I
HELGOL,~NDER MEERESUNTERSUCHUNGEN
Helgol~inder Meeresunters. 49, 375-392 (1995)
Dinoflagellate resting cysts as factors in phytoplankton
ecology of the North Sea
S.
Nehring
Institut ffir M e e r e s k u n d e an der Universit~t K/el~ Dfisternbrooker W e g 20; D-24105 K/e/,
Germany
ABSTRACT: The occurrence and distribution of dinoflagellate resting cysts were investigated at 11
locations in the south-eastern part of the North Sea. Twenty-six known cyst species and 7 unknown
cyst types, which may act as seed population for planktonic dinoflagellate blooms, have been
recorded for the first time in the area. The most common cysts in recent sediments were those of
Smffppsiella trochoidea, Zygabikodinium lenticulatum, Peridinium dalei, Scrippsiella lachrymosa,
Protoceratium reticulatum, Protoperidinium denticulatum, and P. conicum. At all stations, S.
trochoidea dominated the cyst assemblages with a maximal abundance of 1303 living cysts/cm ~ in
the uppermost half centimetre, Cysts of the potentially toxic dinoflagellates Alexandrium cf.
excavatum and A. cf. tamarense were scarce. In the upper 2-cm layer of sediment, dinoflagellate
cysts were found in concentrations of 1.8 up to 682 living cysts/cm :3. Empty cysts constituted 22-56 %
of total cyst abundance. The comparative distribution of the cysts showed a general increase in
abundance from inshore sites to the offshore area, whereby sandy stations exhibited the lowest cyst
abundance and diversity. The wide distribution of living and empty cysts of Scrippsiella lachrymosa
suggests that its motile form, which has not been officially recorded in the area until now, is a
common plankton organism in German coastal waters~ The relatively high abundance o[ cysts in
recent sediments demonstrates the potential importance of benthic resting stages for the initiation of
dinoflagellate blooms in the study area.
INTRODUCTION
M a n y p l a n k t o n g r o u p s i n c l u d e a n o n - m o t i l e d o r m a n t e g g or cyst s t a g e in t h e i r life
history (e.g. c o p e p o d s , c l a d o c e r a n s , tintinnids, diatoms, a n d dinoflagellates). D i n o f l a g e l late cysts are k n o w n to g e o l o g i s t s as an i m p o r t a n t g r o u p of microfossils ('hystrichos p h e r e s ' ) u s e d e x t e n s i v e l y for b i o s t r a t i g r a p h y (e.g. in oil exploration). M o r e t h a n 100
y e a r s ago, l i v i n g d i n o f l a g e l l a t e r e s t i n g cysts w e r e first o b s e r v e d in p l a n k t o n s a m p l e s of
t h e N o r t h S e a (Stein, 1883; H e n s e n , 1887; M d b i u s , 1887) a n d w e r e o c c a s i o n a l l y m e n t i o n e d in t h e p h y c o l o g i c a l literature, w h i c h m a i n l y d e a l t w i t h f r e s h w a t e r e n v i r o n m e n t
d u r i n g t h e first half of t h e t w e n t i e t h c e n t u r y (e.g. Z e d e r b a u e r , 1904; L o h m a n n , 1910;
Klebs, 1912; D i w a l d , 1938; Braarud, 1945; Nordli, 1951). D e t a i l e d i n v e s t i g a t i o n s w e r e ,
h o w e v e r , n o t c a r r i e d out until t h e 1960s w i t h t h e p i o n e e r i n g w o r k of t h e p a l a e o n t o l o g i s t s
Evitt & D a v i d s o n (1964), Wall (1965) a n d W a l l & D a l e (1966, 1968a, b) w h i c h s h o w e d the
c y s t - t h e c a r e l a t i o n s h i p s of m o d e r n d i n o f l a g e l l a t e s . R e g a r d l e s s of t h e s e n e w a r e a s for
a l g o l o g i s t s a n d w i t h t h e tradition of the first d e t e c t i o n of cysts in the late 1800s b y Stein,
H e n s e n a n d M 6 b i u s , little is k n o w n a b o u t t h e e c o l o g i c a l i m p o r t a n c e of d i n o f l a g e l l a t e
cysts in r e c e n t s e d i m e n t s , e s p e c i a l l y in t h e s o u t h - e a s t e r n p a r t of t h e N o r t h Sea.
9 Biologische Anstalt Helgoland, Hamburg
376
S. N e h r i n g
Two types of cysts are found in dinoflagellate life cycles: (1) the a s e x u a l l y formed
temporary cyst, a n d (2) the resting cyst, the formation of which is the c o n s e q u e n c e of a
sexual process (Dale, 1983). Both types of cysts lack a flagella and a c c u m u l a t e on the sea
bottom.
At p r e s e n t m a n y aspects of the timing, location, a n d duration of dinoflagellate
blooms have b e e n l i n k e d to the e n c y s t m e n t / e x c y s t m e n t cycle of those species that form
resting cysts during their life histories (Huber & Nipkow, 1922; Steidinger, 1975; Anderson & Wall, 1978; A n d e r s o n & Morel, 1979; A n d e r s o n et al., 1983; B u r k h o l d e r et al.,
1992). Ecological studies c o n c e r n i n g temporary cysts are few, b e c a u s e the occurrence of
the latter in n a t u r a l waters has rarely b e e n recorded. But there is some e v i d e n c e that the
m e c h a n i s m of the formation of temporary cysts is important in relation to the persistence
a n d recurrence of red tides in a certain limited:area throughout the s u m m e r (Marasovic,
1989; Nehring, 1992).
Within the framework of the "Ecosystem Research W a d d e n Sea Project, Part A",
p h y t o p l a n k t o n a n d their resting stages in brackish-water bodies of the G e r m a n North
Sea coast are investigated. The present publication d o c u m e n t s the occurrence, distribution and a b u n d a n c e of dinoflagellate resting cysts in recent sediments of t h e North Sea,
for the purpose of estimating their potential importance in initiating m e n a c i n g algal
blooms in coastal zones of the North Sea.
MATERIALS AND METHODS
U n d i s t u r b e d surface s e d i m e n t samples of the North Sea were collected with a
Reineck box corer d u r i n g the RV Meteor cruise (No. 19) from 30th S e p t e m b e r to 11th
October 1991 a n d with a modified J o n a s s o n & Olansson (1966) box s a m p l e r d u r i n g the
RV Gauss cruise (No. 202) from 5th March to 12th March 1992 (Table 1). Duplicate
s e d i m e n t cores (10 cm long, 2.6 cm diameter) were o b t a i n e d with the corer a n d were
stored in the dark at 4 ~ until further examination.
Each core was processed using a modified biological technique of A n d e r s o n et al.
(1982) a n d Matsuoka et al. (1989) without a n y chemicals. The u p p e r 2 or 3 cm of a
sediment core was partitioned into 0.5 cm up to 1 cm depth, the rest in 1 cm horizontal
intervals a n d mixed with filtered seawater. These s u b s a m p l e s were sonicated for 1 rain in
a n ultrasonic c l e a n i n g bath (Bransonic 52) to separate the cysts from organic a n d
inorganic aggregates. The s u s p e n s i o n was passed through a 150 ~tm g a u z e a n d accumu~
lated on a 20 ~m gauze. The residue on the 20 ~tm gauze was r e w a s h e d a n d filled up with
filtered s e a w a t e r to m a k e up a final v o l u m e of 20 ml. Several 1000 ~tl aliquots up to the
whole 20 mt of this preparation were c o u n t e d on c o m m o n slides using a n O l y m p u s light
microscope or on Uterm6hl slides u s i n g a Zeiss Axiovert i n v e r t e d microscope. Living
cysts (containing protoplasm) and empty cysts were separately quantified.
Most of the cysts were identified according to descriptions given in the extensive
literature about cysts. Palaeontologists a n d biologists often use different n a m e s for the
life history stages of the same dinoflagellate. The biological (thecate) n a m e s of species
were used in this study.
U n k n o w n cysts a n d individual cysts were used for germination e x p e r i m e n t s to
identify the species by the motile thecate cell. For this purpose, cysts w e r e picked out
from Utermbhl slides, u s i n g a micropipette, a n d w a s h e d twice in filtered seawater. The
D i n o f l a g e l l a t e r e s t i n g c y s t s in p h y t o p l a n k t o n e c o l o g y
377
Table 1. Positions, water depth and sediment type of the North Sea stations. M: RV Meteor;
G: RV Gauss
Station
Coordinates
Water depth
(m)
Sampling date
Sediment type
M644
55 ~ 35,89' N
4 ~ 59,78' E
55 ~ 43~95' N
6~ 25,02' E
54 ~ 15,01' N
7 ~ 29,46' E
54 ~ 14,00' N
8~ 22,80' E
55 ~ 00,00' N
6~ 13,82' E
54 ~ 59,79' N
8~ 15,04' E
54 ~ 39,88' N
6~ 45,20' E
54 ~ 50,0I' N
8~ 00,02' E
54 ~ 05,00' N
7~ 50,00' E
53" 40,67' N
6~ 25,09' E
54 "~08,43' N
8~' 07,04' E
44
6. 10. 91
muddy sand
44
6. 10. 91
sandy mud
41
I0. 10. 91
sandy mud
14
10. 10. 91
muddy sand
45
6. 3. 92
sandy mud
15
7. 3. 92
sand
39
8. 3. 92
sandy mud
16
10. 3. 92
sand
44
11. 3. 92
sandy mud
25
8. 3. 92
sand
23
11. 3~ 92
mud
M645
M668
M671
G4
G9
Gli
G20
G35
G36
GE4
c y s t s w e r e t h e n p l a c e d in s m a l l sterile i n c u b a t i o n c h a m b e r s ( C o r n i n g C e l l Wells) a n d
filled u p w i t h t h e f i l t e r e d s e a w a t e r f r o m t h e s a m p l e l o c a t i o n or t h e m e d i u m F/2 (Guillard
& Ryther, 1962). T h e c y s t s w e r e k e p t at r o o m t e m p e r a t u r e ( ~ 18 ~ u n d e r n a t u r a l l i g h t
c o n d i t i o n s a n d w e r e e x a m i n e d r e g u l a r l y for g e r m i n a t i o n . If t h e y h a d n o t g e r m i n a t e d
w i t h i n 14 d a y s , t h e e x p e r i m e n t w a s a b a n d o n e d .
For S c a n n i n g E l e c t r o n M i c r o s c o p y , t h e c y s t s w e r e a g a i n i n d i v i d u a l l y p i c k e d out a n d
m o u n t e d o n N u c l e o p o r e filters. T h e s e w e r e f i x e d w i t h 2 % f o r m a l d e h y d e for 2 4 h ,
d e h y d r a t e d in a n a c e t o n e s e q u e n c e a n d s u b s e q u e n t l y air d r i e d . A f t e r s p u t t e r c o a t i n g
w i t h g o l d - p a l l a d i u m (Balzers S C D 004), c y s t s w e r e e x a m i n e d i n a Zeiss D S M 940.
S e p a r a t e s e d i m e n t s a m p l e s (top 1-cm layer) w e r e u s e d for d e t e r m i n i n g t h e i g n i t i o n
loss of t h e o r g a n i c c o n t e n t b y c o m b u s t i n g t h e o r g a n i c m a t e r i a l for 24 h at 550 ~
RESULTS
Occurrence
of r e s t i n g c y s t s
M o r e t h a n s e v e n t y s p e c i e s of m a r i n e a n d m o r e t h a n t w e n t y s p e c i e s of f r e s h w a t e r
p l a n k t o n i c d i n o f l a g e l l a t e s p r o d u c e a r e s t i n g c y s t as p a r t of t h e i r s e x u a ] life c y c l e
( N e h r i n g , 1993a). For t h e G e r m a n N o r t h S e a coast, m o t i l e t h e c a t e s t a g e s of 45 cyst-
378
S, N e h r i n g
Table 2. Motile stage of resting cyst-forming dinoflagellate species recorded by Drebes & Elbr~chter
(1976) and Elbr~chter [pers, comm.) in the south-eastern North Sea. ~ benthic species
Alexandrium affine
Alexandrium excavatum
Alexandrfum lusitanicum
Alexandnum ostenfeldii
Alexandrium pseudogonyaulax
Alexandriurn tamarense
Amphidinium carterae
Coolia monotis +
Diplopelta parva
Diplopsalis lebourae
Diplopsalis len ticula
Diplopsalopsis orbiculans
Gonyaulax digitales
Gonyaulax scrippsae
Gonyaulax spinifera
Gonyaulax verior
Gyrodinium instriatum
Gyrodinium uncatenum
Katodinium fungiforme
Oblea rotunda
Peridinium dalei
Polykrikos kofoidii
Polykrikos schwartzii
Prorocentrum lima +
Protoceratium reticulatum
Protoperidiniurn avellana
Protoperidinium claudicans
Protoperidinium conicoides
Protoperidinium conicum
Protoperidinium denticulatum
Protoperidinium divaricatum
Protoperidinium divergens
Protoper~dinium excentricum
Protoperidinium leonis
Protoperidinium minutum
Protoperidinium obtongurn
Protoperidinium pen tagon urn
Protoperidinium punctulaturn
Protope~ffdinium subinerme
Protoperidinium thorianum
Protopendinium thulesense
Pyrophacus horologiurn
Pyrophacus steinii var. steinii
Scrippsiella trochoidea
Zygabikodinium lenticulaturn
forming species are recorded (Drebes & Elbr~ichter, 1976; Elbr~ichter, pers. comm. See
Table 2), but no detailed information about the p r e s e n c e of dinoflagellate cysts is
available for this region.
The p r e s e n t study reveals that living a n d empty cysts are widespread t h r o u g h o u t the
investigated stations. Altogether. 26 different cyst types were identified on species level
(Table 3; Figs 1. 2). Several species were additionally identified from motile cells
g e r m i n a t e d by single-cyst i n c u b a t i o n e x p e r i m e n t s (Gonyaulax polyedra, Perich'nium
dalei, Polykrikos schwartzii, Protoceratium reticulatum, Protoperidinium conicoides, P.
conicum, P. denticulaturn, P. leonis, P. m m u t u m , P. oblongum, P. cf. punctulatum,
Scrippsiella trochoidea). For G e r m a n coastal sediments fStat. M671, G9, G20, G35, GE4),
20 cyst forms of the 45 motile cyst-forming species occurring in the region were detected,
w h e r e b y for Gonyaulax spinifera, Polykrikos kofoichi (Figs IH, I), Protoperidinium
conicoides (Fig. 10), P, divaricatum (Fig. 1R) a n d P. p e n t a g o n u m (Fig. 1U), only empty
cysts were found Gonyaulax spinifera can produce different cyst types (Fig. 1E. F),
p r e s u m a b l y in response to different e n v i r o n m e n t a l conditions (Taylor & Gaines, 1989).
These were d e s i g n a t e d here as a group. To date at least 6 cyst types have b e e n found to
germinate to a thecate cell of Gonyaulax spinifera (Dodge, 1989). In the palaeontological
taxon, n u m e r o u s cyst types of Gonyaulax spinifera are differentiated. Possibly this
extremely varied cyst type indicates that it is, in fact. a species complex.
The most common species, in order of decreasing a b u n d a n c e s of living cysts, were
Scrippsiella trochoidea (Figs 2A-C), Z y g a b i k o d i n i u m lenticulatum [Fig. lV), Peridinium
dalei (Fig. 1G), Scrippsiella lachrymosa (Figs 2D-F), Protoceratium reticulatum (Pigs 1L,
M), Protoperidinium denticulatum (Fig. 1Q), a n d P. conicum (Fig. 1P). Cysts of the
potentially toxic Alexandrium cf. e x c a v a t u m (Fig. 1A), A. cf. tamarense (Fig. 1B) a n d of
the potentially noxious bloom-forming Gonyaulax polyedra (Fig. 1D) were restricted
m a i n l y to the offshore area. The wide distribution of living a n d empty cysts of Scrippsiella
lachrymosa suggests that this form, in addition to S. trochoidea, is a c o m m o n p l a n k t o n
organism i n G e r m a n coastal waters. However, motile forms of S. lachrymosa have not
11,5
0
0
0
0,5
0
O
1.0
0.3
0
3.0
1,6
0
0
0
0
0,9
0~9
0
0
0
0
0
0
0,5
0
0
1A
1,4
0
M671
L
E
0
0
0.3
0.3
0
0
0
3.4
0
0
2.8
0
0
0
0
0.9
2,5
0
0,3
0
0.3
0
0
0.3
3,8
0
5,7
17,9
0.5
682.0347.9581.9661.3180.2155.041.0
0
0
0
2.5
0
0
0
0
0
25.1
1.3
0
0
0
5.0
2.5
16.3
0
5.0
2.5
0.6
0
2.5
36.4
2.5
0
24.5
22.6
5.7
Total
3.1
0.6
0
3.1
0
0.6
0
92.9
0
0
184,0
0
0
2.5
0
0
0
Diplopsalid group
5.0
0
Gonyaulax digitales
15,1 0.6
Gonyaulax polyedra "
1.3
0
Gonyaulax scrippsae
0
0
Gonyaulax spinifera g r o u p
2.5
0.6
Peridinium dalei
22.6 1.9
Polykrikos kofoidii
5.0
0
Polykrikos sch wartzii
74.7 3.1
Protoceratium reticulatum
144.4 1.9
Protopeddinium avellana
0
0
Protoperidinium claudicans
0
0
Protoperidinium compressum
0
0
0
1.3
0
Protoperidinium conicoides
0
0
0
1.3
2.5
Protoperidiniumconicum
6.3
13.8 9.4
26.4 3.8
Protoperidiniumdenticulatum
10,0 13.8 2.5
38.3 3.8
Protoperidinium divaricatum
0
0
0
2.5
0
Protoperidinium leonis
1.3
2,5
0
3.8
0
Protoperidiniumminutum
0
3,8
0
15.1 0.6
Protoperidinium oblongum
8,8
0
0
4.4
5.0
Protoperidinium p e n t a g o n u m
0
0
0
1.3
O
Protoperidinium cf. punctulatum 0
12.6 8.2
11.9 8,2
Protoperidiniumspp.
0
28.9 0
41.4 0.6
Scrippsiellalachrymosa"
7,5
1.3
60.3 23.2 4.4
Scrippsiella trifida *
5.0
0
0
0
0
Scrippsiella trochoidea
547.5204.7 163.2157.645,2
Zygabikodiniumlenticulatum
26.4 6.3
15.7 55.9 20.1
Dinoflagenatecystsunident.
15.1 0
38.3 3,8
77.9
0
0
7.5
22,6
0
2,5
1.3
2,5
0
13.8
5.0
5.0
0
M668
L
E
0
0
0
25.1
1.3
1.3
2,5
[1.3
0
3,8
8.8
0
0
M645
L
E
606.6484.610.3
0
0.1
0
1,9
0
4.9
0,3
0
5.0
2.5
75,4
66,6 23.9
0
2.5
301.4 129.3
6.3
18.8
114.30
0
0
0
0
10.0 0
1,0
0
0
0
0
0
0
0
10,0 0.8
1,3
0
126.80
11.3 0
0
0
0
0.3
0
0
0
0
10.0 1.3
27.6 0.4
0
0
3.8
0
23.9 0
0
0.3
0
0
4.1
1.7
0
0
1.7
0.1
0
0
0
0
0
0
0
0
0
0
0
0,3
0.3
0
0
0
0
0
0
0
0
0
0
0
98.0
0.6
0
0
1.6
0
0.8
0,3
0.5
0
0
0.1
0
0
0
0A
0
0
0
0
0
0
0
0.1
0
0
6
0
0
0
L
126.94.1
0
0
3,8
1.3
0
0
2.5
0
2.5
11.3
3,8
0
0
0
0
1.3
15.1
0
2.5
5,0
1.3
0
13.8 2,5
6.2
32.6
3,8
5.0
0
0
25.1 21.3
1.3
11.3
31.4 3.8
0
0
1.3
2.5
0
0
0
7.5
0
0
1.3
0
0
0
0
0
2.5
0
0
1.3
0
0
A b u n d a n c e (cm 3)
G9
G 11
E
L
E
L
E
0
0
2,5
7.5
0
0
2.5
69.l
0
5,0
3.8
0
0
0
0
5.0
7.5
0
2,5
3,8
1.3
O
L
G4
E
2.3
0,3
0
0
0,8
0
0
0
341.4441.91.8
30.1
5.0
0
62.8
25.1
92.9
47.7
L
E
1.1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0.3
0
0
0
0
0
0
0.5
0
0
0.3
0
0
G36
0
0
0
0
0
0
0
0
0
0
0.3
0
0
0
0
0
0
0
0
0
0
0
5.0 0
125,50.4
7.5
0
0
0
57.8 0.4
37,7 0
72.8 0.7
E
0
0
5.0
0
0
0
0
0
2.5
55.2
2.5
0
0
0
5.0
17.6
20,1
1.3
0
22.6
2.5
1,3
G35
0
0
2.5
0
0
0
O
0
0
0
0
0
0
0
0
7.5
50.2
0
0
15.1
2.5
0
L
o f 11
0
0
5,0
0
0
0
0
0
0
7.5
2.5
0
0
0
0
0
0
0
0
5.0
0
0
2.5
10.0
2.5
0
10,0
2.5
2.5
140,550.0
0
0
2.5
2,5
0
0
0
5,0
0
0
0
0
0
0
0
2.5
12.6
0
2.5
7.5
5.0
0
2.5
5,0
2.5
0
25.1
50.2
15.1
GE4
L
E
two centimetres
of sediment
N o r t h S e a ( s e e T a b l e 2)
0
0
0
0
O
0
0
0
0
0.3
0,3
0
0
0
0
0.5
0,1
0
0
0
0
0
G20
(E) d i n o f l a g e l l a t e
resting cysts in the uppermost
* motile stage not recorded in the south-eastern
A l e x a n d r i u m cf. excavatnm
A l e x a n d r i u m cf. tamarense
M844
L
E
3. O c c u r r e n c e
and abundance
o [ l i v i n g (L) a n d e m p t y
North Sea stations. M: RV Meteor; G: RV Gauss;
S a m p l i n g site
R e s t i n g cyst s p e c i e s
Table
~o
~D
o
o
F
f~
'13
~r
t~
9
~7
~J
,q
b .... ~
dl
"-I
J
O
'D
Z
t
~
~
a
r-
:
,~ ~ : i ~ i
~ii
"1-
•4
..Q
Z
~O
Dinoflagellate resting cysts in phytoplankton ecology
381
b e e n officially r e c o r d e d so far in the region (Elbr~chter, pets. comm.). Probably they h a v e
b e e n o v e r l o o k e d b e c a u s e of their small size an d the difficulty to distinguish t h e m from
closely r el at ed orthoperidinoid species. In contrast to this, the cysts of Scrippsiella species
possess u n e q u i v o c a l morphological distinguishing features. Th e cyst of S. trochoidea has
a highly variable, ovoid to spherical form, dark greyish-coloured with a bright red
a c c u m u l a t i o n b o d y often visible (Figs 2A-C). The cyst is 25 to 48 9m long an d 25 to 44 ~m
wide, c o v e r e d by n u m e r o u s calcareous spines up to 10 ~m long. Th e spine shafts
t e r m i n a t e in blunt, capitate or pointed ends. Th e archeopyle (excystment a p e r t u r e in the
cyst wall) is a split towards one end of the cyst, forming a c a p - s h a p e d operculum. Th e cyst
of S. lachrymosa has an e l o n g a t e oval form and is c o v e r e d with thin, flattened calcareous
plates w h i c h are jointly i n d e n t e d (Figs 2D-F). The cyst is 35 to 47 ~tm long an d 17 to 35 ~m
wide. A bright red accumulation body is visible and the archeopyle is a smooth split
towards the cyst-apex. Only a few cysts of S. trifida w e r e found offshore. Th e s h a p e of this
cyst is oval with a l e n g t h of 29 to 41 ~m and a width of 21 to 30 ~m (Fig. 2G). Th e cyst wall
is c o v e r e d by a n u m b e r of trifurcate, recurved, calcareous spines, and a red b o d y is often
visible. Th e a r c h e o p y l e was not detected, but Lewis (1991) d escr i b ed it as an apical split
w h i c h is s o m e t i m e s notched, r e m a i n i n g a t t a c h e d to one side of the main b o d y of the cyst.
In addition to the identified forms, 7 u n k n o w n cyst types w e r e found. Unfortunately,
in t h es e cases g e r m i n a t i o n e x p e r i m e n t s w e r e not very successful. O n e of t h ese cyst types
(Fig. 1W) (isolated at G35, G36, GE4) was b ro w n and spherical (38 to 40 L~m diameter~
excl. spines) with n u m e r o u s slender, c u r v e d spines (2 to 5 ~tm long). N u m e r o u s small
plastids an d oil globules occur within the microgranular protoplasm. O n e cyst was
g e r m i n a t e d to give a motile thecate cell an d was identified as Protoperidinium cf.
curvipes. At p r e s e n t this cyst-theca relationship is u n k n o w n : therefore, further e x a m i n a tions are in progress. At Station M645. a spherical (34 ~tm diameter) pale b r o w n cyst with
a l o o s e l y - a t t a c h e d and folded, m e m b r a n o u s outer layer was found. This cyst type is
similar to Protopezidinium americanum, which, however, is not well k n o w n an d the
thecate cell has not b e e n previously r e c o r d e d in the North Sea region. Tw o of the
u n k n o w n cyst types w e r e of quantitative i m p o r t a n c e in the central part of the investig a t e d area (G4, G l l . M668). Both cysts are spherical with a pale content, and pale
y e l l o w / o r a n g e accumulation bodies are present. Cyst walls are colourless but both are
Fig. 1 Dinoflagellate resting cysts, isolated from recent North Sea sediments. A: Alexandn'urn cf.
excavatum. B: Alexandrium cf. tamarense. C: Gonyaulax digitalis. D: Empty cyst of Gonyaulax
polyedra. E-F: Empty cysts of Gonyaulax spinifera group, E: Palaeontological taxon Spiniferites
elongatus; F: Palaeontological taxon Spiniferites mirabilis. G: Peridinlum dalei, cell contents with
red body (arrow). H-I: Empty cyst of Polyla~kos kofoidii. H: Optical cross-section, archeopyle
(arrow); I: Surface detail showing rows of hollow processes which sometimes connect adjacent ones.
J-K: Empty cysts of Polykrikos schwartzii. J: Optical cross-section archeopyle (arrow); K: Surface
detail showing complex reticulate network of processes. L-M: Empty cysts of Protoceratiurn
retl"culatum showing variation in process morphology, L: Cyst with long tapering spines with
capitate tips; M: Cyst with short processes fnodular form). N: Protoperidiniurn claudicans. O: Empty
cyst of Protoperidinium conicoides with archeopyle. P: Empty cyst of Protoperidinium conicum. Q:
Empty cyst of Protoperidinium denticulatum with archeopyle. R: Empty cyst of Protoperidiniurn
divancatum. S: Empty cyst of Protoperidinium leonis with archeopyle. T: Protoperidinium oblongum, cell contents with red oil globules (arrow}. U: Empty cyst of Protoperidinium pentagomum. V:
Zygabikodinium lenticulatum, cyst enclosed within the theca. W: Unidentified cyst, probably cyst of
Protoperidinium cur~pes. Scale bar: 40 ~tm in A-D, G-K, N, P, R-V, 20 ~m E, F. L. M, O, Q, W
382
S. N e h r i n g
~~.~.~.~
G
Fig. 2. Scrippsiella resting cysts, isolated trom recent North Sea sediments. A-C: Scrippsiell~
trochoidea. A: Living cyst showing red body (arrow); B: SEM, cyst with numerous calcareous spines..
C: SEM detail of ornament. D-F: Scrippsiefla lachrymosa. D: Living cyst showing red body (arrow);
E: SEM. cyst showing calcareous ornament: F: SEM. detail of ornament. G: Scrippsiella trifida, hving
cyst showing red body (arrow). Scale bars: 20 ~m in A. D, G: 10 am in B, E, 2 ~m in C, F
Dinoflagellate resting cysts in p h y t o p l a n k t o n ecology
383
significantly different in size (19 to 25 [~m d i a m e t e r a n d 48 to 55 ~m d i a m e t e r r e s p e c tively). Previously, a clear cyst type, similar to the former, was d e s c r i b e d from u n i - a t g a l
Scrippsiella trochoidea cultures (e.g. Braarud, 1957). A few spherical, b r o w n cysts (30 to
52 ~m diameter) with a coarsely g r a n u l a r surface a n d with a long slit as a r c h e o p y l e w e r e
found; however, these cysts w e r e frequently deformed. An identification w a s not possible
b e c a u s e this cyst t y p e includes s e v e r a l species (Diplopsafis lebourae, D. lenticula,
Diplopsalopsis orbicularis, Gotoius abei, Oblea rotunda) and were d e s i g n a t e d in this
study as the 'Diplopsalid group'. Reticulate cysts (30 [tm diameter; from Stations G l l a n d
G35) of the 'Diplopsalid group' p r o d u c e d motile cells after incubation w h i c h w e r e
c o m p a r a b l e to the toxic, chainforming Gymnodinium catenatum (Nehring, 1993b). The
several living or empty, spherical, b r o w n cysts (35-68 ,ttm diameter) which w e r e found
either did not g e r m i n a t e in e x p e r i m e n t s (living cysts) or w e r e c o m p r e s s e d (empty cysts)
a n d w e r e d e s i g n a t e d in the study as Protopinchnium spp. At Station M671 one large
spherical, brown, living cyst (90 [tm diameter) b e l o n g i n g to Protoperidinium was found.
Reid (1977) isolated a similar, large but e m p t y cyst, with h e x a g o n a l archeopyle, from
r e c e n t North Sea s e d i m e n t s and a s s i g n e d it to the p a l a e o n t o l o g i c a l taxon Brigantedinium
majusculum. At present, the thecal affinity is u n k n o w n . N e a r H e l g o l a n d (GE4), an
e l o n g a t e ovoidal grey cyst (105 ~m long, 73 ~tm wide) was found, b e a r i n g n u m e r o u s n a p s
(diameter up to 14.5 [tm) (cf. Nehring, 1993a; Figs 5G, H). The cyst m o r p h o l o g y a n d the
circular, "tremic" a r c h e o p y l e (sensu M a t s u o k a , 1985) s u g g e s t that this u n k n o w n cyst
type b e l o n g s to Polykrikos, which most likely r e p r e s e n t s a n e w cyst-theca relationship. At
present, in Polykrikos only the distinctive cysts of P. koifodii (Figs 1H, I) a n d P. schwartzii
(Figs 1J, K) are k n o w n a n d were found in this study, too.
D i s t r i b u t i o n of r e s t i n g c y s t s
For interpretation of the distribution patterns of resting cysts, it is n e c e s s a r y to
d e s c r i b e the s e d i m e n t characteristics of the i n v e s t i g a t e d stations (Table 1). The sediments vary from sand (G9, G20, G36), to fine s a n d with m u d (M644, M671) a n d m u d with
fine s a n d (M645, M668, G4, G11, G35) with the finest s e d i m e n t s occurring n e a r Helgol a n d (GE4). The organic content v a r i e d b e t w e e n 0.3 a n d I0.2 %, b e i n g lowest at s a n d y
stations a n d h i g h e s t at site GE4.
The c o m p a r a t i v e distribution of the cysts s h o w e d a g e n e r a l increase in a b u n d a n c e s
from the inshore areas to the offshore a r e a (Fig. 3) a n d are also closely r e l a t e d to s e d i m e n t
type. In the u p p e r 2-cm s e d i m e n t layer, living dinoflagellate cysts were found offshore in
concentrations of 682 cysts/cm 3 at the m u d d y s a n d station (M644) and 582-607 cysts/cm 3
at the s a n d y m u d stations (M645. G4). E m p t y cysts constituted 34-53 % of the total cyst
a b u n d a n c e . The s a n d y coastal stations (G36, G20. G9) w e r e characterized by the lowest
cyst a b u n d a n c e s (1.8-10.3 living cysts/cma). The fraction of e m p t y cysts was 28-37 % of
the total cyst counts. The m u d d y s a n d inshore station c o n t a i n e d a concentration of 41
living cysts/cm 3 (M671). At the s a n d y m u d stations, living cysts w e r e f o u n d in concentrations of 98-341 cysts/cm 3 (G11, M668, G35) a n d 141 living cysts/cm 3 w e r e found at the
m u d station (GE4). Empty cysts constituted 22-56 % of the total cyst a b u n d a n c e .
The species diversity of living cysts v a r i e d b e t w e e n 2 (G36) a n d 15 (M644) a n d for
e m p t y cysts b e t w e e n 2 (G36) a n d 21 (M645). Species richness m a y be s o m e w h a t h i g h e r
offshore t h a n in the inshore areas. This difference b e c o m e s even more obvious w h e n rare
s p e c i e s (< 1 cysts/cm 3) arp ~xcluded.
S. N e h r i n g
384
J
I
I
5"
Dinophyceae
Im
"
0.!
L!
Iw
I
IL!
I0
~Ek
O.
L
0~5o~1
i-2 I~
Fig. 3 Horizontal and vertical distribution of living and empty resting cysts of dinoflagellates in the
uppermost centirnetres of sediment of the south-eastern North Sea {M: RV Meteor. October 1991:
G: RV Gauss. March 19921
The cyst distribution and a b u n d a n c e s of three c o m m o n species Scrippsiella
trochoidea, Zygabikodinium lenticulatum a nd Protoceratium reticulatum ar e g i v e n in
Figures 4 to 6, At all stations, Scrippsiella trochoidea d o m i n a t e d the cyst a s s e m b l a g e s .
Living cysts of S, trochoidea o b t a i n e d a p e r c e n t a g e of up to 80 % in the u p p e r m o s t 2-cm
s e d i m e n t layer at t h e offshore Station M644. Th e cysts of ZFgabikodinium lenticulatum
w e r e more a b u n d a n t in the n o r t h e r n part (M644, M645) and at stations a r o u n d H e l g o l a n d
t h a n at the other coastal stations or in the central part of the i n v e s t i g a t e d area. In contrast,
a b u n d a n c e s of Protoceratium reticulatum cysts w e r e highest offshore (M645) a n d lowest
at the coastal sites. At three stations in t h e coastal water, only em p t y cysts of this species
w e r e found
Dinoflagellate resting cysts in p h y t o p l an k t o n ecology
I
385
I
Scrippsiella trochoidea
I~
O.I
.
&!
I
-- 33"
Im
IO
t~o
0.1 ~
I00
I0
0.1
9
li
',:I
,.
"1
-
O'liO..OJO-~.l i-2 I>
DEI'TH(~)
Fig. 4. Horizontal and vertical distribution of living and empty resting cysts of the dinoflagellate
Scrippsiella trochoidea in the uppermost centimetres of sediment of the south-eastern North Sea
(M: RV Meteor, October 1991: G: RV Gauss. March 1992}
A l e x a n d r ~ u m cf. e x c a v a t u m cysts w e r e only found in a few s e d i m e n t layers at two
stations (M645, G20) in very low a b u n d a n c e s (max 9.4 living cysts/cma). Th e cysts of A,
cf. t a m a r e n s e w e r e only detected at Station M645, and in even l o w er a b u n d a n c e s than
the former species,
The small-scale vertical distribution of h y i n g an d e m p t y cysts usually exhibited
m a x i m u m concentrations well b e l o w the s e d i m e n t surface. In this context the m a x i m a l
a b u n d a n c e of 1303 living cysts/cm 3 of Scrippsiefla trochoidea in the u p p e r m o s t half
cen t i m et res of s e d i m e n t at Station M644 is a r e m a r k a b l e exception, which m a y be a
result of a r e c e n t b l o o m of S. trochoidea which c e a s e d at this station.
At m n ~ t q t ~ t i n n ~ t h p r a t ] n h ~ t w e ~ l l living and e m n t v cysts of a b u n d a n t specie,~ i n a11
386
S. N e h r i n g
!
5"
I
Zygabikodinium lenticulatum
MS~
-
im
iw
Io
o.t
I
o.I
I
IQo
lalm
'~
G.OJ OJ-I 14
m
li
:I
,.
-
DEPTH (cm)
Fig. 5. Horizontal and vertical distribution of living and empty resting cysts of the dinoflagellate
Zygabikodinium lenticulaturn in the uppermost centimetres of sediment of the south-eastern North
Sea (M: RV Meteor, October 1991; G- RV Gauss, March 1992)
a n a l y z e d s e d i m e n t layers was > 1. This t e n d e n c y was p r o m i n e n t in Scrippsietla
trochoidea a n d Peridinium dalei,
DISCUSSION
The term 'cyst' has b e e n variously a p p l i e d to different stages i n dinoflagellate life
histories (Dale. 1983}, b u t two types are of particular biological interest: r e s t i n g cysts a n d
temporary cysts.
Resting cysts represent the t h i c k - w a n e d diploid stage of the sexual p a r t of dinoflaqellate life cycles (Pfiester. 19891. In contrast to asexually formed t e m p o r a r y cysts, they
Dinoflagellate resting cysts in phytoplankton ecology
I
387
I
5"
Protoceratium reticulatum
o.I
.
.
'
~J
H!:
os-i
I-
o.
O-OJ 0.~* I I-2
Gll
IW
I0
~Ek
,.
I
~J
0-I-I [.2
1>
D E P T H (ca)
Fig. 6 Horizontal and vertical distribution of living and empty resting cysts of the dinoflagellate
Protoceratium reticulatum in the uppermost centimetres of sediment of the south-eastern North Sea
M: RV Meteor. October 1991: G: RV Gauss. March 1992)
a p p a r e n t l y c a n n o t re-establish motile populations immediately b e c a u s e resting cysts may
have a n e n d o g e n o u s l y controlled m a n d a t o r y resting period. This m a y last a n y w h e r e from
weeks to months during which g e r m i n a t i o n is not possible, e v e n w h e n g e r m i n a t i o n
conditions are optimal {Anderson & Keafer, 1987; Pfiester & Anderson 1987). These
benthic stages can act as seed populations~ inoculating the water column in the next
season with vegetative cells to initiate blooms (e.g. A n d e r s o n & Wall, 1978).
Laboratory experiments s h o w e d that resting cysts b e h a v e like fine silt particles in the
s e d i m e n t a r y r e g i m e a n d are thus concentrated by s e d i m e n t a r y processes (Dale 1976).
Hence the a b u n d a n c e distribution, a n d fate of deposited cysts are important variables.
Potential areas of deposition are m u d d y or s a n d y m u d d y regions, In addition, the
388
S. N e h r i n g
c o n v e r g e n c e zone at an estuarine front a n d its associated pycnocline e n a b l e the transfer
of the encysting dinoflagellates from surface waters to their ultimate s e e d b e d locations
(Tyler et al., 1982). At higher s e d i m e n t a t i o n rates of terrigenous debris, cyst concentrations are likely to be lowered b e c a u s e of dilution or burial.
Stein (1883), credited with the first d o c u m e n t a t i o n of resting cyst formation, especially for Pyrophacus horologium, described the resting cyst of Gonyaulax spinifera as
cyst of Cladopyxis brachiolata, both found n e a r Helgoland. From freshwater samples,
Stein described the resting cysts of Ceratium cornuturn and C. hirundinella as C.
macroceros. H e n s e n (1887) recorded from North Sea p l a n k t o n samples the distinctive
living resting cyst of Polykrikos schwartzii as an "umrindete Cyste", a n d possibly the
resting cyst of Protoceratium reticulatum as Xanthidium multispinosum. T h e latter was
also m e n t i o n e d by M6bius (1887). In culture experiments with North Sea plankton, it was
s h o w n that most likely Fragilidinium subglobosum, as well as Cachonina niei, formed
resting cysts (Stosch, 1969a, b). At present, however, no findings of cysts of these species
have b e e n reported in recent sediments. The only record of recent dinoflagellate cysts in
bottom sediments of the south-eastern part of the North sea was given by Chowdhury
(1982). He found only a few empty cysts of Gonyaulax spinifera, Protoperidinium cf.
leonis, P. conicoides and P. pentagonum. The d o m i n a n c e of Scrippsiella spp. cysts in this
area of the North Sea - as d e m o n s t r a t e d in the present study - could not b e detected in
C h o w d h u r y ' s study b e c a u s e his harsh palynological preparation methods for plant spores
only preserved some sporopollenin resting cysts of dinoflagellates and not the calcareous
resting cysts of Scrippsiella spp. This also holds true for other investigations of North Sea
sediments (Reid, 1974, 1975, 1977; Dale, 1976). Moreover, the d o m i n a n c e of Scrippsiella
spp. cysts is remarkable, b e c a u s e as Dale (1986) pointed out, calcareous cysts are
relatively more important in tropical a n d oceanic regions rather than in t e m p e r a t e ones.
But Reid (1975. 1978) also noted that S. trochoidea cysts represent one of the common
dinoflagellate cyst in the p l a n k t o n from British waters.
Cyst morphology is increasingly r e g a r d e d as a n Important p a r a m e t e r in the classification of m o d e r n dinoflagellates. Direct comparison of motile stage details with their
cysts showed that cyst differences b e t w e e n species were more obvious (e.g. i n Diplopsalid complex, Gonyaulax, Scrippsiella). Cyst studies are revealing a b e n t h i c view of
dinoflagellate ecology a n d offer a potential tool for the prediction of future algal pests.
They also m a y suggest the u n d e t e c t e d p r e s e n c e of species in the water c o l u m n (Nehring,
1994a. in press), e.g. in the p r e s e n t study for Scnppsiella lachrymosa a n d possibly for S.
tnfida. Finally, cysts m a y be indicators of water circulation patterns (Nehring, 1993b), e.g.
i n the present study for Gonyaulax polyedra, Protoperidinium amencanum a n d P.
compressum. The findings of vegetative cells of these species are rarely reported from
North Sea investigations a n d no reports are k n o w n for the G e r m a n Bight (Elbr~chter
pers. comm). Because of their small size, cysts are chiefly transported with the residual
currents (Anderson et al., 1985b; Sarjeant et al., 1987) and p e r h a p s here cysts are a n
indicator of water influx t h r o u g h the English C h a n n e l in recent years.
In studies about the vertical distribution of cysts, the b u l k was found to occur in the
uppermost two to three centimetre s e d i m e n t layer (Anderson et al., 1982; Tyler et al.,
1982; White & Lewis. 1982; Nehring, 1994b, i n press). T e m p e r a t u r e (Anderson, 1980;
A n d e r s o n et al., 1985a), fight a n d o x y g e n (Anderson et al., 1987) are i m p o r t a n t factors
that determine w h e t h e r a n e w l y - f o r m e d cyst will e v e n t u a l l y germinate. W h e n buried in
Dinoflagellate resting cysts in p h y t o p l a n k t o n ecology
389
d e e p e r sediment layers by s e d i m e n t a t i o n or bioturbation (Anderson et al., 1982), cysts
may contribute little to bloom initiation, due to anoxia a n d other inhibitory microe n v i r o n m e n t a l factors (Anderson et al., 1987).
Most cyst distribution studies have investigated the presence or a b s e n c e of a
sporopollenin cyst species. Quantitative cyst m a p p i n g is m u c h more time-consuming. At
present, only a few quantitative studies are available, mostly concerned with the a b u n dance of the potentially toxic Alexandrium species (e.g. White & Lewis, 1982; A n d e r s o n &
Keafer, 1985; Cerebella et al., 1988).
The trend in the inshore to offshore diversity as well as the a b u n d a n c e of cysts in the
investigated North Sea sediments can be correlated with the hydrographical a n d biological characteristics of surface water masses. Diatoms a n d the H a p t o p h y c e a e PhaeocFstis
globosa p r e d o m i n a t e in the t u r b u l e n t waters of the W a d d e n Sea, w h e r e b y dinoflagellates
occur preferably in stratified waters further north (Reid et al., 1990; Hesse & Nehring,
1993). Unfortunately very little information on the formation, occurrence a n d distribution
of cysts in the p l a n k t o n is available. Cysts were only found in a relatively small n u m b e r of
offshore samples, but w h e n present, they often occurred in very large n u m b e r s (Reid,
1975, 1978). In contrast, cysts in estuarine samples were observed throughout the year,
but often in low n u m b e r s (< 10 cysts/l) (Balch et al., 1983; Nehring, unpubl.).
The a p p a r e n t discrepancy b e t w e e n the high cyst a b u n d a n c e in North Sea sediments
a n d the poor record of motile stages in the water column is due to an a c c u m u l a t i o n of
living cysts in the s e d i m e n t over m a n y years. This is reflected both by the fact that most
cysts occur in subsurface sediment layers a n d by the observed low p e r c e n t a g e of empty
cysts. Little information is available about the germination rate of dinoflagellate cysts in
natural waters. A n d e r s o n & Keafer (1985) noted that the i n p u t of n e w cells from
Alexandrium tamarense cysts is probably < 10 % of the total cyst a b u n d a n c e . In contrast
to sporopollenin cysts, the ratio of living to e m p t y cysts of the calcareous cysts of
Scrippsiella spp. may not only b e i n f l u e n c e d by a difference in germination rates, but also
by the greater fragility of the empty cyst wall (Lewis, 1988). As a c o n s e q u e n c e of cyst
accumulation, an u n e x p e c t e d n u m b e r of cysts is present in the s e d i m e n t for bloom
initiation. Cysts are able to survive for years in anoxic sediments (Dale, 1983; A n d e r s o n et
al., 1987), and bioturbation or r e s u s p e n s i o n events may bring buried resting stages back
to the sediment surface or into the water column (Balch et al., 1983; Marcus & SchmidtG e g e n b a c h . 1986).
In the present study, few toxic cysts of Alexandlffum cf. excavatum a n d A. cf
tamarense were found. The a b s e n c e of the detectable cysts of a species, however, does
not necessarily indicate that a region is free from the threat of toxic blooms, since there
are m a n y toxic dinoflagellates without observed cyst-stages in their life cycle (e.g.
Dinophysis spp.). Moreover. there is some e v i d e n c e that factors such as cyst r e s u s p e n s i o n
a n d current transport m a y repeatedly infect areas with toxic species (Cerebella et al.
1988: Anderson, 1989; Nehring, 1993b). In addition exotic transport m e c h a n i s m s of
cysts, such as within the m u d attached to birds legs, m a y be relevant m species dispersal
(Langhans, 1925). As has b e e n the case for m a n y coastal m a r i n e macrofaunal organisms
(for review, see Carlton, i985), n o n - e n d e m i c dinoflagellate species can b e i n a d v e r t e n t l y
introduced to a region w h e n their cysts are discharged with the ballast water in marine
harbours (Hallegraeff & Sumner, 1986; Hallegraeff & Bolch, 1991).
390
S. N e h r i n g
CONCLUSION
T h e role of t h e c o m p l e x l i f e - s t r a t e g y of p h y t o p l a n k t o n o r g a n i s m s for t h e d e v e l o p m e n t of a l g a l p e s t s in c o a s t a l z o n e s h a s n o t b e e n c o n s i d e r e d s u f f i c i e n t l y in t h e p a s t . T h e
results, e s p e c i a l l y t h e r e l a t i v e l y h i g h a b u n d a n c e of c y s t s in r e c e n t s e d i m e n t s , d e m o n s t r a t e t h e p o t e n t i a l i m p o r t a n c e of b e n t h i c r e s t i n g c y s t s for t h e i n i t i a t i o n of d i n o f l a g e l l a t e
b l o o m s in t h e i n v e s t i g a t e d a r e a of t h e N o r t h Sea. R e c o g n i z i n g t h e i m p o r t a n t role of t h e
r e s t i n g cyst in t h e life c y c l e of d i n o f l a g e l l a t e s , t h e r e is a n i n c r e a s i n g n e e d to s t u d y c y s t s i n
p h y t o p l a n k t o n e c o l o g y i n c o m b i n a t i o n w i t h s t u d i e s of h y d r o d y n a m i c , c h e m i c a l a n d
b i o l o g i c a l f a c t o r s of t h e w a t e r c o l u m n for a b e t t e r u n d e r s t a n d i n g of t h e s p a t i a l a n d
t e m p o r a l d y n a m i c s of d i n o f l a g e l l a t e b l o o m s .
A c k n o w l e d g e m e n t s . I thank Dr. K.-J. Hesse for valuable discussions. The c o m m e n t s of Dr. M,
Elbr~chter and three anonymous reviewers were greatly appreciated. W Hukriede drafted the
diagrams Part of this study is supported by the Federal Environmental Agency, Environmental
Research Plan of the Minister for the Environment, Nature Conservation and Nuclear Safety of the
Federal Republic of Germany Grant 108 02 085/lj, and the State of Schleswig-Holstein. This is
publication No. 43 of the project "Ecosystem Research Wadden Sea".
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