Reproductive cycle of the broomtail wrasse, Cheilinus lunulatus inhabiting coral reef in Hurghada, Red Sea, Egypt.

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Egypt. J. Aquat. Biol. & Fish., Vol. 19, No. 1: 37-54 (2015) ISSN 1110 – 6131
www.ejabf.eg.net
Reproductive cycle of the broomtail wrasse, Cheilinus lunulatus inhabiting coral
reef in Hurghada, Red Sea, Egypt.
Ahamad M. Azab1, Mostafa A. Mousa2, Hassan M. Khalaf-Allah1and
Mosab A. M. Ali3
1- Marine Biology branch, Zoology Depart., Faculty of Science, Al-Azhar
University, Cairo, Egypt
2- National institute of Oceanography and fisheries, Alexandria
3- Marine Biology branch, Zoology Depart., Faculty of Science, Al-Azhar
University, Assiut branch.
ABSTRACT
The present study deals with demonstrate the reproductive cycle of the
broomtail wrasse, Cheilinus lunulatus which monthly collected from coral reef in Abu
Galawa lagoon, Hurghada, Red Sea, during the period from December 2011 to
November 2012. Results showed that, the averages of male and female gonado-
somatic indices (GSI) were gradually increased during spring and summer months.
Irregular trend was recorded to the female hepatosomatic index during all months of
the year. It may be due to partially spawning in this fish. Shape, weight, size, colour,
texture and structure of gonads were changed with the change of maturity stages. The
testicular activity can be classified into five stages: immature stage, stimulating
spermatogenesis, rapid spermatogenesis, mature (ripe) testis and Spent testis. Seven
stages were recognized during the ovarian activity (previtellogenesis, early-
vitellogenesis, mid-vitellogensis, late-vitellogenesis, pre-spawning, ripe and spent
stages). The testicular and ovarian developments were initiated when the day length
(photoperiod) and water temperature had begun to increase during March to April.
During May to August, however, the gradual increase of both photoperiod and water
temperature reached its maximum values, gonads had ensured completion of testicular
and ovarian development. It was concluded that Cheilinus lunulatus in Abu-Galawa
lagoon of Hurghada, partially spawned during a long spawning season, which
extended from May to October. It synchronizes between both males and females with
coordination to increasing of both photoperiod and water temperature.
Keywords: Reproductive cycle; coral reef fishes; broomtail wrasse; Cheilinus lunulatus; Hurghada.
INTRODUCTION
From the economic importance of view, the Red Sea coasts constitute a very
important sector in the Egyptian fisheries, both for significant total catch and a large
number of economically important species. Research on reef fisheries and fish
biology has a short history. Concurrently, reef fish biology flourished with numerous
academic studies of small elements of reef fish communities. Coral reefs of the Red
Sea support approximately 400 fish species which utilize corals for shelter, food
and/or breeding ground. However, a little is known about the biology of the large
variety of fish living in and around the coral reefs in the Red Sea (ERSR, 1998 and
Mohamed, 1999).
Al-Ghardaqa (Hurghada) has one of the Egyptian shores in the Red Sea. The
shore is deserted with small local settlements. Near the shore, the sea bottom
characterized by reefs, which emerge from the water or are submerged, allowing

Ahamad M. Azab et al.
38
tranquil and complete observation of this extremely rich environment. The first few
meters of the reef are the richest in life and colors, a megalopolis, where a large part
of the fish and other animals are concentrated (Randall and Heemstra, 1991; Heemstra
and Randall, 1993; Osman, 2000; Farghal, 2009; Hamed, 2009 and Abd El-Gaid,
2014). Labridae is one of the most interesting and numerically abundant families of
fish. It is very widely distributed in marine waters; mostly from the coast line to about
160 m depth on sandy bottom, shallow coral and rocky reefs. Most species of wrasse
fish are carnivorous of benthic invertebrates or fish. Some species are planktivores,
corallivores and cleaners that feed on the ectoparasites of other fish. The broomtail
wrasse, Cheilinus lunulatus is a large wrasse with a restricted distribution in the
Arabian Peninsula. It is found in the Red Sea, Horn of Africa and coasts of Yemen;
inhabiting coral reefs and adjacent rubble of sand and sea grass habitats. The
maximum age of this fish is 19 years with a rapid growth rate (in males 55 cm in TL),
it has a primary and initial color phases. It feeds mainly on hard shelled invertebrates
especially mollusks and echinoderms. This fish is protogynous and associated in
colonies of 4–8 females with a single large male (FAO, 1983; Randall, 1983; Gomon
and Randall, 1984; Lieske & Myers, 1994; Allam et al., 2005 and Khalaf Allah,
2013). Knowledges of the gonadal cycles and their functional mechanisms in fish
have essential value for the successful management of either natural fisheries or fish
farming. The histological structure and seasonal variations of the teleostean gonads
have attracted the attention of many investigations notably by Argyris (2005);
Marcano et al. (2007); Ramirez et al. (2008); Mousa (2010); Khallaf et al. (2012);
Konan et al. (2014) and Mohamed et al. (2014).
Few studies are available on the broomtail wrasse, C. lunulatus (Fisher, 1973;
Randall, 1983; Lieske & Myers, 1994 and Khalaf Allah, 2013). However, information
on the reproductive cycle of the broomtail wrasse, C. lunulatus is lacking. Therefore,
the principal objective of the present work is to provide biological informations on
reproductive cycle of the broomtail wrasse, C. lunulatus, inhabiting coral reef in
Hurghada, Red Sea, Egypt.
MATERIAL AND METHODS
Study area:
Abu Galawa lagoon is a small lagoon lies near Abu Galawa reef which
situated about 7 km NE the Marine Biological Station in Hurghada, Red Sea. The
maximum water depth ranged between 15–20m during high tide period. It is situated
between latitude 27º18\43.3\\ N and longitude 33 º48\4.7\\E. The shape of the lagoon
is generally rectangular with front-reef developed in irregular prongs in the east side.
The bottom topography is flat consisting from many faces such as biogenic sand,
algae, seagrass bed and coral reefs. Some sand mounds among the seagrass carpet are
observed and inhabited by suspension feeding burrowing crustacean, some economic
fish and few species of shells. The northern and southern sides are clearly biogenic
sand, the middle part of Abu Galawa lagoon represented by seagrass carpet about
1000 m2. The western side opened to big lagoon relatively deep than this lagoon. The
maximum coral development in the eastern side is covered by dense coral reef and the
maximum depth in this area about 15 meters (Fig. 1).

Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 39
Fig. 1: Map of the Red Sea showing the sampling area.
Environmental factors:
Surface water temperature (oC) was recorded after measuring it by using hydro
lab system, Hanna Instrument, Model: HI 9828. Day length (photoperiod) was
calculated by the “Authority of Meteorology”.
Specimens collection:
A total of 107 specimens of broomtail wrasse, Cheilinus lunulatus formed the
materials for the present study. Fish specimens were monthly collected from Abu
Galawa lagoon in Hurghada, Red Sea, during the period from December 2011 to
November 2012. Long lines net were the main fishing method used to collect the fish.
Wherever possible fish were examined fresh or preserved in 10% formalin solution
for latter examination. In the laboratory, fish were identified; total and standard
lengths were measured to the nearest millimeter and recorded. Fish were also
weighted to the nearest 0.1 gram and then the following studies were carried out.
Reproduction:
Gonado-somatic and hepato-somatic indices:
To study gonado-somatic index and hepato-somatic index, fish were wet
weighted in grams and their standard lengths were measured to the nearest millimeter
and recorded. Gonads and liver were removed and wet weighted to the nearest 0.01
gm. Gonado-somatic index (G.S.I.) and hepato-somatic indexes (H.S.I.) were
calculated for each maturity stages according to the (Sokal and Rohlf, 1969) as in the
following equations:
G.S.I. = (gm)fish ofwet weight
(gm)gonadofwet weight x 100
H.S.I. = (gm)fish ofwet weight
(gm)liver ofwet weight x 100
Maturity stages:
From the intact gonads, the maturity stages were assessed first according to
Mousa (1994). The assessments were based on the bases of seasonal changes in the
histomorphology and gonado-somatic index. The monthly percentage of each
maturity stages in males and females were calculated and recorded.

Ahamad M. Azab et al.
40
Oocyte diameter:
Oocytes were preserved immediately in saline solution, placed on a glass slide
and measured with an ocular micrometer. The diameters of the oocytes were
determined by taking the mean of the maximum and minimum diameter of only those
oocytes, which had been sectioned through the nucleus. The mean diameters of the
oocytes and nuclei were determined by measuring 15 oocytes in each examined ovary.
Gonad histology:
After examination of the gonad condition, gonads were cut into small pieces (5
mm thick) and preserved immediately in Bouin`s fluid for at least 72 hours,
dehydrated in ethyl alcohol, cleared in xylene, embedded in paraplast wax (M.P. 58
°C), sectioned at the thickness of 4-6 microns and stained with Harris`s haematoxylin
and eosin solution. Finally, the slides were microscopically examined, then
photographed and described.
RESULTS
Environmental factors:
The maximum average value of surface water temperature was recorded
during July (33.46oC) and the minimum was 20.84oC during January. The highest
value of photoperiod was recorded during August (13, 51`) and the lowest was 10,
27` during December (Table 1).
Table 1: Monthly variations of environmental factors in the water of the Red Sea, Hurgada during the
year, 2011- 2012.
Months Environmental factors
Temperature (°C) Photoperiod (h)
January 20.84 10,36`
February 21.18 11,12`
March 24.57 12.00`
April 24.59 12,48`
May 27.14 13,30`
June 29.69 13,51`
July 33.46 13,41`
August 31.97 13,06`
September 30.48 12,19`
October 27.82 11,32`
November 25.17 10,49`
December 21.4 10,27`
Gonado-somatic index and hepato-somatic index:
The averages of male and female gonado-somatic indices (GSI) were very low
in December, being 0.06 and 0.26 respectively. They gradually increased during
spring and summer months. The male GSI reached the highest value (0.32) during
September; female reached its highest value (2.54) during July. Then, the average of
GSI of each decreased during October and November (Table 2 and Fig. 2).
The average of male hepato-somatic index slightly increased during April
(1.15). The highest values of male hepato-somatic index were recorded during
October (1.19) and November (1.23) respectively. Iirregular trend was recorded to the
female hepatosomatic index during all months of the year (Table, 2 and Fig. 2).

Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 41
Table 2: Monthly variations in gonado-somatic index (G S I) and hepato-somatic index (H S I) of C.
lunulatus, collected from Red Sea, Hurghada, during the period from December 2011 to
November 2012.
Months Males Females
Fish
No. Mean ± S.D Fish No. Mean ±S.D
G S I H S I G S I H S I
December ٤0.06±0.021 0.91±0.104 ٤0.12±0.03 0.83±0.387
January ٣0.10±0.07 0.92±0.120 ٥0.26±0.079 1.22±0.268
February 2 0.07±0.007 0.86±0.127 6 0.35±0.075 1.04±0.226
March 3 0.09±0.01 0.77±0.107 5 0.40±0.219 0.80±0.170
April 3 0.13±0.00 1.15 ± 0.00 6 0.55±0.202 1.37±0.228
May 5 0.17±0.044 0.04±0.363 6 0.65±0.333 0.81±0.210
June 5 0.15±0.00 0.74 ± 0.00 11 0.99±0.595 1.22±0.304
July 3 0.29±0.225 0.90±0.783 5 2.54±1.684 1.47±0.321
August 3 0.243±0.165 1.06 ± 0.435 5 0.82±0.482 1.02±0.402
September 4 0.32±0.192 0.70±0.228 5 0.27±0.219 1.05±0.099
October 3 0.23±0.185 1.19±0.079 3 0.33±0.215 0.83±0.289
November 4 0.09±0.091 1.23±0.314 4 0.11±0.035 1.02±0.167
Fig. 2: Gonado-somatic index and hepato-somatic index of C. lunulatus, collected from Red Sea,
Hurghada, at different months during the period of study.
Gonad morphology:
The testes of male broomtail wrasse, C. lunulatus, are elongated, opaque and
have the genital blood vessel running along their inner side. The testicular lobes are
generally, equal in size, but occasionally one is shorter than the other. They are known
to remain separated from one another for almost their entire length. At the hind most
part, however, lobes are attached together to form a common spermatic duct. They are
exhibited a remarkable variations in shape, size, color and texture during the
successive developmental stages (Plate, I A).

Ahamad M. Azab et al.
42
The ovaries of female C. lunulatus (Plate, I B) are paired, elongated structures,
lying in the posterior region of the abdominal cavity and being firmly attached to the
dorsal peritoneum by the mesovarium. They are separated throughout most of their
length but they unite posteriorly for a short distance to form oviduct that open at the
tip of urinogenital papilla. The ovary of the fish is circular in cross section. The
ovaries are known to exhibit remarkable variation in shape, colour; and texture during
the successive developmental stages of fish. The size and weight of the ovaries are
found to vary greatly according to the different stages of maturity. During the early
growth phase of the fish, the ovaries appear as flaccid, delicate and translucent
structures of dull pink colour. They become much distended and large in size during
breeding period, when they take a tinge of yellow color they look like mulberry due to
the presence of large ova inside them.
Maturity stages:
The testis of male C. lunulatus can be classified according to the morphological
structure into five maturity stages. These stages are immature, premature, mature, ripe
and spent (Plate, I C). The ovary of female C. lunulatus can be classified according to
the morphological structure into seven maturity stages; these are immature,
premature, mature, prespawning, ripe, spawning and post spawning or spent (Plate, I
D).
Testicular cycle of male C. lunulatus:
Histologically, the testis of C. lunulatus is approximately tongue shaped in
transverse sections with an outer convex and inner concave side. Testis is composed
of numerous seminiferous lobules, which are held together by inter-lobular septa,
mainly of connective tissue. The lobules are varied in size, but a single layer of
fusiform boundary cells with elongated nuclei bound of each. The sperm duct is
situated in the dorsomedian side of the testis and runs throughout its length. A distinct
testicular wall of a connective tissue thin membrane also envelops the whole testis
(Plate, II A&B). Data showed that, the testicular activity can be classified into the
following five stages:
Stage I: Immature
The immature testes were filamentous in shape, thin, translucent, pale in
colour and occupy a very small proportion of the belly cavity (Plate, I C). This stage
was noticed to be concomitant with the lowest value of environmental factors
(temperature and photoperiod). It extends all over the winter and beginning of spring
with different frequencies overlapping with the other stages (Fig. 3). In this stage, the
mean GSI was 0.060.018 and HSI was 0.880.12 (Tables, 3 & 4). The testis contains
small sized lobules and a relatively large interlobular space filled with dense stroma of
connective tissue and interstitial cells. The main components of the lobules are sperm
mother cells and spermatogonia (Plate, II A&B).
Stage II: Stimulating spermatogenesis:
During this stage, the premature testes became slightly enlarged, thin, flattened
and semi-translucent (PLATE, I C). This stage extends from January to late June,
being commenced with the gradual increase in both photoperiod and water
temperature (Fig. 3). The GSI was: 0.310.41 and HSI was: 0.960.26 (Tables 3 &
4). The spermatogenic activity was obviously in progress. The size of the lobules had
noticeably exhibited a gradual increase, being accompanied by a marked reduction of
the interlobular connective tissue.

Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 43
Fig. 3: Testicular and ovarian cycles of C. lunulatus collected from Red Sea in relation to the annual
fluctuations of the day length (photoperiod) and water temperature.
Table 3: Variations in gonado-somatic index (G S I), hepato-somatic index (H S I) and oocyte diameter
of C. lunulatus, at different maturity stages.
Maturity
stages
Males Females
Fish No. Mean ± S.D Fish
No. Mean ±S.D Oocyte diameter
G S I H S I G S I H S I Range Mean ±S.D
I 9 0.06±0.018 0.88±0.12 9 0.25±0.14 1±0.19 20-90 54.6±22.39
II 7 0.31±0.41 0.96±0.26 9 0.31±0.13 0.98±0.35 100-130 114.7 ± 11.23
III 6 0.21±0.12 0.87±0.47 4 0.49±0.12 1.32±0.34 140-170 156 ± 11.81
IV 7 0.30±0.18 0.78±0.41 10 0.64±0.31 1.14±0.28 180-260 213.8 ± 24.99
V 6 0.14±0.16 0.83±0.23 16 1.04±0.92 1.17±0.34 195-360 294 ± 59.15
VI 6 2±1.29 1.17±0.21 290-390 332.5 ± 32.5
VII 6 0.12±0.04 1.06±0.38
Table 4: Monthly variations in maturity stages of C. lunulatus, collected from Red Sea, Hurghada,
during the period from December 2011 to November 2012.
Months Males Females
Fish
No. Maturity stages Fish
No. Maturity stages
I II III IV V I II III IV V VI VII
December 4 100 - - - - 4 100 - - - - - -
January 3 66.6 33.3 - - - 5 80 20 - - - - -
February 2 50 50 - - - 6 66.7 33.3 - - - - -
March 3 33.3 66.7 - - - 5 - 40 40 20 - - -
April 3 - 66.7 33.3 - - 6 - 16.6 16. 7 50 16.6 - -
May 5 - 40 40 20 - 6 - - - 16.7 66.6 16.6
June 5 - 20 50 20 20 11 - - 18.2 45.4 27.3 9.1
July 3 - - 33.3 33.3 33.4 5 - - - 20 40 20 20
August 3 - - 33.3 33.3 33.4 5 - - - 20 40 20 20
September 4 - - 25 50 25 5 - - - - 20 40 40
October 3 - - - 33.3 66.7 3 - - - - 33.3 33.3 33. 4
November 4 - - - 25 75 4 - - - - - - 100

Ahamad M. Azab et al.
44
Moreover, most of the tesrticular lobules became filled with cysts of different
stages of spermatogenesis. However, the predominance of spermatocytes and
appearance of spermatids particularly characterized this stage. Small clusters of
spermatozoa are seen. However, spermatogenesis does not appear to have taken place
simulataneously in all the seminiferus lobules. The interstitial cells are comparatively
abundant in the connective tissue matrix between the lobules. The lobule boundary
cells are seen along the boundaries of the lobules (P Plate, II C).
Stage III: Rapid spermatogenesis:
In this stage, the mature testes lost their translucency and exhibited a pink
colour, owing to their increased vascularity as they also manifested marked increases
of both weight and volume (PLATE, I C). This stage extends from late April to
September, when a gradual increase of both photoperiod and water temperature (Fig.
3). GSI was 0.210.12 and HSI was 0.870.47 (Tables 3&4). In this stage, the
diameter of the seminiferous lobules increased and spermatogenic activity reaches its
peak and the lobules became filled with cysts of all spermatogenic stages. They are
separated from each other by a thin layer of interlobular connective tissue.
Furthermore, this stage was characterized by the predominance of spermatids and
spermatozoa (Plate, II D).
Stage IV: Ripe testis
The ripe testes appeared opaque, milky white, smooth and crumbled in texture.
Milt could be easily extruded from the fish by gentle pressure on their bellies (Plate, I
C). These testes were observed to have tremendously enlarged in size to the extent
that they had almost filled the whole belly cavity. The ripening period was noticed to
start concomitant with the increase of both the photoperiod and water temperatures,
which extends from Mid-May to November (Fig. 3). GSI was 0.300.18 and HIS was
0.780.41 (Tables 3 & 4). The diameters of the testicular lobules attained their
maximum width. The interlobular spaces appeared to be thicker than the previous
ones. Testicular lobules were almost fully packed with mature spermatozoa. Active
spermatogenic process is still visible in some lobules. Clusters of spermatids were
observed at the margins of lobules. Spermatogonia and spermatocytes are completely
absent (Plate, II E).
Stage V: Spent testis
The testes become thin, translucent and yellowish in colour. Their weights are
relatively reduced (Plate, I C). This stage extends from late June to November, when
the values of both photoperiod and water temperature are gradually decreased (Fig. 3).
GSI was 0.140.16 and HSI was 0.830.23 (Tables 3 & 4). It was detected markedly
by almost total cessation of spermatogenic activity and an increase in the interlobular
space of connective tissue. The testicular lobules are diminished in sizes and their
walls became thick, due to the contraction of their contents. Residual sperms, not
expelled during the spawning stage, were abundantly present in a few lobules (Plate,
II F).
Ovarian cycle in female C. lunulatus:
In cross section, the ovary of C. lunulatus appeared circular in shape and limited
by a distinct wall. The germ mother cells or oogonia are commonly found in groups or
nests in the outer cortical regions of the ovary. These oogonia are essentially
responsible for producing the successive developmental stages of the eggs or oocytes.
However, the whole process is known collectively as oogenesis (Plate, III A).
Seven stages of the ovarian development were recognized on the basis of the
morphological and histological appearance of the ovaries, frequency of occurrence as
well as the duration of the different developmental stages of the oocytes and the

Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 45
corresponding values of the gonadosomatic index and hepatosomatic index (Tables 3
& 4). These stages were noticed to include previtellogenesis, early-vitelloogenesis,
mid-vitellogenesis, late-vitellogenesis, pre-spawning, spawning (ripe) and spent.
Stage I: Previtellogenesis
The ovary appeared small in size, translucent, slightly fleshy in colour and
occupied a small area of the body cavity (Plate, I D). This stage was noticed to be
concomitant with the lowest values of environmental factors (temperature and
photoperiod), which extend from December to late February (Fig. 3). The mean GSI
was 0.250.14 and HSI was 10.19 (Tables 3 & 4). The oocytes were apparently
representing the primary oocyte stages (Plate III, A).
Stage II: Early vitellogenesis
The ovaries appeared increase in volume than the preceding stage, occupying
nearly half of the body cavity and their colour was in transition from reddish to
yellowish colour (Plate, I D). This stage extends from late January to late April (Fig.
3). GSI was 0.310.13 and HSI was 0.980.35. The diameter of the oocytes in the
ovaries ranged from 100 to130m. (Tables 3 & 4). This stage marks the beginning of
yolk deposition which was characterized by the appearance of minute spherical yolk
granules (protied yolk) in the outer layer of the cytoplasm of the bitinctorial oocytes;
being synchronized with the prevalence of a ring of oil droplets around the nucleus.
Most of the oocytes in the early vitellogenic ovary are considered to represent the
vesicles or primary yolk stages, owing to the presence of small cytoplasmic vesicles
(Plate, III B).
Stage III: Mid- vitellogenesis
The ovaries acquired a yellowish colour and occupying more than half of the
body cavity (Plate, I D). This stage extends from March to April; when photoperiod
and water temperature are gradually increase (Fig. 3). GSI was 0.490.12 and HSI
was 1.320.34. Oocyte diameter varied from 140 to 170m (Tables 3 & 4). Most of
the oocytes were seen in the primary yolk stages (Plate, III C).
Stage IV: Late- vitellogenesis
The ovaries occupied nearly the entire length of the body cavity. They
exhibited a yellowish colour with more or less turgid structure (Plate, I D). This stage
extends from late March to early August. During this period, photoperiod and water
temperatures are gradually increased (Fig. 3). GSI was 0.640.31 and HSI was
1.140.28. Oocyte diameter ranged from 180 and 260m (Tables 3 & 4). The oocytes
were apparently belonging to the secondary yolk stage (Plate, III D).
Stage V: Pre- spawning
The ovaries were fully distended, occupying nearly the entire body cavity and
exhibiting a translucent golden appearance (Plate, I D). This stage extends from mid-
April to October. This stage accompanied with the successive fall for both
photoperiod and water temperatures (Fig. 3). The mean of GSI was 1.040.92 and
HSI was 1.170.34. Oocyte diameter ranged between 195 and 360 m (Tables 3 & 4).
Most of the oocytes belonged to the tertiary yolk stage (Plate, III, E).
Stage VI: Spawning (Ripe)
The ovaries were completely fully distended. They occupy all the body cavity
and exhibited clear golden appearance (PLATE, I D). This stage extends from late
May to early October and accompanied with the successive maximum values of
photoperiod and water temperatures (Fig. 3). The mean GSI was 21.29 and HSI was
1.170.21. Oocyte diameter ranged between 290 and 390m (Tables 3 & 4). Most of
the ripe oocytes are mainly belonged to the tertiary yolk stage (Plate, III F).

Ahamad M. Azab et al.
46
Stage VII: Post-spawning (Spent):
The ovaries were small in size, reddish in colour and flaccid in appearance with
a thickned ovarian wall (Plate, I D). This stage extends from June to early November,
before the decline of both photoperiod and water temperature to the minimum values
(Fig. 3). The mean GSI was 0.120.04 and HSI was 1.060.38 (Tables 3 & 4). A
great number of deformed oocytes and remains of empty follicles can be observed.
DISCUSSION
In the present study the monthly changes in the maturity stages and gonado-
somatic index (GSI) for males and females indicated that, the spawning period
occurred between May to October. This agrees with most summer spawning fish
recorded by Shenouda et al. (1995) on Clarias lazera; Allam (1996) on Trachinotus
ovatus; Jenny et al. (2007) on Brotula clarkae; Khalaf Allah (2009) on Terapon puta
& Lithognathus mormyrus and Mohamed et al. (2014) on Euthynnus alletteratus.
In the present study, the testes are made up of a plentiful numbers of
seminiferous lobules. The latter's are bound together by means of a thin connective
tissue. Both interstitial (leydig cells) and sertoli cells are present in the testes of the
fish examined. Sertoli cells often occur in close proximity to the developing germ
cells. The interstitial cells are distributed around the sperm duct as well as in between
the testicular lobules. They attain their maximum development during ripeness and
before spermiation. The signs of maximal activity of the interstitial cells were
manifested by the remarkable increase of their number (hyperplasia) and of their size
(hypertrophy). The present study indicated that, the interstitial cells are homologous
with mammalian leydig cells and are the major site of androgen synthesis. Similar
observations were detected by many investigators notably Yoneda et al. (1998),
Mousa and Mousa (1999), Kokokiris et al. (2000), Khalil (2001), Albattal (2002), El-
Greisy (2005 a & b), Marcano et al. (2007) and Khalaf Allah (2009).
Seasonal variations in shape, volume and weight of the testes and ovaries of C.
lunulatus are obviously correlated with the degree of the fish maturity. Gonado-
somatic index (GSI) was increases gradually accompanying the maturation of gonads.
Similar observations were reported by Mousa and Mousa (1999a), Kokokiris et al.
(2000), Loir et al. (2001), Albattal (2002) Moharram (2003), El-Agamy et al. (2004),
El-Greisy (2005 a & b), Marcano et al. (2007) and Khalaf Allah (2009).
Junk (1999) concluded that spawning in fish can be affected by several different
environmental factors; temperature and photoperiod influence fish reproduction by
stimulating sensory organs that induce the production of gonad hormones, which can
induce physiological or behavioral responses. The present study indicated that, such
factors affect spermatogenesis, oogenesis, gonad maturation and spawning in C.
lunulatus.
Environmental cues, such as photoperiod and temperature cycles, synchronize
the internal timing system that controls breeding, control of final gamete maturation,
ovulation and spawning. It has a very marked effect on the physiological and
biochemical processes in fish, and a raised temperature regime has complex effects on
fish reproductive, nerve and endocrine systems (Pankhurst et al., 1996; Luksiene and
Svedang, 1997; Bromage et al., 2001; Kirschbaum and Schugardt, 2002; Rad et al.,
2006; Wilkinson et al., 2010; Oliveira et al., 2011). Additional factors such as food
availability and salinity of the water may play certain critical roles in the timing of
teleost reproduction (Micale et al., 1987; Khalil, 2001 and Khalaf Allah (2009).

Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 47
Seven successive stages of ovarian development (previtellogenic, early-
vitellogenic, mid-vitellogenic, late-vitellogenic, pre-spawning or ripe, spawning and
post-spawning) were observed in the ovaries of these fish. These findings are similar
to those reported by Greeley et al. (1987); Mousa (1994); Merson et al. (2000); Khalil
(2001); Albattal (2002) and Khalaf Allah (2009).
The first stage (previtellogenesis) is characterized by the presence of
previtellogenic oocytes less than the minimum vitellogenic size of 30 - 40 m in
diameter. It is not dependent upon the environmental factors (temperature and
photoperiod). Therefore, it had extended throughout the whole year with different
frequencies overlapping with the other stages.
The vitellogenesis (yolk deposition) occurred at the ovarian stage II (early-
vitellogensis) and vitellogenic stages III, IV and V (mid-; late-vitellogenesis; pre-
spawning) are commenced concomitant with the gradual increase of both photoperiod
and water temperatures. It is generally accepted that photoperiod and temperature are
the two major environmental factors that mediate reproductive activities in fish.
Similar observations were recorded by Lam (1983); Johnston et al. (1987); Albattal
(2002) and Khalaf Allah (2009).
In the pre-spawning stage, most of the oocytes belonged to the tertiary yolk
stage. The oil droplets coalescence and become less in number, i. e. the presence of
some droplets of fat inside the mature oocytes. Pajuelo et al. (2008) mentioned that,
the presence of a large droplet of fat inside the mature oocytes indicates the pelagic
character of its spawning.
The ovarian stage VI (spawning or ripe stage) was observed during the
maximum values of both photoperiod and water temperatures. The spawning females
are characterized by the presence of ripe oocytes. As the spawning occurs during the
reaching of photoperiod and water temperatures to its maximum values, the ovarian
stage VII (post-spawning) extends from late June to early November. Similar
observations were detected by Albattal (2002) and Khalaf Allah (2009).
From the present study, it was clear that, Cheilinus lunulatus exhibited one
spawning season in a year. Maturity peak extended from May to October. The
population of C. lunulatus in Abu-Galawa lagoon at Hurghada, starts spawning during
the late of spring season and continue till the summer with synchronization between
both males and females and increasing of both photoperiod and water temperature.
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Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 51
Plate I
Plate I: General morphology of C. lunulatus gonads.
A: General structure male testis
B: General structure female ovary
C: Male maturity stages; A- Immature, B- Premature, C-Mature, D-Ripe and E-Spent.
D: Female maturity stages; A- Immature, B- Premature, C-Mature, D- prespowning, E-Ripe, F-
Spawning and G- Spent.

Ahamad M. Azab et al.
52
Plate II
Plate II: Photomicrographs of histological sections in testis of male C. lunulatus:
(A): T.S. in immature testis, showing the testicular wall (TW), spermatic duct (SD).
(B): Enlarged portion of previous T.S., displaying interlobular septum (ILS) between seminiferous
lobules.
(C): T.S. in stimulating spermatogeneic testis, showing sperm mother cells (SMC), spermatogonia (SG),
primary spermatocytes (PSC) and secondary spermatocytes (SSC).
(D): T.S. in rapid stimulating spermatogenic testis, showing primary spermatocytes (PSC), secondary
spermatocytes (SSC), spermatids (ST), interstitial cells (ISC), Sertoli cells (SC).
(E): T.S. in ripe testis, showing Interstitial cells (ISC), Sertoli cells (SC) and spermatozoa (SZ).
(F): T.S. in spent testis showing empty spaces inside seminiferous lobules.

Reproductive cycle of the C. lunulatus inhabiting coral reef in Hurghada, Red Sea 53
Plate
III
Plate III: Photomicrographs of histological sections in ovaries of female C. lunulatus:
(A): T.S. in pre-vitellogenic stage showing ovarian wall (OW), primary oocyte (PO) and the ovigerous
lamellae (OL).
(B): T.S. in early-vitellogenic stage, showing vesicle oocyte (VO), including oil vesicles (OV) and
large nucleus (N).
(C): T.S. in mid-vitellogenic stage, showing oil vesicles (OV), yolk globules (YG) and large nucleus
(N) in the primary yolk oocyte (PYO) and thick wall; theca layer (TH), granulosa (G) and
zona radiata (ZR).
(D): T.S. in late-vitellogenic stage, showing the secondary yolk oocyte (SYO) and primary yolk oocyte
(PYO).
(E): T.S. in pre-spawning stage, showing the tertiary yolk oocyte (TYO).
(F): T.S. in spawning ovary, showing homogenized yolk globules (HYG) in ovulated eggs.

Ahamad M. Azab et al.
54
ARABIC SUMMARY
ةروﺪﻟاﻼﻤﻟا كﺎﻤﺳﻷ ﮫﯿﻠﺳﺎﻨﺘﻟاصﺔﻗدﺮﻐﻟﺎﺑ ﺔﯿﻧﺎﺟﺮﻤﻟا بﺎﻌﺸﻠﻟ ﺔﻨطﺎﻘﻟا-ﺮﻤﺣﻷا ﺮﺤﺒﻟا-ﺮﺼﻣ بﺰﻋ ﺪﻌﺴﻣ ﺪﻤﺣأ
١
-ﻰﺳﻮﻣ ﻰﻔﻄﺼﻣ
٢
-ﷲ ﻒﻠﺧ ﺪﻤﺤﻣ تﻮﺤﺸﻣ ﻦﺴﺣ
١
-ﻰﻠﻋ ﺪﻤﺤﻣ ﻰﻠﻋ ﺐﻌﺼﻣ
٣
١- كﺎﻤﺳﻷاو رﺎﺤﺒﻟا مﻮﻠﻋ ﺔﺒﻌﺷ-ناﻮﯿﺤﻟا ﻢﻠﻋ ﻢﺴﻗ - مﻮﻠﻌﻟا ﺔﯿﻠﻛ)ﻦﯿﻨﺑ(-ةﺮھﺎﻘﻟا ،ﺮھزﻷا ﺔﻌﻣﺎﺟ ٢-ﺳﺎﻨﺗ ﻞﻤﻌﻣﺔﯾرﺪﻨﻜﺳﻹا ،ﺪﯾﺎﺼﻤﻟاو رﺎﺤﺒﻟا مﻮﻠﻌﻟ ﻰﻣﻮﻘﻟا ﺪﮭﻌﻤﻟا ،كﺎﻤﺳﻷا ﺦﯾﺮﻔﺗو ﻞ ٣-كﺎﻤﺳﻷاو رﺎﺤﺒﻟا مﻮﻠﻋ ﺔﺒﻌﺷ -ناﻮﯿﺤﻟا ﻢﻠﻋ ﻢﺴﻗ - مﻮﻠﻌﻟا ﺔﯿﻠﻛ)ﻦﯿﻨﺑ( -طﻮﯿﺳأ عﺮﻓ ،ﺮھزﻷا ﺔﻌﻣﺎﺟ
ﻦﻣ ﺪﯾﺪﻌﻟا ﺔﯿﺑﺮﺘﻟ ﺐﺳﺎﻨﻣ ﻲﺌﯿﺑ ﻦطﻮﻣ ﺮﻤﺣﻷا ﺮﺤﺒﻠﻟ ىﺮﺼﻤﻟا ﻞﺣﺎﺴﻟا ﻰﻓ ﺔﯿﻧﺎﺟﺮﻤﻟا بﺎﻌﺸﻟا ﺔﺌﯿﺑ ﺮﺒﺘﻌﺗ ﻤﺳﻷاصﻼﻤﻟا كﺎﻤﺳأ ﺎﮭﻨﻣو ةﺮﯿﺒﻜﻟا ﺔﯾدﺎﺼﺘﻗﻻا ﺔﻤﯿﻘﻟا تاذ كﺎ . ﮫﯿﻠﺳﺎﻨﺘﻟا ةروﺪﻟا ﺔﺳارد ﻰﻟإ ﺚﺤﺒﻟا اﺬھ فﺪﮭﯾ صﻼﻤﻟا كﺎﻤﺳﻷ)ﺲﺗﻻﻮﯿﻨﯿﻟ ﺲﻨﯿﻠﺳ( ،ةوﻼﺟﻮﺑأ ﺔﻧﻮﺠﺑ ﺔﯿﻧﺎﺟﺮﻤﻟا بﺎﻌﺸﻟا ﻦﻣ ﺔﯾﺮﮭﺷ ﺔﻔﺼﺑ ﺎﮭﻌﯿﻤﺠﺗ ﻢﺗ ﻲﺘﻟاو ،
ﺮﺒﻤﺴﯾد ﻦﻣ ةﺮﺘﻔﻟا لﻼﺧ ﺮﻤﺣﻷا ﺮﺤﺒﻟا ،ﺔﻗدﺮﻐﻟا٢٠١١ ﺮﺒﻤﻓﻮﻧ ﻰﻟإ٢٠١٢م
. ﺒﺗ ﺔﯿﺠﯾرﺪﺗ ةدﺎﯾز دادﺰﺗ ثﺎﻧﻹاو رﻮﻛﺬﻠﻟ ﻰﻠﺴﻨﻤﻟا ىﺪﺴﺠﻟا ﻞﻣﺎﻌﻤﻟا تﺎﻄﺳﻮﺘﻣ نأ ﺔﺳارﺪﻟا هﺬھ ﻦﻣ ﻦﯿ
مﺎﻌﻟا ﺮﮭﺷأ ﻢﻈﻌﻣ لﻼﺧ ﺔﻤﻈﺘﻨﻣ ﺮﯿﻏ ثﺎﻧﻺﻟ ىﺪﺒﻜﻟا ىﺪﺴﺠﻟا ﻞﻣﺎﻌﻤﻟا تﺎﻄﺳﻮﺘﻣو ﻒﯿﺼﻟاو ﻊﯿﺑﺮﻟا ﺮﮭﺷأ لﻼﺧ . لﻼﺧ ﺔﯿﻟﺎﺘﺘﻣ تاﺮﺘﻓ ﻰﻠﻋ ﺾﯿﺒﻟا ﻊﻀﺗ كﺎﻤﺳﻷا هﺬھ نأ ﻰﻟا ﻚﻟذ ﻰﻓ ﺐﺒﺴﻟا ﻊﺟﺮﯾ ﺎﻤﺑرﺮﺛﺎﻜﺘﻟا ﻢﺳﻮﻣ.
عﻮﻨﺗ نأ ىﺪﺒﻜﻟاو ﻰﻠﺴﻨﻤﻟا ﻞﯿﻟﺪﻟاو ﻞﺳﺎﻨﻤﻠﻟ ﻰﺟﻮﻟﻮﺘﺴﮭﻟا ﺐﯿﻛﺮﺘﻟا ،ىﺮھﺎﻈﻟا ﻞﻜﺸﻟا ﺔﺳارد ﺖﺤﺿوأ
فﻼﺘﺧﻹا تﺎﺟرد ﻰﻓ ﺞﻀﻨﻟا ﻞﺣاﺮﻣ ﻖﻓاﻮﯾ ﻞﺳﺎﻨﻤﻟا ماﻮﻗو نﻮﻟو نزوو ﻢﺠﺣو ﻞﻜﺷ . ﻞﺣاﺮﻣ ﺲﻤﺧ ﺰﯿﯿﻤﺗ ﻦﻜﻣأ ﻰھو ﮫﯿﺼﺨﻟا طﺎﺸﻨﻟ :ﺔﻌﯾﺮﺴﻟا ﮫﻠﺣﺮﻤﻟا ،ﺰﯿﻔﺤﺘﻟا ﺔﻠﺣﺮﻣ ،نﻮﻜﺴﻟا ﺔﻠﺣﺮﻣ ﺪﻌﺑ ﺎﻣ ﺔﻠﺣﺮﻣو جواﺰﺘﻟا ﺔﻠﺣﺮﻣ ،رﻮﻄﺘﻠﻟ جواﺰﺘﻟا .ﻰھو ﺾﯿﺒﻤﻟا طﺎﺸﻨﻟ ﻞﺣاﺮﻣ ﻊﺒﺳ ﺰﯿﯿﻤﺗ ﻦﻜﻣأ ﻚﻟﺬﻛو : ةﺮﻜﺒﻤﻟا ﺔﻠﺣﺮﻤﻟا ،ﺢﻤﻟا ﺐﯿﺳﺮﺗ ﻞﺒﻗ ﺎﻣ ﺔﻠﺣﺮﻣ
،جواﺰﺘﻟا ﻞﺒﻗ ﺎﻣ ﺔﻠﺣﺮﻣ ،ﺢﻤﻟا ﺐﯿﺳﺮﺘﻟ ةﺮﺧﺄﺘﻤﻟا ﺔﻠﺣﺮﻤﻟا ،ﺢﻤﻟا ﺐﯿﺳﺮﺘﻟ ﺔﻄﺳﻮﺘﻤﻟا ﺔﻠﺣﺮﻤﻟا ،ﺢﻤﻟا ﺐﯿﺳﺮﺘﻟ
ﺪﻌﺑ ﺎﻣ ﺔﻠﺣﺮﻣو جواﺰﺘﻟا ﺔﻠﺣﺮﻣجواﺰﺘﻟا .
ةءﺎﺿﻹا ةﺮﺘﻓ ةدﺎﯾزو ءﺎﻤﻟا ةراﺮﺣ ﺔﺟرد عﺎﻔﺗرا ﺔﯾاﺪﺑ ﻊﻣ ﺾﯿﺒﻤﻟاو ﺔﯿﺼﺨﻟا طﺎﺸﻧ أﺪﺒﯾ) سرﺎﻣ-ﻞﯾﺮﺑإ .( لﺪﻌﻣ ﻰﺼﻗأ ﻰﻟإ ةراﺮﺤﻟا ﺔﺟردو ةءﺎﺿﻹا ةﺮﺘﻓ ﻦﻣ ﻞﻛ لﻮﺻو ﺪﻨﻋ ﻞﺳﺎﻨﻤﻟا رﻮﻄﺗ ﻞﻤﺘﻜﯾو ﺎﻤﮭﻟ)ﻮﯾﺎﻣ -ﺲﻄﺴﻏأ( ؛ إ ﻰﻟﺎﺘﻟﺎﺑو ﺾﯾﺎﺒﻤﻟاو ﻰﺼﺨﻟا ﻦﻣ ﻞﻛ طﺎﺸﻧ ةدﺎﯾز ﻰﻠﻋ ﻞﻤﻌﺗ ﻲﺘﻟاوﺮﺛﺎﻜﺘﻟا ﺔﯿﻠﻤﻋ مﺎﻤﺗ . ﮫﺻﻼﺨﻟا:
ﻲﻟا ﻮﯾﺎﻣ ﻦﻣ هﺮﺘﻔﻟا لﻼﺧ ﺎﮭﺗورز ﻎﻠﺒﺗ ﻲﺘﻟاو مﺎﻌﻟا ﻰﻓ هﺪﺣاو هﺮﻣ ﺮﺛﺎﻜﺘﻟا ﺔﯿﻠﻤﻌﺑ مﻮﻘﺗ صﻼﻤﻟا كﺎﻤﺳا نأ
ﻢﺳﻮﻣ ﺔﯾﺎﮭﻧ ﻦﻣ ةﺮﺘﻔﻟا لﻼﺧ ﺾﯿﺒﻟا ﻊﺿو ﻲﻓ أﺪﺒﺗ اوﻼﺟﻮﺑأ ﺞﯿﻠﺨﻟ ﺔﻨطﺎﻘﻟا صﻼﻤﻟا كﺎﻤﺳأ داﺮﻓأ ﻊﯿﻤﺟو ﺮﺑﻮﺘﻛأ
ﻒﯿﺼﻟا ﻢﺳﻮﻣ ﺔﯾﺎﮭﻧ ﻲﺘﺣو ﻊﯿﺑﺮﻟا عﺎﻔﺗراو هءﺎﺿﻻا هﺮﺘﻓ هدﺎﯾز ﻦﻣ ًﻼﻛ ﻊﻣ ثﺎﻧﻻاو رﻮﻛﺬﻟا ﻦﯿﺑ ﻦﻣاﺰﺘﻟﺎﺑ ﻚﻟذو راﺮﺤﻟا تﺎﺟردة.