Systematic Parasitology 22: 205-213, 1992. © 1992 Kluwer Academic Publishers. Printed in the Netherlands.

Pluviantaenia kassalensis n. g., n. sp. (Davaineidae), a new cestode from the Egyptian plover Pluvianus aegyptius (L.) in the Sudan

Arlene Jones ~, Lotfi F. Khalil ~ and Rodney A. Bray 2 1 International Instituie of Parasitology, 395A Hatfield Road, St. Albans, A L 4 0 X U , UK 2 Department of Zoology, The Natural History Museum, Cromwell Road, London, SW 7 5BD, UK

Accepted for publication 4th September, 1991

Abstract

Pluviantaenia kassalensis n. g., n. sp. (Davaineidae), from the intestine of Pluvianus aegyptius (Charadrii- formes, Glareolidae) in the Kassala area of the Sudan, differs from other davaineid cestodes in having an armed scolex with an inflated pseudorostellum terminating in two fan-shaped lobes, in the absence of suckers, the presence of a very large sucker-like genital atrium provided distally with a powerful sphincter, and the presence of a thin-walled cirrus-sac, smaller than the genital atrium, enclosing a robust, armed cirrus. The genital atrium cirrus-sac complex, but not the female organs, may be duplicated bilaterally and/or additional sets may occur in marginal or submarginal positions.

Introduction

The Egyptian plover Pluvianus aegyptius (L.) (Charadriiformes, Glareolidae), also known as the Crocodile bird, is a species commonly found in the Sudan along all waterways where there are suitable sandbanks. Plovers from the Kassala area have been found to harbour an unusual and ab- errant davaineid cestode which has not, so far, been found in P. aegyptius from other localities. The cestodes previously reported from this host are the hymenolepidid Microsomacanthus stylo- ides (Fuhrmann, 1906) Spasskii & Spasskaya, 1954 and the progynotaeniid Progynotaenia jaegerski- oeldi Fuhrmann, 1909, by Fuhrmann (1906) and (1909), respectively.

Materials and methods

All of three hosts collected from the Kassala area

of the Sudan near the Ethiopian border were in- fected. Each harboured 4-10 cestodes with sco- leces and a large number of fragments. This spe- cies appears to fragment naturally in the gut of the host and no complete worms were recovered. The specimens from one host only were fixed in 70% alcohol and form the basis of the present description. They comprised five strobila with sco- leces, and fragments including mature and gravid proglottids. Most specimens were stained in ace- toalum carmine and mounted in Canada balsam; some detached proglottids were hand-sectioned. One scolex and some detached gravid proglottids were serially sectioned and stained in haematoxy- lin and eosin. The scolex was sectioned in the vertical longitudinal plane and the proglottids in the horizontal longitudinal and transverse planes.

The specimen selected as holotype has a scolex and strobila with early mature proglottids. The description of the mature and gravid regions is based on detached proglottids.

206 Arlene Jones et al.

Family Davaineidae Fuhrmann, 1907

Pluviantaenia n. g.

Generic diagnosis Scolex dorso-ventrally flattened, consisting of a swollen posterior basal region and a cup-shaped anterior region armed with double row of numer- ous small hammer-shaped hooks. Pseudorostel- lum present distally, enormous, inflated, ending in two fan-shaped lobes. Suckers absent. Proglottids numerous, craspedote, wider than long. Paired dorsal and ventral osmoregulatory canals present; ventral canals linked in each proglottid by trans- verse anastomoses. Genital ducts dorsal to osmo- regulatory canals. Genital pores generally alter- nate regularly but may be irregular or bilateral. Genital atrium enormous, sucker-like, with mass- ive sphincter. Duplication of atrium, cirrus-sac and vas deferens may occur. Cirrus-sac thick- walled. Cirrus armed. Internal seminal vesicle present. Vas deferens functions as external semi- nal vesicle. Testes numerous, in band along post- erior margin of proglottid. Vagina sigmoid, dilate, glandular. Ovary median, deeply lobed. Vitellar- ium postovarian, lobed. Seminal receptacle pre- sent. Uterus persistent. Type-species: P. kassalensis n. sp.

Pluviantaenia kassalensis n. g., n. sp. (Figs 1-20)

Type-host and locality: Pluvianus aegyptius (L.); small intestine; Kassala, Sudan. Specimens de- posited in International Institute of Parasitology Helminthological Collection, Accession Nos: holotype $1085A; paratypes $1085B, B1054B.

Description

Scolex (Figs 1-3). The scolex is dorso-ventrally flattened with a permanently protruding pseudo- rostellum. There are no suckers. The scolex is composed of a posterior, slightly swollen, basal region, 665-785 ~Lm wide, which overlaps the base of a cup-shaped anterior region, 684-797~m wide, in which the pseudorostellum is embedded.

There is no histological distinction between the anterior and posterior regions of the scolex. Loops of the osmoregulatory canals and bands of longi- tudinal muscle fibres, continuous with the longi- tudinal musculature of the strobila, extend into the anterior region; the muscle fibres are attached to the base of the pseudorostellum (Fig. 3). The pseudorostellum is muscular, fan-shaped in dorsal or ventral view and terminates in 2 broad dorsal and ventral lobes. It is 835-994 Ixm wide. It has no rostellar sac but is demarcated basally by a strong muscular wall.

A double row of about 800 small hammer- shaped hooks (Fig. 2) is set into the distal rim of the anterior part of the scolex. Hooks of the first and second rows are 14-17lxm and 12-14txm long, respectively. Oblique muscle fibres run from the base of the hooks to the wall of the pseudoros- tellum.

Strobila. None of 4 strobila available was com- plete with mature and gravid proglottids because, once development has progressed to the point where the genital atria and cirrus-sacs are fully formed, groups of several proglottids are normally shed to complete development in the gut of the host. Three such strobila, complete with scoleces, measured 22-38 mm in length and 1.68-1.93 mm in maximum width. The longitudinal musculature, although well developed and continuous between proglottids in the anterior part of the strobila, later becomes attenuated between proglottids, which separate easily. Primordia of the genital atria and cirrus-sacs first appear in the 19th-22nd proglottid and are well-developed in the 45th-53rd proglottid. Primordia of testes and female organs are visible in 2 of 4 strobila.

The proglottids are numerous, craspedote and wider than long. Mature proglottids measure 0.538-0.600 x 1.84-1.96 mm and gravid proglot- tids 0.519-0.886x3.10-3.16mm. The genital pores open in the anterior half of the lateral mar- gin and show a basic pattern of regular alter- nation. Variations from this pattern are described in more detail below. The osmoregulatory system comprises paired dorsal and ventral canals; the ventral canals have transverse anastomoses; dor-

A new cestode from an Egyptian plover 207

2

3

... ~.~q

:'~.::';' , ,~" / I . I

Figs 1-4. Pluviantaenia kassalensis n. g., n. sp. 1. Scolex. 2. Rostellar hooks. 3. Scolex in vertical longitudinal section. 4. Mature proglottid. Scale-bars: 1,4, 0.5 mm; 3, 0.1 mm; 2, 0.01 mm.

sal anastomoses are absent. The genital ducts pass dorsally to the osmoregulatory canals.

Reproduct ive organs (Figs 4-18). The genital atrium is enormous, sucker-like with longitudinal and radial muscle fibres and a massive sphincter at the distal limit of the sucker. It measures 316- 373 x 266-348 p.m in mature proglottids and 569- 633 x 494-519 ~m in gravid proglottids. The atrial sphincter is 156-188 p~m in diameter. The atrial region is protrusible. The cirrus-sac is thin-walled, oval, 203-272 x 196-203 ~m in mature proglot-

tids, and opens into the base of the genital atrium. The cirrus-sac contains a robust armed cirrus, 63- 78 ~m in diameter and 313-344 ~m long when

protruded, and prostate cells distally. The cirrus was seen to protrude in only 2 proglottids; in most proglottids it was curled in the genital atrium or retracted within the cirrus-sac. A small internal seminal vesicle (Fig. 6) is apparent in older pro- glottids. The vas deferens functions as an external seminal vesicle. The testes are numerous, ar- ranged in a band 2 -3 testes deep along the post- erior margin of the proglottid posterior to the female organs, extending laterally beyond the os-

208 Arlene Jones et al.

Fig. 5. Pluviantaenia kassalensis n. g., n. sp. Terminal genital ducts. Scale-bar: 0.3 ram.

moregulatory canals. About 36-40 were counted in whole-mounted proglottids, but the total number is probably higher as more than one hori- zontal layer is apparently present. Testes diameter is 78-125 Ixm.

The ovary is median, deeply lobed, transversely elongated, 633-759 Ixm in diameter. The vagina is postero-ventral to the cirrus-sac, opening post- erior to it into the genital atrium; it is sigmoid, dilated (53-68 Ixm in diameter) and surrounded by gland-cells, communicating through a narrow duct with the oval seminal receptacle which is approx. 130 Ixm in diameter (Figs 10,11). The vit- ellarium is median, lobed and lies between the ovary and the testicular field. The uterus is persist- ent, originating as a transverse, lobed sac with divisions gradually breaking down as eggs ac- cumulate. Because the proglottids separate easily from each other, the lobes of the uterus protrude into the interproglottidal spaces (Figs 12,13-17) and the uterine wall breaks down allowing eggs to pass into the gut lumen of the host. Most eggs are probably released from the host in the faeces rather than within proglottids. The eggs (Fig. 18) have a thin outer envelope 31.6-39 Ixm in di- ameter, widely separated from the oncosphere. The oncosphere is 17-211xm in diameter, en- closed in an envelope 22-28 Ixm in diameter; the oncospheral hooks are approximately 4-5 Ixm long.

Alternation of genital pores and duplication of genital organs. (Figs 19,20). As stated earlier, the genital pores alternate in a basically regular pat- tern but may be irregular or duplicated. In two of the four available strobila, the pores alternate regularly except for one set of 2 consecutive pro- glottids in one strobila and 5 in the other in which the pores are on the same side. In neither is there duplication of the genital atria and cirrus-sacs. The remaining 2 strobila show a basically regular sequence albeit with some irregularities but both have duplicated sets of atria and cirrus-sacs (Figs 19,20). Duplication of female organs has not been seen except for duplication of the vagina in some cases. One strobila (Fig. 19) also has centrally positioned structures which have been interpreted as misdeveloped atria. Many proglottids in the other strobila (Fig. 20) have sets of additional atrium/cirrus-sac complexes marginally or sub- marginally and in most instances they are well developed and normal in appearance.

Discussion

The presence of numerous tiny martelliform ros- tellar hooks identifies this cestode as a davaineid, but this unusual and aberrant worm exhibits sev- eral distinctive morphological characters not shared by other davaineid cestodes. The genus

A new ces tode f rom an E g y p t i a n p love r 209

Figs 6-11. Pluviantaen& kassalens& n. g., n. sp. Terminal genital ducts. 6,7. Genital atrium, cirrus-sac and cirrus in a hand- sectioned whole mount (6) and in histological section (7). 8. Sucker-like genital atrium showing radial muscle fibres and atrial sphincter. 9. Protruded genital atrium. 10, 11. Vagina and seminal receptacle in a hand-sectioned whole-mount (10) and in histological section (11).

is d i s t inguished f rom all o t h e r dava ine ids in the

unusua l s t ruc ture of the scolex. The p seudo ros t e l -

lum has been i n t e r p r e t e d as such because it is

obv ious ly ros te l l a r - l ike in s t ruc ture but does not

d i rec t ly bea r the hooks . The scolex also lacks

suckers . A b s e n c e of suckers is known in m e m b e r s

of o t h e r cyc lophy l l idean famil ies , e .g . , the d ioeco-

cest id Dioecocestus acotylus F u h r m a n n , 1904, in

210

12

Arlene Jones et al.

Fig. 12. Pluviantaenia kassalensis n. g., n. sp. Grav id proglo t t ids . Scale-bar: 1 mm.

which the character is considered of only specific significance, and the hymenolepidid Acotylolepis Yamaguti, 1959, in which it is considered gene- rically significant, but it does not occur elsewhere in the Davaineidae. Pluviantaenia is also distin- guished by its very large sucker-like genital atrium, provided with a powerful sphincter, which exceeds the size of the cirrus-sac. The cirrus-sac is itself unusual for the davaineids in being relatively large and thin-walled, enclosing a large robust cirrus armed with prominent spines. For these reasons, the specimens are considered to repre- sent a new genus and species. The generic and specific names reflect the host and locality of ori- gin of the specimens.

Following an examination of the positions of the genital pores of four available strobila, we have concluded that basically they alternate regu- larly and that variations from this norm constitute an aberrant feature of this cestode. Duplication of the genital atrium, cirrus-sac and vas deferens and the appearance of extra sets of these organs marginally or submarginally may also be aberrant. Neither feature was consistently present in all the

strobila available or in all proglottids of the two strobila in which they appeared, thus differing from the consistent duplication of cirrus-sacs, genital pores, ovaries and vitellaria found in the genera Cotugnia Diamare, 1893 and Abuladzug- nia Spasskii, 1973. No duplication of the female organs has been found in Pluviantaenia, except, in some proglottids, the vagina.

The proglottids are markedly protandrous and are shed from the strobila before development has proceeded much beyond the formation of the genital atria and cirrus-sacs, being the first organs to develop fully. The attenuation of the longitudi- nal musculature and the resultant early shedding of the proglottids are other unusual features of the genus. The distribution of the testes in a band along the posterior margin of the proglottid be- hind the female organs is unusual for a davaineid. It is possible that self-fertilization is common in this cestode as in a number of proglottids sperma- tozoa were found deposited in the genital atrium or emerging from the cirrus while the cirrus was in the atrium and the atrial sphincter contracted.

Escape of eggs from the uterus into the lumen

A new cestode from an Egyptian plover 211

Figs 13-18. Pluviantaenia kassalensis n. g., n. sp. Gravid proglottids. Stages in the breakdown of the longitudinal musculature and separation of the proglottids in horizontal longitudinal (13,14) and transverse (15-17) section. 18. Eggs.

of the gut of the host is facilitated by separation of the proglottids and breakdown of the uterine wall. Large accumulations of eggs can be seen protruding from between gravid proglottids. The eggs are shed in the faeces of the host rather than within gravid proglottids and do not appear to be

equipped to withstand desiccation. However , as the host is always found close to water, they are probably deposited into water. Possibly, an aquatic intermediary is involved in the life-cycle.

According to the traditional division of the Da- vaineidae into three subfamilies based on the nat-

212 Arlene Jones et al.

19

Figs 19-20. Pluviantaenia kassalensis n. g., n. sp. Portions of two strobila showing duplication of genital atria and cirrus sacs bilaterally and appearance of extra sets in marginal or submarginal positions. Scale-bar: 1 mm.

ure of the uterus, persistence of the uterus would class this cestode as a member of the subfamily Ophryocotylinae Fuhrmann, 1907. The traditional classification has not been adopted here because, as a result of the current lack of detailed infor- mation on the nature and origin of davaineid egg capsules, which have not been studied at the ultra- structural level, the situation is not yet well en- ough understood to separate members of the Da- vaineinae and Ophryocotylinae confidently in all cases. For the present, therefore, Pluviantaenia is considered to belong to the Davaineidae Braun, 1900 without allocation to a subfamily. The classi- fication of the family is the subject of another study which will be published separately.

A new cestode from an Egyptian plover 213

Acknowledgements

We are indebted to Mr D W Cooper, The Natural History Museum, for the preparation of serial sec- tions and to Mr R Tranfield, IIP, for photographic assistance.

References

Fuhrmann, O. (1906) Die Hymenolepis - Arten der V6gel. Zentralblatt far Bakteriologie und Parasitenkunde, 1 Abt., 41, 352-358.

Fuhrmann, O. (1909) Die Cestoden der V6gel des weissen Nils. Results. Swedish Zoological Expedition to Egypt and the White Nile, pt. 3 (27), 55 pp.