Bull. Mus. natn. Hist, nat., Paris, 4e sér., 8, 1986,

section A , n° 3 : 543-550.

Witenbergitaenia sinaica gen. n., sp. n. (Anoplocephalidae)

and other Cestodes from small Mammals

in Israel and in the Sinai Peninsula

by G u ta W E R T H E I M , G e r a ld D . S C H M I D T a nd Z a l m an G R E E N B E RG

Abstract . — Twelve species of Cestodes are reported from twenty species of small mammals reco-vered in Israel and Sinai. Eight other adult Cestodes were identified to genus only. New host and locality records are indicated in table 1 and in the text. Witenbergitaenia sinaica gen. n., sp. n., found in Acomys cahirinus in southern Sinai, differs from Markewitchitaenia and Tupaiataenia, the only other genera in Anoplocephalidae with a hermaphrodit ic canal, in having two postovarian fields of testes.

Résumé. — Witenbergitaenia sinaica n. g., n. sp. (Anoplocephalidae) et autres Cestodes parasites de petits Mammifères d'Israël et de la péninsule du Sinaï. — Douze espèces de Cestodes ont été trou-vées chez vingt espèces de petits mammifères récoltés en Israël et dans la péninsule du Sinaï. Huit autres Cestodes adultes ont été identifiés seulement jusqu 'au niveau générique. Les nouveaux hôtes et les nouvelles localités sont indiqués dans le tableau 1 et dans le texte. Witenbergitaenia sinaica n. g., n. sp., récoltée chez Acomys cahirinus dans le sud du Sinaï, diffère de Markewitchitaenia et de Tupaiataenia, les seuls autres genres d'Anoplocephal idae possédant un canal hermaphrodite, par la présence de deux champs de testicules postovariens.

G . WERTHEIM , Laboratory of Helminthology, the Hebrew University-Hadassah Medical School, Jerusalem, Israel. Temporary adress : Professeur Associée, Laboratoire de Zoologie (Vers) associé au CNRS, Muséum national d'Histoire naturelle, 61, rue Buffon, F 75231 Paris, France.

G . D. SCHMIDT , Department of Biology, University of Northern Colorado, Greeley, Co. 80639, USA. Z. GREENBERG, Laboratory of Helminthology, the Hebrew University-Hadassah Medical School, Jerusalem, Israel.

Present adress : Ministry of Health, Government Central Laboratories, P.O. Box 6115, Jerusalem, Israel.

I N T R O D U C T I O N

I n a p rev ious pub l i ca t i on (S C H M I D T , G R E E N B E RG a nd W E R T H E I M , 1986) survey d a ta on

av ian Ces todes were repo r ted as well as i n f o r m a t i on on co l lec t ion sites a nd techn iques used

i n p rocess ing a nd m o u n t i ng t he spec imens. T he present c o m m u n i c a t i on dea ls w i t h Ces-

t odes recovered f r om small m a m m a l s, mos t ly r o d e n t s.

T he ear l iest f ind ings on C e s t o d e s, pub l i shed w i t h the in i t ia t ion of he lm in tho log i cal s tu-

dies in Israel ( then Pa les t ine ), dea lt w i t h t he f auna of domes t ic a nd wi l d ca rn i vo res poss ib ly

because of t he i m p o r t a n ce of these a n i m a ls as a sou rce of h u m an in fec t ions. In s t ray d o gs

a nd ca ts, W I T E N B E R G (1932, 1933, 1934a, b) f o u nd fiv e species of D i lep id inae, o ne species

of Mesoces to id i dae (genus Mesocestoides) a nd fiv e species of T a e n i i d a e, a m o ng t h em Echi-

— 5 44 —

nococcus granulosus ( reco rded a lso f rom the j a c k al Canis aureus). F r om the p resence of

s o me of these taen i ids o ne cou ld infer t hat the ir la rval f o rms wil l be f o u nd in r o d e n ts or

o t h er small m a m m a l s. Th is was la ter p roven w h en extens ive s tud ies of these a n i m a ls were

u n d e r t a k e n. Cys t i cercus of T. taeniaeformis, for e x a m p l e, was r e p o r t ed f rom ra ts ( W E R -THEIM , 1 9 6 3) a nd f r om Nesokia indica, R o d e n t i a - M u r i d ae (G R E E N B E R G , 1 9 7 2 ). O t h er ces todes f rom r o d e n t s, so far r e p o r t ed inc lude Megittina gerbilli, Hymenolepis diminuta a nd

Vampirolepis nana ( W E R T H E I M , 1 9 5 4, 1 9 6 3 ). Vampirolepis negevi (= Rodentolepis negevi), Pseudandrya monardi a nd Mathevotaenia symmetrica ( repo r ted as M. rodentinum) ( G R E E N -BERG, 1 9 6 9) ; Sinaiotaenia witenbergi ( W E R T H E I M a nd G R E E N B E R G, 1 9 7 1) a nd Paranoploce-

phala sp. (W E R T H E I M a nd N E V O , 1 9 7 1 ).

T he p resent p a p er s u m m a r i z es f ind ings f rom e x a m i n a t i on of over t wo t h o u s a nd small

m a m m a ls as well as new host a nd loca l i ty r e c o r d s. Al l loca l i ty reco rds f rom Sinai a re

n e w. In t he d a ta on four species of Ces todes f rom r o d e n ts in Sinai p resen ted in a p rev ious

repo rt (W E R T H E I M a nd G R E E N B E R G, 1 9 7 0) on ly t he hos ts a re l is ted.

R E S U L TS

Ces todes ident i f ied in th is s tudy, as well as d a ta on hos ts a nd loca l i t ies, a re s u m m a-

r ized in tab le 1. C lass i f i ca t ion fo l lows S C H M I D T ( 1 9 8 6 ). M e a s u r e m e n ts a re in m i c r o m e t e rs un less o the rw ise s ta ted. T he let ter n ind ica tes the n u m b er of m e a s u r e m e n ts m a d e. O ne

species is recogn ized as new a nd as rep resen t ing a new g e n u s. We p lace it w i th i n t he L in -

s tow i inae because the eggs lack a py r i f o rm a p p a r a t us a nd the re is on ly o ne egg per capsu le.

D E S C R I P T I ON

W I T E N B E R G I T A E N I A gen. n.

DIAGNOSI S : Anoplocephal idae, Linstowiinae. Dorsoventrally flattened, becoming wider evenly toward the gravid segments. Immature segments wider than long, mature segments about as long as wide, gravid segments longer than wide. Scolex lacking rostellum, hooks or apical organ. Suckers round, powerful, unarmed. Neck present, narrower than scolex. Proglott ids numerous, slightly cras-pedote. Osmoregulatory canals reticulated throughout proglott id. This canal system is identical with that described for Atriotaenia procyonis (Chandler, 1 9 4 2 ), by GALLAT I ( 1 9 5 9 ), to which the reader is referred. Muscle bundles feebly developed. One set of reproductive organs per segment ; genital pores irregularly alternating. Genital atr ium well developed, lacking sphincter muscles, smaller than cirrus pouch. Genital ducts dorsal to osmoregulatory canals. Testes in two lateral fields, mainly postovarian, some lateral to ovary, between outer limit s of osmoregulatory canals. Cirrus pouch elongate, crossing outermost osmoregulatory canals, usually reaching poral edge of ovary. Cirrus absent. Internal and external seminal vesicles absent. Ovary median, with bilateral wings subdivided into slender lobes. Vitellarium with small lobes, posterior to ovary. Vagina posterior to cirrus pouch. Distal end of vagina entering, with cirrus pouch, into common hermaphrodit ic canal that enters genital atr ium. Seminal receptacle small, remaining discrete in gravid segments. Uterus deve-

— 545 —

lops as a thin-walled, reticular sac, which quickly fill s and disappears, leaving abundant developing eggs evenly scattered throughout the medullary parenchyma. Oncospheres each surrounded by a single, thin-walled membrane ; pyriform apparatus absent.

TYP E SPECIES : Witenbergitaenia sinaica sp. n.

Witenbergi taenia sinaica sp. n.

(F ig. 1, A to D)

MATERIA L STUDIED : One specimen found in 1 out of 152 host-animals examined.

DESCRIPT IO N

W i t h t he cha rac te rs of t he genus, as descr ibed a b o v e. Scolex (f ig . 1A) a b o ut 480 long

(measu red to pos te r i or cons t r i c t i on of sco lex), 640 greatest w i d t h. Suckers r o u n d, 175 to

200 w ide. Neck n a r r o w er t h an scolex, a b o ut 1.0 mm long. S t rob i la 71 mm long

(a l t hough as m u ch as o n e - f o u r th m ay be miss ing in the p r e p a r ed s l ide), a b o ut 1.5 mm wide

i n m a t u re p o r t i o n, 2 .0 mm w ide in g rav id segmen ts. P r o g l o t t i ds sl ight ly c r a s p e d o t e, a n a-

po ly t i c. M a le a nd female g o n a ds (f ig . IB ) m a t u re at s a me t i m e. Gen i t al duc ts do rsal to

o s m o r e g u l a t o ry cana ls (f ig . 1C).

Male genitalia : 41 to 62 testes (n = 7) in t wo fields of 23 to 29 (pora l) a nd 18 to 33

(apo ra l ), ma in ly pos te r i or to o v a r y. Tes tes (n = 23) 60 to 100 wide in m a t u re segmen ts.

C i r rus p o u ch (f ig . 1C) (n = 7) e l onga te, n a r r o w ed p rox ima l l y, usua l ly reach ing but n ot

exceed ing p o r al m a r g in of o v a r y, 240 to 270 long, 60 greatest w i d t h. I n te rnal a nd ex te rnal

seminal vesicles absen t. E j a c u l a t o ry duct a nd vas deferens co i led. C i r rus a b s e n t.

Female genitalia : O v a ry m e d i a n, w i t h b i la te ral w ings subd iv ided i n to lobu les ; not reach-

ing ma in la teral o s m o r e g u l a t o ry cana ls ; m a x i m um size (n = 7) 345 to 480 l ong, 560 to

680 w ide. V i te l la r ium (n = 7) pos te r ior to ova ry, l o b a t e d, 160 to 200 l ong, 175 to 255 g rea-

test w i d t h. V a g i na pos te r i or to c i r rus p o u c h, u n a r m e d, p roceed ing d i rect ly to seminal

receptac le, wh ich lies be tween ova ry a nd v i te l l a r ium. Seminal receptac le (n = 7) a s imp le

sac 120 to 140 long, 60 to 90 w ide in m a t u re s e g m e n t s, s lender w i t h a single l o op in g rav id

segmen ts. D is tal end of vag ina jo ins h e r m a p h r o d i t ic duct w i t h c i r rus p o u ch be fo re open ing

i n to geni tal a t r i u m. A t r i u m (n = 7) 70 d e e p, 20 to 30 w ide at d is tal e n d, 10 w ide at b a s e,

n ot except iona l ly m u s c u l ar or g l a n d u l a r. Eggs (f ig . I D ) s u r r o u n d ed by single m e m b r a n e,

54 to 64 w ide (n = 10). O n c o s p h e r es 30 to 40 w ide ; o n c o s p h e re h o o ks 14 to 16 l ong.

TYP E HOST : Egyptian spiny mouse, Acomys cahirinus[ Desm., 1819. Rodentia, Muridae. LOCATIO N : Small intestine. LOCALIT Y : Wadi Atzvira (Southern Sinai). TYP E SPECIMEN : M N H N (Museum national d'Histoire naturelle, Paris) holotype n° 641 HB. ETYMOLOG Y : The genus is named in honor of the late Professor George WITENBERG , who pio-

neered in helminthology in Israel.

1. In a previous publication (WERTHEI M and GREENBERG, 1 9 7 0) the Acomys from Sinai was temporaril y named A. dimidiatus. Professor WAHRMA N inform s us (personal communication) that at a later date, it was chosen, for the time being, to use the name A. cahirinus for all the chromosomal forms.

— 546 -

FIG . 1. — Witenbergitaenia sinaica sp. n. from Acomys cahirinus : A , scolex ; B , mature proglotti d ; C, terminal genital ducts ; D , egg.

D ISCUSSION

T o d a te the re a re t wo gene ra in the a n o p l o c e p h a l id sub fami ly L i ns tow i i nae w i t h a c o m-

m on h e r m a p h r o d i t ic canal as in the p resent species : Markewitchitaenia Sha rp i lo a nd

K o r n y u s h i n, 1975, a nd Tupaiataenia Schm idt a nd Fi le, 1975. Tupaiataenia, f r om t ree

sh rews, is u n i q ue in possess ing a c i r rus a nd m u s c u l ar l appe ts on the suckers.

T he p resent species is m o st s imi lar to Markewitchitaenia b ut c lear ly d i f fers f rom it i n

hav ing t wo la teral f ields of la rge tes tes, ins tead of a single field of small tes tes.

— 547 —

Because t he p resence of t wo fields of testes versus o ne field has t rad i t i ona l ly been

accep ted as a gener ic cha rac ter (as in Kowalewskiella, Schizorchis, Cycloskrjabinia, Latero-

taenia a nd m a ny o thers) we p r o p o se o ur new species to represent a new genus a nd n a me it

Witenbergitaenia.

I n o rder to s h ow that W. sinaica is n ot a dev iant M. rodentinum ( J o y e u x, 1927) — the

on ly species in Markewitchitaenia — the fo l lowin g c o m p a r i s o ns a re g iven : (1) t he grav id

s t rob i la of M. rodentinum is a b o ut 44 mm long by 710 /un greatest w id th, c o m p a r ed w i t h

at least 70 mm long by 2 .0 mm greatest w id th in W. sinaica ; (2) t he c i r rus p o u ch of

M. rodentinum is 137 to 154 /un long by 33 to 38 /un w ide a nd reaches t he mid l i ne level of

the ova ry, whi l e t hat of W. sinaica is 240 /un long by 64 /un w ide a nd bare ly reaches t he

p o r al edge of t he ova ry ; (3) t he to tal n u m b er of testes is 33 to 47 (usual ly 38 to 40) in

M. rodentinum, c o m p a r ed w i t h 41 to 62 in W. sinaica. T h us i t is c lear t h at t wo d i f ferent

species a re rep resen ted.

Acknowledgments

The authors wish to express their gratitude to Pr Y . SCHLEIN , Department of Parasitology, The Hebrew University-Hadassah Medical School, for his help in collecting the animals. Thanks are due to Mrs Hermina ZYLBERMAN , Mrs Simona RADAI , Mr M . MUALLE M and Mr Y . GATTA S for technical

assistance. G . W . , on sabbatical leave from the Hebrew University, wishes to express her appreciation to the

Department of Biological Sciences, University of Northern Colorado, for its cooperation and hospita-lit y during the period of this research.

TABL E 1. — Cestodes from small mammals of Israel and Sinai.

HOST CESTODE LOCALIT Y * H U J P

Vaucher no.

Acomys cahirinus Desm., 1819 Hymenolepis diminuta (Rudolphi, Bar Giyora, Zova 1943 1819)

Witenbergitaenia sinaica gen. n., t Wadi Atzvira S140 sp. n.

***Mathevotaenia symmetrica (Bay- Elat, t Sharm el Sheikh, S211 lis, 1927) f W a di Azvira, t Wadi

Latai, t Wadi Ajar Mathevotaenia sp. Timna 2025 Pseudandrya monardi Fuhrmann, Jerusalem, **Bet Alpha, 232

1943 Ein Far 'a Tetrathyridium Jerusalem, Zova, Dimona,

Ein Hussub, t Mitl a Pass, t Monastery of St. Catherine, t Wadi Kid, t Wadi Abu G'eada

Vampirolepis nana (Siebold, 1852) Jerusalem, t Monastery of S275 St. Catherine

— 548 —

HOST CESTODE LOCALIT Y *HUJP

Vaucher no.

Vampirolepis negevi (Greenberg, Elat, Yotvata, Wadi Mé- 2039 1969) nayeh, t D a h ab | E1

Tur, t Ras Nusrani, f Wadi Isla, t Wadi Kid

Acomys russatus Wagner, Tetrathyridium Masada 1840

Apodemus mystacinus Danf. Paranoplocephala sp. **Ei n Hemed 524A and Alst., 1877

Taenia taeniaeformis (Batsch, 1786) """Jerusalem, **Ei n He-strobilocercus med

Gerbillus (Dipodillus) dasyu- Meggittina gerbilli (Wertheim, 1954) **Elat , "Jerusa lem, f Ge- 1956 rus Wagner, 1842 bel Abu Zarub, t Mo-

nastery of St. Cathe-rine, t Wadi Abu G'ea-da

Sinaiotaenia witenbergi Wertheim t Gebel Yi'allaq S486 and Greenberg, 1971

Taenia sp. coenurus Ein Hazeva Tetrathyridium t Gebel Yi'allaq

Gerbillus allenbyi Thomas, ***Raillietina (R.) trapezoides (Ja- **Herzliya, **Caesarea 854A 1918 nicki, 1904)

Gerbillus gerbillus Olivier, Mathevotaenia symmetrica t Abu Rudeis, f El Tur, S53 1801 t N a bq

***Meggittina gerbilli **Be'er Sheva, t M i t l a 2203 Pass

***Raillietina (R.) trapezoides **Be'er Sheva Sinaiotaenia witenbergi t Wadi Nafk ***Taenia pisiformis (Bloch, 1780) f Abu Zenima, t Bir Gaf- S65

cysticercus gafa Gerbillus pyramidum Geof- ***Mathevotaenia symmetrica t Ras Sudar, t Sharm el S386

froy, 1825 Sheikh Meggittina gerbilli Be'er Sheva, Holon, **Pal- 862

machim, **Rishon le Ziyon, t Bir Gafgafa

***Raillietina (R.) trapezoides Be'er Sheva, **Hadassim, **Holon , **Palmachim, **Rishon le Ziyon

Taenia taeniaeformis strobilocercus **Holo n 81 Jaculus jaculus L., 1758 ***Raillietina (R.) trapezoides t Sabkhet el Bardawil, S489

t El 'Arish Meriones crassus Sund., 1842 ****Hymenolepis sp. Wadi Taiyiba S288

***Meggittina gerbilli t Mitl a Pass S470 ***Raillietina (R.) trapezoides **Nizana 1608 Sinaiotaenia witenbergi t Mitl a Pass, t Wadi Ak- S470

dar ***Taenia sp. polycephalus cyst **Ei n Yahav Tetrathyridium t Mitl a Pass

Meriones sacramenti Thomas, Hymenolepis diminuta Holon 857 1922

***Raillietina (R.) trapezoides Holon, Palmachim, **Ne - 858 bi Rubin

— 549 —

HOST CESTODE LOCALIT Y * H U J P Vaucher no.

Meriones tristrami Thomas, 1892

Microtus guentheri Danf. and Alst., 1880

Mus musculus L., 1758

Nesokia indica Gray and Hardw., 1832

Procavia capensis Pallas, 1766 Psammomys obesus Cretzmar,

1828 Rat tus rat tus L., 1758

Rat tus norvegicus Berk, 1769

Sekeetamys calurus Thomas, 1892

Hymenolepis diminuta ****Hymenoiepis sp. ***Raillietina (R.) trapezoides ***Vampirolepis nana ***Taenia pisiformis Cysticercus Tetrathyridium ****Andrya sp.

Vampirolepis nana Catenotaenia pusilla (Goeze, 1782) Hymenolepis diminuta Taenia taeniaeformis strobilocercus ****Inermicapsifer sp. ***Raillietina (R.) trapezoides

Hymenolepis diminuta Vampirolepis nana Hymenolepis diminuta Taenia taeniaeformis strobilocercus Vampirolepis nana ****Hymenolepis sp. Hymenolepis sp. (juv.) Sinaiotaenia witenbergi

***Taenia pisiformis Cysticercus

Spalax ehrenbergi Nehring, ****Paranoplocephala sp. 1898

**Mishmar Ha 'Emek 19 Mishmar Ha 'Emek 465 **Mishmar Ha 'Emek 37 **Mishmar Ha 'Emek 16 **Mishmar Ha 'Emek 8 Akk o Mishmar Ha 'Emek 105

Mishmar Ha 'Emek 290 **Aminadav 511A Jericho 2204 Jericho Gilboa 1657 **Jericho

Tel Aviv , **Rosh Pina 1642 **Rosh Pina Haifa, Tel Avi v (ports) Tel Aviv Haifa, Tel Avi v (ports) Gebel Abu Zrur S382 t Gebel Sorbal S66 t Gebel el Tin, t Wadi el

Sheikh **Wadi Milhek, t Gebel

Abu Zrur S382 Kuneitra N24

*HUJ P : Hebrew University Jerusalem, Parasitológica! Collection, t A site in the Sinai peninsula. **Ne w locality record in Israel. ***Ne w host record. ****T o be discussed in a later publication as it may represent a new species.

LITERATURE CITED

GALLATI , W. W., 1959. — Lif e history, morphology and taxonomy of Atriotaenia (Ershovia) pro-cyonis (Cestoda : Linstowiidae), a parasite of the raccoon. J. Parasit., 45 : 363-377.

GREENBERG, Z ., 1969. — Helminths of mammals and birds of Israel. I. Helminths of Acomys spp. (Rodentia, Murinae). Israel J. Zool., 18 : 25-38.

— 1973. — Helminths of birds and mammals from Israel. IV . Helminths from Nesokia indica Gray and Hardwicke, 1832 (Rodentia, Muridae). Israel J. Zool., 21 : 63-70.

SCHMIDT , G. D., 1986. — Handbook of Tapeworm identification. CRC Press, Boca Raton, 675 p.

SCHMIDT , G. D ., and S. FILE , 1977. — Tupaiataenia quentini gen. et sp. n. (Anoplocephalidae : Lin-stowiinae) and other tapeworms from the common tree shrew, Tupaia glis. J. Parasit., 63 : 473-475.

— 550 —

SCHMIDT , G . D ., Z. GREENBERG, and G . WERTHEIM , 1986. — Raillietina {Raillietina) a lectori sp. n. and other avian Cestodes from Israel and Sinai. Bull. Mus. natn. Hist, nat., Paris, 4e ser., 8, section A , (1) : 101-109.

SHARPILO , V. P ., and V. U. KORNYUSHIN , 1975. — A new genus of cestodes : Markewitchitaenia gen. nov. (Cestoda, Linstowiidae). Parazity i Parazitozy Zhivotnych i Cheloveka, Kiev, USSR « Naukova Dumka » : 217-222.

WERTHEIM , G . , 1954. — A new anoplocephalid cestode from the gerbil. Parasitology, 44 : 446-449.

— 1963. — Helminth parasites of the rat Rattus norvegicus from Haifa and Tel-Aviv. Bull. Res. Coun. Israel, 10 E : 125-129.

WERTHEIM , G . , and Z. GREENBERG, 1970. — Notes on Helminth parasites of myomorph rodents from Southern Sinai. J. Helminth., 44 : 243-252.

WERTHEIM , G . , and Z. GREENBERG, 1971. — Helminths of mammals and birds from Israel. II . Sinaio-taenia witenbergi gen. et sp. n. (Cestoda Anoplocephalidae) from desert rodents. Proc. Hel-minth. Soc. Wash., 38 : 93-96.

WERTHEIM , G . , and E. NEVO , 1971. — Helminths of birds and mammals from Israel. I I I . Helminths from chromosomal forms of the mole-rat, Spalax ehrenbergi. J. Helminth., 45 : 161-169.

WITENBERG , G . , 1932. — On the cestode subfamily Dipylidiinae Stiles. Z. ParasitK.de., 4 : 542-584. — 1933. — Zur Kenntnis der Verbreitung von Echinokokkus und Trichina in Palestina. Arch.

Schiffs-u. Tropenhyg., 37 : 37-41. — 1934a. — Parasitic worms of dogs and cats in Palestine. The Veterinary Record, 14 : 232-239.

— 19346. — Studies on the cestode genus Mesocestoides. Archo zool. ital., 20 : 467-507.

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