Sea
anemones from the coral reefs of
the Red Sea at Al- Ghardaqa.
Dr.
Fayez. A. Shoukr
Zoology
Department, Faculty of Science, Tanta University,
Tanta
31527,Egypt.
Shoukr, F.A. (1990): Actinians
associated with coral reefs at Al- Ghardaqa, Red sea. Bull. Fac.
Sci., Zagazig Univ., 12
(2): 827-846.
The gross anatomy and histological
structure of three anemones namely; Entacmaea
quadricolor (Rueppell & Leuckart, 1828), Antheopsis crispus (Ehrenberg, 1834) and Anthopleura
stellula (Ehrenberg, 1834) are described from the Egyptian fauna for the
first time. The confusion in anemone identification is also discussed.
INTRODUCTION
Taxonomic studies on Egyptian actinians from the Red Sea are relatively few and
fragmentary. The earlier works of Gohar (1934 and
1948) were mainly devoted to the ecology and behavioral characteristics of
anemones and fish association. The taxonomic work of Carlgren
(1949) referred to the occurrence of some anemone species in the Red Sea
without description. Therefore, Red Sea anemones can not be accurately
identified on the basis of the existing literature. Nevertheless, a preliminary
taxonomic key for Egyptian anemones was proposed by Shoukr (1984) owing to
their morphological characters in the field. In fact, most taxonomic criteria
for precise identification were obtained from the anatomical and histological
points of view. These characters include the type of sphincter, basilar and
retractor muscles , nematocysts , number of
mesenteries distally and proximally as well as the presence of acrorhagi, verrucae, suckers,
vesicles and acontia.
Thus, the present study is an attempt to furnish some information about
the internal anatomy and histological structure of three anemone species
collected from the coral reefs of the Red Sea at Ghardaqa.
Specimens of sea anemones were
sampled from the western Red Sea, at about 340 km. south of Suez, during
1985-1988. The individuals were collected from the coral communities and
intertidal coasts at Al-Ghardaqa harbor, Shab Abou-Sadaf, vicinity of marine Biological Station and Hur
palace village. They were collected by digging using a hammer and chisel
through snorkeling. Anemones were narcotized, in a container of sea water, by
adding magnesium sulphate crystals and fixed in 10 % formalin or hot Bouin's fluid. Paraffin sections, 5-10 um in thickness,
were stained with either Ehrlich's haematoxylin-eosin or Mallory's triple
stains.
Entacmaea quadricolor (Rueppell
& Leuckart, 1828)
Tentacles: They
are regularly arranged according to the formula: 6+6+12+24+48+96 and ranged in
number between 76 and 300. No more than one tentacle per each endocoel and exocoel. Exocoelic tentacles are marginal. Bifurcate tentacles are
present. They have a longitudinal muscle layer on the ectodermal side of the mesoglea and a circular muscle layer on its endodermal side.
Moreover, symbiotic zooxanthellae are present in the tentacular endoderm (Fig. 1).
Column: It is
devoid of verrucae and marginal spherules. The
ectodermal longitudinal muscle layer of the column extends along the whole
length. Mesoglea is thick, fibrous and highly
provided with granular and agranular cells. The
endodermal circular muscle layer is concentrated just below the margin forming
a strong diffuse to circumscript sphincter muscle (Fig.
2). The intracellular symbiotic zooxanthellae are
found in the endoderm.
Stomodaeum: It has
2-4 siphonoglyphs. Each one attached to a pair of
directive mesentery. The stomodaeal ectoderm has ciliated epithelial cells,
gland cells and nematocysts (Fig. 3).
Mesenteries: Their
number (50-85 pairs) varies with the anemone size (18-70 mm base diameter). It
differs at both ends of the column, so the number in the proximal part exceeds
that at the distal part (Table 1). Thus, development of mesenteries is upwards
and appeared as ridges lacking retractors and filaments. Retractor muscles are
restricted to diffuse with long lamellae (Fig. 4). The mesogleal
lamellae of the stronger retractors are more highly branched than those of
younger mesenteries. The parietobasilar and basilar
muscles are well developed (Figs. 4 & 5). Mesenteries of the 1st, 2nd, 3rd
and some of the 4th cycles possess filaments. At the level of the stomodaeum,
the mesenteric filaments appeared tripartite containing ciliated tracts (Fig.
6). Below the stomodaeum, the ciliated tracts are absent and the filaments
being oval shaped. Cnidoglandular tract has gland
cells and nematocysts among the endodermal epithelium.
Gonads:
Individuals are unisexual. Gonads are located on mesenteries of the 1st, 2nd
and 3rd cycles of large specimens except the directives. Oocytes (49-450 um) of
female specimens appeared oval-shaped.
Some oocytes (95
- 120 um) have a tubular structure termedd trophonema (plate 1A). Mesoglea of some
mesenteries being empty of ova suggesting the discharge of mature oocytes
(Plate 1B). On the other hand, packets of male mesenteries (120 – 178
um) contain different stages of spermatogenesis.
Cnidae: Spirocysts of the oral disc (7.7 - 36 x 2.3 - 3.9 um) are
larger than those of tentacles (9.3 - 23.3 x 2.3 - 3.7 um) in a specimen having
32 mm across the base. The large sized nematocysts (Fig. 13,i)
are obtained from the actinopharynx (10.7 - 30 x 2 -4.5
um) and mesenterial filaments (8.7 - 28.3 x 1.7 - 4.7 um).
Antheopsis crispus (Ehrenberg, 1834)
Tentacles: They
are crowed at the periphery without radial arrangement and ranged in number
from 140 to 285. Usually, one tentacle communicates with each endocoel and one per each exocoel.
Only one specimen, among the investigated samples, has two tentacles in an endocoel of the second order. Some tentacles have
perforated tips, basal buds but rarely bifurcate. A strong tentacular
retractor muscle is recognized just beneath the ectodermal nerve net of
tentacles. The endoderm of tentacles has the symbiotic zooxanthellae
as in Entacmaea quadricolor.
Column: It has
adhesive endocoelic verrucae
concentrated at its upper region. The mesoglea of the
column is thick and has condensed fibers and mesogleal
cells (Plate 1C).The endodermal circular muscle layer forms a strong
circum-script sphincter muscle (Fig. 7) in the column margin.
Stomodaeum: It has
two siphonoglyphs and devoid of stomodaeal ridges.
The mesoglea is very thick and the ciliated
ectodermal epithelium has gland cells and nematocysts.
Mesenteries: The
number of mesenteries (62-90 pairs) is usually lesser than the number of
tentacles. They grow from the proximal end upwards (Table 2). Retractors are
strong diffuse (Fig. 8). Parietobasilar muscles are
well developed with short pennon and distinct fold. Basilar muscles are
moderately strong. Mesenterial filaments have gland cells and large-sized
nematocysts and lacking zooxanthella tracts.
Gonads: Sexes
are separate. In large specimens, the mesenteries of the lst.,
2nd., 3rd. and some of the 4th. cycles are fertile except the
directives. A female gametogenic mesentery has large
oocytes (400 um) as well as cavities that represent discharged eggs. Trophonema
is observed in oocytes undergoing vitellogenesis. The mature seminiferous tubules (185 um) of a male gametogenic
mesentery contain different stages of spermatogenesis (Plate 1D).
Cnidae: Spirocysts are of moderate size (7.3 - 23.3 x 1.7 -3 um) and being
restricted only in tentacles. Nearly, nematocysts have the same size in
tentacles (11.7 - 26.7 x 1.3 -2.7um), oral disc (12.3 - 21.7 x 1.3 - 2.7 um),
column (7.3 - 2 5 x 2.7 - 4.7 um), verrucae (5 - 25 x
2.3 - 4.7 um) and actinopharynx (18 - 24.2 x 3.8 - 5.2
um ). On contrary, nematocysts (Fig. 13,ii) of the mesenterial filaments have the largest size (8.3
- 38.3 x 1.3 - 3.7 um).
Anthopleura
stellula (Ehrenberg, 1834)
Tentacles: Their
number ranged from 22 to 48 with hexamerous arrangement. Ectoderm of tentacles
is heavily loaded with spirocysts, nematocysts and
spherical gland cells. The ectodermal longitudinal muscles are highly developed
and can retract the tentacles upon disturbance, and so are termed tentacular retractors. The endoderm harbor
endosymbiotic algae; the zooxanthellae.
Column: It
bears adhesive endocoelic verrucae
(12-24 rows). The verruca (Fig. 9) is glandular
bearing spherical and elongated gland cells as well as peripheral nematocysts.
They are surmounted at the margin by imperforated acrorhagi.
The latter develop as evagination from the column wall. They contain huge
numbers of large specific nematocysts (Fig. 10) as found in the acrorhagi of Anemonia sulcata in Alexandria coasts (Ghobashy
et al., 1979). The internal cavity of the acrorhagi
is continuous with endocoels of the mesenteries.
Unlike verrucae, the ectoderm of acrorhagi
lacks gland cells, so they are not adhesive. The endodermal circular muscle
layer is concentrated just below the column margin forming the sphincter
muscle. It is a circumscribed (Fig. 11) to diffuse for retraction.
Stomodaeum: It has
many longitudinal ridges and two symmetrically situated siphonoglyphs.
Its ectoderm has ciliated epithelial cells incorporating nematocysts and ovoid
or elongated gland cells.
Mesenteries: The
number of mesenteries ranged between 18-30 pairs in the anemones measuring 3-20
mm across the base. However, this number varies at the proximal and distal ends
indicating an upward growth. Two pairs of directive mesenteries are present.
The mesenteries of the 1st, 2nd, and rarely of the 3rd, cycle are provided with
mesenterial filaments. The latter lack zooxanthellae
tract but contain gland cells and large-sized
nematocysts. The retractors are strong and generally diffuse (Fig. 12),
although others appear circumscribed diffuse or reniform. Both parietobasilar and basilar muscle are almost strong.
Gonads: Sexes
are separate. Gonads are located on mesenteries of the 1st cycle and some of
the 2nd cycle while the directives lack them. Female specimens have oocytes,
73-125 um in diameter, and male specimens have gonadal
packets, 80 - 120 um in diameter.
Cnidae: The
largest nematocysts (Fig. 13,iii) obtained from the acrorhagi (23.3 - 30 um x 2.7 - 3.5 um) are followed by
those of the mesenterial filaments (13 - 21.4 x 4 -4.7
um). Nematocysts are smaller and nearly of equal size in the column, verrucae and actinopharynx.
DISCUSSION
In spite of the presence of
huge numbers of sea anemones in the coral reefs of Al-Ghardaqa district (Red
Sea), they have never been investigated from the anatomical and histological
points of view for precise taxonomic determination. Recently, the taxonomy of
the Egyptian anemones has attracted the attention of Shoukr (1978 & 1984)
who gave a field guide for their preliminary identification based on the
morphological characters . With respect to this key,
the anemones Entacmaea quadricolor,
Antheopsis crispus and
Anthopleura stellula
were easily identified in Al-Ghardaqa. These anemones were common inhabitants
of the fringing and barrier coral reefs as well as the intertidal zone. They
were extremely abundant (especially Entacmaea
quadricolor and Antheopsis
crispus) along the reef-flat among a wide
variety of benthic invertebrates including fleshy soft corals e.g. Sarcophyton, Dendronephthya,
Heteroxenia and Xenia ;
echinoderms as the long spined sea-urchin Diadema
setosum and the large tough black sea-cucumber Holothuria marmorata
as well as the hermatypic corals Acropora,
Coeloria and Favia.
Branched colonies of the living elk-horn coral Acropora
frequently harbor large individuals of Entacmaea
quadricolor. Others were firmly attached within
coral crevices on sand reefs and usually lack the pedal disc during collection.
In the present work, the common
sea anemone Entacmaea quadricolor
showed two forms differing in size, density and habitat. The first form was
large (reached to 120 mm. at base diameter), solitary, hole-dwelling and often
deeper water living as that obtained from the barrier coral reefs of Shab Abou Sadaf.
The second form was smaller (about 25 mm. in base diameter), clustering in
small clumps at shallow water zones as found on stones in the fringing coral
reefs and intertidal region at the vicinity of the Marine Biological Station at
Al-Ghardaqa.
Careful examination of these
two forms was necessary for accurate identification, taking into consideration
the morphological variation during development. It seems that, these forms are
related to the same species and so insufficient investigation may lead to
confusion in their identification. Thus, the first form was erroneously called Radianthus gelam while
the second form was misnamed Physobrachia douglasi (Alien, 1972) or Physobrachia
ramsayi (Mariscal,1972).
These species are synonymised to the species Entacmaea
quadricolor as mentioned by Dunn (1981) in Japan.
Observations through
snorkeling, in Al-Ghardaqa coral reefs as in Shab Abou Sadaf and in vicinity of Hur
palace village, showed that the large anemones of Entacmaea
quadricolor and Antheopsis
crispus accompanied some brightly colored
fish. The latter
live
amongst the stinging tentacles without ill effects. During feeding, the fish
appears as an active hunter for its anemone partner with a small share of food.
The symbiotic association between anemones and clown fishes is well known in
the Red Sea and studied by several authors e.g. Gohar,
1934, 1948 ; Fishelson, 1964
; Schlichter, 1968 ; Mariscal,
1970 and Dunn, 1981. On the other hand, the anemone Entacmaea
quadricolor showed strong contraction on touching
without stings from their tentacles. The latter change its shape from
digitiform to bulbous form and this may be governed by sun light or presence of
anemone-fish (Gohar, 1934 ; Fishelson, 1965 and Dunn, 1981).
The investigated material of Entacmaea quadricolor resemble those described by Dunn
(1981) except some differences. The most notable of which is the presence of
fertile directives and typically diffuse sphincter muscle in Dunn's specimens.
With respect to trophonema, it appears that these tubular structures may carry nourishment
to the developing ova during vitellogenesis. Wedi and
Dunn (1983) suggested that trophonema influence the position of oocytes. Although
oocytes of Aiptasia diaphana
lack trophonema, their germinal vesicles exhibit the same orientation in the
same mesentery. Moreover, results of the present study are in accordance with
those of England (1987) who reported that Antheopsis
crispus usually lack radial rows of tentacles and
secondary tentacles. Thus, the anemone Antheopsis
crispus is not conspecific with the species which
Dunn (1981) referred to as Heteractis crispa which has multiple endocoelic
tentacles.
REFERENCES
Allen , G. R. (1972): The anemone fishes: their
classification and biology.
Neptune City, N.J.,
T.F.H. Publ., Inc. Ltd, 289 PP.
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(3)1(1):1-121.
Dunn, D.F.
(1981): The clownfish sea anemones: Stichodactylidae
(Coelenterata,
Actiniaria) and other sea anemones symbiotic with pomacentrid
fishes.
Transactions of the
American philosphical Society 71(1); 1-115.
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K. W. (1987): Certain actiniaria (Cnidaria,
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of Red Sea coral fishes.
Bull.Sea Fish.Res. Sta. Haifa 37: 11-26.
Fishelson, L. (1965):
Observations and experiments on the Red Sea anemones and their
symbiotic
fish Amphiprion bicinctus. Bull Israel Sea Fish. Res. Sta. 39:3-16.
Ghobashy, A.F.;
Abdel-Hamid, M.E. and Shoukr, F.A. (1979): Sea
anemones in
Alexandria waters. Bull. Fac.
Sci. Assiut Univ., 8(2):
77-98.
Gohar, H.A.
(1934): Partnership between fish and anemone. Nature,
134,291.
Gohar, H.A.
(1948): Commensalism between fish and anemone. Publ. Mar. Biol. Station,
Ghardaqa, 6: 35-44
Mariscal, R.N.
(1972): Behaviour of symbiotic fishes and sea
anemones. In: Behaviour of
Marine Animals, H.E..
Winn and B.L.011a,eds (New York, plenum pub. corp.),
327-360.
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Anemonenfischen. Z. Tierpsychol.
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(1978): Studies on sea anemones in Alexandria waters.
M. Sc. Thesis, Fac.
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Shoukr,
F.A. (1984): A field guide to identification of Egyptian members of actiniaria. Bull.
Fac. Sci.
Zagazig Univ., 6: 683-703.
Wedi, S.E. and Dunn, D.F. (1983): Gametogenesis and reproductive periodicity of the
subtidal sea anemone Urticina
lofotensis (Coelenterata:
Actiniaria) in
California. Biol. Bull. 165:
458-472.
LEGEND TO FIGURES AND PLATES
Entacmaea quadricolor
Fig. 1: T.S. of a
tentacle showing symbiotic zooxanthellae.
Fig. 2: T.S. of column
margin showing sphincter muscle.
Fig. 3: T.S. of
stomodaeum showing the general histological
structure.
Fig. 4: T.S. of a mesentery
showing restricted retractor
muscle and parietobasilar muscle.
Fig. 5: L.S. of
the base showing basilar muscle.
Fig. 6: T.S. of
mesenteric filament through ciliated tracts.
Antheopsis crispus
Fig. 7: L.S. through a
circumscribed sphincter muscle.
Fig. 8: T.S. of a
mesentery showing strong diffuse retractor muscle.
Anthopleura
stellula
Fig. 9 : T.S. through a verruca showing adhesive gland cells.
Fig.10: T.S. through an acrorhagus
with a battery of large
nematocysts.
Fig.11: L.S. through a circumscribed sphincter
muscle.
Fig.12: T.S. of a
mesentery showing diffuse retractor muscle.
Fig.13: Nematocysts
capsules. (i) Entacmaea
quadricolor.(ii) Antheopsis crispus
(iii) Anthopleura
stellula .A., acrorhagi
; Ac., actinopharynx ; C., column ; M.F.,
mesenteric
filament ; O.D., oral disc ; T., tentacles ; V., verrucae.
Plate 1:
Fig. A:
T.S. through mature ovum with trophonema in Entacmaea
quadricolor,
haematoxylin
and eosin, x 400.
Fig. B:
T.S. through mesenteries of Entacmaea
quadricolor showing spawned-out
oocytes, haematoxylin and eosin, x 400.
Fig. C:
T.S. through mesoglea of Antheopsis
crispus, haematoxylin and eosin, x 1000.
Fig. D: T.S. through
male gonads of Antheopsis crispus showing spermatogenesis,
haematoxylin
and eosin, x 400.
Abbreviations: b. m,
basilar muscle; c. m. f., circular muscle fibers; ca.,
cavity; ci., cilia; ci. t., ciliated tract; cn. g. t., cnindoglandular tract; ec., ectoderm ; en. , endoderm; ep. c. ,epithelial cells ; g. c., gland cell ; int. c.,
interstitial cells ; int. t., intermediate tract ; l. m. f., longitudinal
muscle fibers ; m., mesoglea; m. c., mesogleal cell ; m. f., mesogleal
fibers, me. f., mesenterial filament; nc.,
nematocyst; nu., nucleus; n. n., nerve net; o., ovum
; pb. m., parietobasilar
muscle; r. m., retractor muscle; r. t., reticular tract; s. c., sensory cell ; st., stomodaeum ; spc., spermatocyte; spg., spermatogonia; spz., spermatozoa; sph. m.,
sphincter muscle; tr., trophonema ; y. g., yolk
granules; z., zooxanthella ; z. t., zooxanthella tract.
Table (I): Variation in
number of paired
mesenteries
at base and disk with the
animal size in 10 specimens
of Entacmaea
quadricolor.
|
Base Diameter (mm.) |
No. of Mesenteries |
|
|
Base |
Disk |
|
|
18 |
58 |
50 |
|
23 |
62 |
58 |
|
30 |
62 |
52 |
|
34 |
70 |
68 |
|
A3 |
72 |
62 |
|
50 |
72 |
72 |
|
52 |
78 |
78 |
|
60 |
80 |
80 |
|
65 |
82 |
80 |
|
70 |
85 |
83 |
Table (2): Variation in number of paired
mesenteries at base and disk with
the animal size in 10 specimens
of Antheopsis
crispus.
|
Base Diameter (mm.) |
No. of Mesenteries |
|
|
Base |
Disk |
|
|
25 |
64 |
62 |
|
28 |
70 |
64 |
|
30 |
72 |
65+1 |
|
33 |
72 |
70 |
|
35 |
72 |
69+1 |
|
40 |
83+1 |
78 |
|
48 |
85 |
80 |
|
51 |
85 |
82 |
|
55 |
86 |
80+1 |
|
60 |
90 |
82+1 |
Shoukr, F. A. (1990): Actinians associated with coral reefs
at Al- Ghardaqa, Red sea. Bull. Fac. Sci., Zagazig Univ., 12 (2):
827-846.