Obainia petteri n. sp. (Rhigonematidae; Nematoda) from Pachybolus laminatus (Diplopoda) in Ivory Coast :

description and studyof the spermiogenesis Martin L. ADAMSON* and Daniel Van WAEREBEKE**

Muséum national d’Histoire naturelle, Laboratoire des L’ers, 61, rue de Buffon, 75005 Paris, France.

SUMMARY

Obainia petteri n. sp. from Pachybolus laminatus from Dabou in the Ivory Coast, most closely resembles O. gabonensis Adamson, 1983, but differs from this species by its shorter spicules and by small differences in the arrangement of the caudal papillae. Peculiarities of the reproductive system and spermatogenesis are discussed, and in particular, the existence of a network of tubular formations secreted by the epithelium of the seminal vesicle; t h i s network apparently enmeshes spermatids, thus forming a sort of spermatophore which is transferred to the large vaginal chamber of the female during copulation.

RÉSUMÉ

Obainia petteri n. sp. (Rhigonematidae; Nematoda] parasite de Pachybolus laminatus (Diplopodal en Côte d’lvoire : description et étude de la spemtiogenèse.

Obainia petteri n. sp. parasite du Diplopode Pachybolus laminatus provenant de Dabou, Côte d’Ivoire, ressemble a O. gabonensis Adamson, 1983, mais s’en distingue par le spicule plus court et la disposition légerement différente des papilles caudales. Les particularités concernant l’appareil génital et la spermatogenèse sont exposées, et en particulier l’existence d‘un réseau de tubules formés par les cellules de la paroi de la vésicule séminale; ce réseau emprisonnant les spermatides, et se retrouvant dans la vaste chambre vaginale de la femelle après fécondation, semble ainsi jouer le rôle d’un spermatophore.

Following a collecting trip to the Ivory Coast Prof. F. Petter returned with a number of specimens of Pa- chybolus laminatus (Pachybolidae; Spirobolida), a large diplopod common in West Africa. They were infected with a number of nematode parasites belonging to at least five genera, namely, llelastoma, Desmicola (The- lastomatidae; Oxyurida), Brunzptaemilius, Rhigonema and Obainia (Rhigonematina; Ascaridida).

The specimens of Obailzia represent a new species which we name O. petteri n. sp. Examination of male and female reproductive systems of the new species revealed several peculiarities apparently related to sper- miogenesis. In the present communication we describe O. petteri n. sp. and give an illustrated account of these peculiarities.

Obainia petteri n. sp. (Fig. 1)

MENSURATIONS

Male (paratype; n = 2). L = 9.01, 9.58 mm; b = 27.2,

* École Pratique des Hautes Études, Paris. ** Entomo-nématologiste de I’ORSTOM.

Revue Nématol., 8 (3) : 241-247 (1985)

26.7; c = 22.5, 21.5; T = 66.3, 66.7; oesophagus = 331, 350 pm long consisting of corpus 123, 131 pm long and 147, 163 pm wide, and bulb 199,219 pm long and 21 1,223 pm wide; nerve ring 120,135 pm and excretory pore 129, 155 pm from anterior extremity; spicules 412, 421 pm and tail 400,445 pm long.

Female (paratype; n = 5). L = 9.93 (9.63-10.56) mm; V = 65 (63-66); percentage of body occupied by reproductive system = 43.4 (42-45); b = 26. 1 (25.2-27.7); c = 33.6 (31.7-36.2). Oesophagus 380 (378-382) pm long including corpus 140 (127-151) pm long and 161 (159-167) pm wide and bulb 222 (215-231) pm long and 237 (235-243) pm wide. Nerve ring 142 (135-147) pm, excretory pore 155 (143-167) pm, and vulva 6.42 (6.16-6.85) mm from anterior extremity. Tai1 295 (289-304) pm long. Eggs 111-118 pm long and 79-84 pm wide.

Holotype (.male> : L = 9.05 mm; b = 26.7; c = 22. T = 68; oesophagus = 339 pm; corpus = 135 x 147 pm; bulb = 132 x 122 pm; spicules = 412 Pm; tail = 412 pm.

24 1

M. L. Adamson & D. Van Wuerebeke

"

f

E V

/?

Fig. 1. Obuiniu petten' n. sp. A, B and C : cephalic extremity in lateral, dorsal and ventral views; D : caudal end of male, ventral view; E : detail of end of tail of male; F : caudal end of male, lateral view; G : spicule, lateral view; H : detail of end of spicule. Obuiniu gubonensis Adamson, 1983. 1 : spicule (paratype).

242 Revue Nématol., 8 (3) : 241-247 (1985)

Obainia petteri n. sp. (Rhigonematidae)

DESCRIPTION

Male : Cephalic extremity elongate dorsoventrally. Body cuticle covering anterior extremity forming ce- phalic cap surrounding oral opening and short posterior collar separated from cap by groove. Cephalic sense organs consisting of four prominent round submedian papillae on the cephalic cap, and two amphids just posterior to groove separating cap and collar. Body cuticle posterior to collar bearing fine striations about 2 pm apart each stria with tiny, posteriorly directed spines which diminish in size posteriorly. Coelomocytes consisting of two groups of four cells in tandem just before anterior end of reproductive tract. Valve-like formation present about 1 mm posterior to oesophago- intestinal junction. Anterior to valve, intestinal lumen quadriradiate and epithelial cells with basal or near basal nuclei. Posterior to valve, lumen lambda-shaped and cytoplasm of epithelial cells distinctly divided into basal portion and finely granular, swollen apical portion; nuclei located at junction between basal and apical zones (Fig. 2, C and D). Sexual charaeters. Two prominent lateral bands of muscles present, extending from just posterior to base of oesophagus to near level of first pair of caudal papillae. Spicules similar, equal and arcuate. Twenty-three caudal papillae (Fig. 1, D, E and F) : four pairs of subventral preanal; one median on anterior lip; four pairs of subventral (Fig. 1 D : a, b, c, d), one pair of lateral (e) and two pairs of dorsolateral, postanal (Fig. 1 E : f and g).

Female : Identic to the male, except for sexual cha- racters. Didelphic, amphidelphic. Vagina muscular, directed anteriorly from vulva and forming large cham- ber before narrowing and flexing posteriorly to divide into anterior and posterior uterine branches.

HOST AND ORIGIN

Posterior intestine of the diplopod Pachybolus lamina- tus Cook (Pachybolidae; Spirobolida) at Dabou, Ivory Coast (Coll. Dec. 1983 by F. Petter).

TYPE MATERIAL

Holotype and paratypes deposited in the collection of the Muséum national d’Histoire naturelle, Laboratoire des Vers, Paris, France.

DIAGNOSIS Obainia petteri n. sp. is very similar to O. gabonensis

Adamson, 1983, the type and only species. Although the males are the same size, the spicule is shorter and more robust in the new species and the arrangement of the ventral postanal caudal papillae differs slightly. Thus, the first pair (Fig. 1, D : a) is further from the anus and the second postanal papilla-pair (b) is located just

Revue Nématol., 8 (3) : 241-247 (1985)

posterior to the first postanal pair in O. petteri n. sp.; in O. gabonensis, the second postanal papilla-pair is about equidistant from the first and thirth (c) postanal pairs. In addition, the tail (as expressed in absolute lengh and in the de Man value, c) is shorter in the new species and the value of T is smaller (66-68 ZIS 71 to 76 in o. ga- bonensis).

Anatomy of reproductive system and spermiogenesis

(Figs. 2, 3 and 4)

MALE REPRODUCTIVE SYSTEM

The testis extends anteriorly from the posterior half of the body and flexes posteriorly well behind the base of the oesophagus. It is divided into three parts : 1. ger- minative and growth zones, II. meiosis zone, and III. maturation zone (Fig. 2, E).

Near the end of the growth zone, spermatocytes are arranged in clusters of a dozen or more cells which appear to develop synchronously and independant of other such clusters. Meiosis gives rise to subspherical spermatids about 12 Fm in diameter, containing 6 or 7 round to oval chromosomes. Thus, the chromosome number is apparently 13 in males and 14 in females. Chromosomes persist as independant entities through- out spermiogenesis.

ln the maturation zone spermatids increase in volume and become elongate. Large globular amber-coloured granules are secreted by the epithelium in this zone and spermatids were frequently observed in direct contact with these granules.

The entrance to the seminal vesicle from the testis is in the form of a short funnel-shaped region (Fig. 2, F). The seminal vesicle may be over 2 mm long and its ephithelial cells contain large spherical vacuoles filled with transparent membranous tubular stuctures (Fig. 3, j). These vacuoles apparently release their contents into the lumen where they form a dense matrix amongst the spematids. Spermatids at this stage are about 50 pm long with a maximum diameter of about 10 pm; they are elongate with a swollen anterior end which bears a short conical terminal knob. The chromosomes are in the anterior half of the spermatid.

FEMALE REPRODUCTIVE SYSTEM

The vagina forms a large chamber which occupies 20 to 25 % of the body length and whose Wall is composed of low circular muscle cells. The lumen is filled with developing spermatids enmeshed in membranous tubu- lar formations. A common duct leads from the anterior extremity of the vaginal chamber to opposed uteri. The seminal receptacles are voluminous and are lined with swollen columnar epithelium near their junction with the uteri (Fig. 3, N).

243

E 1

O O Ln

A

50 rn D

l 1 5 0 pm

, G F

d

1-1

L’

Fig. 2. Obainia petteri n. sp. A : anterior end showing valve-like formation in intestine and anterior group of coelomocytes. B : transverse section just posterior to oesophagus. C : transverse section of intestine near midbody. D : detail of epithelial cells in C. E, F and G : male reproductive system : E, entire; F : detail of region 4 of E; G : detail of region 6, junction of seminal vesicle and aas dejèrens. H : reproductive system of female. 1 : detail of vulva and vagina. 244 Revue Nématol., 8 (3) : 241-247 (1985)

Fig. 3. Obainia petteri n. sp. Spermiogenesis. A to E, various stages in development of spermatids : A : immediately following meiosis; B : from seminal vesicle; C : from vaginal chamber of female; D : from uterus; E : from seminal receptacle; F : spermatozoa from seminal receptacle; G, H and 1 : longitudinal sections through zones 1, 2 and 3 respectively of testis (see Fig. 1, E). J : epithelium of the seminal receptacle. K : detail of Wall of vagina in longitudinal section. L and M, detail of vaginal chamber in longitudinal and transverse section. N : posterior end of seminal receptacle. Revue Nématol., 8 (3) : 241-247 (1985) 245

Obainia petteri n. sp. (Rhigonematidae)

Spermatids undergo pronounced morphological changes in the vagina and uteri of the female (Fig. 3, C et D). They increase in length reaching 85 pm and become more slender while decreasing in volume. Sper- matids were in close contact with the epithelium of the seminal receptacle and in this organ transformed into small spherical spermatozoa about 6 pm in diameter (Fig. 3, 0.

INTERPRETATION OF SPERMIOGENESIS

In Obainia petteri n. sp., as in other rhigonematids (Van Waerebeke, Adamson & Kermarrec, 1984; Van Waerebeke, 1984), spermiogenesis involves major chan- ges in volume and form; in these species, spermatids enter into close contact with amber-coloured granules secreted by the testicular epithelium just posterior to the meiosis zone. This occurs just prior to the initial growth phase of the spermatids and it is likely that the granules serve as a source of energy for the changes which the spermatids subsequently undergo (Van Waerebeke, 1984).

Membranous tubular elements secreted by the epithe- lium of the seminal vesicle have not been previously reported in nematodes. Apparently they agglomerate spermatids in a packet; such a packet would thus be analogous to a spermatophore, facilitating sperm trans- fer during insemination.

The final stages of spermiogenesis occur in the se- minal receptacle of the female where elongate sperma- tids give rise to subspherical spermatozoa about 6 km in diameter. During this transformation, spermatids are wedged between cells of the seminal receptacle epithe- lium; these latter may stimulate the transformation or absorb material given off by the spermatids.

Accepté pour publication le 20 mars 1985.

Spermatids of O. gabonensis apparently undergo changes similar to those described here. Changes in form of spermatids which occur during spermiogenesis in Ichtyocephalus anadenoboli Van Waerebeke, Adamson & Kermarrec, 1984 are similar to those described here. However the most advanced stage observed in that species has a large anterior end capable of pseudopod formation and a long filiform tail end and thus resem- bled advanced spermatids of Obainia (Fig. 3, C and D). We referred to these as spermatozoa but the present study suggests that we may have missed the fiial stages of spermiogenesis in Ichthyocephalus anadenoboli.

ACKNOWLEDGEMENTS

The authors thank Prof. F. Petter, Laboratoire de Zoologie, Mammifères et Oiseaux, Muséum national d'Histoire natu- relle, Paris, for collecting the material studied.

REFERENCES

ADAMSON, M. L. (1983). Obainia gabonensis n. gen., n. sp. and Rhigonema pachyboli n. sp. (Rhigonematidae), Nematoda) from Pachybolus sp. (Pachybolidae, Spirobolida, Diplopoda, Myriapoda) in Gabon. Bull. Mus. Natn. Hist. nat., Paris, 4e sér., 5, section A (2) : 531-542.

VAN WAEREBEKE, D. (1984). Rhigonenza madecassum n. sp. (Rhigonematidae; Nematoda), parasite de Diplopode à Madagascar : description et étude de la spermiogenèse. Revue Nématol., 7 : 276-282.

VAN WAEREBEKE, D., ADAMSON, M. L. & KER", A. (1984). Spermiogenèse et fonction du sac vaginal chez Ichthyocepha- lus anadenobolin. sp. (Rhigonematidae; Nematoda) parasite d'dnadenobolus politus (Rhinocridae; Diplopoda) en Gua- deloupe. Ann. Parasitol. hum. co?np., 59 : 101-109.

Revue Né'natol., 8 (3) : 241-247 (1985) 247