T H E LIFE-CYCLE A N D BIOLOGY OF HEMIURUS COMMUNIS O D H N E R , 1 9 0 5
( D I G E N E A , HEMIURIDAE)
KØIE M.*
S u m m a r y :
Previously undescribed cystophorous cercariae which develop in sporocyst germinal sacs in the opisthobranch snail Retusa trunca- tula (Bruguiére) are shown to be the cercariae of Hemiurus commu- nis Odhner, 1905 (Hemiuridae), a common stomach parasite of non-clupeid fishes off the north-western coasts of Europe. The free- swimming cercaría is ingested by calanoid copepods. The cerca- rial body is injected into the copepod haemocoel via the delivery tube. The cystophorous cercaria and life-cycle of H. communis are compared with those of other hemiurids from the North-East Atlantic and the known biology of this species is reviewed
Résumé : CYCLE ET BIOLOGIE D'HEMIURIS COMMUNIS ODHNER, 1 9 0 5 (DIGENEA, HEMIURIDAE)
Il est démontré que des cercaires cystophores non encore décrites qui se développent dans les sacs germinaux du Mollusque opisto- branche Retusa truncaluta (Bruguière) sont celles de Hemiurus com- munis Odhner, 1905 (Hemiuridae), parasite stomacal de Poissons des côtes nord-occidentales d'Europe. La cercaire nageante est ingérée par des Copépodes calanoïdes. Le corps cercarien est injecté dans l'hémocoele du Copépode par le tube inoculateur. La cercaire cystophore et le cycle biologique de H. communis sont comparés avec ceux des autres Hémiurides de l'Atlantique nord- oriental et la biologie des espèces connues est passée en revue.
INTRODUCTION
H
emiurus communis O d h n e r , 1 9 0 5 ( D i g e n e a , H e m i u r i d a e ) is a c o m m o n sto- m a c h parasite o f non-clupeid fishes in t h e b o r e a l region o f the North-East Atlantic. Its molluscan h o s t h a s h i t h e r t o b e e n u n k n o w n . S i n c e t h e larval s t a g e s o f t h e h e m i u r i d s Hemiurus luehei O d h n e r , 1905, Lecitbocladium excisum (Rudolphi, 1 8 1 9 ) Lühe, 1901 a n d Brachyphalius crenatus ( R u d o l p h i , 1 8 0 2 ) O d h n e r , 1 9 0 5 w e r e f o u n d in b u l l o m o r p h o p i s t h o - b r a n c h gastropods (Philine denticulata, P. aperta a n d Retusa obtusa, respectively) ( K ø i e 1 9 9 0 c , 1 9 9 1 , 1 9 9 2 ) , it w a s e x p e c t e d that the larval stages o f H. communis w o u l d also b e found in this group o f opisthobranchs.In this p a p e r it is s h o w n that a previously undescri- b e d c y s t o p h o r o u s cercaria found in Retusa trunca- tula from t h e Øresund a n d t h e Isefjord, Z e a l a n d , Denmark, is the cercaria o f H. communis.
T h e t a x o n o m y , m o r p h o l o g y a n d distribution o f t h e s p e c i e s o f the North-East Atlantic Hemiuridae, inclu- ding H. communis, w e r e r e v i e w e d b y G i b s o n & Bray ( 1 9 8 6 ) . T h e t a x o n o m y o f t h e h e m i u r o i d d i g e n e a n s was reviewed b y G i b s o n & Bray ( 1 9 7 9 ) , w h o restric- ted t h e Hemiuridae to e c s o m a t e forms : this classifica- tion is followed in t h e present paper.
* Marine Biological Laboratory, University of Copenhagen, DK-3000 Helsingør, Denmark. Tel. + 45 49 21 33 - Fax + 45 49 26 11 65.
MATERIALS AND METHODS
p e c i m e n s o f Retusa truncatula ( B r u g u i è r e ) ( G a s t r o p o d a , O p i s t h o b r a n c h i a , B u l l o m o r p h a , Retusidae) w e r e d r e d g e d in t h e Ø r e s u n d (January a n d February 1 9 9 2 ) a n d the Isefjord (March, May, J u n e a n d A u g u s t 1 9 9 2 , a n d M a y 1 9 9 3 ) at a depth o f 6-15 m. In t h e laboratory t h e snails w e r e o b s e r v e d for t h e release o f cercariae. Within t w o days o f dredging all the snails w e r e dissected to reveal a n y immature infections. F r e e - s w i m m i n g c e r c a r i a e from c r u s h e d snails a n d l a b o r a t o r y - r e a r e d Acartia tonsa D a n a ( c o p e p o d i d s a n d adults) w e r e p l a c e d together in 2 5 0 ml b l u e - c a p bottles, which w e r e immediately attached to a rotating w h e e l . T h e e x p o s e d c o p e p o d s w e r e k e p t at 15°C a n d treated as described b y Køie ( 1 9 9 1 ) . S p e c i m e n s o f t h e t h r e e - s p i n e d s t i c k l e b a c k , Gasterosteus aculeatus L., previously kept in aquaria for o n e year a n d fed o n frozen food only, w e r e used a s e x p e r i m e n t a l f i n a l h o s t s a n d c o n t r o l s . M e t a c e r c a r i a e a n d adult s p e c i m e n s w e r e f i x e d in B e r l a n d ' s fluid (glacial a c e t i c acid : 4 0 % formalde- hyde, 19:1), cleared in lactic acid a n d m o u n t e d in gly- cerine-jelly.
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- 1 9 5K E Y W O R D S : D i g e n e a . T r e m a t o d a . H e m i u r i d a e . c e r c a r í a , life-cycle.
Hemiurus. Retuso, copepod. fish. MOTS CLES : Digenea. Trémalode. Hemiuride. cercaire. cycle de vie H e m i u r u s . Retusa. poisson, copépode.
Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/199502s2195
Table II. - Known hemiurid cercariae from the North-Hast Atlantic and their molluscan hosts.
RESULTS
NATURAL INFECTION OF THE MOLLUSCAN HOST
A
total o f 2 3 ( 1 0 % ) o f the 2 3 4 s p e c i m e n s o f Retusa truncatula e x a m i n e d w e r e infected.I n f e c t e d snails w e r e f o u n d in all s a m p l e s , apart from August. D u e to the small n u m b e r o f snails e x a m i n e d any s e a s o n a l variation in p r e v a l e n c e can not b e determined. During J a n u a r y and February only germinal sacs containing germinal balls w e r e found in the snails. In March a few snails c o n t a i n e d apparently fully-developed infective c e r c a r i a e , and in May and J u n e all, apart from o n e , o f the 10 infected snails har- b o u r e d infective cercariae. In J a n u a r y the snail shells m e a s u r e d 1.5-2.0 m m in length, in March they w e r e 2 . 5 - 4 . 0 m m a n d in M a y a n d J u n e 3 . 0 - 4 . 5 m m . In August only small ( < 1.0 m m l o n g ) and empty shells o f the parent generation w e r e found.
CERCARIAE
T h e cercariae d e v e l o p in sporocyst-like germinal sacs o f up to 1.5 m m in length. No gut c a e c u m o r pharynx w e r e s e e n . T h e c e r c a r i a e l e a v e t h e g e r m i n a l s a c through the terminal birth pore. T h e e x a c t position o f the germinal sacs in the snails was not determined.
V a r i o u s d e v e l o p m e n t a l s t a g e s o f t h e c e r c a r i a e are s h o w n in Fig. 1. Fig. 3 s h o w s the cercaria o f H. com-
munis b e s i d e t h e t h r e e o t h e r h e m i u r i d c e r c a r i a e found in o p i s t h o b r a n c h snails in Danish waters ( s e e table II). T h e m e a s u r e m e n t s o f fully-developed c e r c a - riae o f H. communis are p r e s e n t e d in table I, w h e r e t h e y are c o m p a r e d with t h o s e o f t h e t h r e e related cercariae from opisthobranchs.
T h e p r e s u m p t i v e cercarial b o d y is s p h e r i c a l in t h e earliest stages (Fig. 1 A-C). T h e tail is provided with two projections, the primordium o f the delivery tube and the motile e x c r e t o r y a p p e n d a g e (Fig. 1 B - D ) . In the fully-developed intra-sporocyst cercaria (Figs. 1 E, 3 A, a ) the delivery tube is withdrawn into the caudal cyst. Here it is coiled and attached to the internal stir- face o f the pointed e n d o f the almost pyriform caudal cyst. Cercariae at this d e v e l o p m e n t a l stage s q u e e z e through the birth canal o f the germinal sac. Shortly after e m e r g e n c e from t h e snail, t h e c e r c a r i a l b o d y retracts, via the cyst aperture, into the c a u d a l cyst (Fig. 1 F ) . T h e oral and ventral s u c k e r s are approxi- mately identical in size. No o t h e r details w e r e s e e n in t h e c e r c a r i a l b o d y . In t h e f r e e - s w i m m i n g infective cercaria the cercarial b o d y o c c u r s coiled within the caudal cyst (Figs. 1 G, 3 A , b ) . T h e motile e x c r e t o r y a p p e n d a g e is attached externally o n the caudal cyst,
196 Mémoire
Parasite, 1995, 2, 195-202Fig. 1. - Different developmental stages of the cercaria of Hemiurus communis. Interference contrast micrographs, all to same scale. A-D.
Undeveloped cercariae from germinal sacs. E. Recently released cercaria. The delivery tube is withdrawn into the caudal cyst. F. Cercaria shortly after emergence from the snail host. The cercarial body is partly withdrawn into the caudal cyst. G. Infective, free-swimming cerca
ria. Both the delivery tube and the cercarial body are withdrawn into the caudal cyst. H. In vitro delivery tube eversal. Half of the cercarial body has entered the everted delivery tube. Arrow shows extension on delivery tube. I. Base of delivery tube after passage of the cerca
rial body showing the extension (arrow). Abbreviation: ca. cyst aperture, the aperture through which the cercarial body has withdrawn;
cb, cercarial body; dt, delivery tube; ea, excretory (motile) appendage; os, oral sucker; vs. ventral sucker.
Fig. 2. - A, B. Metacercariae of Hemiurus communis, max. of 14 days old, from experimentally infected Acarlia tonsa. Interference contrast micrographs of live specimens, to same scale. C.
Adult specimen o f H. communis, 4 w e e k s old, from experimentally infected sticklebacks.
Interference contrast micrograph of fixed specimen.
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LIFE-CYCLE O F HEMIURUS COMMUNIS
Fig. 3. - Cercariae of four hemiurids which develop in Retusa spp. (A, C) and Philine spp. (B, D). A. Hemiurus communis. B. Hemiurus
luehei. C. Bracbyphallus crenalus. D. Lecithocladium excisum. a, cercaria immediately after emergence from the snail host, b, free-swimming infective cercaria, c, cercaria with cercarial body in everted delivery tube. Arrows indicate position of cyst aperture.
1 9 8
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Parasite, 1995, 2, 195-202LIFE-CYCLE OF HEMIURUS COMMUNIS
w h i c h is p r o v i d e d with m e m b r a n o u s folds o r out- growths. T h e e x c r e t o r y a p p e n d a g e is flattened, has a m e d i a n longitudinal furrow o n e a c h side and p o s - sesses a finely annulated surface. Apart from the api- cal o a r - s h a p e d fin-fold, t h e a p p e n d a g e is rich in small, highly refractile droplets.
C o v e r s l i p p r e s s u r e i n d u c e d d e l i v e r y t u b e e v e r s i o n and the extrusion o f the cercarial b o d y through the thin m e m b r a n e o u s tube (Figs. 1 H, I, 3 A , c ) . T h e for- cibly e v e r t e d delivery t u b e has an apical e n d p i e c e a n d o n e s m a l l h e m i s p h e r i c a l extension, w h i c h appears split apically, c l o s e to the tube b a s e . T h e cer- carial b o d y b e c o m e s e x t r e m e l y e l o n g a t e during the expulsion, w h i c h usually o c c u r s simultaneously with t h e e v e r s i o n o f t h e delivery t u b e . Shortly after t h e extrusion, the cercarial b o d y attains its normal shape.
Less than 1 0 0 infective cercariae, i.e. free-swimming cercariae with a withdrawn cercarial body, w e r e avai- lable after dissection o f the sporocysts released from e a c h crushed snail.
EXPERIMENTAL AND NATURAL INFECTION OF THE CRUSTACEAN HOST
Acartia tonsa readily b e c a m e infected w h e n e x p o s e d to free-swimming cercariae. No attempts w e r e m a d e to infect other c o p e p o d s p e c i e s . Natural infections o f m e t a c e r c a r i a e o f H. communis h a v e b e e n found in Acartia sp., Sagitta sp. and Pleurobrachia pileus from w e s t e r n K a t t e g a t , t h e Øresund a n d t h e I s e f j o r d , Zealand ( K ø i e , 1 9 8 3 ) .
METACERCARIAE AND ADULTS FROM EXPERIMENTAL INFECTIONS
D u e to the limited n u m b e r o f infective cercariae avai- lable, only a few m e t a c e r c a r i a e from experimentally infected Acartia tonsa w e r e studied. Live t w o - w e e k - o l d m e t a c e r c a r i a e ( F i g . 2 A, B ) w e r e 6 0 0 - 8 0 0 p m long, t h e p h a r y n x w a s 4 0 p m in d i a m e t e r a n d the oral and ventral suckers w e r e about 6 0 pm and 1 0 0 pm in diameter, respectively. T e g u m e n t a l annular pli- cations c o v e r most o f the surface.
T w o - w e e k - o l d m e t a c e r c a r i a e w e r e i n f e c t i v e w h e n they, via infected c o p e p o d s , w e r e fed to sticklebacks.
Small trematodes o b t a i n e d from the stomach o f e x p e - rimentally infected s t i c k l e b a c k s a few days post-infec- tion w e r e identical with the infective metacercaria o f H. communis. F i x e d four-week-old adults o f H. com- munis from sticklebacks (Fig. 2 C, D ) m e a s u r e d 1.4 - 1.5 m m in l e n g t h ( 1 . 2 m m with t h e e c s o m a with- d r a w n ) . T h e pharynx was 6 0 p m in diameter and the oral and ventral suckers w e r e 1 8 0 - 2 0 0 p m and 1 2 0 - 1 3 0 p m in d i a m e t e r , r e s p e c t i v e l y . S e v e r a l h u n d r e d eggs o c c u r r e d in the uterus and a few w e r e found in t h e h e r m a p h r o d i t i c duct. T h e s t i c k l e b a c k c o n t r o l s w e r e not infected with H.communis.
DISCUSSION
In D a n i s h w a t e r s t h e snail h o s t o f H. communis, Retusa truncatula, h a s b e e n r e c o r d e d f r o m t h e Isefjord, the Skagerrak, the western Kattegat and the western part o f the Limfjord, the Little and Great Belts and also from the Øresund, w h e r e it is rare (reviewed b y R a s m u s s e n , 1 9 4 4 ) . It is p r e s e n t t h r o u g h o u t t h e Isefjord, and often very numerous, particularly in the d e e p e r muddy-sandy areas. It is also often taken from stony ground with algae (depth 8-10 m ) and is abun- d a n t in t h e q u i t e
shallow
s a n d a n d m u d f l a t s (Rasmussen, 1 9 7 3 ) . It o c c u r s from the intertidal z o n e d o w n to 5 0 m or m o r e all around the British Isles, w h e r e it feeds u p o n foraminiferans and small mol- l u s c s ( T h o m p s o n , 1 9 8 8 ) . E l s e w h e r e , it h a s b e e n r e p o r t e d from the w e s t e r n B a l t i c S e a , N o r w a y ( u p e v e n to F i n n m a r k ) , H e l g o l a n d , the Dutch, B e l g i a n , French and Portuguese coasts, the Canary Islands and from the Mediterranean Sea as far east as the A e g e a n and as d e e p as 2 0 0 m (Rasmussen, 1 9 4 4 ; T h o m p s o n ,1 9 8 8 ) .
In the Isefjord the breeding o f R. truncatula occurs from May ( m a x . s p a w n i n g ) until J u l y ( R a s m u s s e n ,
1 9 7 3 ) . M a x i m u m s i z e is a t t a i n e d b y May, a n d in August n e i t h e r living s n a i l s n o r e g g m a s s e s w e r e found (Rasmussen, 1 9 4 4 ) . In O c t o b e r the n e w g e n e - ration had a shell length o f 1-2 mm. T h e seasonal size dispersion indicates that R. truncatula in the Isefjord has an annual life history (Rasmussen, 1 9 7 3 ) .
T h e s e reports conform with m y observations. It is not k n o w n at what size the snails o f the n e w generation b e c o m e s infected with H. communis, but it is obvious that n o c e r c a r i a e are r e l e a s e d after the time o f the death o f the spawning generation o f snails and the a p p e a r a n c e o f infected s p e c i m e n s o f the n e w genera- tion, i.e. p r o b a b l y b e t w e e n late s u m m e r and early spring. T h e parasite survives this period as metacerca- riae in pelagic invertebrates a n d / o r adults in fishes.
T h e distribution o f R. truncatula d o e s n o t e x a c t l y c o i n c i d e with that o f H. communis in fishes. Most r e c o r d s o f H. communis are from t h e c o n t i n e n t a l shelf b e t w e e n T r o n d h e i m in Norway and Brittany in F r a n c e . It is c o m m o n a r o u n d t h e British Isles a n d e x t e n d s eastwards into the Baltic. T h e distribution o f H. communis is thus mainly boreal. Reported records from the B l a c k Sea are very dubious ( G i b s o n & Bray, 1 9 8 6 ) , and the lack o f records from the Mediterranean Sea is noteworthy.
Hemiurus communis has b e e n found in c o d Gadus morhua from throughout Danish waters, e x c e p t for the Baltic off B o r n h o l m (Køie, 1 9 8 4 ) . It is less c o m - m o n in d a b Limanda limanda a n d e e l Anguilla anguilla ( s e e K ø i e 1 9 7 3 , 1 9 8 8 ) . In the Danish waters H. communis a n d Brachyphallus crenatus usually
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199o c c u r sympatrically and often in the s a m e fish host s p e c i m e n ( s e e K ø i e 1 9 8 4 , 1 9 8 8 ) . In the Isefjord the t w o s p e c i e s often o c c u r concurrently in fishes such as stickleback, flounder and turbot (unpubl. o b s . ) ; but, while H. communis mostly o c c u r s in shallow seas, B.
crenatus e x t e n d s into d e e p e r water and further north ( s e e G i b s o n & Bray, 1 9 8 6 ; Køie, 1 9 9 2 ) . H. communis w a s found in a few s p e c i m e n s o f saithe, Pollachius virens, caught near Tórshavn, the Faroes, but did not o c c u r in l o c a l F a r o e s e fishes ( K ø i e , u n p u b l . o b s . ) , i n d i c a t i n g that t h e s a i t h e must h a v e a c q u i r e d t h e parasite in a n o t h e r area, p r o b a b l y the coastal regions o f Scotland or Norway.
Small fish s p e c i e s , s u c h as s t i c k l e b a c k a n d y o u n g s p e c i m e n s o f t h e o t h e r a b o v e - m e n t i o n e d s p e c i e s , acquire the parasite b y ingesting infected c o p e p o d s ( a n d / o r c t e n o p h o r e s o r c h a e t o g n a t h s ) . Metacercariae p r o b a b l y o c c u r in c o p e p o d s b e t w e e n late March and late a u t u m n , j u d g i n g from t h e p e r i o d o f c e r c a r i a l release (March to J u l y ) and the lifespan o f a c o p e p o d (if c o p e p o d s are ingested by c t e n o p h o r e s or c h a e t o - gnaths, then the period o f infection via pelagic inver- t e b r a t e s m a y b e e x t e n d e d ) . L a r g e r f i s h e s a s t h e a b o v e - m e n t i o n e d s p e c i e s a r e b e l i e v e d u s u a l l y to a c q u i r e t h e p a r a s i t e b y i n g e s t i n g s m a l l e r i n f e c t e d fishes ( K ø i e , 1 9 8 4 ; G i b s o n & Bray, 1 9 8 6 ) . T h e fin- d i n g s o f s m a l l p a r a s i t e s p e c i m e n s in fishes might serve as an indicator o f t h e s e a s o n a l o c c u r r e n c e o f t h e p a r a s i t e in t h e p l a n k t o n i c i n t e r m e d i a t e h o s t s . Apart from a p o s s i b l e a c c u m u l a t i o n o f parasites in large piscivorous fishes in late autumn and winter, n o apparent s e a s o n a l o c c u r r e n c e might b e e x p e c t e d to o c c u r in D a n i s h a n d
neighbouring
w a t e r s . N o o b v i o u s s e a s o n a l variation was found in the 0 r e s u n d throughout a two-year study period (K øie, 1 9 8 4 ) . An accumulation similar to that found by Meskal ( 1 9 6 7 ) in t h e largest s p e c i m e n s o f c o d at B e r g e n w a s not o b v i o u s in the Danish material.G i b s o n & Bray ( 1 9 8 6 ) found an increased p r e v a l e n c e in autumn o f H. communis in flounder Platichthys flesus from an estuary o n the east c o a s t o f Scotland.
Möller ( 1 9 7 5 ) found a slightly increased p r e v a l e n c e in l a t e s u m m e r a n d a u t u m n in c o d from t h e K i e l e r Förde, the Baltic. Raymont ( 1 9 5 2 ) found that the h e a - viest infections o f H. communis ( p r o b a b l y including s o m e s p e c i m e n s o f B. crenatus) in saithe in an e n c l o - s e d l o c h in Argyll, Scotland, o c c u r r e d during J u n e - J u l y , w h e r e a s from A u g u s t t o F e b r u a r y v e r y f e w
parasites w e r e e n c o u n t e r e d . Meskal ( 1 9 6 7 ) o b s e r v e d that most y o u n g w o r m s w e r e found in N o v e m b e r and that the m a x i m u m shedding o f aged w o r m s occurred in July. He suggested that the average lifespan o f H.
communis is eight months.
T h e cercaria o f Hemiurus communis is m o r p h o l o g i - c a l l y v e r y s i m i l a r t o t h e c e r c a r i a e o f H. luebei.
Brachyphallus crenatus and Lecitbocladium excisum ( s e e K ø i e 1 9 9 0 c , 1992, 1 9 9 1 ) . Apart from their occur- r e n c e in different snail hosts, t h e s e cercariae are most easily separated b y the distance b e t w e e n the e x c r e - tory a p p e n d a g e a n d t h e cyst a p e r t u r e a n d b y t h e s h a p e o f the e x t e n s i o n o n the everted delivery tube (table I ) . T h e s e cercariae differ from o t h e r c y s t o p h o - r o u s c e r c a r i a e b y their m o t i l e , f l a t t e n e d e x c r e t o r y a p p e n d a g e with an apical o a r - s h a p e d structure and the small m o r e or less pyriform caudal cyst provided with m e m b r a n o u s folds.
T h e life-cycle o f H. communis w a s discussed, inter alia, b y L e b o u r ( 1 9 2 3 , 1 9 3 5 ) a n d D o l l f u s ( 1 9 2 3 ) . Dollfus ( 1 9 2 3 ) suggested that a c y s t o p h o r o u s cercaria, Cercaria calliostomae D o l l f u s , 1 9 2 3 , f o u n d in t h e m a r i n e s n a i l Calliostoma ziziphinum at R o s c o f f , F r a n c e , m i g h t b e t h e larval s t a g e o f a s p e c i e s o f Hemiurus. T h e identity o f this c e r c a r i a , w h i c h w a s r e d e s c r i b e d b y M a t t h e w s ( 1 9 8 2 ) , is still u n k n o w n . Metacercariae o f H. communis ( o r t h o s e b e l i e v e d to b e H. communis) w e r e r e c o r d e d in Acartia clausi b y L e b o u r ( 1 9 2 3 . 1 9 3 5 ) f r o m o f f P l y m o u t h a n d b y Candeias ( 1 9 5 7 ) from off the north coast o f Portugal.
M e e k ( 1 9 2 8 ) recorded the metacercaria from the b o d y cavity o f Sagitta setosa, and Y i p ( 1 9 8 8 ) found it in the s t o m a c h o f Pleurobrachia pileus. N o b l e ( 1 9 7 2 ) dis- c u s s e d t h e possibility o f using p a r a s i t e s o f m a r i n e p l a n k t o n a s b i o l o g i c a l i n d i c a t o r s . H e f o u n d t h a t Sagitta elegans is h o s t t o t h e m e t a c e r c a r i a o f Hemiurus levinseni, w h i l e S. setosa h a r b o u r e d t h e metacercaria o f H. communis.
T h e adult H. communis was r e d e s c r i b e d b y Dollfus ( 1 9 6 0 ) and G i b s o n & B r a y ( 1 9 8 6 ) . G i b s o n & B r a y ( 1 9 8 6 ) o b s e r v e d that w e l l - f i x e d s p e c i m e n s c o u l d usually b e split into two m o r p h o l o g i c a l groups s e p a - rated by size, tegumental plication, the s h a p e o f the vitelline m a s s e s and the n u m b e r o f invaginations o f the e c s o m a . T h e present s p e c i m e n s from the e x p e r i - mental infected s t i c k l e b a c k s and from small natural infected fishes from the Isefjord b e l o n g to g r o u p B , b e i n g small, distinctly plicated, with l o b e d vitelline m a s s e s a n d a d o u b l e i n v a g i n a t i o n o f t h e e c s o m a . However, the latter authors suggest it most likely that form “B” is merely a y o u n g e r condition o f form "A".
Kryvi ( 1 9 7 2 , 1 9 7 3 ) s t u d i e d t h e t e g u m e n t a n d t h e m u s c l e s o f the ventral s u c k e r o f H. communis using transmission e l e c t r o n m i c r o s c o p y , a n d M a t t h e w s &
M a t t h e w s ( 1 9 8 8 ) h a v e c o m p a r e d t h e t h i c k s o m a l tegument with the e c s o m a l tegument o f H. communis using ultrastructural, histochemical and autoradiogra- phic t e c h n i q u e s .
Apart from the cercaria o f L. excisum t w o o t h e r cysto- p h o r o u s cercariae h a v e b e e n found in Philine aperta ( s e e Køie, 1 9 9 1 ) . It is likely that they also b e l o n g to the Hemiuridae. Candidates are Hemiurus appendi-
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Parasite, 1995, 2, 195-202LIFE-CYCLE O F HEMIURUS COMMUNIS
culatus ( R u d o l p h i , 1 8 0 2 ) , Ectenurus lepidus L o o s s , 1 9 0 7 a n d Synaptobothrium caudiporum ( R u d o l p h i , 1 8 1 9 ) w h i c h all have a Lusitanean/Mediterranean dis- tribution ( s e e G i b s o n & Bray, 1 9 8 6 ) and have b e e n r e c o r d e d o f f t h e F r e n c h c o a s t w h e r e t h e i n f e c t e d snails w e r e found.
Experiments have s h o w n that the cercaria b e l i e v e d to b e that o f Hemiurus levinseni O d h n e r , 1 9 0 5 ( s e e Køie, 1 9 9 0 a ) is the cercaria o f an unidentified d e r o g e - nid.
Apart from the larval stages in the four species o f bul- lomorph opisthobranchs, m e m b e r s o f the Hemiuridae in the North Atlantic have b e e n found in unrelated p r o s o b r a n c h s , i . e . Gibbula s p p . ( D i o t o c a r d i a ( A r c h a e g a s t r o p o d a ) , T r o c h a c e a , T r o c h a c a e ) a n d Nassarius trivitattus ( S t e n o g l o s s a ( N e o g a s t r o p o d a ) , B u c c i n a c e a , Nassariidae). T h r e e s p e c i e s o f Gibbula harbour e a c h o n e s p e c i e s o f Lecithochirium (table II) ( s e e Køie, 1 9 9 0 b ) and N. trivitattus is the snail host o f t h e dinurine Tubulovesicula pinguis (Linton, 1 9 4 0 ) ( s e e Stunkard, 1 9 8 0 ) . It thus appears that related para- sites o c c u r in snails which are not systematically clo- sely r e l a t e d . Within t h e s u b f a m i l y L e c i t h o c h i r i i n a e s o m e species use prosobranchs o f the genus Gibbula, w h e r e a s o n e s p e c i e s use the o p i s t h o b r a n c h Retusa obtusa (table II). If the c h o i c e o f snail hosts reflects the relationships o f the parasites, then Brachyphallus crenatus should b e m o r e closely related to H. com- munis than to Lecithochirium spp. G i b s o n & B r a y ( 1 9 7 9 ) suggested that the subfamily Lecithochiriinae might b e divided into t w o groups a c c o r d i n g to the s h a p e and n u m b e r o f vitelline m a s s e s . T h i s w o u l d s e p a r a t e t h e g e n e r a Lecithochirium a n d Brachyphallus. U n f o r t u n a t e l y t h e s n a i l h o s t s a r e k n o w n f o r o n l y t w o o f t h e n i n e g e n e r a o f t h e Lecithochiriinae m e n t i o n e d by G i b s o n & Bray ( 1 9 7 9 ) . An even more p r o n o u n c e d discrepancy b e t w e e n the t a x o n o m y o f the molluscan hosts and that o f the para- site is found within the hemiuroid genus Lecithaster ( L e c i t h a s t e r i d a e ) . H e r e s o m e c e r c a r i a e a p p a r e n t l y o c c u r in s p e c i e s o f t h e p r o s o b r a n c h g e n u s Thais (Lapillus), while other cercariae o c c u r in s p e c i e s o f the opisthobranch genus Odostomia ( s e e Køie, 1 9 8 9 ) . Free-swimming c y s t o p h o r o u s cercariae are apparently k n o w n for t h e H e m i u r i d a e a n d D e r o g e n i d a e ( s e e Køie 1 9 7 9 , 1 9 9 0 a ) only. Most c y s t o p h o r o u s cercariae are u n a b l e to swim or have only a limited motility.
Non-motile s p e c i e s w h i c h use free-swimming c o p e - p o d s m a y b e almost spherical ( s e e Ching, 1 9 6 0 ) o r h a v e a n i n f l a t e d c a u d a l c y s t w a l l t o i m p r o v e b u o y a n c y ( s e e Køie, 1 9 8 9 ) . Cercariae which d e v e l o p in snails living o n algae may b e non-swimming and are provided with a p p e n d a g e s w h i c h e n a b l e the cer- cariae to b e c o m e entangled in the algae so that they
m a y b e i n g e s t e d b y h a r p a c t i c o i d c o p e p o d s ( K ø i e , 1 9 9 0 b ; Køie & Gibson, 1 9 9 1 ) .
A l a r g e n u m b e r o f m a r i n e c y s t o p h o r o u s c e r c a r i a e have b e e n described from various kinds o f molluscs, including s c a p h o p o d s , bivalves, pteropods and hete- r o p o d s ( s e e , inter alia, C h i n g , 1 9 6 0 ; Arvy, 1 9 7 2 ; Wardle, 1 9 7 5 ; V a n d e Vusse, 1 9 8 0 ; Lester & Newman, 1 9 8 6 ) .
S o m e o f t h e c y s t o p h o r o u s c e r c a r i a e from p r o s o - branchs are larvae o f the Didymozoidea ( s e e K 0 i e &
Lester, 1 9 8 5 ) , and it is likely that (many or all) cysto- phorous cercariae from h o l o p l a n k t o n i c snails, such as pteropods and h e t e r o p o d s , also b e l o n g to this group.
No c o m p l e t e didymozoid life-cycle has yet b e e n elu- cidated ( s e e K ø i e & Lester, 1 9 8 5 ) .
ACKNOWLEDGEMENTS
T
he author is indebted to Ms Harriet H. Hansen for technical assistance and to Dr D.I. Gibson, T h e Natural H i s t o r y M u s e u m , L o n d o n , for valuable c o m m e n t s on an early draft o f this paper.REFERENCES
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Accepté le 19 Janvier 1995
Parasite, 1995, 2, 195-202
Mémoire
