A.H., 1964) Siddiqi 1969 Subfamily Pungentinae Siddiqi, 1969 Genus Enchodelus Thorne, 1939

Diagnosis (emended): Lip region slightly or distinctly set off by depression. Odontostyle long with a small aperture. Odontophore with broad basal flanges or simple rod-like. Basal expanded part of oesophagus relatively slnall. Gonads amphidelphic, reflexed. Males ha'/ing well developed spicules, lateral guiding pieces and 4- 12 ventromedian supplements. Prerectum usually many times anal body-width. Rectum about one anal body-~idth long. Tails similar in both sexes, vary from short-conoid or elongate-conoid to hemispherical or rounded with or without saccate bodies.

Type species: Enchodelus macrodorus (de Man, 1880) Thorne 1939 * Other species:

E. altherri Vinciguerra & de Francisci, 1973

E. analatus (Ditlevsen, 1927) Thorne, 1939

E. arcuatus Thorne, 1939

E. brevidentatus Thorne, 1939

E. conicaudatus (Ditlevsen, 1927) Thorne, 1939

E. constrictus Jairajpuri & Loof, 1968 *

E. distinc t us n. sp*

E. faeroensis (Ditlevsen, 1928) Thorne, 1939

E. groenlandicus (Ditlevsen, 1927) Thorne, 1939

E. hopedoroides Altherr, 1963

E. hopedorus (Thorne, 1929) Thorne, 1939

E. i rregularis Altherr, 1972

E. laevis Thorne, 1939

E. longidens Jairajpuri & Loof, 1968 *

E. magnificus ( Altherr, 1952) Altherr, 1963

E. maximus Baqri & Jairajpuri, 1974 *

E. microdoroides Baqri & Jairajpuri, 1974 *

E. nepa l ensis Zullini,] 973

E. parateres Baqri & Jairajpuri, 1974 *

E. parvus Loof, 1971

E. rhaeticus Altherr, 1952

E. satendri Baqri & Jairajpuri, 1974 *

E. signyensis Loof, 1975

E. striatus Thorne, 1939

E. teres Thorne, 1939

E. thornei Baqri & Jairajpuri, 1974 *

E. vestibulifer Altherr, 1952

E. vesuvianus (Cobb, 1893) · Thorne, 1939

E. zonatus Jairajpuri & Loof, 1968 *

List of synonyms and transfers

E. microdorus Schiemer, 1965 (= Rhyssocolpus microdorus (Schiemer, 1965) Andrassy, 1971)

E. brasiliensis Meyl, 1957 (= Rhyssocolpus brasiliensis (=Meyl, 1957) Andrassy, 1971)

E. dolichurus Loos , t 946 (= Prodorylaimus dolichurus (Loos, 1946) Siddiqi, 1969)

E. minusculus Loos, 1946 (= Eudorylaimus minusculus (Loos, 1946) Siddiqi, 1969)

Species inquirendae

E. macrodoroides (Steiner, 1914) Thorne, t 939 by Jairajpuri & Loof, 1968*

E. hedicki (Pearse, 1941) Andrassy, 1960 by Zullini, 1973

The species recorded from India are marked with *

Relationship: The genus Enchodelus is related to the genera Pungentus Thorne & Swanger, 1936, Rhyssocolpus Andrassy, 1971 and Enchodorus Vinciguerra, 1976. From Pungentus it differs in the absence of four cuticularized pieces around the vestibule, well set off lip region and in the presence of well developed.flanges at base of odontophore. It can be differentiated from Rhyssoco/pus in the absence of peculiar striations near the vulval region and in possessing longer odontostyle. From Enchodorus it differs in having longer odontostyle and in having elongate-conoid or rounded tails (tail long filiform in Enchodorus ).

NOTES ON THE MORPHOLOGY

The species of the genus Enchodelus have been reported from U.S.A., Italy, Sweden, Switzerland, Nepal, India, etc. They were mostly collected from high altitudes from soil around roots of mosses, grasses, etc. When killed with hot fixative they assume ventrally curved or C-sbaped postures. The size of body ranges from 0.59 mm ( E. parvus ) to 2.80 mm ( E. faeroensis ). The body is cylindrical tapering slightly towards extremities.

Although both sexes occur but in majority of the species males are rare. In some species like E. parateres males are as frequent as females. Both sexes are similar in shape and in basic morphology, but in some species the males have more ventrally curved tails.

Cuticle: The cuticle is marked usually with fine but rarely with coarse striations ( E. striatus ). Radial striati~ns have also been seen in the tail region of some species (E. macro4orus). The thickness of the cuticle varies at different regions on the body, usually thickest on tail tip (23 Jlm in E. maximus ). The lateral chords are granular, narrow, about one-eight to one-fourth of the body-width near middle.

Lip region: The lip region is either slightly set off by a depression (E.,'esuvianus) or distinctly set off by a constriction ( E. parateres ). These differences are helpful in the identification of species. The contour of lip region may be angular (E. hopedorus) or rounded ( E. arcuatus ). The lip region bears six lips of equal size, each with a papilla on the inner as well as on the outer circlet. The submedian lips have an additional papilla on each. The subdorsal and subventral lips, therefore, bear two papillae on the outer circlet, but the laterals have only a single papilla. There are in aU 6 + 10 papillae on both the circlets (cf, Jairajpuri & Loof, 1968).

Amphids: The amphids are well developed, stirrup or cupshaped, with curved slit-like apertures occupying 慢潵縠 i-I of the corresponding body-width. The amphidial pouch is followed by a canal which leads to the sensillar pouch. The sensil1ae inside the pouches are supposed to be chemoreceptors.

Feeding apparatus: The feeding apparatus consists of an odontostyle, odontophore, guiding sheath and guiding ring. The odontostyle or spear is long but attenuated. It develops in a cell which is located on the submedian wall of the anterior slender part of oesophagus. The odontostyle is forked at its junction with odontophore. The length of odontostyle ranges from 8 Ilm ( E. parvus ) to 70 Ilm (E. nepalensis), but in majority of the species, it is in the range of 25- 45 /-lm. The length of odontostyle is one of the most important taxonomic characters in this genus. The odontophore or spear extension is also weJl developed and provided with conspicuous flanges or smaII swelling at its base. Some species have simple rod-like or linear extension ( E. constrictus , E. zonatus ).,

The flanges are three in number and are forlned by the cuticular layers of oesophagus, which are embedded in the oesophageal tissues. In a cross-section, the 晬慾来猠 appear symmetrically arranged. The length of odontophore rang~s from 9 t'm ( E. parvus ) to 56tlm ( E. maximus ). In nlajority of the species usually the length of odontophore is equal to that of odontostyle. The length and nature of development of odontophore is also very.helpful in the identification of species. The guiding apparatus is present near the base of odontostyle and consists of two rings, one is fixed and the other is movable. The position of the fixed guiding ring is 捾渵瑡測琠 and therefore taxonomically important. The length of guiding sheath is variable corresponding to the length of the odontostyle. In some species like E. macrodorus , the stomal walls are very much thickened anterior to guiding ring. The gujding sheath becolnes gradually thinner posteriorly and eventually fuses with odontostyIe.

Oesophagus: The oesophagus is divided into an anterior slender and a posterior expanded portion. The nerve ring surrounds the anterior slender part of oesophagus at about 㐰ⴵ〱縠 of neck length from anterior end. The lumen of basal expanded part is tripartite in crosssection. The basal expanded part of oesophagus comprises five oesophageal glands, one dorsal and two pairs of subventrals. All these glands open into the lunlen of oesophagus near the placement. The dorsal gland and its nucleus is comparatively more developed than the others. Thorne (1939) reported only three oesophageal gland nuclei, one dorsal and a pair of subventrals in E. macrodorus . The position of gland nuclei and their orifices is also itnportant taxonomically.

According to Loof & Coomans (1970) the genus Enchvdelus has provisional characters as: distance -DO-DN moderate to rather long: 4-6%' both S 1N very indistinct, S':l縠 in, or,slightly behind the middle of the distance DN-S 2N, SgN located anteriorly, 83-88%, DO anterior to level where oesophagus attains its full width, 81N generally close together.

Cardia: Cardia is well developed and hangs in the intestinal tissues. It is usually elongate hemispheroidal but may be cylindrical ( E. teres ).

Intestine: Intestine is sac-like, consisting of six cells in circumference (cf Thorne, 1939). Granules of various sizes and colours are present in it. The lumen of the intestine is filled with masses of green chlorophyll-like material which indicates that they may be parasites of plants.

Prerecturn: Prerectum is separated from the intestine by a faint or deep constriction. The cells of prerectum are very similar to intestine. The length of prerectum is usually 1 -5 times the anal body-width, but exceptionally it may be 7 anal body-widths long ( E. zonatus ). The length of prerectum in relation to anal body-width is an important taxonomic character.

Rectum: The rectum. is dorsoventrally flattened, separated form the prerectum by a constriction. It is usually about one anal body-width long. The rectum opens to the exterior through anus.

Female reproductive organs: In all the species of Enchodelus reported so far the 晥繡汥猠 are amphidelphic. Each sexual branch consists of an ovary, oviduct, uterus, vagina and vulva.

Ovary: The ovary is refiexed lying dorsally or ventrally to the oviduct. It consists of two zones, the distal germinal zone and the proximal growth zone. In the germinal zone the cells are small, restricted to the apical part where the proliferation of germ cells takes place (telogony). In the growth zone the oocytes are arranged in a single row increasing in size towards the proximal end of the ovary. Due to subterminal connection between the ovary and oviduct, the proximal part of the latter forms a blind sac (cf, Coomans, 1964). The ripe oocytes grow in size in this region until they reach their full size. After maturation, they are passed on to the oviduct.

Oviduct: The oviduct consists of a distal narrow tube with high columnar epithelium surrounded by a thin layer of connective tissue and an enlarged proximal part with low columnar epithelium. The proximal part is irregular in outline and mayor may not contain ova. It is also quite flexible and may serve as spermatheca (cf., Chitwood & Chitwood, 1950).

Sphincter: Usually the oviduct and uterus are separated by a well developed sphincter. The 獰桩湣瑥縠 is more prominent in species like E. IOllgidens, E. distinctus and E. parateres , etc. The sphincter may also be present at the junction of oviduct and ovary ( E. microdoroides .) ·

Uterus: The uterus is the most variable part of female reproductive organs. Usually it consists of a proximal and a distal part. The proximal part consists of a single layer of columnar cell surrounded by a muscular layer. The distal' part is narrow and highly muscular. The eggs are usually present in the proximal part of uterus where they are c~ated with a shell. The proximal parts of the two uteri join to form an ovijector. In some species, this region may be completely filled with sperm.

Vagina: The vagina extends to one-third or half of the corresponding body-width. Its lumen is narrow and usually'at its proximal end it may be surrounded by cuticularization and at distal end by sphincter muscles. In some species, the sphincter muscles are not visible ( E. thornei , E. longidens ).

Vulva: The vulva is a ventral transverse slit. The slit is formed by invagination of body cuticle and is controlled by various muscles. Dilatator vulvae are clearly visible in SOlne species ( E. satendri ).

Male reproductive organs: The male genital tract consists of two testes, vas deferens and a cloaca. The males are diorchic and both the testes lie left to the intestine. 呾攠 testes are outstretche<:\ and telogonic, i.e., the Ploliferation of germs cells takes place at the apical region. Each testis can be divided into a proximal germinal part \ and a distal growth part./The maturation of sperm takes place at the end of growth part. The vas deferens is joined with the testes; it is made up of a tubular and a glandular region and is not differentiated into an anterior slender and a posterior ejaculatory duct. The cloaca is lined with cuticle and opens to the exterior through the cloacal aperture.

Besides primary sex organs as described above, the males are also provided with accessory structures which consists of spicules, lateral guiding pieces, ventromedian supplements and copulatory muscles.

Spicules: The paired spicules are similar in shape and size. These are stout, heavily sclerotized and bluntly tipped. The spicules are usually ventrally curved. Each spicule consists of a head or capitulum and a lamina. The length of spicules varies from 42 Ilm (E. thorne;) to 60 Jlm (E. nepalensis). During action each spicule is guided by a set of protractor and retractor muscles. Two lateral guiding pieces, present on the distal end of spicules, taper distally and strengthen the spicules during copulation.

Supplements The supplements consist of an adanal pair and a variable number of ventromedians spaced, regularly or irregularly. The latter may vary from four ( E. constrictus ) to twelve ( E. macrodorus ). They are very distinct and elevated and are supplied with nerve endings. The copulatory muscles are very prominent occupying the area up to the last supplement.

The shape and size of spicules, the shape and size of lateral guiding pieces, the number and arrangement of ventro-median supplements, the number and area occupied by the copulatory muscles are fairly useful characters in the taxonomy of Enchodelus .

Tail The tails are similar in the two sexes of species of Enchodelus but the length and shape of tail are most variable in the species of this genus. It varies from elongate-conoid to completely hemispherical. The conoid tails may be short or long, straight ( E. conicaudatus ) or ventrally curved ( E. brevidentatus ) with acute ( E. faeroensis ), or blunt terminus ( E. zonatus ). The other type of tails may be convex-conoid (E. microdoroides), bluntly-conoid (E. vesuvianus) or smoothly founded (E. macrodorus). In species like E. teres , E. hopedorus and E. vestibulıfer saccate bodies are present in pairs on both the sides of tail. The number of these bodies is variable. Usually the tails of all the species are provided with a pair of caudal papillae on each side. The length and shape of tail is one of the most important taxonomic characters in this genus at species level.

SYSTEMATICS OF THE GENUS EN CH ODELUS THORNE, 1939 ‘lhorne (1959) proposed tne genus ızncnoaeıus Ior some specıes 0ı Dorylaimus Dujardin, 1845 and Dorylaimellus Cobb, 1913 which possess well developed flanges at base of odontophore, double guiding ring, amphidelphic gonads. The new genus included E. macrodorus (de Man, 1880) as type species, seven species transferred from other genera and five new species. It was grouped under the subfamily Tylencholaiminae Filipjev, 1934 of the family Dorylaimidae de Man, 1876 along with other genera like Tylencholaimus and Discomyctus . Loos (1946) added two more species viz., E. dolichurus and E. minusculus to this genus.

Altherr (1952) described two new species, viz., E. vestibulıfer , E. E. vestibulifer , E. rhaeticus and proposed a new genus Heterodorus with the type. H. magnificus . In 1963 he transferred H. magnificus to Enchodelus and synonymized E. rhaeticus with E. magnificus . Meyl.(1957) and Schiemer (1965) also added E. brasiliensis and E. microdorus respectively.

Jairajpuri and A. H. Siddiqi (1964) proposed a new subfamily Nordiinae for the genus Nordia . Siddiqi (1969) gave family rank. to Nordiinae , proposed a new subfamily Pungentinae and placed Enchodelus along with Pungentus under it. Siddiqi (1.c.) considered E. dolichurus Loos, 1946 and E. minusculus Loos, 1946 as Prodorylaimus dolichurus and Eudorylaimus minusculus respectively. In 1960, Andrassy reported E. hedicki which was considered as species inquirenda by Zullini (1973).

Jairajpuri & A. H. Siddiqi (1964) recorded the occurrence of this genus for the first time from India when they reported a single female of E. macrodoroides (Steiner, 1914) Thorne, 1939 from soil around roots of pine at Simla, Himachal Pradesh. Jairajpuri & Loof (1968) added three new species from India, viz., E.longidens , E. zonatus and E. conf)trictus to this genus and considered E. macrodoroides as species inquirenda.

Andrassy (1971) proposed a new genus Rhyssocolpus under Pungentinae for E. microdorus and E. brasiliensis because of peculiar striations in the cuticle at vulva region.

Recently more species have been added to the genus Enchodelus from various parts of the world: two by x\ltherr (1963 & '72), two by Loof (\971 & '75), five by Baqri & Jairajpuri (1974) and one each by Vinciguerra (\973) and Zullini (1973). While describing E. nepaiensis from Nepal, Zullini (l.c.) discussed the synonymies and departures of species under Enchode1us and also provided a key to its species. A revised key was given by Baqri & Jairajpuri ⠱㤷 㐩縠

More recently, Vinciguerra (1976) reported a closely related genus Enchodorus fronl around roots of Inosses in Italy and also placed it in Pungentinae . Enchod6rus differs from Enchodelus in having a shorter odontostyle, shorter odontophore without flanges or with inconspicuous swelling at base and a long filiform tail.

Enchodelus Thorne, 1939 contains two fairly distinct groups of species, one with conoid tails and the other with rounded tails. Altherr (1952) erected a genus Heterodorus for the type species H. magnificus having conoid tail and peculiar ovoid chamber in the gonads but later on in 1963 he synonymized it with Enchodelus . Siddiqi (1969) stated that the species of Enchodelus represent two distinct genera and he suggested that those having conoid tails may be kept under Heterodorus Altherr, 1952 . Loof (1971) did not agree with this and considered that Enchodelus is not divisible because the species possess some common characters, like the long odontostyle with short apertures, thick-walled stoma and in the location of oesophageal gland nuclei etc. Zullini (1973) also agreed with the views of Loof (1971). Recently Vinciguerra (1976) has also suggested that the species of Enchodelus comprise two distinct groups differentiated on the shape of tails.

Enchodelus is heterogeneous containing species which have ' lip region of different shapes, odontostyle of different sizes, odontophore with well developed or very poorly developed flanges at base, variable shapes of tail and different arrangements of supplements. The characters shared by all the species are the long odontostyle with a small aperture, lip region set off from the body, relatively small expanded part of oesophagus, similar arrangement of oesophageal gland nuclei and their orifices and amphidelphic gonads. In order to solve the existing problem of diversity within Enchodelus it is proposed to split the genus into five groups and by giving each of these the status of a separate subgenus:

(i) Subgenus Enchodelus (Thorne, 1939) n. rank

(ii) Subgenus Rotundus nov.

(iii) Subgenus Heterodorus (Altherr, 1952) n. rank

(iv) Subgenus Paraenchodelus nov.

,(v) Subgenus Nepalus nov.

KEY TO SUBGENERA OF GENUS ENCHODELUS

1. Tail hemispherical or bluntly-conoid.,. 2

Tail short-conoid or elongate-conoid '" 3

2. Odontostyle fairly long; odontophore with broad basal flanges Enchodelus

Odontostyle short; odontophore without basal flanges Rotundus

3. Lip region not set off from body; female gonads with a peculiar ovoid chamber Heterodorus

- Lip region slightly or distinctly set off from body; peculiar ovoid chamber absent 4

4. Odontostyle over 50 μm; odontophore with moderately developed basal flanges Nepalus

- Odontostyle less than 50 μm; odontophore rod-like or with very poorly developed basal flanges Paraenchodelus Relationship of the subgenera The subgenus Enchodelus includes species with fairly long odontostyle, and well developed flanges at base of odontophore, tail bluntly-conoid or hemispherical, and the males having regularly spaced ventromedian supplements. Rotundus is closely related to it but differs in absence of flanges at base of odontophore and in the males having irregularly spaced ventromedian supplements. In the other three subgenera, viz., Heterodorus , Paraenchodelus and Nepalus , the tails are short-conoid to elongate-conoid. The subgenus Heterodorus has rod-like odontophore and a peculiar ovoid chamber in the female gonads. Paraenchodelus and Nepalus are quite closely related to each other. Paraenchodelus has simple rodlike or with very poorly developed flanges at base of odontophore while Nepalus has moderately developed flanges at base of odontophore. The lengths of body and odontostyle are comparatively longer in Nepalus than in other subgenera. In Enchodelus and Rotundus the ventromedian supplements are within the spicular range while in Paraenchodelus and Nepalus they begin above the range of spicules.