HELGOL,~NDER MEERESUNTERSUCHUNGEN
Helgol~inder Meeresunters. 45,423-443 (1991)
A perforated gastrovascular cavity in the symbiotic
deep-water coral Leptoseris fragilis: a new strategy to
optimize heterotrophic nutrition*
Dietrich Schlichter
Zoologisches Institut der Universitfit Kdln; Weyertal 119, D-W-5000 K61n 41,
Federal Republic of Germany
ABSTRACT: The organization of the zooxanthellate scleractinian coral Leptoseris fragilis was
studied. The architecture of the corallite and the histology of the polyparium were analysed for
adaptations that enable efficient capture and retention of suspended particles which would increase
energy supply. The data indicate that the gastrovascular system of L. fragilis is not a blind but a flowthrough system. Water entering the coelenteron through the mouth leaves the body not only through
the mouth but also through microscopic pores (~ 1-2 [Lm) which are located near the crests of the
sclerosepta in the oral epithelia. Irrigation is achieved by flageliar and probably also by muscular
activity. This type of filtration enables L. [ragilis, which lacks tentacles, to utilize suspended organic
material including bacteria. The supposed suspension feeding in combination with effective photoadaptations (presented in former communications) seems to be the basis for the survival of L. [ragilis
in an extreme habitat (between - 9 5 and -145 m) and for its, successful competion with other
scteractinian species provided with larger catching surfaces, and with other invertebrates depending on filter feeding.
INTRODUCTION
T h e bathymetric distribution of Leptoseris fragilis (Milne Ed w ar d s & Haime)
b e t w e e n - 9 5 and - 1 4 5 m (maximum) is extraordinary for a zooxanthellate scleractinian
coral species (Fricke & S c h u h m a c h e r , 1983). Therefore, the photoadaptations responsible
for the outstanding photosynthetic capacity h a v e b e e n studied (Schlichter et al., 1985,
1986, 1988; Pricke et al., 1987, 1991; Schlichter & Fricke, 1990, 1991). In situ studies of
photosynthesis r e v e a l e d two important results: (a) The photokinetic p a r a m e t e r s determ i n e d for L. fragilis are the lowest e v e r reported for symbiotic cnidarian species; i.e.
L. fragih's stands out for its efficient utilization of low photon flux densities of particular
spectral composition; (b) Calculations of e n e r g y b u d g e t s - b ased on 24-h in situ m e a s u r e ments - s h o w e d that m e t a b o l i s m can b e m a i n t a i n e d by autotrophy (phototrophy) only
during summer, while during months with low solar elevation the c o m b i n e d m e t a b o l i s m
of host and symbionts n e e d s additional heterotrophic fueling (Fricke et al., 1987, 1991).
Other strategies to c o m p e n s a t e r e d u c e d phototrophy could be the r ed u ct i o n of m e t a b o l ism for several months a n d / o r the utilization of storage products.
Heterotrophic f e e d i n g habits of the coral host include (a) the absorption of dissolved
* Dedicated to W. Weber 1923-1987
9 Biologische Anstalt Helgoland, Hamburg
424
Dietrich Schhchter
organic m a t e r i a l (DOM; carbohydrates, amino acids, fatty acids) a n d (b) t h e utilization of
particulate organic material (POM; detritus, bacteria, plankton) (Sebens, /987).
The a p p a r e n t necessity of supporting the c o m b i n e d m e t a b o l i s m of h o s t a n d symb i o n t s . - at l e a s t . t e m p o r a r i l y - b y heterotrophic m e a n s p r o m p t e d r e s e a r c h on the
structural basis for effective P O M feeding. Especially intriguing are t h e facts that L.
fragilis lacks tentacles a n d that this species grows in a h a b i t a t far from the more
productive levels n e a r the surface. In addition, L. fragifis hves in c o m p e t i t i o n with motile
a n d sessile i n v e r t e b r a t e species including, for example, azooxanthellate scleractinians
w h i c h a p p e a r to b e far b e t t e r a d a p t e d to c a p t u r i n g POM, as t h e y are e q u i p p e d with
tentacles - thus e n l a r g i n g the catching surface - a n d have far m o r e n e m a t o c y s t s .
A n a l y s i n g the organization of L. fragflis is not only interesting fro m an a d a p t i v e point
of view - i m p r o v e m e n t of c a p t u r i n g efficiency - b u t also from a c o m p a r a t i v e aspect: the
discoidal organization of L. fragflis differs from the g e n e r a l features of m a d r e p o r a r i a n
species (Chevalier, 1987; H o e k s e m a , 1989; Le Tissier, 1990).
MATERIALS AND METHODS
S p e c i m e n s of Leptoseris fragilis a n d Dendrophyllia minuscula (Bourne) w e r e coll e c t e d with the r e s e a r c h s u b m e r s i b l e G E O at d e p t h s b e t w e e n - 1 0 0 a n d - 1 3 5 m in front
of the Heinz Steinitz M a r i n e Biology L a b o r a t o r y at Eilat, Gulf of A q a b a , Red Sea. The
corals w e r e d e t a c h e d with a chisel a n d s u b s e q u e n t l y transferred into i n c u b a t i o n c h a m bers, w h i c h w e r e m o u n t e d on a platform b e l o w the front d o m e of the s u b m e r s i b l e . T h e
c h a m b e r s (273-276 ml) were closed a n d the s p e c i m e n s r e m a i n e d u n d i s t u r b e d for a b o u t
15 rain. T h e n g l u t a r d i a l d e h y d e was injected into the c h a m b e r s giving a final concentration of 4 %. M i x i n g was p e r f o r m e d with a m a g n e t i c stirring bar. T h e p r e s e r v e d
s p e c i m e n s w e r e b r o u g h t to the surface. On b o a r d a supporting vessel, s m a l l p i e c e s w e r e
cut off from the skeletons a n d w e r e s u b s e q u e n t l y post-fixed in 2 % o s m i u m tetroxide for
2 h at a m b i e n t t e m p e r a t u r e . S p e c i m e n of Goniopora planulata (Ehrenberg) originating
from shallow w a t e r w e r e p r e s e r v e d in the l a b o r a t o r y in the s a m e way.
Electron microscopy was p e r f o r m e d a c c o r d i n g to s t a n d a r d l a b o r a t o r y methods.
M a t e r i a l for transmission electron microscopy w a s t r e a t e d a n d e m b e d d e d after the
d o u b l e p r o c e d u r e of Pilkington (1969), The d e h y d r a t e d pieces w e r e e m b e d d e d in Spurrresin (Spurr, 1969). For decalcification, the plastic material w a s r e m o v e d from the
e m b e d d e d p i e c e s until the skeletons a p p e a r e d on the surface. The s m a l l c u b e s w e r e
t r e a t e d for s e v e r a l hours with 4 % acetic acid u n d e r vacuum. After rinsing a n d drying, the
d e m i n e r a h z e d p i e c e s were r e e m b e d d e d in Spurr-resin.
RESULTS
G e n e r a l r e m a r k s o n t h e c o r a l l i t e a n d t h e p o l y p a r i u m of Leptoseris fragilis
Skeletons of t h e p l a t e - s h a p e d coral L. fragflis attain a d i a m e t e r of u p to 8 c m
{Fig. la). The coralhte is thin a n d fragile. T h e gross m o r p h o l o g y is f u n d a m e n t a l l y in
a c c o r d a n c e with the b a s a l plate of a just m e t a m o r p h o s e d coral planula. T h e calyx (axial
hole) is laterally c o m p r e s s e d to a s l e n d e r oval cylinder. The central a x i a l e d g e s of t h e
sclerosepta - forming the contour of the axial hole - tower a b o v e the o t h e r parts of the
A perforated gastrovascular cavity in a stony coral
425
Fig. 1. Skeleton of the symbiotic deep water coral Leptoseris fragilis, a: Surface view; b: Profile of the
oral area. Scale bars: a: 10 ram; b: 3 mm
skeleton hke the walls of a crater (Pig. lb). The columella is composed of fused papillae
producing a m e a n d r i n e structure which shows periodic growth accretions. Frequently,
the skeletons are attached to the substrate by carbonate depositions which form rib-hke
walls b e t w e e n the aboral side of the skeletons a n d the bottom (Fig. 4a}. The skeleton is
covered by thin epitheha (20---40 btm). However, the underside of the skeleton is more or
less free of tissue a n d almost totally covered by epibionts.
The surface of h y i n g specimens shows a regular pattern of alternating dark a n d pale
stripes. The p a t t e r n corresponds to the distal a n d proximal parts of the sclerosepta {crests
a n d grooves). The colour p a t t e r n results from the distribution of zooxanthellae a n d
chromatophores. In situ living specimens appear dark brownish, almost black. The rim of
the disc appears whitish, i. e. zooxanthellae are absent, indicating that areas of fastest
h n e a r growth are without symbionts.
The surface of h v i n g specimens sometimes showed greyish p l a q u e s {bacteria, fungi).
Along the external parts of the sclerosepta, short, coiled portions of filaments could be
observed; the filaments were s q u e e z e d out due to tissue d a m a g e d u r i n g h a n d l i n g .
Fig 2. A sector of the oral skeleton surface of Leptoseris fragilis. The insertion of new sclerosepta is
marked by arrows. Scale bar: 1 mm
Fig. 3. View into the axial hole of Leptoseris fragflis. Principal sclerosepta are conspicuous in size.
The columella is visible at the bottom of the calyx. Scale bar: 1 mm
426
Dietrich Schlichter
The skeleton
In L, fragflis t h e v e r t i c a l b o d y axis is c o m p r e s s e d , p r o d u c i n g its t y p i c a l d i s c o i d a l
s h a p e . T h e s h t - h k e c a l y x a d d s to t h e b i l a t e r a l s y m m e t r y of t h e b o d y (Figs l a , 3, I7a, b).
T h e s c l e r o s e p t a r a d i a t e f r o m the centre. T o w a r d s t h e p e r i p h e r y , y o u n g e r s c l e r o s e p t a a r e
i n s e r t e d (Pig. 2). T h e b o r d e r of t h e c a l y x is c o m p o s e d of u p to 30 s c l e r o s e p t a , 6 or 12 of
w h i c h a r e c o n s p i c u o u s in size (Fig. 3}. T h e s c l e r o s e p t a are solid in t h e i r c e n t r a l axial parts
Fig: 4. a: Vertical section through the calyx of a skeleton of Leptoseris fragilis. Below the corallite
proper, structures are visible cementing the corallite to the ground. Scale bar: 1 ram. b: The central
part of the corallite displays perforated sclerosepta and fused lateral lamella of the sclerosepta. Scale
bar: 1 ram. c: Denticulated surface of the sclerosepta. Scale bar: 200 ~tm. d: Carbonate deposition in
the form of needles, Scale bar: 3 ~m. Abbreviations: C = columella, CS = cavern system~ arrow =
sponge
A perforated gastrovascular cavity in a stony coral
427
bordering the calyx, a n d the surface is d e n t a t e d or nodulated. Distal to the calyx the solid
region is followed by a portion which is perforated (Fig. 4b), b u t towards the periphery
the sclerosepta are a g a i n sohd. In the central part of the coralhte the perforated portions
of the sclerosepta produce a filigree lattice-work. The sclerosepta show a n interesting
microarchitecture. The flanks a n d especially the crests are d e n t a t e d (Fig. 4c). The flanks
of the sclerosepta are sculptured along their horizontal, longitudinal axis into lamella
which form a system of ducts (Figs 5a, b; 6a, b; 8a, b). The n u m b e r of gastric ducts of each
scleroseptum decreases from the centre towards the periphery because the height of
septa decreases (Fig. 5a).
a
Fig. 5. a: Diagram of a part of a scleroseptum. The decrease of lateral lamella from the centre of the
skeleton towards the periphery is shown. The details are not drawn to scale and perforations and
surface structures were omitted, b: Fracture of adjacent sclerosepta. The callicoblastic epidermis is
detached from the corallite. Some of the gastric ducts encircled by the lateral lamellae are packed
with debris while others are not. The arrows indicate the insertion of subsidiary scierosepta.
Abbreviations: SS = scleroseptum, LL = lateral lamella, GC -- gastric duct. Scale bar: 430 ~m
In the u p p e r regions, the sclerosepta grow vertically a n d produce n e w lamella
laterally, w h e r e a s in the lower regions the gastric ducts lose their function due to the
fusion of a d j a c e n t lamellae (forming dissepiments) leading to a complete separation of
the lower from the u p p e r ducts (Fig. 6a, b). This m e c h a n i s m is the basis for vertical
growth of the skeleton. The free lamellae of adjacent sclerosepta stand i n zigzag
geometry (zip-like) which may have functional c o n s e q u e n c e s (see "Discussion"). Circular depressions in the skeleton, at which points the living callicoblastic ectoderm
(= aboral epidermis) is attached to the corallite, are a b u n d a n t . At the back of the corallite,
costal structures are only weakly developed.
The skeletons are frequently i n v a d e d b y filamentous algae which stain the corallite
g r e e n and/or b r o w n - b e i g e . The algal filaments grow along the tissue/skeleton interface
(Figl 7a, b). This m a k e s parasitic or mutuahstic m e t a b o h c interactions hkely. Of particular
interest is the observation that the endolithic algae alter the cristalline structure of the
sclerosepta (Figs 5b, 6b).
428
Dietrich Schhchter
Fig. 6. a: L a t e r a l l a m e l l a of a d j a c e n t s c l e r o s e p t a m a y f u s e (arrows) a n d t h e g a s t r i c d u c t s lose t h e i r
function, as i n d i c a t e d b y t h e a b s e n c e of tissue; b: In t h e central r e g i o n of t h e s c l e r o s e p t u m t h e
crystalline s t r u c t u r e is altered, d u e to activities of e n d o h t h i c a l g a e (see Figs 5b, 7a, b, 16a). A b b r e viations: SS = s c l e r o s e p t u m , LL = lateral lamella, G C = gastric duct. Scale bars: a: 1 m m ; b: 150 ~ m
Fig. 7. S k e l e t o n of Leptoseris fragflis i n v a d e d b y f i l a m e n t o u s a l g a e {sections from d e c a l c i f i e d
s a m p l e s ; for o r i e n t a t i o n s e e insert 1 in Fig. 8a). a: Survey; b: T h e interface b e t w e e n callicoblastic
e p i d e r m i s a n d f i l a m e n t o u s a l g a e living w i t h i n t h e sclerosepta. For o r i e n t a t i o n s e e i n s e r t in F i g u r e 7a.
A b b r e v i a t i o n s : O T = oral e p i d e r m i s a n d g a s t r o d e r m i s , A T = aboral e p i d e r m i s a n d g a s t r o d e r m i s ,
FA = f i l a m e n t o u s a l g a e , G V = g a s t r o v a s c u l a r s y s t e m , SS = s c l e r o s e p t u m , C L = cleft (callicoblastic
e p i d e r m i s d e t a c h e d from corallite}. Scale bars: a: 10 ~m; b: 10 ~ m
A perforated gastrovascular cavity in a stony coral
/..
429
2
9
CE
" 9 'S~-. ' ..
a
b
Skeleton
:'
Fig. 8. a: Diagram of a section of two adjacent sclerosepta covered with the polyparium. The oral
tissues are stretched tentlike b e t w e e n the sclerosepta. Gastrovascular pockets, lined by mesenteries,
are divided by one scleroseptum into two compartments a n d these are further subdivided into
gastric ducts by lateral lamella of the sclerosepta. The n u m b e r e d insertions are referred to in
subsequent figures of this paper, b; Section of a decalcified specimen. Abbreviations: OE = oral
epidermis, M = mesogloea, OG = oral gastrodermis, Z = zooxanthellae, P = pigment granules,
CE = callicoblastiC epidermis, AOG = aboral gastrodermis, GV = gastrovascular system, GC = gastric
duct, SS = scleroseptum, LL = lateral lamella, MT = mesentery. Scale bar: 100 ~m
T h e t i s s u e s of t h e p o l y p a r i u m
In t h e f o l l o w i n g s e c t i o n s , t h e h i s t o l o g y of t h e p o l y p a r i u m of L. fragiiis is d e s c r i b e d i n
detail. T h e s c h e m a t i c d r a w i n g of a v e r t i c a l c r o s s - s e c t i o n t h r o u g h t h e s k e l e t o n a n d t h e
o v e r l y i n g t i s s u e s d e p i c t s t h e m i c r o s c o p i c a l a n a t o m y (Fig. 8a).
T h e a b o r a 1 e p i t h e 1 i a. T h e c a l l i c o b l a s t i c e p i d e r m i s ( = a b o r a l e c t o d e r m ) a n d
t h e a b o r a l g a s t r o d e r m i s ( = a b o r a l e n d o d e r m ) a r e t h i n , b o t h l a y e r s r a n g i n g b e t w e e n 0.5
a n d 2 t~m i n t h i c k n e s s , i.e. t h e a b o r a l e p i t h e l i a l cells a r e e x t r e m e l y c o m p r e s s e d . T h e
m e s o g l o e a ( m e s o l a m e l l a ) b e t w e e n t h e t w o cell l a y e r s s e e m s to b e t o t a l l y r e d u c e d . T h e
a b o r a l g a s t r o d e r m i s is e q u i p p e d w i t h f e w flagella, a n d z o o x a n t h e l l a e a r e a b s e n t (Fig. 9}.
T h e o r a 1 e p i d e r m i s ( = o r a l e c t o d e r m ) c o n s i s t s m a i n l y of a s p o n g y l a y e r of
cells w h o s e e x t e r n a l (apical) m e m b r a n e is p r o v i d e d w i t h m i c r o v i l h , m a c r o v i l h a n d
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Dietrich Schlichter
Fig. 9, View of the aboral gastrodermis {insert 1 in Fig. 8a). The aboral tissues are extremely thin.
The surface is sparsely covered with flagella (compare with Fig, 14). SS = scleroseptum. Scale bar:
30 ~rn
n u m e r o u s flagella, prerequisites for s u s p e n s i o n feeding (Fig. 10c, d). The flagella have
accessory structures a r o u n d their base. Towards their base, the epithelio-muscular cells
taper into c o l u m n a r processes c o n t a i n i n g the nucleus, a n d terminate in contact with the
mesogloea. The large intercellular spaces (Fig. 10a, b) m a y facilitate the p e n e t r a t i o n of
light to the zooxanthellae a n d to the chromatophores, Further cell types w h i c h can be
sporadically identified are mucous ceils a n d functional nematocysts (Fig. 11a, b). The
nematocysts are f o u n d in groups a r o u n d large secretory cells. The s t i n g i n g batteries are
located on or n e a r the top of the sclerosepta. In Figure 13, a g l a n d u l a r cell is shown,
indicating the synthesis of secretory g r a n u l e s by the Golgi apparatus.
The oral gastrodermis
(= oral endoderm) consists of a layer of c o l u m n a r
cells, h a r b o u r i n g zooxanthellae (12 ~tm in diameter in maximum) (Figs 9, 10, 12). Each
host cell contains only one symbiont (Fig. 12). The host cells c o n t a i n i n g the algae are
A p e r f o r a t e d g a s t r o v a s c u l a r cavity in a s t o n y coral
431
Fig. 10. The histological organization of the oral epithelia. For orientation see inserts 2 and 3 in Fig.
8a. a: The oral epidermis is of spongy consistency and the mesogloea is weakly developed. The oral
gastrodermis is prominent and harbours zooxanthellae, b: The oral epidermis shows large intercellular spaces. The oral gastrodermis displays conspicuous, dense accumulations of pigment granules
(see also Fig. 12). During preservation the aboral epithelia became detached from the skeleton, c, d:
The flagella of the oral epidermis are provided with accessory structures at the base of which two
types exist (arrows). Abbreviations: OE = oral epidermis, I = intercellular space, M = mesogloea,
OG = oral gastrodermis, Z = zooxanthellae, P = pigment granules, AT = aboral epidermis and
gastrodermis, GV = gastrovascular system, OD = organic debris. Scale bars: a: 10 ~m; b: 12 ~m;
c: 5 ~m; d: 2 ~m
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Dietrich Schlichter
Fig. 11. Stinging batteries are localized in the upper regions of the sclerosepta or near the top (insert
4 in Fig. 8a). a: Survey; b: detail. Abbreviations: BN = battery of nernatocysts, SS -- scleroseptum,
Z = zooxanthellae. Scale bars: a: 50 ~m; b: 20 ~m
largely r e d u c e d which might indicate particular metabolic conditions. The zooxanthellae
lie p r e d o m i n a n t l y in one p l a n e thus avoiding self-shading (Fig. 10a). T h e intercellular
spaces b e t w e e n the cells h a r b o u r i n g the algae are filled by ramifications of
chromatophore cells. The ramifications are d e n s e l y p a c k e d with granules which contain
autofluorescent p i g m e n t s transforming short w a v e l e n g t h s into longer ones. The p i g m e n t
g r a n u l e s form a continuous stratum u n d e r l y i n g a n d partially covering the z o o x a n t h e l l a e
(Schhchter et al,, 1985, 1986). The oral gastrodermis, in contrast to the a b o r a l gastrodermis, is e q u i p p e d with a high density of flagella (Fig. 14). The a b s e n c e of a g a s t r o d e r m a l
b r u s h b o r d e r m a y indicate the u p t a k e of POM b y endocytosis. A w e a k l y d e v e l o p e d
mesogloea is present. Contractile, n e u r o i d e a n d sensory structures are r a r e l y observed
The oral epithelia of L. fragilis a n d of two colonial scleractinian coral species were
compared: (a) the zooxanthellate species Goniopora planulata, originating from shallow
waters, a n d (b) Dendrophyllia minuscula, without zooxanthellae, collected at - 1 2 7 m
depth. The two symbiotic species show - with the exception of the c h r o m a t o p h o r e system
- strong histological similarities (compare Figs 10a a n d 15a). In both, the oral epidermis is
poorly developed, few nematocysts are p r e s e n t a n d the gastrodermis with z o o x a n t h e l l a e
is three times thicker t h a n the epidermis. In the azooxantheUate deep w a t e r species, the
Fig. 13. Formation of secretory granules in the oral epidermis. Abbreviations: SG
secretion
granules, GA -- Golgi apparatus. Scale bar: 5 ~m
Fig. 14. Surface view of the oral gastrodermis (insertions 2, 3 in Fig, 8a), densely covered with
flagella in contrast to the aboral gastrodermis (see Fig. 9). Scale bar: 20 ~rn
--
A p e r f o r a t e d g a s t r o v a s c u l a r c a v i t y in a s t o n y c o r a l
433
Fig. 12. Z o o x a n t h e l l a e are f o u n d exclusively in the oral g a s t r o d e r m i s of Leptoseris fragih's (insertions
2 a n d 3 in Fig. 8a). a: Each g a s t r o d e r m a l cell contains only one cytosymbiont, b: T h e z o o x a n t h e l l a e
are s u r r o u n d e d b y n u m e r o u s p i g m e n t granules b e l o n g i n g to a c h r o m a t o p h o r e s y s t e m of the host
(see Fig. 10a, b). Abbreviations: Z = zooxantheUae, HC = host dell, P = p i g m e n t granules, M =
mesogloea, PV = perialgal vacuole, G V = gastrovascular system, N --- nucleus. Scale bars: a: 5 gm;
b: 4.3 ~m
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Dietrich Schhchter
Fig. 15. Comparison of the oral tissue layers of zooxanthellate and an azooxanthellate scleractinian
coral species, a: In Goniopora planulata, containing symbionts, as also in L. fragflis, the algaecontaining gastroderrnis predominates (see Fig. 10a). b: In Dendrophyllia rninuscula, without
zooxanthellae, the oral epidermis predominates. Abbreviations: OE = oral epidermis, M = mesogloea, OG = oral gastroderrnis, Z = zooxanthellae, PV = perialgal vacuole, NE = nernatocysts.
Scale bars: 10 ~rn
e p i d e r m i s is p r o m i n e n t a n d n e m a t o c y s t s a n d g l a n d u l a ~ cells a r e f r e q u e n t (Fig. 15b). T h e
g a s t r o d e r m i s is w e a k l y d e v e l o p e d a n d a b o u t a q u a r t e r as t h i c k a s t h e e p i d e r m i s .
T h e organization of the gastrovascular system
The aboral epithelia (gastrodermis and epidermis) cover the corallite. The oral
epithelia (also gast~odermis and epidermis) stretch tent-like from one scleroseptum to the
next (Figs 5b; 8a, b; 16a). The oral epidermis thus forms an undulating coat dropping
inwards slightlybetween the sclerosepta (Figs 8a, b; 16a). In contrast, the oral gastrodermis reaches d o w n between the sderosepta and fuses with the aboral gastrodermis. Each
gastrovascular pocket, laterallydefined by mesenteries, is divided into two subunits by a
scleroseptum (Fig. 8a, b). The gastrovascular pockets communicate along the crests of
the sclerosepta and in the central area of the corallite through the scleroseptal perforations (Fig.4b).
The gastrovascular pockets, divided into two smaller chambers by sclerosepta, are
further subdivided into radial gastric ducts by the lateral lamellae on the flanks of the
sclerosepta (Figs 5, 6). The number of functioning ducts stacked upon each other differs,
reaching more than 7 in the centre (Fig. 5). Fractures show that only those ducts which
are not yet completely closed are lined with living tissue (Fig. 6b). O n the periphery, the
number of ducts declines to two {Figs 5a, 6b). In the mesenteries, consisting of a central
mesogloea and two gast/odermal cell layers, contractile elements are present, The
contractile filaments of epithelio-muscular cells run vertically forming retractor muscles.
A p e r f o r a t e d g a s t r o v a s c u l a r cavity in a stony coral
435
Fig. 16. The organization of the gastrovascular system in the periphery of the corallite, a: Section
through adjacent sclerosepta covered with the polyparium. Due to detachment of the epithelia the
natural topography is somewhat disturbed (see insertions 2--4 in Fig. 8a). b: Longitudinal section
through a mesentery {see insertion 5 in Fig. 8a). The nucleus of the epithelio-muscular cell is located
excen~rically. The myofibrilar components are anchored within the mesogloea. Abbreviations: OE =
oral epidermis, OG = oral gastrodermis, AOG = aboral gastrodermis, GV = gastrovascular system,
MT = mesentery, CE = apical membrane of the callicoblastic epidermis (detached from the
corralite), LL = lateral lamella, SS = scleroseptum, CF = contractile filaments, M = mesogloea,
N = nucleus, P = pigment granules. Scale bars: a: 100 [~m; b: 1 [tm
T h e m y o f i b r i h a r c o m p o n e n t s of t h e e p i t h e h o - m u s c u l a r cells a r e a n c h o r e d in t h e m e s o g l o e a (Fig. 16b).
The oral area (peristome
and stomodaeum)
T h e slit-hke s t o m o d a e u m is l o c a t e d in t h e l a t e r a l l y c o m p r e s s e d c a l y x b o r d e r e d b y
t h e axial e d g e s of t h e s c l e r o s e p t a (Figs 3, 17a, b). T h e m o u t h has a c i r c u l a r a p p e a r a n c e
a n d m a y w o r k h k e a n iris d i a p h r a g m .
T h e p h a r y n x is d e n s e l y c o v e r e d w i t h f l a g e l l a (Fig, 18a, b). F r o m t h e p h a r y n x t h e
gastric ducts r a d i a t e o u t w a r d s to t h e p e r i p h e r y p e r p e n d i c u l a r l y ; a c e n t r a l g a s t r a l cavity is
l a c k i n g (Figs 4, 17, I8a).
436
Dietrich Schhchter
Fig. 17a, b: Leptoseris fragilis. V i e w into t h e c e n t r a l s t o m o d a e u m a n d p h a r y n x ( p r e s e r v e d specim e n s ) . At t h e b o t t o m of t h e g a s t r o v a s c u l a r s y s t e m :the c o l u m e l l a is visible. A b b r e v i a t i o n s :
S = s t o m o d a e u s , C = columella. Scale bars: a: 1 ram; b: 1 r a m
Fig. 18. Leptoseris fragilis, a: V i e w t h r o u g h t h e s t o m o d a e u m into t h e p h a r y n x ( c o m p a r e w i t h Figs 4a,
17b). b: C l o s e - u p of t h e flagellar c o v e r of t h e p h a r y n x . A b b r e v i a t i o n s : s = b o r d e r of t h e s t o m o d a e u m ,
a s t e r i s k s = c e n t r a l axial e d g e s of sclerosepta, a r r o w s = a c c e s s into t h e g a s t r i c ducts. Scale bars:
a: 150 ~tm; b; 20 ~tm
A p e r f o r a t e d gastrovascular cavity in a stony coral
437
Pores in the oral epithelia
N e a r the top of the crests of the sclerosepta, the oral e p i t h e l i a are p e r f o r a t e d b y
microscopic pores. T h r o u g h the pores (1-2 ~tm in diameter), the g a s t r o v a s c u l a r s y s t e m
c o m m u n i c a t e s with the s u r r o u n d i n g w a t e r (Fig. 19). Up to 20 p o r e s are c o m b i n e d into
functional units (interpore distance is 4-8 ~m). The a r r a n g e m e n t m a y b e d e s c r i b e d , in
a n a l o g y to l a b o r a t o r y equipment, as m e m b r a n e filters.
Fig. 19. Leptoseris fragitis. Microscopical pores in the oral epithelia near the crests of the sclerosepta
(see insertion 6 in Fig. 8a). a: A group of pores, b: An individual pore. Scale bars: a: 6 ~m; b: 3 ~m
DISCUSSION
In this section, functional aspects of the e p i d e r m a l pores are discussed with special
reference to the retention of particles. The explanations, a l t h o u g h b a s e d on the d a t a
p r e s e n t e d h e r e a n d on additional observations, are s o m e w h a t speculative a n d n e e d
further corroboration.
C o n v e n t i o n a l o r g a n i z a t i o n a n d i r r i g a t i o n of t h e c o e l e n t e r o n
The g a s t r o v a s c u l a r system (coelenteron) of corals serves several functions: (a) Its
fluid constitutes a h y d r a u h c s k e l e t o n a n d gives stability in cooperation with the lime
skeleton, the m e s o g l o e a a n d the mesenteries; (b) The coelenteron is t h e s p a c e for the
distribution a n d extracellular digestion of e n g u l f e d p l a n k t o n or detritus; final digestion
occurs in food v a c u o l e s within g a s t r o d e r m a l cells; (c) The gastrovascular s y s t e m is
involved in respiration a n d in elimination of all kinds of w a s t e p r o d u c t s , furthermore in
ion- a n d o s m o r e g u i a t i o n a n d in reproduction. The functions listed are all closely r e l a t e d
to the fluid of the gastrovascular system a n d its renewal.
438
Dietrich Schlichter
The gastrovascular system of sohtary anthozoans is a s s u m e d to b e a b h n d sac. The
single o p e n i n g is mouth and anus equally. In tentacle b e a r i n g species t h e l u m e n of the
t e n t a c l e s c o m m u n i c a t e s with the gastrovasr
pockets. Due to f l a g e l l a r activity, w a t e r
a n d other contents are p r o p e l l e d within the system a n d also into a n d out of t h e mouth.
L a r g e r o p e n i n g s occasionally o b s e r v e d in the tentacle tips of a n t h o z o a n s most
p r o b a b l y exist a n d w o r k only temporarily: Due to the a b s e n c e or r e d u c t i o n of the
m e s o g l o e a in that particular region, the tissue layers m a y b e m e c h a n i c a l l y p e r f o r a t e d e.g.
b y i n c r e a s e d p r e s s u r e in the gastrovascular system c a u s e d b y m u s c u l a r activity. Those
l a r g e o p e n i n g s a r e not r e l a t e d to the p e r m a n e n t microscopical pores in t h e e x t e r n a l tissue
layers of Leptoseris fragilis.
In small coral polyps in w h i c h horizontal transport over only short distances is
required, it is c o n c e i v a b l e that the a f o r e m e n t i o n e d m e c h a n i s m is sufficient. The fluid
circulation p o w e r e d b y flagella is sometimes s u p p o r t e d b y m u s c u l a r actions, i.e. the
contraction of l o n g i t u d i n a l muscles l e a d s to an e x c h a n g e of the contents of the c o e l e n t e ron. Gladfelter (1983) discussed for Acropora cervicornis the circulation of fluids within
canals 100 ~m in diameter, p o w e r e d only b y flagellae. In colonial species, however, the
distances are shorter. In L fragilis, transport has to b e m a n a g e d b y m e a n s of gastral ducts
less than 25 ~m in d i a m e t e r a n d s e v e r a l centimeters in length. T h e s e d i m e n s i o n s m a k e
the operation of t h e conventional irrigation system in L. fragflis doubtful,
T h e m o d i f i e d i r r i g a t i o n s y s t e m of Leptoseris fragilis
The flagella w h i c h d e n s e l y cover the b o d y surface of L. fragifis (Pigs 10c, 18a, b),
transport w a t e r a n d particles either t o w a r d s the s t o m o d a e u m or in the o p p o s i t e direction.
The accessory structures surrounding the b a s a l parts of the flagella (Pig. 10c, d) m a y h a v e
sensory functions that control the transport of useful/useless particles. For the discoidal
g e n u s Fungia a n d other coral species, a m e c h a n i s m controlling the selection b e t w e e n
useful u n d useless particles has b e e n d e s c r i b e d (Yonge, 1930; Abe, 1938; S c h u h m a c h e r ,
1979). In addition, flagellar activity inhibits the formation of unstirred l a y e r s on the b o d y
surface which w o u l d i m p e d e diffusion in g e n e r a l a n d also the a b s o r p t i o n of dissolved
o r g a n i c c o m p o u n d s or the supply of inorganic nutrients to the zooxanthellae. The oral
e p i d e r m i s is well e q u i p p e d with microvilli (Pigs 10c, 18), facilitating the a b s o r p t i o n of
dissolved nutrients. L. fragilis is a b l e to absorb a n d a c c u m u l a t e D O M (Schhchter, in
preparation). S w e l h n g of the polyparium, due to excess fluid filling the g a s t r o v a s c u l a r
system which m a y cause s h p p i n g of particles from the surface, could not b e observed.
The e x t e r n a l transport of particles in L. fragilis t a k e s p l a c e along the g r o o v e s formed b y
a d j a c e n t sclerosepta (Pigs 5b, 8b, 11a, 16a). On r e a c h i n g the slope of the oral crater, the
particles are t r a n s p o r t e d in an u p w a r d direction onto the peristome, t h e n d o w n w a r d into
the s t o m o d a e u m . The u p w a r d transport could b e a m e c h a n i s m to fractionate the particles
according to size, m a s s or electrostatic c h a r g e (Solow & Gallager, 1990), in c o n s e q u e n c e
of which only a d e q u a t e particles w o u l d b e ingested. E l e c t r o n m i c r o g r a p h s give the
i m p r e s s i o n that particles are not c o a t e d with mucous during transport along the surface.
However, the possibility that m u c o u s w a s e h m i n a t e d d u r i n g histological p r e p a r a t i o n m a y
not be excluded. However, c o m p a r e d with the n u m e r o u s m u c o u s cells in the oral
e p i d e r m i s of Fungia klunzingeri (D6deflein), m u c o u s cells in L. fragflis are scarce.
Particles are i n g e s t e d into the s t o m o d a e u m a n d are t h e n m o v e d into the pharynx. The
A p e r f o r a t e d gastrovascular cavity in a stony coral
439
particles are t r a n s p o r t e d either directly b y flagellar activity a n d / o r b y an i n w a r d l y
directed s t r e a m of water. T h e w a t e r flow within the eoelenteron is g e n e r a t e d b y (a) a
"fiagellar e n g i n e " l o c a t e d in the p h a r y n x (Fig. 18), (b} the flagellar lining of the gastrovascular system (Fig. 14), a n d / o r at least temporarily b y (c) a lowering a n d e l e v a t i o n of
the oral epithelia b y muscles (see below). The i n g e s t e d particles arrive at t h e p h a r y n x
w h e r e they are distributed directly into the gastrovascular pockets a n d ducts (Figs 17,
18). Minute particles a p p e a r to be g l u e d to the columellar flagellae (Fig. 20). This
Fig. 20a, b: Surface view of the aboral gastroderrnis coating the columella (compare with Fig. I0c).
Abbreviation: OD = organic debris. Scale bars: a: 13.6 ~m; b: 3.8 ~m
contrasts with the particle transport on the external b o d y surface. In the central regions of
the corallite, the gastrovascular p o c k e t s c o m m u n i c a t e through perforations of the
sclerosepta (Fig. 4b). T h e a r r a n g e m e n t r e s e m b l e s a system of sieves of different m e s h
size which m a y allow the fractionation of particles in different categories: L a r g e r particles
are r e t a i n e d in the central regions, thus avoiding blocking of the ducts l e a d i n g to the
periphery. The d i a m e t e r of the e x p a n d e d gastric ducts r a n g e s b e t w e e n 20 a n d 50 ~tm,
and the l e n g t h of the flagella lining the gastrovascular system a v e r a g e s 15 to 20 btm. At
the p e r i p h e r y of the corallite the perforations of the s c l e r o s e p t a d i s a p p e a r a n d the
transport within the gastric ducts has theoretically to w o r k to a n d fro, a c c o r d i n g to the
conventional irrigation concept.
The l u m e n of the gastric ducts is confined b y the lateral l a m e l l a e of the sclerosepta.
The n u m b e r of gastric ducts p e r s c l e r o s e p t u m declines from the centre t o w a r d s the
p e r i p h e r y (Fig. 5a). The o p e n sides of the gastric ducts opposite the l a m e l l a are b o r d e r e d
by mesenteries. The m e s e n t e r i e s can p r o b a b l y close the canals t e m p o r a r i l y (Fig. 16a).
Closing of the gastric ducts a n d c h a n g e s in their d i a m e t e r - which is i m p o r t a n t for their
440
Dietrich Schlichter
function - m a y b e c a u s e d b y differences in w a t e r pressure p r e s s i n g t h e m e s e n t e r i e s
a g a i n s t the o p e n sides of the ducts. The zip-like a r r a n g e m e n t of the l a m e l l a e of a d j a c e n t
sclerosepta m a y facilitate closing. Forces influencing the w a t e r p r e s s u r e in the coelenteron are due to flagellar a n d m u s c u l a r activity. The flagellar m e c h a n i s m h a s a l r e a d y b e e n
discussed (see above}. Contraction of the m e s e n t e r i a l retractor m u s c l e s w o u l d l e a d to
v o l u m e reduction of the gastral pockets, which w o u l d b e the first step in t h e irrigation of
the gastrovascular system (see Figs 8a, 16a, b). The original position could b e r e e s t a b lished h y d r a u l i c a l l y b y filling the gastrovascular system a g a i n with w a t e r d u e to flagellar
activity. Tissue retraction c a u s e d e x p e r i m e n t a l l y b y light stress w a s often so strong that
the sharp d e n t i c u l a t e d crests of t h e sclerosepta p e n e t r a t e d the oral epithelia. Studies in
the future will show which of the two irrigation m e c h a n i s m s m e n t i o n e d is p o w e r f u l
e n o u g h to p r o d u c e the waterflow t h r o u g h the pores.
The efficiency of particle c a p t u r e a n d of retention of useful particles, as w e l l as the
efficiency of assimilation are of importance in the nutrition of filter f e e d e r s {Rubenstein &
Koehl, 1977; Solow & Gallager, 1990}. No d a t a are available on t h e efficiency of
assimilation; however, some information exists on the efficiency of particle c a p t u r e a n d
retention.
The g a s t r o v a s c u l a r system of solitary a n t h o z o a n s is a s s u m e d to e n d b l i n d l y w h i c h
complicates the transport of w a t e r a n d particles b a c k a n d forth in n a r r o w t u b e s of
c o n s i d e r a b l e length. L. lragilis m a y h a v e solved the p r o b l e m of efficient irrigation a n d
s u s p e n s i o n filter f e e d i n g in the following way: Particle capture is o p t i m i z e d b y the p l a t e like s h a p e a n d the d e n s e cover with flagella of the external b o d y surface (Fig. 10c, d).
T h e gastral cavity is not a b l i n d b u t a flow-through system. The n u t r i e n t - c o n t a i n i n g w a t e r
current enters L. fragiZs t h r o u g h the s t o m o d a e u m a n d l e a v e s the g a s t r o v a s c u l a r system
not only t h r o u g h the mouth b u t also t h r o u g h e p i d e r m a l pores {Fig. 19}. T h e "lips" of the
pores s u g g e s t that w a t e r streams only in one direction (Fig. 19b}. T h e d i a m e t e r of the
pores is small e n o u g h to k e e p b a c k p i c o p l a n k t o n which does not h a v e to b e n e c e s s a r i l y
c o a t e d with mucous. Irrigation is p o w e r e d b y a p r e s s u r e difference across the p o r e units.
The pressure difference m a y be caused by the "pharyngeal flagellar engine" (Fig. 18)
and flagellaecoating the gastricducts {Fig. 14).This unidirectionalwater flow leads to an
accumulation of particles in the gastric ducts. As mentioned above, the irrigation could
also be achieved by muscle actions (Figs 8a, b, 16b}: Contraction of the mesenterial
retractor muscles would produce a water current, and provided the stomodaeum remains
closed, the water would be pressed through the pores and suspended particles would be
retained and concentrated. The continuous unidirectional water current through the
gastrovascular system would also improve other functions of the coelenteron listed
above.
Stated simply, the gastrovascular system of L. [ragilisworks like the filtrationsystem
of poriferans but in reverse with respect to the diameter of in- and outlets: In i. fragilis,
water - free of suspended particles- leaves the body through microscopical pores of the
oral epithelia.
The transport of wastes from the gastric ducts out through the mouth could be
m a n a g e d by flagellar activity or by the lowering and lifting mechanism. If the
stomodaeum remains open during contraction of the mesenterial retractor muscles,
indigestible material could be rejected through the mouth. This mechanism m a y work if
the ducts are not set at a fixed size and the epithelia coating the gastric ducts are flexible
A perforated gastrovascular cavity in a stony coral
441
and only partially attached to the coralhte. The final deposition of undigestible material
within the lowest gastric ducts could be another alternative to eliminate waste products,
for the ducts lose their nutritive function in any case due to vertical growth of the skeleton
(or in connection with carbonate deposition). The epidermal pores may also have nontrophic functions, e.g. the release of water more rapidly from the coelenteron during
stress situations (e.g. fish grazing).
One aim of this study was to elucidate trophic adaptations in L. fragilis which may be
responsible for the extraordinary bathymetric distribution of this zooxanthellate coral
species. Energy calculations based on in situ measurements of respiration and photosynthesis indicate that in the northern part of the Gulf of Aqaba {Red Sea) the phototrophic
input is not high enough to compensate the energetic requirements of host and symbionts
during 6 to 8 months of the year (Pricke et al., 1987, 1992). The observations and
morphological studies described here show how the capture and the retention of particles
may be supported in a scleractinian coral species lacking tentacles. Due to the abihty to
extract even microscopical POM, the heterotrophic contribution to the nutrition of both
host and symbionts appears to be optimized. Heterotrophy of the zooxanthellae themselves was proved by Steen (1986). Another strategy to endure periods of insufficient
autotrophic supply would be to reduce metabohsm or to use stored reserves, e.g. stored
lipids which are of particular metabolic importance in corals. In zooxanthellate cnidarians
it has been clearly shown that the cytosymbiotic algae are involved substantially in the
synthesis of lipids of the host (Patton et al., 19771 Schhchter & Kremer, 1985~ Spencer
Davis, 1991).
The occurrence of zooxanthellae in L. fragilis, growing on the border of the photic
zone, should therefore be discussed under this synergistic point of view: During months
of high solar elevation the zooxanthellae contribute to the, synthesis of lipid reserves of
the host. Thus, the algae have an essential metabolic function which may explain the
extreme efforts of the host to support photosynthesis by unique photoadaptations.
L. fragiiis could also successively utilize organic material accumulated within the gastric
ducts during periods of high POM supply in the habitat. L. fragilis lives successfully with
respect to energy supply in a habitat which favours neither phototrophic nor heterotrophic feeding habits. Solar irradiation in the habitat is low and of particular spectral
composition. The habitat is far from the shallow, more productive zones, thus the supply
with, for example, net plankton is considerably reduced (Johannes et al., 1970), Microbial
biomass and detritus are abundant also in deeper reef areas {Marshal et al., 1975; Lewis,
19771 Mitskevich & Kriss, 19821 Moriarty et al., 1985). Linley & Koop (1986) a r g u e d that
even pelagic bacteria are a potential major food resource for benthic filter feeders.
L. fragilis displays structural and physiological adaptations which compensate the
barren trophic conditions of the habitat. Adaptations enabling photosynthesis were
discussed in detail (Fricke et al., !987, 1991; Schlichter et al., 1985, 1987, 1988~ Schlichter
& Pricke, I990, 1991). The present study indicates adaptations supporting POM feeding.
L. fragilis successfully competes with other motile or sessile invertebrates in catching
POM. In a speculative sense, the ability of L. fragilis to capture and keep back suspended
particles of a diameter of 1 to 2 gm could be the "secret" of gaining sufficient energy
heterotrophically. The ability of scleractinians to retain suspended particles was already
shown, for example by Lewis (1976). The fiowthrough system of L. fragilis operates faster
and more efficiently than blind gastrovascular systems. To my knowledge a similar
442
Dietrich Schlichter
s y s t e m h a s n o t y e t b e e n d e s c r i b e d for corals. T h e r e d u c t i o n of c a t c h i n g s u r f a c e s i n L.
[ragilis, i.e. t h e a b s e n c e of t e n t a c l e s , s e e m s to b e b a l a n c e d b y t h e a b i l i t y to u t i l i z e
p a r t i c l e s w h i c h a r e e x t r a c t e d i n t h e g a s t r i c d u c t s . T h e c a p t u r e of l a r g e r p l a n k t o n w h i c h
m a k e s t e n t a c l e s a n d n e m a t o c y s t s n e c e s s a r y (the s y n t h e s i s of b o t h n e e d s e n e r g y ) s e e m s
to b e of less i m p o r t a n c e for L. fragilis; t h e n e m a t o c y s t s m i g h t h a v e a p r e d o m i n a n t l y
protective function.
T h e g r o w t h f o r m s of s c l e r a c t i n i a n c o r a l s i n g e n e r a l a r e d i s c u s s e d i n t e r m s of
e c o p h y s i o l o g i c a l or a n a t o m i c a l a d a p t a t i o n s to p a r t i c u l a r e n v i r o n m e n t a l c o n d i t i o n s . T h e
p l a t e - h k e o r g a n i z a t i o n of L. fragilis is a m e a n s to kill t w o b i r d s w i t h o n e s t o n e : (a) T h e
z o o x a n t h e l l a e c a n - w i t h o u t s h a d i n g e a c h o t h e r - b e o p t i m a l l y e x p o s e d to l o w i r r a d i a t i o n ; (b) t h e p l a i n s u r f a c e , d e n s e l y c o v e r e d w i t h f l a g e l l a e , o p e r a t e s as a t r a p c o l l e c t i n g
s u s p e n d e d p a r t i c l e s n o t c a u g h t b y t h e t e n t a c l e s or b y t h e n e m a t o c y s t s . D u e to t h e
perforated gastrovascular cavity the particles can efficiently be accumulated within the
gastric ducts.
Acknowledgements. This study was supported by the Deutsche Forschungsgemeinschaft (Schl. 115/
7-1 and Fr. 369/7-1). I would hke to express my gratitude to Professor H. W. Fricke a n d the crew of
the research submersible GEO for considerable help and encouragement. I t h a n k M. Grosmann, H.
Krisch, H.-P. Bollhagen a n d J. Jacobi for skillful technical assistance. I am i n d e b t e d to Drs E. Robson,
M. LeTisier, G. Scheer a n d H. S c h u h m a c h e r for critical reading of the m a n u s c r i p t a n d for helpful
comments and valuable suggestions. I, however, take responsibility for any errors.
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