C
e r c o p it h if il a r ia s h o h o i n.
s p. ( N
e m a t o d a: F
il a r io id e a) FROM THE RELICT BOVIDAE, C A PR IC O R N IS CRISPUS, IN JAPAN
UNI S.*, SUZUKI Y.** & KATSUMI A.***
S u m m ary :
Cercopithifilaria shohoi n. sp. was found in the relict bovid, Capricomis crispus, in Japan, and is described and compared with other species in the genus. Adult male and female worms were found in subcutaneous tissues of the trunks of 6 serows shot in Mt. Zao, Yamagata Prefecture, in the northern part of Honshu, the largest island of Japan. The one complete male found was
19.7 mm long, and the five females were 31.6-50.9 mm long.
Unsheathed or sheathed microfilariae 104-122 μm long were taken from the females. One microfilaria was found in the sediment of the preservation solution of the tissues, but none were found in the blood of the infected serows, so microfilariae may be limited to the skin. Males of this species had one pair of papillae between perianal and subterminal groups of caudal papillae. In having this intermediate pair, C. shohoi n. sp. resembled species such as C. faini from an African bovid and C. rugosicauda from a European deer. From its morphological characteristics, C. shohoi n. sp. seems to be one of the more primitive species in the genus Cercopithifilaria.
KEY WORDS : Nematoda, Filarioidea, Cercopithifilaria shohoi n. sp., Bovidae, Capricornis crispus, Japan.
R é s u m é : Ce r c o p it h if il a r ias h o n o in. s p. ( Ne m a t o d a :
Fil a r io id e a) c h e zle b o v i d é r e l iq u e Ca p r ic o r n isc r is p u s, a u Ja p o n
Cercopithifilaria shohoi n. sp. retrouvé chez le bovidé relique Capricornis crispus, au Japon, est décrit et comparé aux autres espèces du genre. Des vers adultes mâles et femelles ont été trouvés dans les tissus sous-cutanés du tronc de 6 serows du Japon abattus au Mont Zao, dans la Préfecture de Yamagata, dans la région nord du Honshu, la plus grande île du Japon. Le seul mâle complet qui ait été trouvé mesurait 19,7 mm de long, et les cinq femelles mesuraient de 31 ,6 à 5 0 ,0 mm de long. Des
microfilaires dégainées ou gainées de 104 à 122 μm de long ont été relevées sur les femelles. Une microfilaire a été trouvée dans le sédiment de la solution de conservation des tissus, mais aucune n'a été trouvée dans le sang des serows infectés ; ainsi, il semblerait que les microfilaires résident uniquement dans la peau.
Les mâles de ce genre avaient une paire de papilles entre les groupes périanal et subterminal des papilles caudales. Du fait de cette paire intermédiaire, C. shohoi n. sp. ressemble à des espèces comme C. faini d'un bovidé africain et C. rugosicauda du cerf européen. D'après ses particularités morphologiques, C. shohoi n. sp. semble être une espèce relativement primitive du genre Cercopithifilaria.
MOTS CLÉS : Nematoda, Filarioidea, Cercopithifilaria shohoi n. sp., Bovidae, Capricornis crispus, Japon.
INTRODUCTION _____
T
he genus C e rco p ith ifila ria was named originally as a subgenus by Eberhard (1980) for a parasite o f an African primate, and em ended
* Department o f Medical Zoology, Osaka City University Medical School, Abeno-ku, Osaka 545-8585, Japan.
** Laboratory of Veterinary Anatomy, Faculty of Agriculture, Gifu Uni
versity, Gifu 501-1193, Japan.
*** Animal Husbandry Research Center, Yamagata-ken Agricultural Co-op, Yamagata 990-0894, Japan.
Correspondence: S. Uni.
Tel: +81-6-645-2066 - Fax: +81-6-646-3590.
E-mail: uni@msic. med. osaka-cu. ac. jp Parasite, 1998, 5, 119-126
as a genus by Bain et al. (1982). Bain e t al. (1982) des
cribed many species o f the genus C erco p ith ifila ria in Africa, and placed som e species o f D ip e ta lo n em a and other genera into the genus C ercopithifilaria. Host ani
mals, found throughout the world, range from marsu
pials to primates. Chabaud & Bain (1994) suggest that the means by which the genus C ercop ith ifila ria under
w ent evolutionary expansion is unusual. The purpose o f this report is to describe C erco p ith ifila ria s h o h o i n.
sp. from an ungulate, the Japanese serow ( C a p rico m is crispus), a relict Bovidae, Rupicaprinae, and to iden
tify the relationship o f the species to other species among the genus in terms o f m orphological features, geographic distribution, and evolution. This species is the second in this genus to be reported in Jap an ; the first was C. j a p o n ic a (Uni, 1983) from black bears.
Mémoire 119
UNI S., SUZUKI Y. & KATSUMI A.
MATERIALS A N D METHODS
J
apanese serows (C a p r ic o rn is crispu s) seem to be one o f the most primitive species o f bovids (Ima- izumi, 1966). Serows inhabit mountains higher than 1,000 m. Thirty-one Jap an ese serow s w ere killed within a three-w eek period (February 16, February 23, and March 2) in 1997 on Mt. Zao (1,841 m) in Yama- gata Prefecture in the northern part o f Honshu, the main island o f Japan, in accordance with the policy o f the Agency o f Cultural Affairs, Japan, concerning the conservation and control o f Jap anese serows.Serows shot in the mountains w ere immediately trans
ferred to the Animal Husbandry Research Center in Yamagata City and necropsied by m embers o f the staff o f the Japan Wildlife Research Center (Tokyo). Tissues in which parasites w ere seen w ere stored in 2 % for
malin in saline, and later the worms w ere removed from the tissues under a dissection m icroscope. Blood smears were made from samples from each animal and stained with Giem sa’s solution, but skin snips w ere not made.
O ne microfilaria found in the sediment o f the preser
vation solution for tissues was stained with G iem sa’s solution. Microfilariae w ere taken from the terminal part o f the uterus o f som e o f the preserved adult females. Part o f the midbody o f a female worm was em bedded in 2 % agar in phosphate-buffered saline, sectioned, and stained with hematoxylin and eosin.
Drawings o f the worms w ere made with a camera lucida. Three female worms were studied by scanning electron m icroscopy (SEM) by methods reported pre
viously (Uni, 1983). The ages o f the serows w ere esti
mated by researchers at the Jap an Wildlife Research Center, w ho counted the rings on the horns. Sixteen ticks w ere collected from the serows, and kept alive in a plastic tube containing a small piece o f wet filter paper.
All parts o f three Ja p a n e se serow s shot betw een D ecem ber 1983 and March 1984 in Gifu Prefecture o f the central part o f Honshu w ere preserved in 10 % for
malin, and connective tissues were exam ined for para
sites on April 9, 1997.
DESCRIPTION
Ce r c o p i t h i f i l a r i a s h o h o i n. s p.
General: Filarioidea, O nchocercidae (Leiper, 1911) Cha- baud & Anderson, 1959; O nchocercinae Leiper, 1911;
C e rc o p ith ifila ria (Eberhard, 1980) Bain, Baker & Cha- baud, 1982.
Small, slender nem atodes inhabiting subcutaneous co n n e ctiv e tissues. A nterior en d slightly b u lbo u s (Fig. 1); eight circumoral papillae on cephalic plate elongated along lateral axis: two laterodorsal and two lateroventral at corners o f cephalic plate in outer circle, and four small papillae in inner circle. Amphidial pores at lateral side (Fig. 2). Small, refractile, pre-esophageal cuticular ring at the anterior end (Fig. 3 ). Esophagus short, simple, and not divided into anterior muscular and posterior glandular portions (Fig. 1). Cuticle with transverse striations. Tail o f fem ale terminated with three conical protuberances (Fig. 4). Caudal papillae o f male at perianal area, area betw een anus and sub
terminal end, and subterminal area (Fig. 5). Many microfilariae from uteri w ere unsheathed, but som e w ere sheathed. Parasites o f Jap an ese serows.
MALE
(O ne com plete specim en and two posterior parts):
Body 19.7 mm long, midbody 102-122 (m ean, 115) μ m wide. Nerve ring 104 μm from anterior end. Eso
phagus 510 μm long. Ratio o f esophageal length to body length 2.6 %. Tail 166-172 (169) μ m long, tapered, with three conical protuberances (Fig. 5).
Perianal papillar group: Single, mid-ventral, sessile papilla immediately anterior to anus; one pair o f small papillae immediately posterior to anus; four pairs o f pedunculate papillae lateral to anus.
Intermediate group: O ne pair o f pedunculate papillae located subventrally approximately halfway betw een anus and posterior end.
Subterm inal group: Tw o pairs o f sem ipedunculate papillae and one pair o f phasmidial pores present just anterior to posterior end.
Caudal end terminated in a cuticular cone and two cuti
cular petaloid appendages. Narrow caudal alae present.
Spicules w ere dissimilar in structure and o f unequal lengths (Fig. 6 ); left spicule 257-286 (269) μm long, divided into shaft and lam ina; right spicule with bul
bous end 68-70 (69) μm long; spicule ratio 3.8-4.1 (3.9). G ubernaculum absent. Area rugosa present at coiled caudal region o f the males. Raised transverse bands numbering 117-124 (121) each with longitudinal striations found on the ventral surface, extending from the anterior border 1,404-1,560 (1,482) μ m from the anus to the posterior border 156-338 (247) μm from the anus.
FEMALE
(Five com plete specim ens, two anterior parts, and three posterior parts): Body 31.6-50.9 (41.4) mm long, m idbody 112-158 (141) μm wide. Microfilariae w ere in the uteri at the midbody level (Fig. 7). T he small round mouth was surrounded by elevated cuticle when view ed by SEM (Figs. 8 and 9). Nerve ring 192-245
120 Mémoire Parasite, 1998, 5, 119-126
Figs. 1-6. —
Cercopithifilaria shohoi
n. sp. 1. Female anterior end; lateral view. 2. En face view of head of female. 3. Enlarged anterior end; lateral view. 4. Female posterior end; lateral view. 5. Male posterior end; ventral view. 6. Male posterior end; lateral view; Scale bar, micrometers.P a ra s ite , 1 9 9 8 , 5 , 1 1 9 -1 2 6
Mémoire 121
UNI S., SUZUKI Y. & KATSUMI A.
Fig. 7. — Cercopithifilaria shohoi n. sp .; stained cross-section of mid
body o f female. Lateral internal thickening o f the cuticle (arrow).
Scale bar, micrometers.
(2 2 0 ) μ m fro m a n te rio r e n d (F ig. 1). E s o p h a g u s 632- 8 4 7 (7 0 8 ) μ m lo n g . R atio o f e s o p h a g e a l le n g th to b o d y le n g th 1 .7 -2 .3 ,% ( 1 .7 % ). V u lv a 643-999 (830) μ m fro m a n te rio r e n d , at a p o s te s o p h a g e a l p o sitio n . C u ticle w ith fin e tra n s v e r s e stria tio n s at in te rv a ls o f 0 .4 -1.3 μ m o n part o f th e m id b o d y (F ig. 10). T ail 203-294 (2 4 5 ) μ m lo n g , ta p e r e d to w a r d tip , c u r v e d v e n tr a d , w ith th re e c o n ic a l p r o tu b e r a n c e s (F ig . 1 1 ) .
MICROFILARIAE
( 1 5 s p e c im e n s fro m te rm in a l p a rt o f u te ri o f fe m a le s ):
10 4 -12 2 (1 0 9 ) μ m lo n g b y 5 -10 (7 ) μ m w id e . D e lic a te s h e a th w a s fo u n d o n s o m e m ic r o fila ria e (F ig . 12 ), b u t m a n y m ic ro fila ria e at th e te rm in a l p a rt o f th e u te ru s w e r e u n s h e a t h e d ( F ig . 1 3 ) . A n t e r io r e n d b lu n t ly r o u n d e d , a n d r e f r a c t ile a p p a r a tu s a t h e a d o f th e c e p h a lic s p a c e . T h e p o s te r io r p art a fte r th e p h a sm id s ta p e r e d s h a r p ly (F ig . 13 , a rro w ). T h e m ic r o fila r ia e w e r e fla tte n e d d o rs o v e n tra lly .
O n e m ic ro fila ria ta k e n fro m th e s e d im e n t o f th e p r e s e r v a tio n s o lu tio n m a tc h e d th e m ic ro fila ria e ta k e n fro m fe m a le s p e c im e n s o f C. s h o h o in. sp . (F ig . 14 ). M ic ro fila r ia e w e r e n o t fo u n d in th e b lo o d s m e a rs o f th e in fe c t e d s e r o w s o r 20 h is to lo g ic a l s e c tio n s o f c o n n e c tiv e tissu e s. F o u r la r g e tic k s ( H a e m a p h y sa liss p .) w e r e s e le c t e d a n d d is s e c te d th r e e w e e k s later, b u t la rv a e o f filarial p a r a s ite s w e r e n o t fo u n d .
T h is d e s c r ip tio n w a s b a s e d o n th e s p e c im e n s fro m Y a m a g a ta P r e fe c tu re . T h e p a ra s ite s w e r e fo u n d in six s e r o w s all 0.5-9-5 y e a r s o ld , a lth o u g h th e s e r o w s e x a m in e d w e r e u p to 20 y e a r s o f a g e .
S p e c im e n fro m G ifu P re fe c tu re : O n e fe m a le s p e c im e n w a s f o u n d in th e c o n n e c t iv e tis su e o f a h in d le g o f a J a p a n e s e s e r o w . B o d y 49.0 m m lo n g , m id b o d y 14 3 μm w id e . N e r v e r in g 2 4 7 μm fr o m a n te r io r e n d . E s o p h a g u s 969 μ m lo n g . R a tio o f e s o p h a g e a l le n g th to b o d y le n g th 2.0 % . V u lv a 1 ,2 5 5 μm fro m a n te rio r e n d . T a il 234 μm lo n g , w ith th r e e c o n ic a l p r o tu b e r a n c e s . M ic r o fila ria e ( fiv e s p e c im e n s fro m te r m in a l p a rt o f u te ru s): 1 0 9 - 1 1 7 ( 1 1 4 ) μm lo n g , a n d 5-8 ( 7 ) μm w id e . T h e y w e r e u n s h e a th e d .
M o r p h o lo g ic a l c h a ra c te r is tic s, in c lu d in g p r e - e s o p h a - g e a l c u tic u la r rin g a n d u n d iv id e d e s o p h a g u s o f th e fe m a le , a n d th e m e a s u r e m e n ts o f th is fe m a le a n d th e m icro fila ria e c o r r e s p o n d e d w ith th o s e o f th e s p e c im e n s fro m Y a m a g a ta P r e fe c tu re d e s c r ib e d a b o v e .
T y p e h o st: C a p r ic o m is c r is p u s ( T e m m in c k , 18 4 5 ).
L o c a tio n in h o st: S u b c u ta n e o u s c o n n e c t iv e tis su e s o f tru n k.
T y p e lo c a lity : Mt. Z a o , Y a m a g a ta P r e fe c tu re , J a p a n . T y p e s p e c im e n s : H o lo t y p e ( m a le ) , M u s e u m N a tio n a l d ’H istoire N atu relle, Paris, N o . 3 18 S E ; a llo ty p e (fe m a le ) at th e s a m e p la c e . O th e r s p e c im e n s h a v e b e e n d e p o sited in th e D e p a rtm e n t o f M e d ic a l Z o o lo g y , O s a k a C ity U n iv e rs ity M e d ic a l S c h o o l.
E ty m o lo g y : In h o n o r o f D r. C h u z a b u r o S h o h o , J a p a n e s e p a r a s ito lo g is t.
DISCUSSIO N __________ _____
C
e r c o p ith ifila r ia s h o h o i n. sp . w a s f o u n d in J a p a n e se s e r o w s (C a p r ic o m is crisp u s)in Y a m a g a ta a n d G ifu P r e fe c tu r e s in th e n o r th e rn a n d c e n tra l p arts o f H o n s h u . T h e m a n y c a u d a l p a p illa e o f th e m a le s a n d th e s o m e w h a t lo n g e s o p h a g u s o f th e fe m a le s , w h ic h a re c h a ra c te r is tic s k e y to th e c la ss ific a tio n o f th e s p e c ie s , s e e m e d to b e p rim itiv e fo r s p e c ie s in th is g e n u s .
A c c o r d in g to B a in e t al. (1 9 8 2 ) a n d C h a b a u d & B a in (1 9 9 4 ), 22 s p e c ie s h a v e b e e n p la c e d in th is g e n u s : (a ) 12 s p e c ie s fro m A fr ic a ; C . k e n y e n s is E b e rh a rd , 1980, C. d e g r a a ffi B a in et a l., 19 8 2 , C. n a r o k e n s is B a in e t a l., 1988, C. e b e r h a r d i B a in et a l., 198 8, a n d C. v erveti B a in e t a l., 19 8 9 fr o m p rim a te s p e c ie s , C.
m a n d a e (F a in & H e rin , 19 5 5 ), C. d e r m ic o la (F a in , 1 9 7 7 ) , C . f a i n i ( C h a b a u d e t a l., 19 7 8 ), a n d C . c e p h a - lo p h i B a in e t a l., 19 8 2 fro m u n g u la te s , C. g a b o n e n s is B a in e t a l., 19 8 2 a n d C . r o u s s ilh o n i B a in e t a l., 198 6 fro m a ro d e n t, a n d C . c o m e t iB a in e t a l., 1 9 8 7 fr o m a c a r n iv o r e ; ( b ) fiv e s p e c ie s fro m N o rth a n d S o u th A m e ric a ; C . le p o r in u s B artlett, 19 8 3 fro m a h a re , C . d id e l- p h i s (E s s lin g e r & S m ith , 19 7 9 ) fro m m a rs u p ia ls , C.
g r a s s i i ( N o e , 19 0 7 ) ( c ite d in B a in e t a l., 19 8 2 ; A lm e id a
& V ic e n te , 19 8 2 ) a n d C . b a in a e A lm e id a & V ic e n t e , 198 4 fro m a c a rn iv o r e , a n d C. v e n e z u e le n s is(E b e rh a r d
1 2 2 - Parasite, 1998, 5, 119-126
Mémoire
Figs. 8-11. — SEM o f Cercopithifilaria shohoi n. sp. 8. En face view o f head of female. The mouth is surrounded by an elevated cuticular ring ( * ). Papillae (arrows), A; amphid. 9. Enlarged mouth opening with cuticular ring (arrow) o f another female specimen. 10. Trans
verse striations on cuticle o f midbody of female. 11. Posterior end o f female with three conical protuberances. Scale bar, micrometers.
Parasite, 1998, 5, 119-126
Mémoire 123
UNI S., SUZUKI Y. & KATSUMI A.
Figs. 12-14. — Microfilariae o f Cercopithi- fila r ia shohoi n. sp. 12. Delicate sheath of anterior part o f microfilaria taken from female (arrow). 13. Unsheathed microfi
laria taken from fem ale, with sharply tapered tail end (arrow). 14. Microfilaria stained with Giemsa’s solution. Scale bar, micrometers.
e t al., 1993) from armadillos (Edentata), (c) two spe
cies from E u rop e; C . g r a s sii from a carnivore and C.
r u g o s ic a u d a (Bohm & Supperer, 1953) from an ungu
late, (d) two species from Asia; C. la e m m le r i (Dasgupta e t al., 1978) from a rodent, and C. ja p ó n i c a (Uni, 1983) from a carnivore, and (e) two species from Australia;
C. j o h n s t o n i (Mackerras, 1954) from marsupials and rodents and C. p e a r s o n i (Spratt & Varughese, 1975) from a marsupial. C. b a in a e was nam ed only on the basis o f m orphological differences o f the microfilariae from those o f C. g r a s sii, and the drawing was not published in the original paper (Almeida & Vicente, 1984). C. v e n e z u e le n s is was reported as a new genus, S tr ia n e m a (Eberhard et a l ., 1993), but it was later placed in the genus C e r c o p ith ifila ri a (Chabaud & Bain, 1994).
C . s h o h o i n. sp. can be distinguished from these spe
cies from these characteristics: the length and features o f sp icu les, num bers and arrangem ent o f caudal papillae o f males, lengths o f microfilariae and adults, features o f the posterior ends o f fem ales and males, and the relation o f the position o f the vulva to the eso phageal end. By light microscopy, longitudinal stria- tions w ere seen under or on the cuticle, but by SEM, the cuticle was striated only transversely. The cuticle with fine transverse striations o f C. s h o h o i n. sp.
seem ed to be slightly different from that with thicker striations o f C. v e n e z u e le n s is (Eberhard et a l., 1993), but C . s h o h o i n. sp. differed more clearly in having both a p re-esophageal cuticular ring and an area rugosa, and in the microfilariae not having a filamen
1 2 4
tous tail. From the m orphological characteristics o f a p re-eso p h ageal cuticular ring and undivided e s o phagus, the species described in our report belongs in the genus C e r c o p ith ifila r ia . C . ja p o n i c a in black bears (U rsu s th ib e ta n u s ) in Jap an has b een described (Uni, 1983, 1984, Uni e t a l., 1995), and can be distin
guished from C. s h o h o i n. sp. by its large microfilariae (about four times longer), the dilatation o f the ante
rior part o f the female, and the few papillae o f the male.
O f the five species found in ungulates, C. s h o h o i n. sp.
may b e closely related to C. f a i n i (Chabaud e t al., 1978), to judge from the arrangement o f caudal papillae and the bulbous end o f the right spicule (both in males), but can be distinguished by its shorter micro
filariae and by the three conical projections o f the tail end o f the male. The resem blance o f the two parasites may reflect the historical relationship betw een Asian and African bovids. C. s h o h o i n. sp. differs slightly from C. r u a n d a e (Fain & Herin, 1955) in its short microfi
lariae and the small subterminal papillae o f the male.
C. s h o h o i n. sp. may be similar to C. r u g o s ic a u d a (B ö hm & Supperer, 1953) in the arrangement o f caudal papillae o f the male, but differs in its short spicules, short microfilariae, less dilatated anterior part o f the fem ale, and postesophageal position o f the vulva.
C. s h o h o i n. sp. differs from C. c e p h a lo p h i Bain et al., 1982 in the shorter esophagus o f the females, the post
esophageal position o f the vulva, and the shorter micro
filariae. C. s h o h o i n. sp. differs from C. d e r m ic o la in its longer females and shorter microfilariae (Fain, 1977).
P a r a s ite , 1 9 9 8 , 5 , 1 1 9 -1 2 6
Mémoire
th ifila ria , such papillae w ere described in the species from ungulates, a hare, a rodent, and armadillos:
C. m g o s ic a u d a (Bohm & Supperer, 1953), C. r u a n d a e (Fain & Herin, 1955), and C. f a i n i (Chabaud et al., 1978); C. lep o rin u s in Canada (Bartlett, 1983); C. rous- s ilh o n i from a porcupine (B ain et al., 1986); and C. v en ez u elen sis (Eberhard et al., 1993). C. s h o h o i n. sp. from an ungulate seem s to belong on this list.
Intermediate papillae have not been found in species from primates, carnivores, a rodent, and marsupials:
C. ken yen sis, C. e b erh a rd i, and C. n a ro k en sis from African primates (Eberhard, 1980; Bain et al., 1988);
C. grassii, C. j a p o n ica, and C. c o rn eti from carnivores (Almeida & Vicente, 1982; Uni, 1984; Bain e t al., 1987); C. g a b o n e n s is from a rodent (Bain et al., 1982);
and C. p e a r s o n i and C. d id e lp h is from marsupials (Spratt & Varughese, 1975; Esslinger & Smith, 1979).
C. jo h n s t o n i belongs in this group if the specim en shown in Spratt & Varughese (1975) is referred to, but papillae near the subterminal group w ere present as well in the specim ens show n in Mackerras (1954) and Spratt & Varughese (1975).
Species with papillae intermediate in position in the males had females that seem ed to have slightly higher ratios o f esophageal length to body length than those o f species without such papillae, w hen calculated from m easurements given in the original texts. Species with papillae in this position had the follow ing ratios:
C. v en ezu elen sis, 3 .3 % (Eberhard et al., 1993); C. lep o rinus, 2.4-2.6 % (Bartlett, 1983); C. r u a n d a e , 2.4 % (Fain & Herin, 1955); C. m g o s ic a u d a , 2.2-2.4 % (B ö hm
& Supperer, 1953); C. fa in i , 1.5 % (Chabaud et al., 1978); and C. rou ssilhon i, 1.1 % (Bain et al., 1986). C.
s h o b o i n. sp. had the ratio o f 1.7-2.3 %. Species without papillae in this position had the following ratios: C. cor- neti, 2.4 % (Bain et al., 1987); C. j a p o n ica, 2.0 % (Uni, 1983), and 2.3 % (Uni, 1984); C. eb erh a rd i, 1.9 % (Bain et al., 1988); C. d id elp h is, 1.4 % (Esslinger and Smith, 1979); C. ken yen sis, 1.4 % (Eberhard, 1980); C. n a r o kensis, 1.3 % (Bain et al., 1988); C. g a b o n en sis, 0.8 % (Bain et a l., 1982); C. jo h n sto n i, 0.6-0.8 %, and C. p e a r son i, 0.4 % (Spratt & Varughese, 1975). Variation was found, but in general, species with such papillae had high ratios (2.0-3.3 %); many species without such papillae had low er ratios (0.4-1.9 %). A higher ratio means that the esophagus o f that species was less atrophied than one with a low er ratio. The esophagus o f C. s h o h o i n. sp. seem ed to be only slightly atrophied for a species in this genus.
With regard to the evolution o f O n c h o c e r c a species from Jap anese serows (Yagi et al., 1994), O. s u z u k ii Yagi et al., 1994, with its stout esophagus, is included in the primitive group found in tropical dom estic
phied esophagus, and is among the more evolved mem bers o f the genus. O f the various specim ens of O. sk rja b in i, Jap an ese specim ens reported by Yagi et al. (1994) and Suzuki et al. (1997) have primitive cha
racteristics: longer esophagus, more anterior vulva, and less atrophied caudal papillae than European spe
cim ens from red deer, C ervus ela p h u s (Bain & Schulz- Key, 1974).
If structures o f O n c h o c erc a species being com plex means that the species are primitive (Yagi et al., 1994), the same pattern may apply to other genera, including C ercop ith ifila ria. Eberhard et al. (1993) have pointed out that several species assigned to the genus do not sh are th e m o rp h o lo g ic a l fea tu re s d e sc rib e d for C. kenyen sis. W e suggest that the species o f the genus C erco p ith ifila ria be divided into two groups; primitive m em bers with intermediate caudal papillae and less atrophied esophagus and evolved mem bers without such papillae and with an atrophied esophagus. By this definition, C. s h o h o i n. sp. is another primitive member o f the genus. That C. s h o h o i n. sp. was found in a modern (bovid) host rather than in hosts such as por
cupines or marsupials supports the hypothesis o f Cha
baud (1981) and Bain et al. (1986, 1988) that the evo
lution o f hosts and nematode parasites is not in parallel in this genus. Larvae o f C. sh o h o i n. sp. were not found in ticks taken from Jap an ese serows in this study, but investigation o f the vector o f this species may confirm the suggestion o f Chabaud & Bain (1994) that the m eans o f evolutionary expansion o f the genus C erco p it h ifila r ia is unusual in depending not on the defi
nitive host (as is usual for nematode parasites o f ver
tebrates) but rather on the vector.
ADDENDUM
W hile this manuscript was at the publisher’s, a survey o f serow parasites was done (on 22 February 1998).
Microfilariae o f C. s h o h o i n. sp. w ere found alive in skin snips o f three o f the seven serows examined. The microfilariae w ere unsheathed, 107-112 μm long, and 5-8 μm wide. No microfilariae w ere found in blood smears o f the animals with microfilariae in the skin.
ACKNOWLEDGEMENTS
W e thank Yamagata City for official permis
sion to study serows, and Drs. A. Kimura, T. Nakashima, and S. Hirata o f the Japan Wildlife Research Center, Tokyo, for their cooperation.
W e thank Dr. C. Shoho for his encouragem ent during
Parasite, 1998, 5, 119-126
Mémoire 125
this study, and Ms. C. Latta for reading the manuscript.
Dr. O. Bain, Museum National d’Histoire Naturelle, Paris, kindly arranged for the accessioning o f the type specim ens.
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Reçu le 10 septembre 1997 Accepté le 15 décembre 1997
126 Mémoire Parasite, 1998, 5, 119-126
