HELGOI.ANDER MEERESUNTERSUCHUNGEN
Helgol~inder Meeresunters. 42, 583-591 (1988)
Syltodinium listii g e n . et spec. n o v . , a m a r i n e
e c t o p a r a s i t i c d i n o f l a g e l l a t e o n e g g s of c o p e p o d s a n d
rotifers*
Gerhard Drebes
Bio]ogische Anstalt Helgoland (I_a'tora]station); D-2282 List/Sylt Federal Republic of
Germany
ABSTRACT: Syltoch?fium fistii is described as a n e w marine ectoparasitic dinoflagellate. In culture
experiments the species was found feeding on eggs of planktonic copepods a n d rotifers. The
dinospore penetrates the host by a peduncle, and transforms into a trophont by sucking out the egg
contents phagotrophically. After detaching from the host, the mature trophont settles down to
become a palmelloid multiplication stage. By repeated binary fission, up to 16 or 32 gymnodinoid,
colourless dinospores are formed inside a gelatinous envelope. The parasite retains its dinoflagellate
(monadoid) nature throughout its whole vegetative life cycle. Even during the trophic a n d multiplication phase the species remains latently motile. Despite some resemblance to Dissodinium, there
are sufficient reasons for the establishment of the new genus Syltodinium.
INTRODUCTION
E c t o p a r a s i t i c d i n o f l a g e l l a t e s o n e g g s of c r u s t a c e a n s w e r e first d e s c r i b e d b y D o g i e l
(1906). His t h r e e n e w s p e c m s w e r e t r a n s f e r r e d b y C h a t t o n (1912) to a n e w g e n u s ,
Chytriodinium, l a t e r r e i n v e s t i g a t e d b y C a c h o n & C a c h o n (1968). Dissodinium K l e b s i n
P a s c h e r i n c l u d e s t w o s p e c i e s p a r a s i t i z i n g e g g s of p l a n k t o n i c c o p e p o d s ( G b n n e r t , 1936;
D r e b e s . 1969, 1978). D. pseudocalani ( G b n n e r t ) D r e b e s e x Elbr. & D r e b . w a s f o u n d
f e e d i n g o n e g g s of o n l y Pseudocalanus elongatus B o e c k , w h e r e a s D. pseudolunula
(Swift) e x Elbr. & D r e b . p r e f e r s e g g s of Temora longicornis M f i l l e r a n d Acartia sp., a n d
e v e n of t h e r o t i f e r Synchaete sp. ( D r e b e s , 1984). D. pseudolunula c o u l d b e m a i n t a i n e d
c o n t i n u o u s l y i n c u l t u r e , so far as h o s t s u b s t r a t e w a s a v a i l a b l e , b u t u n t i l n o w o n l y t h e
v e g e t a t i v e life c y c l e w a s o b t a i n e d u n d e r l a b o r a t o r y c o n d i t i o n s . In a d d i t i o n , i n p l a n k t o n
c a t c h e s f r o m t h e N o r t h S e a , s t a g e s w e r e m e t w i t h w h i c h w e r e i n t e r p r e t e d as r e s t i n g cysts
of t h e p a r a s i t e ( D r e b e s , 1981; J o h n & Reid 1983).
F u r t h e r a t t e m p t s to g e t s e x u a l r e p r o d u c t i o n of D. pseudolunula i n c u l t u r e failed, b u t
l e d to a s u r p r i s i n g result. A f t e r a d d i n g a h i g h c o n c e n t r a t i o n of e g g s of Temora a n d
Acartia, f r e s h l y c o l l e c t e d f r o m t h e sea, into a Dissodinium c u l t u r e , a f e w u n k n o w n life
s t a g e s s o o n o c c u r r e d . S i n c e t h e y c o u l d n o t b e r e l a t e d to Dissocfinium, t h e y w e r e
s e p a r a t e d a n d t h e i r f u r t h e r d e v e l o p m e n t f o l l o w e d A s a result, w e w e r e d e a l i n g w i t h a
n e w e c t o p a r a s i t i c d i n o f l a g e l l a t e , o n l y d e t e c t e d b y c h a n c e a s a c o n t a m i n a t i o n in a
9 Dedicated to Dr. Dr. h. c. P. Kornmann on the occasion of his eightieth birthday
9 Biologische Anstalt Helgoland, H a m b u r g
584
Gerhard Drebes
Dissodinium culture. Once recognized, the n e w species described herein for the first time
could b e observed also in p l a n k t o n samples t a k e n from the W a d d e n Sea ( G e r m a n Bight).
T h o u g h the cultures w e r e prematurely lost a n d the observations thus still incomplete, the
vegetative life cycle can be roughly outlined.
MATERIALS AND METHODS
First observed in August 1985 in a Dissodinium culture fed with copepod eggs,
Syltodinium listii Drebes gen. et spec. nov. was later directly isolated from p l a n k t o n
samples t a k e n from the W a d d e n Sea n e a r List/Sylt (German Bight, North Sea). Clonal
cultures of the parasite were established a n d m a i n t a i n e d in Petri dishes in a n u t r i e n t
e n r i c h e d f/2 m e d i u m (McLachlan, 1973). Kept at a t e m p e r a t u r e of 15 ~ a n d a n illumination of 14 h per day, S. listii was regularly supplied with the appropriate host substrate.
Accordingly, once a w e e k the parasite was fed with eggs of Temora longicornis, Acartia
sp., or sometimes of Synchaete sp.
The vegetative hfe cycle was studied on living material at room t e m p e r a t u r e s u s i n g
sea w a t e r immersion objectives (Leitz). For a raw analysis of the various cell structures,
cytological methods common in light microscopy were applied.
RESULTS
Syltodinium Drebes gen. nov.
Ectoparasitic dinoflageUate on eggs of p l a n k t o n i c crustaceans a n d rotifers. Dinospores gymnodinoid. Food uptake phagotrophically by a peduncle. After feeding, the
trophont detaches from the host and,transforms into a palmelloid multiplication stage,
e m b e d d e d in a gelatinous envelope. Dinospores are formed by r e p e a t e d b i n a r y fission.
Type species: S. listii Drebes sp. nov.
Latin diagnosis: Dinoflagellata extoparasitica ad ova crustaceorum et rotatoriorum
planctonicorum. Dinosporae g y m n o d i n o i d e a e . Receptio a h m e n t i modo phagotrophico
per p e d u n c u l u m . Receptio alimenti finita trophontus separatus de hospite transformat in
stadium p a l m e l l o i d e u m multiplicationis involucro mucoideo circumdato. Dinosporae per
bipartione repitita formantur. Typus generis: S. fistii Drebes sp. nov.
S y l t o d m l u m flst11 D r e 0 e s sp. n o v .
Ectoparasitic on eggs of m a r i n e copepods (Temora longicornis, Acartia sp.,
Pseudocalanus elongatus) and rotifers (Synchaete sp.). Dinospores colourless, 27-33 ~m
long, 22-27 ~m wide. Epicone conical, hypocone hemispherical or conical. Girdle
m e d i a n , left-handed, sulcus e x t e n d i n g from a n t a p e x to apex. Nucleus r o u n d i s h oval,
Figs 1-4. Syltodinium listii. Fig. 1. A mature trophont having emptied an egg of Acartia sp. On the
right a dinospore sticking to the egg surface. Fig. 2. As in Fig 1, 17 rain. later. Detached from the egg
the trophont is swimming away. The dinospore has driven a peduncle into the egg interior. Fig. 3.
Egg of Synchaete sp. infested with four dinospores, the right one already being a young trophont.
Fig. 4. Trophont sucking on an egg of Synchaete sp. Figs 1-4: Scale bar = 50 ~tm
Syltodinium, an ectoparasific dinoflagellate
585
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Gerhard Drebes
lying in t h e epicone. Trophont oval, slightly constricted b y the girdle, u p to 80 ~tm in
length. Tubiforrn p e d u n c l e with a wall, left inside the host after d e t a c h m e n t of the
parasite. D e t a c h e d trophont initially motile, t h e n b y secretion of a g e l a t i n o u s e n v e l o p e
d e v e l o p i n g into a p a l m e l l o i d multiplication stage. By r e p e a t e d b i n a r y fission up to 16 or
32 dinospores are formed. T y p e locality: G e r m a n Bight n e a r List/Sylt.
Latin diagnosis: Ectoparasitico a d ova c o p e p o d o r u m m a r i n o r u m (Temora longicornis, Acart/a, sp., Pseudocalanu$ elongatus) et rotaroriorum (Synchaete sp.). D i n o s p o r a e
sine colore, longitudo 27-33 btm, latitudo 22-27 btm. Epiconus conicus, h y p o c o n u s
h e m i s p h a e r i c u s vel conicus. C i n g u l u m m e d i a n u m , sinistrorsum d e s c e n d e n s , sulcus a
a n t a p i c e a d a p i c e m extendens. Nucleus globosus ovo similis in epicono situs est.
Trophontus ovo similis, cingulo leviter constrictus, longitudine u s q u e a d 80 btm. P e d u n cu_lus tubiformis cure muro in hospite reliquitur post s e p a r a t i o n e m p a i a s i t a e . Trophontus
s e p a r a t u s mobilis primo, d e i n d e secretione involucrae m u c o i d e a e in stadio p a l m e l l o i d i o
multiplicationis transformans. Dinosporae u s q u e a d 16 vel 32 p e r b i p a r t i o n e r e p e t i t a
formantur.
Locus typicus: In m a r e sino g e r m a n i c o iuxta List/Sylt. Typus: F i g u r a e 1-11.
The g e n e r i c n a m e a n d the e p i t h e t refer to the t y p e locality.
OBSERVATIONS
As yet, Syltodinium Iistii has b e e n found only sporadically in the North S e a plankton,
d u r i n g the s u m m e r months J u n e - A u g u s t . The species w a s r e c o g n i z e d b y its gelatinous
p a l m e l l o i d multiplication stages (Figs 7-9)~ The dinospores resulting from these stages
are athecate, g y m n o d i n o i d , l a c k i n g chloroplasts, a n d h a v e the roundish nucleus l o c a t e d
in the epicone n e a r the girdle region. In the middle, the cell b o d y is conspicuously
constricted b y the girdle, which describes a l e f t - h a n d e d spiral, d i s p l a c e d n e a r l y its own
width (Figs 10, 11). The sulcus e x t e n d s ' t o the e p i c o n e r u n n i n g there up to the a p e x as a
n a r r o w d e e p l y incised furrow in a sigmoid curvature. O n the hypocone, the sulcus
flattens d i s a p p e a r i n g u n d e r a left ventral flap. The size d a t a of the dinospores u s e d for the
diagnosis are d e r i v e d from a few m e a s u r e m e n t s , m a d e either from infecting dinospores
a t t a c h e d to the host, or from a 16-celi stage inside a gelatinous envelope. Occasionally,
t h e r e are also d i n o s p o r e s only 22 btm in length, possibly originating from a 32-cell stage.
Most p r o b a b l y chemotactically attracted, the dinospore attaches to the host b y the
posterior e n d of the h y p o c o n e (Fig. 1). Starting from the a n t a p e x a l o n g tubiform
p e d u n c l e is formed which p e n e t r a t e s the e g g (Figs 2, 5). In cases of multi-infections
dinospores often form a p e d u n c l e in vain, b e c a u s e other dinospores h a v e a l r e a d y
e m p t i e d the egg. Then, an u n u s e d p e d u n c l e t a p e r s t o w a r d s the front e n d a n d r e m a i n s
closed (Fig. 5). In contrast, a functioning p e d u n c l e a p p e a r s e n l a r g e d at the distal end, as
can b e o b s e r v e d in F i g u r e 4. As only living s p e c i m e n s w e r e e x a m i n e d , the m o u t h of the
p e d u n c l e cannot b e d e s c r i b e d in detail, since it is a l w a y s m a s k e d b y the food contents,
Figs. 5, 6. Syltodinium fistii. Fig. 5. Multi-infection on an egg of Acartia sp. Two mature trophonts,
and four (two out of focus) dinospores trying to reach by their peduncles the rest of the host material.
Fig. 6. Two trophonts feeding exceptionally (?) on a nauplius of Temora longicornis. Figs. 5, 6: Scale
bar =50 ~m
Syltodinium, an ectoparasitic dinoflagellate
587
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Figs. 7-10. Syltodinium listii. Fig. 7. Early multiplication stage inside a gelatinous envelope. Fig. 8. 8cell stage, surface of the gelatinous envelope crowded with bacteria. Fig. 9. 16-cell stage. Fig. 10.
Liberated dinospore in oblique ventral view. Figs 7-9: Scale bar = 50 ~tm. Fig. 10: Scale bar = 20 ~m
Syltodinium, an ectoparasitic dinoflagellate
589
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Fig. 11. Syltodinium listii.
Half-schematic drawing of a dinospore
e v e n after d e t a c h m e n t of the host (Figs 1, 2). The wall of the peduncle, p r e s u m a b l y
cellulosic, shows a cuff-like t h i c k e n i n g in the region w h e r e it p i e r c e s the e g g envelope.
C o m m e n c i n g food u p t a k e t h r o u g h the p e d u n c l e , the d i n o s p o r e transforms into a
trophont. Increasing considerably in size the trophont elongates a n d a s s u m e s an oval
s h a p e (Figs 1, 2, 4-6). Thereby, girdle a n d sulcus b e c o m e flattened. T h e time n e e d e d for
food u p t a k e m a y vary, d e p e n d i n g on the a m o u n t of host material available. In general,
the e g g s are s u c k e d out within ca 90 min. The m a t u r e trophont d e t a c h e s a n d b e c o m e s
i m m e d i a t e l y motile b y flagellar movement. T h e peduncle, or b e t t e r its wall, is left b e h i n d
inside the e m p t y egg. The trophont swims a r o u n d for a while, t h e n settles d o w n to the
bottom of the Petri dish.
By secretion of m u c i l a g e the immobile stage b e c o m e s a p a l m e l l o i d multiplication
stage. E m b e d d e d in an a m o r p h o u s n o n l a m e l l a t e gelatinous envelope, multiplication
(sporogenesis) t a k e s p l a c e by r e p e a t e d b i n a r y fission resulting in colonies of up to 16 or
32 dinospores (Figs 7-9). In cultured m a t e r i a l the outer surface of the gelatinous e n v e l o p e
is c r o w d e d with bacteria. In p l a n k t o n s a m p l e s additionally a d h e r i n g detritus a n d other
contaminants m a y fortify the e n v e l o p e to a certain extent.
In the course of digestion of the food content, especially during the first ceil divisions,
the ceils b e c o m e d e n s e l y c r o w d e d with highly light-refractive lipid g r a n u l e s (Figs 7, 8).
H a v i n g g a i n e d a finite size the cluster of ceils b e c o m e s motile, a n d the dinospores l e a v e
their slimy envelope. The whole multiplication p h a s e takes a b o u t t h r e e days.
It is worth m e n t i o n i n g that the colonial cells retain their g y m n o d i n o i d outlines
t h r o u g h all the d e v e l o p m e n t a l stages of s p o r o g e n e s i s (Figs 7-9). A l t h o u g h flagella are
not obvious in these p a l m e l l o i d stages, t h e y are p r o b a b l y p r e s e n t in a functional
condition to j u d g e from the r a p i d i t y with w h i c h cells swim a w a y after b e i n g artificially
f r e e d from the gelatinous matrix b y a needle. But if done with early s p o r o g e n e t i c stages,
e. g. in a 2-or 4-cell stage, p r e m a t u r e l y l i b e r a t e d ceils soon settle d o w n a n d b e c o m e a
590
Gerhard Drebes
gelatinous "cyst" again, As the trophont also resembles an enlarged stillfunctional
dinospore, S. list//remains latently motile during the trophic and the sporogenetic phase
as well.
Freshly r e l e a s e d dinospores are c a p a b l e of infecting e g g s of c o p e p o d s or rotifers
within the s a m e day. In the a b s e n c e of hosts t h e y r e m a i n motile for a few w e e k s a n d do
not encyst. T w o - w e e k old dinospores can still infect freshly offered eggs.
O w i n g to the scarcity of the p a r a s i t e in nature, the host r a n g e was o b t a i n e d u n d e r
l a b o r a t o r y conditions. The species was found feeding on e g g s of the c o p e p o d s Temora
longicornis, Acania sp., Pseudocalanus elongatus, and of the rotifer Synchaete sp. In one
single case a n a u p h u s of Temora was i n f e c t e d (Fig. 6); p e r h a p s this w a s o n l y possible
u n d e r the limitations of a small Petri dish.
The short time of culturing S. listii did not allow e x t e n d i n g the e x p e r i m e n t s on
possible sexual reproduction. F u r t h e r more, no resting stages h a v e b e e n o b s e r v e d as yet.
DISCUSSION
The ectoparasitic dinoflagellates Chytdoch'nium, Dissodinium, a n d t h e n e w g e n u s
Syltodinium h a v e hosts in common: c r u s t a c e a n eggs, partly also e g g s of rotifers. T h e host
r a n g e s of D. pseudolunula a n d S. listii e v e n a p p e a r quite identical. Likewise, the
d i n o s p o r e s of b o t h species a r e of a similar g y m n o d i n o i d structure, b u t t h o s e of Syltodinium are on a v e r a g e a httle l a r g e r a n d l a c k chloroplasts. H o w e v e r , b e s i d e other
similarities, e. g. p h a g o t r o p h i c f e e d i n g b y a peduncle, Syltodinium has its o w n characteristics. Thus, after the trophic p h a s e palintomic multiphcation t a k e s p l a c e in a p a l m e l loid stage e m b e d d e d in a gelatinous envelope. I refrain from d e s i g n a t i n g this stage a
"gelatinous cyst" ("Gallertcyste": L i n d e m a n n , 1928), since the cells r e t a i n their
m o n a d o i d s h a p e a n d r e m a i n latenfly motile during the multiplication p h a s e . The
m o n a d o i d state of S. Bstii is a p p a r e n t d u r i n g the whole v e g e t a t i v e life cycle. This is in
contrast to Dissodinium, w h e r e the m o n a d o i d state is restricted to t h e dinospores
(Elbr~ichter & Drebes, 1978). Additionally, in Dissodinium s p o r o g e n e s i s t a k e s p l a c e inside
two successive cyst stages, t e r m e d p r i m a r y a n d s e c o n d a r y cysts.
T h o u g h sharing a similar host substrate (crustacean eggs), Syltodinium is clearly
d i s t i n g u i s h e d from Chytriodinium. The three m e m b e r s of Chytriodinium a r e d e s c r i b e d as
f e e d i n g osmotrophically on e g g s of E u p h a u s i a c e a , a n d s p o r o g e n e s i s has a l r e a d y started
while still a t t a c h e d to the host a n d before food u p t a k e has finished ( C a c h o n & Cachon,
1968, 1987). That means, t h e r e is no s e p a r a t i o n b e t w e e n the parasitic s t a g e a t t a c h e d to
the host a n d the sporogenetic stage free floating in the plankton, as k n o w n in Dissodinium a n d Syltodinium.
With r e g a r d to the taxonomic r a n k of Syltodinium a m o n g the p a r a s i t i c dinoflagellates, this is, as yet, uncertain.
Acknowledgements. I am grateful to Mrs. H. Halliger for technical assistance. Mr. J. Frank (List)
kindly corrected the Latin diagnoses.
Syltodinium, a n e c t o p a r a s i t i c d i n o f l a g e l l a t e
591
LITERATURE CITED
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Dogiel, V., 1906. Beitr~ge zur Kenntnis der Pefidineen. - Mitt. zool. Stn Neapel 18 (1), 1-45.
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