Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2000073201
SARCOCYSTIS A
WITH
A
NEW
STENODACTYLICOLUBRIS SARCOSPORIDIAN
SNAKE-GECKO
N.
SP.,
COCCIDIUM
HETEROXENOUS
LIFE
CYCLE
MODRY D.* **, KOUDELA B.* ** & ŠLAPETA J.R.* ,
,
Summary :
Résumé:
Oocysts/sporocysts of Sarcocystis sp. measuring 9,7 (9-10) x 7.6 (7-8) µm were found in the intestinal contents of the Dahl's whip snake Coluber najadum. Of wide spectrum of experimentally inoculated hosts, only species of the family Gekkonidae - Ptyodactylus guttatus and Stenodactylus grandiceps - were found to be susceptible intermediate hosts. Transparent, barely visible sarcocysts found in tail, limbs and tongue striated muscles of the geckoes were 1 75-200 µm x 3 5 - 5 0 µm in size at 7 8 DPI. Ultrastructurally, the primary cyst wall was characteristic by spine-like villar protrusions up to 8 0 0 nm long, 2 0 0 - 2 5 0 nm in diameter at their base, tapering to thinner apex. Protrusions appear typically lobular or irregular in the cross-sections. Back-transmission from P. guttatus to Coluber rogersi leaded to oocysts/sporocysts excretion since 38 days post infection. Based on sarcocyst morphology and experimental data, Sarcocystis stenodactylicolubris is apparently a new species. Based on obtained and already published results, Sarcosporidia parasitising colubrid snakes as definitive hosts are suggested to be family specific on the level of their intermediate host.
Des oocystes/sporocystes de Sarcocystis sp. mesurant 9,7 19-10) x 7,6 (7-8) um ont été trouvés dans le contenu intestinal du serpent Coluber najadum. Expérimentalement, seules des espèces de la famille des Gekkonidae - Ptyodactylus guttatus et Stenodactylus grandiceps - se sont révélées être de possibles hôtes intermédiaires de ce parasite. Les sarcocystes transparents et à peine visibles, trouvés dans les muscles striés de la queue, des pattes et de la langue de ces geckos mesurent 175-200 µm x 35-50 µm. Au niveau ultrastructural, la paroi externe du cyste est caractérisée par des protrusions villositaires ressemblant à des épines, de 800 nm de longueur, 200-250 nm de diamètre à leur base, et effilées à leur extrémité. En coupe, ces protrusions sont lobulées ou irrégulières. La transmission de Ptyodactylus guttatus à Coluber rogersi conduit à une élimination d'oocystes/sporocystes à partir du 38 jour après I'infestation. La morphologie des sarcocystes et les données expérimentales font apparaître Sarcocystis stenodactylicolubris comme une nouvelle espèce.
SARCOCYSTIS STUNODACTYLICOLUBRIS N. SP., UNE NOUVELLE COCCIDIE PRÉSENTANT UN CYCLE HÉTÉROXÈNE SERPENT-GECKO
e
MOTS CLES : Sarcocystis stenodactylicolubris n.sp., serpent, gecko, cycle KEY WORDS : Sarcocystis stenodactylicolubris n. sp., snake, gecko, life parasitaire. cycle.
INTRODUCTION
S
nakes are often reported as definitive hosts o f the coccidian genus Sarcocystis (e.g. Matuschka, 1985; McAllister et al., 1993, 1995, 1996; Paperna & Finkelman, 1998; Upton et al., 1 9 9 2 ) . Seventeen Sarcocystis species are described with a full life cycle (Matuschka, 1987a; Odening, 1998; Šlapeta et al., 1999; Volf et al., 1 9 9 9 ) . Although s o m e o f these species use lizards o f saurian families Lacertidae and Scincidae as intermediate hosts, n o Sarcocystis cycling b e t w e e n snakes and g e c k o e s ( G e k k o n i d a e ) w a s described to date. However, a f e w records o f sarcocysts from tis sues of gekkonid lizards were reported (Bertram, 1892;
* Department of Parasitology, University of Veterinary and Pharma ceutical Sciences, Palackého 1-3, 612 42 Brno, Czech Republic. ** Institut of Parasitology, Academy of Sciences of the Czech Repu blic, Branišovská31, 370 05 České Budějovice, Czech Republic. Correspondence: David Modry. Tel: +420-5-41562979 - Fax: +420-5-41562266. e-mail:
[email protected] Parasite, 2000, 7, 201-207
Chatton & Avel, 1923; D u p o u y & Kechemir, 1973; Paperna & Finkelman, 1998; W e b e r , 1909, 1910). Presented paper provides the results of series o f transmissional experiments with an isolate of Sarcocystis ori ginated from a colubrid snake Coluber najadum. Fur thermore, the endogenous developmental stages of this species are described within its intermediate ( g e c k o ) and final (colubrid s n a k e ) hosts after an experimental infection. D e s c r i b e d Sarcocystis differs significantly from all hitherto described m e m b e r s of the genus and is therefore considered to b e a n e w species.
MATERIALS A N D M E T H O D S INFECTIOUS MATERIAL
A
n adult, melanistic male of Dahl's whip snake, Coluber najadum (Eichwald, 1831) was col lected in black lava desert near Ar Rashiedeh in SW Syria during the herpetological and parasitological field research in April 1994. Snake was trans-
Mémoire
201
MODRY D., KOUDELA B. & SLAPETA J.R.
ported to the D e p a r t m e n t o f Parasitology o f Univer
o f 5 - 1 5 days, d e p e n d i n g u p o n the irregular feeding
sity o f Veterinary and Pharmaceutical S c i e n c e s , B r n o ,
habit o f the s n a k e .
Czech Republic. T h e s n a k e w a s kept in an isolated terrarium and force-fed with sucking laboratory m i c e . Fresh faecal samples w e r e collected from terrarium and e x a m i n e d repeatedly using modified Sheater's sugar solution (s.g. 1.30) flotation t e c h n i q u e . T h e s n a k e was euthanized due to b a d health status three w e e k s after importation and tissue samples w e r e fixed for further examination. Sporocysts from the f a e c e s and intestinal content w e r e concentrated by flotation, e x a m i n e d mor phologically and p h o t o g r a p h e d using Nomarski inter ference
contrast o p t i c s ( N I C ) . M e a s u r e m e n t s
were
m a d e using a calibrated ocular m i c r o m e t e r and are reported in micrometers, as m e a n s , f o l l o w e d b y the ranges in parentheses. Sporocysts w e r e stored at a tem perature o f 4 - 5 ° C in 2.5 % (w/v) a q u e o u s potassium d i c h r o m a t e solution. Prior the inoculation sporocysts w e r e w a s h e d in tap water and c o u n t e d using h a e m o cytometer.
HISTOLOGY At n e c r o p s i e s , following tissue samples w e r e c o l l e c t e d and fixed in 10 % buffered formalin: naturally infected Coluber
- seven equidistantly spaced sections
najadum
o f the intestine; lizards - stomach, small intestine, large intestine, cloaca, heart, lung, liver, kidney, a b d o m i n a l wall, tongue, b i c e p s femoris m u s c l e and tail; rodents - o e s o p h a g u s , stomach, d u o d e n u m , middle jejunum, ileum,
caecum,
colon,
r e c t u m , heart, l u n g s ,
s p l e e n , kidney, urine bladder, t o n g u e ,
liver,
diaphragm,
heart, muscles o f the abdominal wall, brachial muscles and left b i c e p s femoris m u s c l e . Tissue samples w e r e c o n s e q u e n t l y p r o c e s s e d for the histology using stan dard methods. Paraffin sections w e r e stained with h a e matoxylin and eosin (H & E ) and G i e m s a stains. ELECTRON MICROSCOPY
Muscles o f Stenodactylus
INFECTION AND MAINTENANCE OF EXPERIMENTAL ANIMALS
grandiceps
containing sar
cocysts w e r e fixed in 2.5 % glutaraldehyde in c a c o dylate buffer (0.1 M, pH 7 . 4 ) at 4 ° C and postfixed in
Following laboratory b r e d lizards, w h i c h can naturally
1 % o s m i u m tetroxide in the s a m e buffer. S p e c i m e n s
o c c u r in f o o d spectrum o f Coluber
in Syria,
w e r e w a s h e d three times in the s a m e buffer, dehy
w e r e u s e d for intermediate host studies ( n u m b e r s o f
drated in graded alcohols and e m b e d d e d in Durcupan.
infected and control animals u s e d in e x p e r i m e n t s are
Ultrathin sections w e r e stained with uranyl
n o t e d in p a r e n t h e s e s ) : Lacertidae:
and lead citrate and then e x a m i n e d with a J E O L 1 0 1 0
grandis
(2, 1); Mesalina
Chalcides
ocellatus
k o n i d a e : Ptyodactylus grandiceps
brevirostris
(3, 2 ) , Mabuya guttatus
najadum
Acanthodactylus (2, 1); Scincidae: vittata
(2, 1),
(2, 1); G e k
acetate
transmission electron m i c r o s c o p e . S p e c i m e n s for scanning electron m i c r o s c o p y
(SEM)
Stenodactylus
w e r e fixed in 4 % buffered paraformaldehyd at 4° C
( 1 , 1). All lizards w e r e c a g e d separately in
Small portions o f tissue w e r e rinsed several times in
plastic terraria and fed on laboratory reared crickets
distilled water, d e h y d r a t e d in a l c o h o l a n d
with mineral and vitamin supplementation. Each e x p e
series and desiccated b y critical point drying in c a r b o n
rimental lizard w a s inoculated orally with 2 x 1 0 s p o
dioxide. The
rocysts b y a s t o m a c h tube. Additionally, five BALB/c
spraying device and e x a m i n e d with a J E O L JMS 6 3 0 0
m i c e and five laboratory reared c o m m o n voles
scanning electron m i c r o s c o p e .
5
tus arvalis)
(Micro-
samples were
acetone
then gold-coated
in
w e r e infected orally with 1 0 sporocysts and 5
kept as described previously (Slapeta et al., 1999). E x p e rimentally inoculated and control lizards w e r e eutha nized by ether and dissected 7 8 days after the infec tion ( D P I ) and experimentally inoculated rodents w e r e e x a m i n e d o n 150 and 180 DPI, respectively. In the definitive host study o n e adult, laboratory kept, coccidia free colubrid s n a k e Coluber
rogersi
w a s used.
Snake w a s fed solely o n laboratory m i c e . F a e c e s w e r e m o n i t o r e d using flotation t e c h n i q u e with
negative
result for 12 m o n t h s prior the experimental infection. O n e living, captive born male o f Ptyodactylus
guttatus,
inoculated orally with 2 x 1 0 sporocysts 80 days before, 5
w a s fed to this s n a k e . Terminal half o f the tail o f this g e c k o w a s biopsied two days before the feeding e x p e riment for p r e s e n c e o f sarcocysts in muscles. Faecal samples o f inoculated s n a k e w e r e e x a m i n e d using flo tation m e t h o d for the p r e s e n c e o f coccidia in intervals
202
RESULTS STAGES IN FOUND THE DEFINITIVE HOST
E
xamination o f t h e intestinal c o n t e n t o f naturally infected Coluber
najadum
revealed
liberated sporocysts o f Sarcocystis
numerous
sp. (Fig. 1 ) .
Oocysts w e r e only rarely seen. Sporocysts are tetrazoic, ellipsoidal, 9.7 ( 9 - 1 0 ) x 7.6 ( 7 - 8 ) pm, s h a p e index 1.3. Stieda and substieda b o d i e s are absent. Sporocyst resi duum is present, c o m p o s e d o f n u m e r o u s small gra nules o f the equal size. Sporocyst wall is single-layered, s m o o t h and colourless; s p o r o z o i t e s are long oval. N u m e r o u s sporocysts, structurally and
morphologi
cally identical with the original isolate, w e r e first found on 3 9 DPI in f a e c e s o f experimentally infected
Mémoire
Coluber
Parasite, 2000, 7, 201-207
SARCOCYSTIS STENODACTYLICOLUBRIS, NEW SARCOSPORIDIUM WITH SNAKE-GECKO CYCLE
rogersi. Only few oocysts (less than 1 %) were observed,
Sarcocysts found in S. grandiceps
having thin, colourless oocyst wall closely adjacent to
gate, reached a length o f 1 7 5 - 2 0 0 µm and a width o f
7 8 DPI w e r e elon
the t w o fully sporulated sporocysts. Shedding o f the
35-50 µm. W h e n studied with the light microscope, the
oocysts/sporocysts b y experimentally infected
primary cyst wall o f sarcocysts w a s about
rogersi
Coluber
lasted at least for three c o n s e q u e n t months.
Histological examination o f naturally infected
pm
Coluber
S e c o n d a r y cyst wall was not observed. Elongated cys-
oedematous
tozoites, 5-6 x 1.5 µm with centrally located nucleus
lamina propria o f the proximal part o f intestine. T h e
w e r e observed inside cysts, together with few scattered
lamina propria w a s p a c k e d with bisporocystic oocysts
metrocytes.
(Fig. 7 ) which mostly collapsed during the previous
Ultrastructurally, the sarcocyst wall b e l o n g s to the type
najadum
revealed greatly t h i c k e n e d
1-2
thick, with barely visible villar protrusions (Fig. 2 ) .
fixation and processing, similar findings w e r e obtained
II. according D u b e y et al. ( 1 9 8 9 ) . T h e r e w e r e charac
u s i n g SEM o f t h e c r o s s - s e c t i o n
intestinal
teristic spine-like villar protrusions arising from the cyst
m u c o s a (Fig. 9 ) . However, the majority o f stages was
wall. Ground substance was ca. 2 0 0 - 3 0 0 nm thick with
through
lost during the sample processing and mostly only hol
numerous septa stretched dividing the cyst into c o m
lows in m u c o s a indicated the previous location
of
partments containing cystozoites (Fig. 5 ) . Protrusions
oocysts/sporocysts (Figs 9, 10). SEM photographs o f the
are up to 8 0 0 nm long, 2 0 0 - 2 5 0 nm in diameter at their
mucosal surface revealed areas o f extensive erosions
base, tapering to thinner a p e x , ca 100 pm in diameter.
with liberating sporocysts, organised usually in clus
T h e wall o f protrusions a p p e a r e d slightly undulated in
ters (Figs 8, 11). Distinct sutures c o n n e c t i n g plates o f
longitudinal sections. Protrusions are typically lobular
sporocyst wall a p p e a r e d on detailed SEM photographs
or irregular in the cross-sections, mainly at the basis
o f sporocysts surface (Fig. 1 2 ) .
(Fig. 6 ) . E n d o d y o g o n y (Fig. 4 ) w a s the only repro duction m o d e o b s e r v e d within e x a m i n e d sarcocysts.
STAGES IN EXPERIMENTAL INTERMEDIATE HOSTS,
Sarcocysts o b s e r v e d in experimentally infected
SARCOCYST MORPHOLOGY
dactylus
Lizards o f seven species, b e l o n g i n g to three families and t w o s p e c i e s o f rodents w e r e inoculated with the original isolate from naturally infected Coluber dum
( T a b l e I ) . Only g e c k o e s Stenodactylus
and Ptyodactylus
najagrandiceps
p r o v e d susceptible to the
guttatus
infection. Numerous sarcocysts w e r e o b s e r v e d in wet smears s q u e e z e d under a c o v e r glass as well as in his tological sections o f musculature o f tail, limbs
and
tongue o f all infected g e c k o s . Sarcocysts w e r e
not
o b s e r v e d in the musculature o f any other lizards n o r r o d e n t s . N e i t h e r clinical signs n o r mortality
were
o b s e r v e d in experimentally infected hosts.
guttatus
tical to that reported a b o v e .
TAXONOMIC SUMMARY Sarcocystis
stenodactylicolubris
Exogenous
stages:
Stenodactylus grandiceps (Gekkonidae) Ptyodactylus guttatus (Gekkonidae) Mesalina abrevirostris (Lacertidae) Acanthodactylus grandis (Lacertidae) Mabuya vittata (Scincidae) Chalcides ocellatus (Scincidae) Microtus arvalis (Cricetidae) Mus BAL/c (Muridae)
Infectious dose Euthanized (sporocysts) (DPI)
Oocysts only rarely seen, fully spo
found in the f a e c e s . Sporocysts tetrazoic, ellipsoidal, 9-7 ( 9 - 1 0 ) x 7.6 ( 7 - 8 ) µm. Sporocyst residuum present, c o m p o s e d o f n u m e r o u s small granules o f the equal size. Sporocyst wall single-layered, smooth and colour less, with distinct sutures observed by SEM; sporozoites elongately oval. Sarcocysts are elongated, 7 8 DPI are 175-
2 0 0 pm long and 3 5 - 5 0 µm wide. Sarcocyst wall type Result (+/-)
II. according Dubey et al. (1989). Primary sarcocyst wall ca. 2 µm thick, with n u m e r o u s spine-like villar pro
+
trusions, lobular or irregular in the cross-section.
78
+
wald, 1 8 3 1 ) (Serpentes: Colubridae).
2 x 1(P
78
-
2 x lfp
78
-
2 x l(f
78
-
2 x 1()
78
-
2 x 10
5
2 x 10
5
5
1
x 10
1
x 1(P
5
Table I. - Intermediate host experiments. Parasite, 2000, 7, 201-207
n. sp.
rulated free sporocysts represent a majority o f stages
Sarcocysts: Experimentaly inoculated host
Ptyo-
7 8 DPI w e r e morphologically iden
78
Type host: Dahl's w h i p snake, Coluber Other
hosts:
Coluber
experimentally
rogersi
najadum
(Anderson, 1 8 9 3 ) (final,
i n f e c t e d ) ; Stenodactylus
Haas, 1952; P. guttatus
(Eich-
grandiceps
Heyden, 1827 (intermediate, all
infected experimentally). Type locality.
Ar Rashiedeh, SW Syria (32° 4 0 ' N , 37° 3 ' E)
Type specimens:
Photosyntypes and histological slides
1211
-
are deposited in Parasitological Institute o f Academy
180
-
vice, coll. No. R 181/94.
o f S c i e n c e s o f the Czech Republic in České BudějoSymbiotypes:
Symbiotype o f the type host
(alcohol
preserved) is deposited in the Herpetological collec-
Mémoire
203
MODRY D . , K O U D E L A B . & S L A P E T A J . R .
Figs 1-6. - Basic morphological features of Sarcocystis stenodactylicolubris sp. n. Fig. 1. Sporocysts isolated from faeces of C. najadum, scale bar = 5 µm. Fig. 2. Histological section of the tail musculature of S. grandiceps with sarcocyst, note barely visible villar protrusions (arrowheads). Fig. 3- Ultrastructure of sarcocyst of Sarcocystis stenodactylicolubris showing several cystozoites, septa and protrusions. Fig. 4. Cystozoites dividing by the endodyogony. Fig. 5. Spine-like villar protrusions of the primary cyst wall, scale bar = 200 nm. Fig. 6. Crosssection through the zone of protrusions showing their lobular character. 204
Mémoire
Parasite, 2000, 7, 201-207
SARCOCYSTIS STENODACTYUCOLUBRIS, NEW SARCOSPORIDIUM WITH SNAKE-GECKO CYCLE
Figs 7-12. - Developmental stages of Sarcocystis stenodactylicolubris sp. n. in Coluber najadum. Fig. 7. Histological section of intestinal mucosa with oocysts/sporocysts (arrows), scale bar = 10 pm. Fig. 8. SEM picture of mucosal surface showing erosions with liberating spo rocysts (arrow). Fig. 9. SEM picture of cross section through intestinal mucosa with numerous hollows indicating previous location of deve lopmental stages (arrow). Fig. 10. Detail view of the same region. Fig. 11. Sporocysts liberating in clusters from erosions in the mucosal surface. Fig. 12. Oocyst (arrow) and sporocysts liberated from the intestinal mucosa. Note rib-like prominating sutures of plates of sporo cyst wall (arrowheads). Parasite, 2000, 7, 201-207
Mémoire
205
MODRY D., KOUDELA B. & SLAPETA J.R.
tion o f the National Museum Prague, coll. No. NMP6W34896. Etymology: T h e specific n a m e stenodactylicolubris reflects the generic n a m e o f the intermediate (Stenodactylus) and definitive host (Coluber).
DISCUSSION
C
occidia o f the g e n u s Sarcocystis are c o m m o n parasites a m o n g snakes o f family Colubridae, w h i c h serve as definitive hosts ( M a t u s c h k a ,
1985, 1987a; McAllister et al., 1993, 1995; Paperna & Finkelman, 1998; Roudabush, 1937; Volf et al., 1 9 9 9 ) . In contrast to c o m m o n findings o f these parasites in colubrids, only six species w e r e described with their life cycle u p to date ( B l e d s o e , 1980; Matuschka, 1981,
1986, 1987b; Sakran, 1993; Volf et al., 1 9 9 9 ) . Various lizards are intermediate hosts o f four of these species, w h i c h are therefore c o m p a r e d with Sarcocystis stenodactylicolubris sp. n. Sarcocystis gongyli Trinci 1911 is described from colu brid s n a k e Spalerosophis diadema and scincid inter mediate host Chalcides ocellatus (Abdel-Ghaffar et al., 1990; Sakran, 1993, Trinci, 1911). Sarcocysts of this spe cies differ significantly from S. stenodactylicolubris in having leaf-like protrusions (Bashtar et al., 1 9 9 1 ) . Sarcocystis cbalcidicolubris Matuschka 1987 described from the Mediterranean region u s e s also colubrid snake, namely Coluber ravergieri as definitive hosts and skink Chalcides ocellatus as intermediate hosts. S. stenodactylicolubris can b e differentiated well from this species ultrastructurally b y different protrusions. Similarly, Sarcocystis podarcicolubris Matuschka, 1981 from colubrid snakes of the genus Coluber and Macroprotodon a n d from lacertids b e l o n g i n g to g e n e r a Lacerta, Podarcis and Algyroides differs significantly in ultrastructural features o f sarcocysts. Protrusions o f S. podarcicolubris are described as palisade-like (Matu schka et al., 1 9 8 4 ) , in contrast to villar, spine-like pro trusions o f S. stenodactylicolubris. Sarcocystis lacertae Babudieri, 1932 cycles b e t w e e n c o l u b r i d s n a k e Coronella austriaca and lizards Podarcis muralis. Also this species differs significantly in its ultrastructure, having spine-like, typically arching protrusions with spongiform appearance of the ground substance (Volf et al., 1 9 9 9 ) .
thick sarcocyst wall and b e l o n g evidently to a species different from S. stenodactylicolubris. T h e final host o f S. platydactyli remains u n k n o w n and n e e d s further research. Recently, Paperna & Finkelman ( 1 9 9 8 ) reported p r e s e n c e of sarcocysts in tissues o f Ptyodactylus hasselquistii from Israel. Ultrastructurally, sarco cysts p r e s e n t e d b y these authors differs in having undulating, spongiforme-like ground substance with numerous fine invaginations and protrusions with only slightly undulating circumference in cross-section. Majority of snakes of the genus Coluber is typically saurophagous, feeding on wide variety o f lizards. In many ecosystems they have opportunity to feed on saurians o f families S c i n c i d a e , G e k k o n i d a e a n d Lacertidae. However, the composition o f their prey differs greatly b a s e d o n the s n a k e species, type o f the habitat and the season. G e c k o e s o f genera Stenodactylus and Ptyodactylus are the most c o m m o n saurian species in black lava desert of southern Syria and their involvement in the life cycle o f Sarcocystis species is therefore not sur prising. Possibly, more species of Sarcocystis can occur together in colubrid snakes o f the region, using also scincids and lacertids as intermediate hosts. B a s e d o n results of our experiments and o n previously published data w e can suggest that sarcosporidia parasitising colubrid snakes as final hosts are family specific on the level o f their intermediate hosts, usually transmissible to m o r e host genera. Pathogenicity and pathology o f Sarcosporidia in final ophidian hosts w a s only scarcely reported. O u r fin dings in the intestine o f naturally infected Coluber najadum are similar to that published by Daszak & Cunningham ( 1 9 9 5 ) in Pituophis melanoleucus. Simi larly, the a b s e n c e of clinical and pathological findings in infected intermediate hosts corresponds well with previously published studies (Matuschka, 1981, 1985, 1987a; Volf et al., 1 9 9 9 ) . Sporocysts wall c o m p o s e d of four collapsible plates joined in rib-like prominating sutures w a s repeatedly reported in m e m b e r s o f genera Isospora, Toxoplasma and Sarcocystis ( B o x et al., 1980; Speer et al., 1973, 1976). O u r results showing sporocysts surface of S. stenodactylicolubris using SEM are identical and confirm this feature to b e a c o m m o n feature for Sarcocystis spp. B a s e d on all morphological and biological differences reported in this study it is evident, that Sarcocystis stenodactylicolubris represents a n e w species.
A few records o f sarcocysts from tissues o f g e k k o n i d lizards are reported to date. Bertram ( 1 8 9 2 ) had des c r i b e d Sarcocystis platydactyli from Mediterranean g e c k o Tarentola mauritanica. Later on, several authors reported tissue cysts in this c o m m o n Mediterranean g e c k o ( W e b e r , 1909, 1910; Chatton & Avel, 1 9 2 3 ; D u p o u y & Kechemir, 1 9 7 3 ) . However, tissue cysts reported by all o f these authors are typical in having 206
ACKNOWLEDGEMENTS
W
e are indebted to J . Moravec for confirming the s n a k e determination and M. Modry and H. Modrá for help during the field trip to Syria. W e thank V. S c h a c h e r l o v á for the preparation o f histological and SEM samples. This study w a s sup-
Mémoire
Parasite, 2000, 7, 201-207
SARCOCYSTIS STENODACTYLICOLUBRIS,
p o r t e d b y t h e grant N o . 5 2 4 / 0 0 P 0 1 5 o f t h e Grant A g e n c y o f the Czech Republic, a n d in part also b y t h e grant No. 1228/1999 o f Ministry o f Education.
NEW SARCOSPORIDIUM WITH SNAKE-GECKO CYCLE
wall lizards (Podarcis tiliguertd), S. gallotiae from naturally infected Canarian lizards (Gallotia galloti) and S. dugesii from Madeiran lizards (Lacerta dugesii). Protistologica, 1984, 20, 133-139. MCALLISTER C.T., UPTON S.J., GARRETT CM., STUART J.N. & PAIN
REFERENCES ABDEL-GHAFFAR F., BASHTAR A. R., ASHOUR M . B. & SAKRAN T.
Life cycle of Sarcocystis gongyli Trinci 1911 in the skink Chalcides ocellatus and the snake Spalerosophis diadema. A light and electron microscopic study. Parasitology Research, 1990, 76, 444-450. BASHTAR A. R., ABDEL-GHAFFAR F., ASHOUR M . B. & SAKRAN T.
Endodyogony and cyst formation of Sarcocystis gongyli (Trinci 1911) from the skink Chalcides ocellatus. Journal of the Egyptian Society of Parasitology, 1991, 21, 383-393. BERTRAM A. Beiträge zur Kenntnis der Sarcosporidien nebs einem Anhang über parasitische Schläuche in der Leibeshôhle von Rotatorien. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere, 1892, 5, 581-604. BLEDSOE B. Sarcocystis idahoensis sp. n. in deer mice Peromyscus maniculatus (Wagner) and gopher snake Pituophis melanoleucus (Daudin). Journal of Protozoology, 1980, 27, 93-102. Box E. D., MARCHIONDO A. M . , DUSZYNSKI D. W. & DAVIS P .
Ultrastructure of Sarcocystis sporocysts from passerine birds and opossums: comments on classification of the genus Isospora. Journal of Parasitology, 1980, 66, 68-74. CHATTON E. & AVEL M . Sur la Sarcosporidie du gecko et ses
cytophanères. La paroi et le réticulum sarcosporidiens appartiennent en propre au parasite. Comptes Rendus des Sciences de la Société de Biologie (Paris), 1923, 89, 181-185. DUPOUY J . & KECHEMIR N. Les Cestodes de reptiles en Algérie. Essai de revision du genre Oochoristica Lühe (Cestoda, Anoplocephalidae9. Bulletin de la Société Histoire Naturelle d'Afrique Nord (Alger), 1973, 64, 47-98. DASZAK P. & Cunningham A. A report of intestinal sarcocystosis in the Bullsnake (Pituophis melanoleucus sayi) and re-evaluation of Sarcocystis sp. from snakes of the genus Pituophis. Journal of Wildlife Diseases, 1995, 31, 400-403. MATUSCHKA F.-R. Life cycle of Sarcocystis between pokilothermic hosts. Lizards are intermediate hosts for S. podarcicolubris sp. nov., snakes function as definitive hosts. Zeitschrift fur Naturforschung, 1981, 36c, 1093-1095. MATUSCHKA F.-R. Experimental investigations on the host range of Sarcocysds podarcicolubris. International Journal for Parasitology, 1985, 15, 77-80. MATUSCHKA F.-R. Sarcocystis clethrionomyelaphis n.sp. from snakes of the genus Elaphe and different voles of the family Arvicolidae. Journal of Parasitology, 1986, 72,226-231. MATUSCHKA F.-R. Reptiles as intermediate and/or final hosts of Sarcosporidia. Parasitology Research, 1987a, 73, 22-32. MATUSCHKA F.-R. Sarcocystis chalcidicolubris n. sp.: Reco gnition of the life cycle in skinks of the genus Chalcides and snakes of the genus Coluber. Journal of Parasitology, 1987b, 73, 1014-1018. MATUSCHKA F.-R. & MEHLHORN H. Sarcocysts of
podarcicolubris
TER C.W. Hemogregarines and Sarcocystis sp. (Apicom plexa) in a Western Green Rat Snake, Senticollis triaspis intermedia (Serpentes: Colubridae), from a New Mexico. Journal of the Helminthological Society of Washington, 1993, 60, 284-286. MCALLISTER C. T., UPTON S. J . , TRAUTH S. E. & DIXON J . R. Coc-
cidian parasites (Apicomplexa) from snakes in the Southcentral and Southwestern United States: new host and geo graphical records. Journal of Parasitology, 1995, 81, 63-68. MCALLISTER C.T., UPTON S.J., BARKER D.G. & PAINTER C.W. Sar-
cocystis sp. (Apicomplexa) from a New Mexico Ridgenose Rattlesnake, Crotalus willardi obscurus (Serpentes: Viperidae) from Sonora, Mexico. Journal of the Helminthological Society of Washington, 1996, 63, 158-130. ODENING K . The present state of species-systematics in Sarcocystis Lankester, 1882 (Protista, Sporozoa, Coccidia). Systematic Parasitology, 1998, 41, 209-233. PAPERNA I. & FINKELMAN S. Sarcocystis infection among snakes in Israel. Parassitologia, 1998, 40, 447-456. ROUDABUSH R.L. Some coccidia of reptiles found in North America. Journal of Parasitology, 1937, 23, 354-359. SAKRAN T.F.A. Sarcocystis gongyli (Sarcocystidae-Sporozoa), predator-prey monoxenous life cycle. Journal of the Egyptian German Society for Zoology, 1993, 11 (D), 91-105. SPEER C.A., HAMMOND D.M., MAHRT J.L. & ROBERSTS W.L. Struc
ture of the oocyst and sporocyst walls and excystation of sporozoites of Isospora canis. Journal of Parasitology, 1973, 59, 35-40. SPEER C.A., MARCHIONDO A.A., DUSZYNSKI D.W. & FILE S.K.
Ultrastructure of the sporocyst wall during excystation of Isospora endocallimici. Journal of Parasitology, 1976, 62, 984-987. SLAPETA J.R., MODRY D. & KOUDELA B. Sarcocystis
n.
TRINCI G. Nota sopra una Sarcocystis parasita di Gongylus ocellatus Wagl., con considerazioni critiche sulla morfologia a sulla biologia dei Sarcosporidi. Monitore Zoologico Italiano, 1911, 22, 309-326. VOLF J . , MODRY D., KOUDELA B. & ŠLAPETA J.R. Discovery of
the life cycle of Sarcocystis lacertae Babudieri, 1932 (Api complexa: Sarcocystidae), with a species redescription. Folia Parasitologica, 1999, 46, 257-262. WEBER A. Sur la morphologie dela Sarcosporidie du gecko (Sarcocystis platydactyli Bertram). Comptes Rendus des Sciences de la Societe de Biologie (Paris), 1909, 66, 10611062. WEBER A. Recherches sur la Sarcosporidie du gecko cystis platydactyli Bertram). Archives de Anatatomie scopique, 1910, 66, 1061-1062.
Sarcocystis
from experimentally infected Tyrrhenian
Parasite, 2000, 7, 201-207
atheridis
sp., a new sarcosporidian coccidium from the Nitsche's Bush Viper, Athens nitschei Tornier, 1902 from Uganda. Parasitology Research, 1999, 85, 758-764.
Mémoire
(SarcoMicro-
Reçu le 16 mars 2000 Accepté le 27 juin 2000
207