males, during the third and final year of their life. KEY WORDS. : Digenea. Opecoelidae. Opecoelinae. Genitocotyle. Genitocotyle mediterranea n. sp.
Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/1994014363
GENITOCOTYLE MEDITERRANEA N. SP. (DIGENEA, OPECOELIDAE) FROM SYMPHODUS OCELLATUS (TELEOSTEI, LABRIDAE) IN THE WESTERN MEDITERRANEAN BARTOLI P.*. GIBSON D.I.** and RIUTORT, J.-J.***
Summary : Genitocotyle Symphodus
Résumé
mediterranea
n. sp. is reported from the intestine of
ocellatus off the western coast of Corsica (in the
Scandola Nature Reserve). T h i s is the first species of
Genitocotyle
to be described from European waters : other members of this genus are parasites of fishes off the Atlantic and Pacific coasts of North America. G. mediterranea
can be distinguished from its
congeners by the anterior limit of the vitelline fields, which is at the level of the ventral sucker, and, in the case of the Pacific species, by egg-size. T h i s species occurs only in older fish, especially in
KEY W O R D S
: Digenea. Opecoelidae.
Opecoelinae.
Genitocotyle mediterranea n. sp. Symphodus ocellatus. Mediterranean. MOTS CLES : Digenea.
Opecoelidae.
Opecoelinae.
tus de la Réserve Naturelle Corse).
Contrairement
parasitent
Genitocotyle mediterranea n. sp. Symphodus ocellatus. Méditerranée.
INTRODUCTION
SP.
(DIGENEA,
OPECOELIDAE)
l'Amérique
du Nord,
de Scandola
(côte occidentale
de la
à toutes les autres espèces de ce genre
des poissons
des côtes atlantiques
et pacifiques
G . mediterranea est la première
décrite des mers européennes.
qui
de
espèce
G. mediterranea se distingue
ment des autres espèces de ce genre par l'extension
de ses
aiséchamps
qui atteignent la ventouse ventrale et, dans le cas des par la taille de ses œufs. Les individus
cette nouvelle espèce se rencontrent seulement chez les âgés, spécialement
Genitocotyle.
N.
MÉDITERRANÉE OCCIDENTALE
espèces du Pacifique, Genitocotyle.
MEDITERRANEA
I Genitocotyle mediterranea n. sp. est décrit chez Symphodus ocella-
vitellins
males, during the third and final year of their life.
GENITOCOTYLE
:
PARASITE DE SYMPHODUS OCELLATUS(TELEOSTEI, LABRIDAE) DE
de
poissons
chez les mâles, au cours de la troisième et der-
nière année de leur vie.
MATERIALS AND METHODS
T
he s u b f a m i l y O p e c o e l i n a e O z a k i , 1 9 2 5 . as d e f i n e d b y G i b s o n a n d Bray ( 1 9 8 2 ) , c o m prises o p e c o e l i d s w h i c h lack both a distinct cirrus-sac containing an internal seminal vesicle and a canalicular seminal receptacle (terminology o f G i b s o n and Bray. 1 9 7 9 ) but possess a naked seminal vesicle a n d a u t e r i n e s e m i n a l r e c e p t a c l e . T h i s is a g r o u p w h i c h is not c o m m o n in E u r o p e a n waters, w h e r e o p e c o e l i d s u s u a l l y b e l o n g to t h e large s u b f a m i l y Plagioporinae Manter, 1947. T h e latter group has, at least in part, b e e n dealt with in relation to NE Atlantic waters by G i b s o n and Bray ( 1 9 8 2 ) and, in a series o f six papers on those occurring in sparids in the w e s tern Mediterranean, by Bartoli et al. which culminated in a key ( 1 9 9 3 ) .
S
p e c i m e n s o f Symphodus ocellatus w e r e kept alive until just b e f o r e autopsy. Most digeneans w e r e c o l l e c t e d live f r o m their h o s t s , slightly flattened b e t w e e n slide and coverslip, and heat-fixed in hot B o u i n - H o l l a n d e f l u i d ; others w e r e d r o p p e d into Berland's fluid for o n e minute and then stored in 8 0 % alcohol. All w e r e stained in G r e n a d i e r ' s carmine and mounted in Canada balsam. T h e drawings w e r e m a d e with the aid o f a camera lucida. Measurements are given in micrometres as the range followed by the m e a n in parentheses. T h e t y p e - s p e c i m e n s a r e d e p o s i t e d in T h e Natural History M u s e u m . L o n d o n . R e g i s t r a t i o n n u m b e r s : Holotype : BM(NH) Reg. No. 1 9 9 4 . 7 . 1 2 . 1 ; paratypes : BM(NH) Reg. No. 1994.7.12.2-4.
During the course o f his investigations o n e of us ( P B ) e n c o u n t e r e d numerous o p e c o e l i n e s in the intestine o f the small labrid fish Symphodus
ocellatus
(Forsskal)
RESULTS
off Corsica. T h e present work describes these worms as Genitocotyle
mediterranea
O p e c o e l i n a e Ozaki, 1925
n. sp.
O p e c o e l i n a e (Ozaki, 1 9 2 5 ) Genitocotyle * Laboratoire de Biologie Marine et d'Écologie du Benthos. Faculté des Sciences de Luminy, case 901, 13288 Marseille cedex 9, France. ** Department of Zoology, The Natural History Museum. London SW7 5BD, UK. STARESO, 20260 Calvi, France. Dr D.I. Gibson - Tel. +44-71-938-9485; Fax +44-71-938-8754.
Parasite, 1994, 1, 365-370
Park, 1937 GENITOCOTYLE MEDITERRANEA N. SP
T y p e - h o s t : Symphodus
ocellatus
(Forsskal,
1775)
(Labridae).
Mémoire
363
BARTOLI P., GIBSON D.I. and RIUTORT J.-J.
Fig. 1. - Genitocotyle mediterranea n. sp. from intestine of Symphodus ocellatus, Scandola, Corsica. A. Ventral view-. B. Dorsal view
364
Mémoire
Parasite, 1994, 1, 365-370
GENITOCOTYLE
Type-locality : Western Mediterranean Sea off the w e s t e r n c o a s t o f C o r s i c a , at t h e S c a n d o l a Nature Reserve. Site : Intestine, never the rectum. O c c u r r e n c e : In 2 7 o f 2 5 9 S. ocellatus e x a m i n e d off Scandola : prevalence 1 0 . 4 %; abundance 0 . 7 4 ; mean intensity 7 . 1 8 . T h e s e parasites occur only in older fish, especially in dominant males, at the e n d o f the last (third) year o f their life: the figures for these dominant males are : prevalence 6 2 . 5 % ; abundance 4 . 4 ; mean intensity 7 . 0 . Consequently, it would appear that maintenance o f the life-cycle o f this digenean depends on transmission to o n e sex ( t h e male) and during a relatively short period o f the life span o f the host. MATERIAL STUDIED : 2 5 adult a n d 5 immature w o r m s .
DESCRIPTION (figs 1 - 3 ) G e n e r a l m o r p h o l o g y . B o d y e l o n g a t e with parallel sides, tapering anteriorly, rounded posteriorly. Dorsoventrally flattened. T e g u m e n t . Unarmed. S u c k e r s . Oral s u c k e r ventro-terminal ; lacking postoral ring. Ventral sucker powerful, r o u n d ; at junction o f first a n d s e c o n d thirds o f b o d y ; s o m e w h a t protuberant such that in dorso-ventral mounts its aperture is often pushed to o n e s i d e ; with anterior a n d posterior lips but lacking papillae; m o r e o r less encircled b y f o l d s o f b o d y w a l l in f l a t t e n e d
preparations.
Accessory sucker devoid o f limiting m e m b r a n e , with well-delimited transversely ovoid aperture and c o n s p i c u o u s radiating muscles; just sinistral to posterior limit o f o e s o p h a g u s , a b o u t half-way
that, according to Pearson's ( 1 9 9 2 ) terminology, the stricto.]
Digestive system. Prepharynx short; encircled by small g r o u p o f p r e p h a r y n g e a l cells. Pharynx large. O e s o p h a g u s more than twice length o f p h a r y n x ; thin-walled. Intestinal bifurcation just postero-medial to a c c e s s o r y sucker, at a b o u t junction o f third a n d fourth quarters o f f o r e b o d y . C a e c a t h i c k - w a l l e d in acetabular zone; parallel to lateral body wall in hindbody; e n d blindly near posterior e n d o f body. Male reproductive system. T e s t e s 2 ; tandem, contig u o u s , in m i d - h i n d b o d y ; regularly r o u n d e d , entire. P o s t - t e s t i c u l a r field a l w a y s s h o r t e r than
forebody.
Cirrus-sac a b s e n t . Vasa e f f e r e n t i a unite at b a s e o f seminal vesicle. Seminal vesicle free in p a r e n c h y m a ; long, r e a c h i n g b a c k into h i n d b o d y a n d in m a t u r e w o r m s to o n e third o r e v e n half o f distance b e t w e e n ventral s u c k e r a n d ovary; t u b u l a r but m o r e dilate p r o x i m a l l y ; proximal wide region oval to s a u s a g e s h a p e d , in a n t e r i o r h i n d b o d y ; p r o x i m a l a n d distal regions linked by narrower section (fig. 2 ) ; long, distal Parasite. 1994. 1. 365-370
tubular region straight, sinuous o r c o n v o l u t e d , gradually tapers in forebody. Pars prostatica sausage-shaped, wider than distal region of seminal vesicle; lined with typical anuclear blebs but apparently devoid o f external gland-cells. Ejaculatory duct very short; not apparently forming cirrus; o p e n s into genital atrium. Female reproductive system. Ovary median, immediately anterior to anterior testis; distinctly or indistinctly tri-lobed. transversely e l o n g a t e ; median l o b e p o s t e riorly oriented. Laurer's canal opening dorsally posterior to ovary. O ö t y p e a n d Mehlis' gland large; anterior to ovary. Canalicular seminal r e c e p t a c l e a b s e n t . Uterine seminal r e c e p t a c l e present. Uterus pre-ovarian, i n t e r - c a e c a l ; u t e r i n e field e x t e n d i n g b e t w e e n ovary a n d ventral sucker; uterus narrows as it passes d o r s a l l y t o ventral s u c k e r ; in f o r e b o d y it m a y b e straight or winding and forms metraterm with thicker walls w h i c h o p e n s into genital atrium. N u m b e r o f eggs usually not large, 7 - 3 9 ( 1 8 ) . Vitellarium follicular; follicles relatively large; lateral fields extend from region o f ventral sucker to posterior extremity, confluent in post-testicular region. Transverse vitelline ducts a n d vitelline reservoir anterior to ovary. Genital atrium. Small, spherical; limited by thickened wall; devoid o f surrounding gland-cells. Genital pore relatively l a r g e ; limited b y thickened m a r g i n ; sinistrally s u b m e d i a n ; in anterior half o f forebody, midw a y b e t w e e n prepharynx a n d accessory sucker. Excretory system. Excretory vesicle I-shaped, tubular; thin-walled; passes dorsal to testis, reaching to level o f ovary. Excretory pore terminal.
between
genital p o r e a n d ventral sucker. [It is worth noting accessory sucker is not a sucker sensu
MEDITERRANEA N. SP. FROM SYMPHODUS OCELLATUS
DIMENSIONS Measurements are based Lipon 1 0 flattened adults. Length of body : Breadth of body : Forebody : Hindbody : Oral sucker : Ventral sucker : Accessory sucker : Prepharynx: Pharynx : Oesophagus: Genital atrium (diam.) : Anterior testis : Posterior testis : Pars prostatica : Ovary : Fggs :
746-2,201 (1,307) 213-421 (284) 266-576 (364) 522-1.396 (816) 74-108 x 80-128 (89 x 101) 130-217 x 130-217 (170 x 169) 43-98 x 48-82 (64 x 66) 11-39 (17) 46-72 x 56-93 (55 x 71) 91-228(129) 30-80 (51) 98-228 x 130-304 (144 x 203) 98-250 x 130-271 (160 x 193) 36-77 x 14-29 (54 x 19) 50-108 X 102-228 (74 X 152) 49-59 x 24-32 (53 x 28)
Ventral sucker to ovary : Ventral sucker to end of seminal vesicle : Ventral sucker to anterior testis : Post-testicular region : Sucker-ratio : Oral sucker/pharynx ratio : Forebody/hindbody ratio : Forebody, length of body ratio :
Mémoire
109-325 (169) 43-119 (79) 130-434 (239) 174-477 (279) 1:1.67-2.12 (1.91) 1:0.53-0.69 (0.62) 1:1.71-2.54 (2.20) 1:3.2-4 (3.7)
365
BARTOLI P., GIBSON D.I. and RIUTORTJ.-J.
Fig. 2. - Genitocotyle
366
mediterranea
n. sp. from intestine of Symphodus
Mémoire
ocellatus,
Scandola, Corsica. Ventral view of terminal genitalia. Parasite, 1994, 1, 365-370
GENITOCOTYLE MEDITERRANEA N. SP. FROM SYMPHODUS OCELLATUS
Fig. 3. - Genitocotyle reproductive system.
mediterranea
n. sp. troni intestine of Symphodus
Scanclola, Corsica. Ventral view of proximal temale
a g e n u s previously r e p o r t e d from the Atlantic and Pacific coast o f North America.
DISCUSSION
A
ocellatus.
n unusual feature of these worms is the pre-
T h e r e are four nominal species o f Genitocotyle
s e n c e o f a small a c c e s s o r y s u c k e r b e t w e e n
acitrus
the genital pore and the ventral
rata
sucker.
by Manter ( 1 9 4 7 ) and acirra
T h e r e are three o p e c o e l i n e genera which possess this
S h o n (1965)1; G. atlantica
f e a t u r e : Anisoporus
chi
Ozaki, 1928;
O d h n e r , 1928; and Genitocotyle
Opecoeloides
Park, 1937. T h e fun-
: G.
Park, 1937 [erroneously e m e n d e d to G. Manter, 1 9 4 7 ; G.
M o n t g o m e r y , 1957 ; and G. cabled
Short, 1965. G. acitrus,
heterosti-
Nahhas and
mainly from embiotocids and
damental differences b e t w e e n these genera relate to
occasionally from sciaenids, clinids, etc. and G.
the termination of the intestinal caeca. In
rostichi,
the
caeca
Opecoeloides
open
through
a
single
Anisoporus anus,
in
they o p e n into the b a s e of the excretory
acir-
by Nahhas and
hete-
from a clinici, o c c u r on the Pacific coast o f
North America, w h e r e a s G. atlantica, r a n g e o f families, and G. cabled,
from a wide
r e c o r d e d from a
the
bothid and a syngnathid. occur on the Atlantic coast
c a e c a are blind. In possessing blind c a e c a , the speci-
o f North America. Aspects o f the life-history of the
m e n s from S. ocellatus
type-species,
vesicle to form a uroproct, and in Genitocotyle
Parasite, 1994, 1. 365-370
clearly belong to
Genitocotyle.
Mémoire
G. acirrus,
w e r e d e s c r i b e d by Pratt
367
BARTOLI P., GIBSON D.I. and RIUTORTJ.-J.
( 1 9 7 0 ) . Genitocotyle s p p . have not previously b e e n reported from labrids. G. mediterranea n. sp. is most readily distinguished from its c o n g e n e r s b y the anterior limit o f the vitelline fields w h i c h o c c u r s at t h e level o f the ventral sucker. In G. atlantica the vitell i n e f i e l d s e x t e n d i n t o t h e f o r e b o d y a n d in t h e remainder o f the species t h e fields either e n d in the anterior hindbody or reach only as far as the posterior m a r g i n o f t h e v e n t r a l s u c k e r ( M a n t e r , 1 9 4 7 ; Nahhas a n d Short, 1 9 6 5 ) . G. mediterranea c a n also be readily distinguished from the Pacific forms b y its smaller e g g - s i z e ( 4 9 - 5 9 vs 6 6 - 8 0 p m - Park. 1 9 3 7 ; M o n t g o m e r y , 1 9 5 7 ) . T h e r e a r e also o t h e r features, such as ovarian shape, posterior limit o f the seminal vesicle, etc. w h i c h have b e e n previously used t o distinguish species ; but these really require confirmation in a wide range o f well-fixed material. T h e s p e c i m e n s closest to G. mediterranea which w e have s e e n are two worms taken from the intestine o f a cardinal fish Apogon imberbis (L.) ( A p o g o n i d a e ) , w h i c h originated from o f f Madeira but died in t h e a q u a r i u m o f L o n d o n Z o o in 1 9 5 1 . T h e s e flattened w o r m s in t h e c o l l e c t i o n o f T h e N a t u r a l H i s t o r y M u s e u m . London [BM(NH) R e g . N o . 1 9 8 0 . 7 . 1 7 . 2 2 8 ] differ from t h e s p e c i m e n s from S. ocellatus in that they a r e larger, c o n t a i n a m u c h greater n u m b e r o f eggs, have a longer post-testicular z o n e a n d the seminal vesicle appears restricted to the forebody. T h e latter feature would rate as important and resembles t h e description o f G. heterostichi, but it is very possible that the posterior regions o f the seminal vesicle in the hindbody are o b s c u r e d b y eggs. In other respects the s p e c i m e n s from A. imberbis resemble those from S. ocellatus and may, therefore, prove to b e conspecific, but this will require confirmation in fresh material. It is worth noting that t h e range o f A. imberbis does e x t e n d into t h e M e d i t e r r a n e a n a n d that R u d o l p h i ( 1 8 1 9 ) d e s c r i b e d Distomum apertum, a species of uncertain affinities (Dollfus. 1 9 6 8 ) from this host at Naples, in w h i c h h e m e n t i o n e d t h e p r e s e n c e o f a genital structure b e t w e e n the suckers.
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59-67.
DOLFUS R.P. Les nematodes de l'histoire naturelle des helminthes de Félix Dujardin ( 1 8 4 5 ) . Mémoires. Muséum National d'Histoire Naturelle, Paris, Série A, Zoologie, 1968,
54. 1 1 9 - 1 9 6 + 4 7 plates.
GIBSON D.I. and BRVI R.A. The Hemiuroidea : terminology,
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Museum
GIBSON D.I. and BRAY R.A. A study and reorganization of
Plagioporus Stafford, 1 9 0 4 (Digenea : Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. Journal of Natural History. 1982,
16, 5 2 9 - 5 5 9 .
MANTER H.W. The digenetic nematodes of marine fishes of Tortugas, Florida. American Midland Naturalist, 1 9 4 7 , 38,
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MONTGOMERY W.R. Studies on digenetic nematodes from marine fishes of La Jolla, California. Transactions of the American Microscopical Society, 1 9 5 7 , 76, 1 3 - 3 6 . NAHHAS F.M. and SHORT R.B. Digenetic nematodes of marine fishes from Apalachee Bay, Gulf of Mexico. Tulane Studies in Zoology., 1 9 6 5 , 12, 3 9 - 5 0 . PARK J . T . A new nematode. Genitocotyle acirrus, gen. now, sp. nov. (Allocreadiidae), from Holconotus rhodoterus. Transactions of the American Microscopical Society, 1 9 3 7 , 56. 6 7 - 7 1 .
PEARSON J . C . On the position o f the digenean family Heronimidae : an inquiry into a cladistic classification of the Digenea. Systematic Parasitology. 1 6 9 2 , 21, 8 1 - 1 6 6 . PRATT I.; Life cycle and host specificity of the marine digenetic nematode, Genitocotyle acirra Park. Journal of Parasitology, 1 9 7 0 , 5(5 ( 4 : ICOPA, section II. part 1 ) . 273-274.
RUDOLPHI C.A. Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Sumtibus Augusti Ruckner, Berolini. 1 8 1 9 . 8 1 1 p. Accepté le 2 1 septembre 1 9 9 4
ACKNOWLEDGEMENTS
F
Opecoelidae
(Digenea) of sparid fishes of the western Mediterranean. VI. A redescription of Macvicaria mormyn (Stossich, 1 8 8 5 ) n. comb, and a key to the opecoelids of western Mediterranean sparids. Systematic Parasitology, 1 9 9 3 , 26,
ieldwork o n Corsica w a s carried out under t h e a u s p i c e s o f t h e C o m i t é S c i e n t i f i q u e d e la Réserve Naturelle d e Scandola, a n d the senior
author w a s funded by t h e Ministre Chargé de l ' E n v i r o n n e m e n t d e la Région Corse. Dr R.A. Bray kindly c o m m e n t e d o n a draft version o f t h e manuscript.
368
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