T
r ic h o b il h a r z ia r e g e n t in . s p . (S
c h is t o s o m a t id a e, B
il h a r z ie l l in a e), A NEW NASAL SCHISTOSOME FROM EUROPE
HORÁK P.*, KOLÁŘOVÁ L.** & DVOŘÁK J.*
Summary :
Members of the genus Trichobilharzia are parasitic in visceral or nasal body parts of their avian hosts. The examination of water snails in South Bohemia revealed a schistosome infection in Radix peregra snails. The experimental infection of ducklings (Anas platyrhynchos, Cairina moschata) confirmed that a new Trichobilharzia species - T. regenti n. sp. - was found. The adults, eggs and larvae (miracidia and cercariae) of the species were morphologically characterized. The adults occupy the nasal blood vessels where they lay the eggs; the miracidia hatch from the eggs directly in the tissue and leave the host during drinking/feeding of the infected birds.
KEY W ORDS : Trichobilharzia, Schistosomatidae, nasal schistosome, life cycle, Radix.
R é s u m é : Tr ich o bilh a r z ia r eg en tin. sp. (Sc h isto so m atid ae, Bilharziellinae), nouveausch istosom e nasald’Europe
Les membres du genre Trichobilharzia parasitent les régions viscérale et nasale de leurs hôtes aviaires. L'examen de mollusques d'eau douce en Bohème du Sud a montré une infestation par schistosome de Radix peregra. L'infestation expérimentale de canetons (Anas platyrhynchos, Cairina moschata) confirme la découverte d'une nouvelle espèce de Trichobilharzia, T. regenti n. sp. Les formes adultes, les oeufs et les larves (miracidies et cercaires) de l'espèce sont caractérisés sur le plan morphologique. Les adultes occupent les vaisseaux sanguins nasaux où ils déposent leurs œufs; les miracidies éclosent directement dans les tissus et quittent l'hôte quand les oiseaux infectés boivent ou s'alimentent.
MOTS CLÉS : Trichobilharzia, Schistosomatidae, schistosome nasal, cycle parasitaire, Radix.
INTRODUCTION______________________________
T
he genus T r ic h o b ilh a r z ia comprising o f about 40 species is the largest genus o f the family Schistosomatidae (Blair & Islam, 1983). In thetw o-host life cycle, the adults parasitize birds w hereas the larvae (miracidia) invade different pulmonate snails giving rise to sporocysts. The furcocercariae released from intermediate hosts are know n as the causative agent o f human cercarial dermatitis.
Adults are parasitic either in visceral or nasal areas of the infected host. The latter, i.e. the parasites o f nasal cavity, represent a m inor group within the genus.
T h e y w e re re p o rte d fo r th e first tim e b y F ain (1955a,b,c, 1956a,b, 1959) in Rwanda, Africa. Later, the parasites w ere found in India (Lalitha & Alvar, 1960), Australia (Bearup, 1957; Blair & Ottesen, 1979; Blair
& Islam, 1983; Islam, 1986a) and Switzerland (Palmer
& Ossent, 1984). Until now, seven species o f nasal Tri
c h o b ilh a r z ia w ere described (Table I).
In our contribution, the description o f a new nasal Tri
c h o b ilh a r z ia from Central Europe is presented. The species uses R a d ix p e r e g r a as intermediate host; anatid birds represent a susceptible final host under labora
tory conditions.
Table I. - Descriptions of nasal Trichobilharzia species.
* Department o f Parasitology, Charles University, Vinič na 7, CZ-128 44 Prague 2, Czech Republic.
** Department o f Tropical Medicine, 3rd Clinic of Infectious and Tro
pical Diseases, Faculty Hospital Bulovka, Charles University, Stud- nič kova 7, CZ-128 00 Prague 2, Czech Republic.
Correspondence: Petr Horák.
Tel: ++420-2-21953196 - Fax: ++420-2-299713 E-mail: [email protected]
MATERIALS AND METHODS
D
uring the period June-Septem ber 1997, snails o f the species R a d ix p e r e g r a p e r e g r a and R. p . ov a ta were collected in two South Bohemian ponds: ž oldánka and Podkadovskỳ, both near
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Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1998054349
HHORÁK P.*, KOLÁŘOVÁ L. & DVOŘÁK J.
Blatnâ, district Strakonice. In the laboratory, the snails w ere exposed to illumination and in case o f schisto- som e infection, the released cercariae w ere processed further.
A part o f the cercariae was used for experimental infec
tion o f ducklings and chickens. The infection dose varied with respect to the num ber and size o f infected snails and ranged approx. from 50 to 500 cercariae/one bird. Ducklings o f the species A n a s p la ty rh y n c h o s f . d o m e s tic a (o n e specim en) and C a ir in a m o s c h a ta f . d o m estic a (nine specim ens) and chickens G allus g allu s f . d o m estic a (tw o specim ens) w ere infected by the cer
cariae as described by Meuleman et a l. (1984). Star- ting on day 10 p.i., the bird faeces w ere tested for the presence o f schistosom e eggs. The birds w ere deca- pitated betw een 18-30 d.p.i. and their organs (intes
tine, liver, kidney, lungs, heart, nasal area) and adja
cent blood vessels w ere exam ined for the presence o f schistosom e eggs and/or adults by tearing o f the organs in 0 .8 5 % saline.
The m orphological characterization (the position and shape o f organs) o f adult schistosom es was made on fresh unfixed material using Nomarski interference contrast, while all m easurements w ere made on fixed and mounted worms. The worms w ere fixed in hot 4 % formaldehyde overnight. Then, they w ere w ashed and stained either by hem atoxylin-eosin or by Gomori (a trichrom e). The stained worms w ere dehydrated in ethanol and toluene and mounted in Histoclad (Clay Adams, USA).
The size and shape o f eggs was determined on fresh, unfixed material. M orphology o f miracidia and cerca
riae w as o bserv ed on native larvae (in terferen ce contrast) as well as on formaldehyde-fixed worms. The fixed larvae w ere m easured and their inner m orpho
logy was evaluated by staining o f w hole larvae as well as their h istological sectio n s in J B -4 resin (Poly- sciences). Borax-carm ine, hem atoxylin-eosin, Giemsa and Gomori w ere used as stains. In case o f miracidial plate counting, surface labelling by fluorescein-conju- gated lectins (A vachis h y p o g a e a agglutinin and R icin u s c o m m u n is agglutinin; 100 pg/ml in Tris buffer, pH 7.8;
see Horák, 1995 for de tails) served as a marker. Sen- sory papillae o f 100 cercariae were exam ined after stai
ning in 2 % silver nitrate in distilled water; permanent mounts w ere made using Swan em bedding medium m odified by Holman. Chaetotaxical nom enclature o f Richard (1971) has been used for evaluation.
Freshly em erged miracidia w ere also used for infec
tion experim ents. A total o f 21 R. p e r e g r a snails (shell height about 7-10 mm) collected in natural ponds and free o f trematode infection as well as 20 specim ens (shell height about 10 mm) o f laboratory reared Lym- n a e a sta g n a lis snails w ere exposed individually to five miracidia for two hours.
The type material is deposited in the Natural History Muse um, Vienna, Austria: NHMWien ZOOEV 3681:
holotype (anterior end o f a male) ; 3682: allotype (ante
rior end o f a female) ; 3683: paratype (anterior and pos- terior ends o f a m ale).
RESULTS
Pr e v a l e n c e o f t h e n a t u r a l i n f e c t i o n
I
n the locality Zoldânka, 422 specim ens o f R. p e r e g ra w ere collected and two snails (0.5 %) w ere positive for schistosom e cercariae. In the pond Podkadovsky, 613 R. p e r e g r a snails w ere collected and 16 specim ens (2 .6 % ) w ere infected by schistosom es.The m em bers o f both subspecies - R. p . p e r e g r a and R. p . o v a ta - released the schistosom e larvae. Although other species o f snails w ere also exam ined ( L y m n a e a sta g n a lis: 105 specim ens; L. p alu stris: 41 specim ens;
P h y sa a c u t a: three specim ens), no infection by schis
tosom es was revealed. However, in 19 out o f the total 945 R. a u r ic u la r ia snails (2 % ), a schistosom e infec
tion was revealed. The systematic position (species identification) o f these schistosom e larvae needs to be further studied and, therefore, they are not the subject o f the below m entioned descriptions.
La b o r a t o r y i n f e c t i o n o f b i r d s
Ten ducklings and two chickens w ere infected by schistosom e cercariae from R. p e r e g r a . W hereas the in fection developed in all ducklings, the chickens remained infection-free. Both duck species A. p la ty rh y n ch o s and C. m o s c h a ta represent susceptible final host. Worms w ere found in the nasal area; other organs w ere infection-free. Although adult worms were recovered by day 15 p.i. already, the prepatent period (d e tection o f eggs in nasal se cre tions) w as about 20 days p .i.; no eggs w ere found in faeces. Dissection o f the nasal area show ed that adult worms are loca- lized partly within blood vessels and partly in soft nasal tissue outside vessels. Course o f infection is probably o f short duration: although two ducklings w ere hea
vily infected and released high num ber o f miracidia (see below ), they possessed only one-tw o worms in nasal area by day 25 p.i.
Ad u l t s c h i s t o s o m e s
No intact adult worm was recovered from nasal tissue.
Therefore, total length was not measured. With respect to body parts being found, total length o f males is esti- mated to be about 11 mm. All other m easurements w ere made on fragments from thirteen males and six females (Table II and III). The longest fragment from a m ale was 5.22 mm, from a fem ale 7.11 mm.
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Values obtained from extremely contracted/relaxed worms (not included in the above presented means and SD):
1 min. 0.028, max. 0.101; 2 min. 0.230, max. 0.387; 3 min. 0.064, max.
0.1 1 3 ; 4 min. 0 .150, max. 0.3 6 8 ; 5 max. 0 .2 2 3 x 0 .0 3 5 ; 6 max.
0.2 1 9 x 0 .0 2 3 ; 7 max. 0.230.
* Vesiculae seminales externa and interna were not distinguishable in all specimens; therefore, se minal vesicle as a whole is also reported.
Table II. - Measurements of male Trichobilharzia regenti n.sp.
No.
M easured Mean ± SD (m m )
Table III. - Measurements of female Trichobilharzia regenti n.sp.
• Male (Fig. 1A, Table II) has filiform body o f almost uniform width which is covered in anterior part by spo
radic tubercles; their number was not determined. Also, several pigmented spots occur in this area. Surface of
worms is longitudinally striated. Tegument of oral sucker bears anteriorly several cilia o f putative sensory function.
Sucker encom passes the oral opening which is situated subterminally. There is a relatively short and wide gynae- cophoric canal (ventral groove), walls o f which are covered by 0.003-0.005 mm long spines. The posterior end (tail) is broadened and in fresh worms coil-shaped.
Reproductive system consists o f numerous testes (more than 120), collecting duct and vesicula seminalis. Slightly oval testes start close to posterior end o f gynaecophoric canal and continue nearly to body end. Seminal vesicle is usually divided into extemal and internai parts. Eja- culatory duct opens on genital papilla lying at the begin- ning of gynaecophoric canal. Conceming digestive tract, long oesophagus passes from oral opening to caecal bifurcation lying just before acetabulum, surface of which is covered by spines. Reunion o f caeca was observed at posterior end o f or behind se minal vesicle.
This position may slightly vary in contracted/dilated worms. Reunited intestine continues dorsal to gynaeco
phoric canal and its sinuous course in testes area ends just before coiled tail. Intestine, mainly in bifurcation part, was filled by dark-brown pigment, probably hematin created during haemoglobin digestion. As far as excre- tory system is concem ed, it was impossible to count number of flame cells; collecting duct visible throughout entire body contained numerous ciliary patches.
• Female (Fig. 1B, Table III) is also filiform and its sur
face characteristics correspond with those of males. Pos
terior body end (tail) is usually club-shaped but not so extremely as in m ales ; coiled end was never observed.
Morphology o f suckers and digestive tract is generally the same as in m a le s. Reunion o f caeca is localized behind seminal receptacle; this feature seems to be stable. Intestine is visibly more filled by brown pigment;
therefore, sinuous intestine in posterior body parts repre- sents, by its brown colour, the most dominant organ.
Concerning reproductive system, long tubular ovary fol- lowed by se minal receptacle are the most visible organs in anterior body part. Numerous vitelline follicles are localized betw een se minal receptacle and body end.
Granular vitelloduct passes ovary area forward and opens in ootype area before ovary. Also, oviduct star- ting at posterior ovary end and joining se minal recep
tacle duct, turns back and passes ovary area to ootype lying before ovary. Short and sometimes curved uterus continues from ootype and ends by genital opening just behind acetabulum. Exclusively one egg was found in ootype/uterus. Although usually described in other Tri
c h o b ilh a r z ia species, Laurer’s canal was not observed.
Excretory system is basically the same as in m ales.
Eg g s
Thirty one eggs w ere m easured in total. The size of e lo n g a te eg g s (F ig . 1C) is 0 .2 8 9 ± 0 .0 2 9 mm x
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Fig. 1. - Trich obilharzia regenti n. sp. A: anterior and posterior end o f a m ale ; B: anterior and posterior end o f a female ; C: egg ; D: mira
cidium ; E: miracidial plates. A, acetabulum ; CG, canalis gynaecophorus ; E, egg ; EC, excretory duct ; GO, ge nital opening ; GP, ge nital papilla ; I, intestine ; O, ovary ; OD, oviduct ; OE, oesophagus ; OS, oral sucker ; OT, ootype ; RS, receptaculum seminis ; T, testes; U, utérus ; VD, vitelloduct ; VI, vitellaria ; VSE, vesicula seminalis externa ; VSI, vesicula seminalis interna. Scale in µm.
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Tr ic h o bilh a r z ia r eg e n t i, a n a sa l s c h i s t o s o m e f r o m Eu r o p e
0.089 ± 0.013 mm (m ean ± SD); variability in shape was characterized as length:width ratio and this parameter ranged betw een 2.8-4.6. Eggs are nearly symmetrical about to long axis and have two extremities (p o les) - one is longer with rounded end and one is shorter with slender and curved process at top. Within few days for
mation o f miracidia is completed. Mature eggs are very fragile and tend to disrupt once under slight pressure (e.g. coverslip).
Mi r a c id i a
Fifty specim ens w ere m easured in total. Size o f pyri- form m iracidia (Fig. 1D ) w as 0 .1 0 6 ± 0.015m m x 0.041 ± 0.005 mm (m ean ± SD). O n surface, ciliated plates are arranged in four tiers and pattern is 6:9:4:3;
second tier is the longest one (Fig. 1E). On border bet
w een first and second tier, two late ral horns are loca- lized. Under surface layer numerous vacuoles o f unde- term ined sh ape and function are located. W ithin miracidia there are two kinds o f glands in anterior re gion - one apical gland (head gland) w hich is coar- sely granular and light-blue-stained using Giemsa and tw o long late ral glands reaching posterior end o f neural mass which are finely granular and pink-stained using Giemsa. Both types o f glands open at miracidial anterior end (terebratorium) - apical gland terminally and two late ral glands subterminally. Apical gland is follow ed by nerve mass surrounded by circle o f cells.
Distal half o f body is filled by one group o f germinal cells. Group o f rounded cells o f unknow n function occupies région betw een germinal cells and neural mass. Miracidia possess two pairs o f flame cells; first and second pairs lie at anterior and posterior level o f second ciliated tier, respectively. Excretory system opens at border betw een second and third tier o f ciliated plates.
Maximum recovery o f miracidia was by days 24 and 25 p.i. Miracidia show photo-positive and geo-nega- tive orientation. They hatch from eggs in water as well as in saline. Examination o f nasal area show ed that miracidia are able to leave eggs even within nasal tissue; nasal area o f ducklings being without contact with water for 10-12 h contained several freely moving miracidia. After rinsing out nasal cavity with tap water, exclusively free miracidia and no eggs w ere found in the water.
Ce r c a r ia e
Measurements o f body parts and organs o f twenty two cercariae released from R. p e r e g r a are presented in Table IV. Gross morphology o f ocellate furcocercariae (Fig. 2A) is basically the sam e as for T. o c e lla ta type.
Surface is covered by fine spines which appear to be o f the same length on body and tail stem. Localiza- tion o f silver-stained sensory papillae is show n on
Table IV. - Measurements of cercariae Trichobilharzia regenti n.sp.
Fig. 2. - Trichobilharzia regenti n. sp. A: cercaria ; B: excretory system o f cercarial body. F, flame cell ; CP, ciliary patches. Scale in pm.
Figure 3 and Table V. Dominant head organ fills ante
rior body end. Acetabulum lies behind body centre.
O ne pair o f eye spots is localized at half distance bet-
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Fig. 3. - Surface sensory papillae o f Trichobilharzia regenti n. sp. cercariae. V, ventral body view ; L, late ral body view ; D, dorsal body view ; UV, ventral tail view ; UD, dorsal tail view.
Body
Table V. - Chaetotaxy of Trichobilharzia regenti n.sp. cercariae.
w een head organ and acetabulum. Intestine with bifur
cation and two short caeca is localized centrally along with body axis; it starts subterminally in head organ and ends before circumacetabular glands. Tw o pairs o f cir- cumacetabular pe netration glands surround acetabulum;
posterior body pan is filled by three pairs o f postace- tabular pe netration glands. Content o f circumacetabular glands remains unstained whereas that o f postacetabular glands is pink-stained using Giemsa. Massive gland ducts pass cercarial body forward thru head organ and
354
open at anterior end. Excretory system is com posed of seven pairs o f flame cells and two pairs o f cilia patches within collecting ducts. Flame cell formula is 2 [3 + 3 + (1)] = 14 (Fig. 2B). Excretory system leads into excre
tory junction at body base and continues throughout tail stem and furcae. Tail stem is obliquely striped and filled by star-shaped cells; furcae are cross-striped and finfolds are well developed nearly along entire furcae.
Furcae end in 0.015 mm long thorns.
Cercariae exhibit photo-positive reaction. However, they do not strongly attach to the container wall. They often float in water column and finally, they also rest at the bottom. They becom e active by shadow or mechanical stimuli w hen they quickly swim to water surface.
La b o r a t o r y in f e c t io n o f snails
Although ten R. p e r e g r a snails died during experi
ment, remaining eleven specimens becam e infected; no infection established in L. stagn alis (20 specimens). Pre
patent period under laboratory conditions was only estimated - after three w eeks p.i. no cercariae w ere shed, w hereas by five w eeks p.i. snails releasing schis
tosom e larvae w ere detected.
Sy st e m a t ic su m m a ry
Species: T r ic h o b ilh a r z ia reg en ti n.sp.
Type host (experimental infection): A n a s p la ty rh y n ch os f . d o m . L., C a ir in a m o s c h a ta f . d o m . (L.)
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Intermediate host: R a d ix p e r e g r a p ereg r a , R. p . o v a ta (natural and experim ental hosts)
Site o f infection: blood vessels and mucous tissue o f the nasal cavity
Type locality: Blatnâ, South Bohem ia, Czech Republic Prevalence in the intermediate host: 0.5-2.6%
De position o f types: Natural History Muse um, Vienna, Austria: NHMWien ZOOEV 3681: holotype (anterior end o f a m a le ) ; 3682: allotype (anterior end o f a fem ale); 3683: paratype (anterior and posterior ends o f a m a le ).
Etymology: regent is a governor o f a kingdom/princi- pality; the title was frequently used in South Bohem ia (i.e. the area w here the schistosom e cornes from) in the Middle Ages. At present the nam e represents a famous South Bohem ian brewery (founded in 1379).
DISCUSSION
S
o far w e know, only Trich o b ilh a r z ia species cau- sing visce ral infections o f birds w ere systemati- cally described from Europe. The site o f infectio n (n a sa l a re a ) as w ell as th e m o rp h o lo g ic a l characterization proved that T. regen ti n.sp. is a new European schistosom e sp ecies; it cannot be confused with the sympatrically occurring species T. o c e lla ta (LaValette, 1855) Brumpt, 1931, T. s z id a ti Neuhaus, 1952 and T. f r a n k i Müller & Kimmig, 1994.
O ne report on T ricb o b ilh a rz ia sp. in nasal cavity of mute sw ans from Switzerland has b een published (Palmer & Ossent, 1984). However, the report is cen- tred mainly on histopathological evaluation; it lacks a deeper morphological characterization and species des
cription as well as detail data on the parasite life cycle.
Due to the death o f the experimentally infected R. p e r eg ra snails in the Palmer’s and O ssent’s experiments, it is impossible to say w hether the intermediate host spe- cificity o f that parasite was the same as in our case.
Nevertheless, L. stagn alis appeared to be resistant to the infection as has also been proved in our experiments.
As far as the seven nasal Trich o b ilh a r z ia species are concerned, they differ from T. regen ti n.sp. in the fol- lowing major m orphological features (size différences are not considered): (1) The caeca o f m ales reunite at the middle part o f the se minal vesicle (T. n a s ic o la Fain, 1955; T. r o d h a in i Fain, 1955; T. sp in u la ta Fain, 1955;
T. d u b o is i Fain, 1959; T. a r c u a t a Islam, 1986a); in T.
regen ti n.sp., although varying to a certain degree, the reunion was found at the posterior level o f or even behind the se minal vesicle. (2) The posterior end o f males is only slightly broadened (T. n a sic o la , T. sp i
n u la ta ); in T. reg en ti n. sp. the posterior end is stri- kingly broadened and coil-shaped. In none o f the for- merly d escribed avian T r ic b o b ilh a r z ia species the
coil-shaped posterior end o f m ales was noted. (3) The surface papillae (tubercles) appear also at the poste
rior end o f m a le s (T. r o d h a in i), or the surface is covered by 0.006-0.010 mm spines (T. sp in u la ta ).
These morphological features were not found in T.
regen ti n.sp. m ales. (4) The female caeca reunite at the posterior ovarial end (T. sp in u la ta ) or at the level o f receptaculum seminis (T. a r c u a t a ), while in T. regen ti n.sp. the reunion lies behind the se minal receptacle.
(5) Contrary to T. reg en ti n.sp. females, no tubercles w ere noted at the anterior end o f T. a r c u a t a females.
(6) The eggs o f all seven nasal T ricb o b ilh arz ia ( T . n a si
co la, T. r o d h a in i, T. sp in u la ta , T. d u boisi, T. a u r e lia n i Fain, 1956; T. a r c u a ta , T. a u stra lis Blair & Islam, 1983) seem to have diffe rent size, shape, or both. In case o f som e Trich o b ilh a r z ia species from Rwanda, the above mentioned morphological diffe rences may be o f limited value due to the low num ber o f adult flukes observed in the original descriptions, i.e., the intraspecific varia- bility o f particular characters is poorly known.
As the life cycle o f only two nasal Trich o b ilh a r z ia spe
cies w as co m p leted (B la ir & Islam , 1 9 8 3 ; Islam , 1986a,b), the morphological and/or behavioural com- parison on the larval level was made exclusively bet
w een T. regen ti n. sp. and T. au stralis/T . a r c u a ta . (1) The arrangement o f miracidial anterior gland cells o f T. a r c u a ta / T. au stralis is diffe rent from that observed in T. regenti n. sp. where the two latéral, finely-granular, and elongate glands reach the posterior part o f the neural mass. (2) T. a r c u a t a miracidia possess two groups o f germinal cells whereas those o f T. regen ti n.sp. only one germinal mass. (3) The number o f cer- carial flame cells is 16 in T. a r c u a t a and T. au stralis;
cercariae o f T. regen ti n. sp. have the usual T richobil- h a r z ia num ber (14 flame cells). (4) The finfolds o f T.
a r c u a t a cercariae are present only on two thirds of furcae w hereas in T. regen ti n. sp. the finfolds cover nearly the entire furcae. (5) The distribution pattern o f the silver-stained cercarial papillae o f T. regen ti n. sp.
differs from that in T. a rcu a ta /T . australis. (6) The res- ting behaviour o f T. regen ti n. sp. cercariae seem s to be diffe rent from that o f T. au stralis and T. a r cu a ta . Although clear diffe rences in cercarial chetotaxy exist betw een T. regen ti n. sp. and T. au stralis/T . a r c u a t a (e.g., ventral papillae C IV and A I and dorsal papillae C II), a com ple te com parison is rather impossible.
This is based on the fact that late ral body ( T. a r c u a ta ) and ventral/dorsal tail ( T. a r c u a ta , T. au stralis) views are not drawn in the original descriptions (Blair &
Islam, 1983; Islam, 1986a) and papillae positions are not defined. Therefore, the com parison o f T. regen ti n.sp. with T. a r cu a ta /T . a u stra lis arose from our per- sonal evaluation o f Blair’s and Islam’s drawings.
It appears that the European Trich o b ilh a r z ia species exhibit a strong intermediate host specificity. The ori-
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ginal descriptions o f T. o c e lla ta as well as T. sz id a ti mention L. stag n alis as the intermediate host (LaValette, 1855; Brumpt, 1931; Neuhaus, 1952); T. f r a n k i deve- lops exclusively in R. a u r ic u la r ia (Müller & Kimmig, 1994) and T. regen ti n. sp. in R. p ereg ra. The confu
sion arisen from numerous descriptions o f C erca ria o c e lla ta from diffe rent snail hosts, i.e., without know ledge o f the adults and the parasite life cycles, is not considered in this discussion. However, it can be hypo- thesized that the European findings o f C. o c e lla ta from R. p e r e g r a (e.g., Nasincová, 1992) might belong to T.
regen ti n. sp. The specificity o f T ric h o b ilh a rz ia para
sites to the intermediate hosts is supported by Kalbe’s e t al. (1997) observation that T. o c e lla ta (the strain is identical to the T. s z id a ti stock) miracidia are attracted exclusively to L. stag n alis and not to G a lb a tru n catu la, R. p e r e g r a or even planorbid snails. The susceptibility o f a snail host to a trematode infection is probably genetically linked; the 18S rDNA sequence analysis o f lymnaeid snails shows that L. stagn alis (the original host o f T. o c ella ta /T . szid ati) belongs to a diffe rent group than R. a u r ic u la r ia /R . p e r e g r a (snail hosts o f the recently described species T. f r a n k i and T. regen ti n. sp., respectively). This snail grouping seem s to be reflected by transmission pattern o f other trematodes, e.g., fasciolid flukes (Bargues & Mas-Coma, 1997).
The nasal avian schistosom es seem to be well adapted to the transmission. As already m entioned by Islam (1986a,b), the miracidia hatch from eggs in pond water as well as in 0 .8 5 % saline. W e observed, moreover, that free miracidia are present in the nasal tissue. They might hatch directly in the nasal area either without a stimulus or after a short contact with water incoming during the duck drinking/feeding. The exam ination o f water after rinsing out the nasal cavity show ed that only freely-moving miracidia and no eggs w ere pre
sent. Taken together, the miracidia leave the eggs and their duck host via openings o f the bill/nasal cavity during the duck drinking/feeding. T he incom ple te border betw een the bill (m outh) and the nasal cavity might contribute to this m ode o f transmission.
In conclusion, a new species o f nasal T rich o b ilh a rz ia , T. reg en ti n. sp., has morphologically b een characte- rized. The description concerns the adults, eggs, mira
cidia and cercariae. A strict intermediate host specifi
city and a new m ode o f T r ic h o b ilh a rz ia transmission has been pointed out.
ACKNOWLEDGEMENTS
T
he work has b een supported by the AKTION Program Czech Republic-Austria (grant No.19p 15), C harles U niversity (grant N o .106/
1998/B/BI) and the Czech Ministry o f Health (grant No.
IGA MZ ČR 4945-3). Our appre ciation is expressed to Dr. H. Sattmann, Natural History Muse um, Vienna, Austria, for de position o f the type material.
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Reçu le 18 mars 1998 Accepté le 11 juin 1998
Parasite, 1998, 5, 349-357
Mémoire 357
