Scholarly article on topic 'Reproductive periodicity of sea cucumber Bohadschia vitiensis (Echinodermata: Holothuroidea) in Hurghada area, Red Sea, Egypt'

Reproductive periodicity of sea cucumber Bohadschia vitiensis (Echinodermata: Holothuroidea) in Hurghada area, Red Sea, Egypt Academic research paper on "Biological sciences"

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Abstract of research paper on Biological sciences, author of scientific article — H.A. Omar, F.A. Abdel Razek, S.H. Abdel Rahman, N.A. El Shimy

Abstract Sea cucumbers form an important part of multispecies fisheries existing for over 1000years along the Indo-Pacific region. The “beche-de-mer”, is considered as a good source of income for fishermen and has an important role in the benthic community. A small scale sea cucumber fishery began on Red Sea Coast, by the year 2000. This fishery had expanded dramatically, leading to over exploitation. The sea cucumber Bohadschia vitiensis is currently one of the most valuable species recorded in Egyptian Red Sea Water especially in Hurghada area. The present study is concerned with reproduction of this species. Samples were collected monthly, between March, 2003 and February 2004, at Hurghada area. Gonad index and macroscopic examination were estimated for each individual gonad. Gametogenesis began in May and peak of spawning occurred in June and July in males and females. The gonad index correlated significantly with gonad tubule length and diameter. This is considered a good predictor of sexual maturity and reproduction. The gonad index showed a significant correlation with temperature which may play a role in controlling reproduction. The minimum biological size was 24.5cm and 26.1cm for males and females, respectively. There was a shift in sex ratio from 1:1 to a significant rise in number of males throughout the sampling period. This species is considered as a summer spawner as most of Egyptian tropical sea cucumber species of Red Sea.

Academic research paper on topic "Reproductive periodicity of sea cucumber Bohadschia vitiensis (Echinodermata: Holothuroidea) in Hurghada area, Red Sea, Egypt"

Egyptian Journal of Aquatic Research (2013) 39, 115-123

National Institute of Oceanography and Fisheries Egyptian Journal of Aquatic Research

Egyptian Journal of Aquatic Research

http://ees.elsevier.com/ejar www.sciencedirect.com

FULL LENGTH ARTICLE

Reproductive periodicity of sea cucumber Bohadschia vitiensis (Echinodermata: Holothuroidea) in Hurghada area, Red Sea, Egypt

H.A. Omar a, F.A. Abdel Razek a *, S.H. Abdel Rahman a, N.A. El Shimy b

a National Institute of Oceanography and Fisheries, Kayet Bay, Alexandria, Egypt b Zoological Department, Faculty of Science, Assiut University, Egypt

Received 18 June 2013; accepted 26 June 2013 Available online 9 August 2013

Abstract Sea cucumbers form an important part of multispecies fisheries existing for over 1000 years along the Indo-Pacific region. The "beche-de-mer'', is considered as a good source of income for fishermen and has an important role in the benthic community. A small scale sea cucumber fishery began on Red Sea Coast, by the year 2000. This fishery had expanded dramatically, leading to over exploitation. The sea cucumber Bohadschia vitiensis is currently one of the most valuable species recorded in Egyptian Red Sea Water especially in Hurghada area. The present study is concerned with reproduction of this species. Samples were collected monthly, between March, 2003 and February 2004, at Hurghada area. Gonad index and macroscopic examination were estimated for each individual gonad. Gametogenesis began in May and peak of spawning occurred in June and July in males and females. The gonad index correlated significantly with gonad tubule length and diameter. This is considered a good predictor of sexual maturity and reproduction. The gonad index showed a significant correlation with temperature which may play a role in controlling reproduction. The minimum biological size was 24.5 cm and 26.1 cm for males and females, respectively. There was a shift in sex ratio from 1:1 to a significant rise in number of males throughout the sampling period. This species is considered as a summer spawner as most of Egyptian tropical sea cucumber species of Red Sea.

© 2013 Production and hosting by Elsevier B.V. on behalf of National Institute of Oceanography and

Fisheries.

KEYWORDS

Sea cucumber B. vitiensis; Population analysis; Maturity stages; Spawning periodicity

Corresponding author. Tel.: +20 1006620222. E-mail address: Fatma_abdelrazek@hotmail.com (F.A. Abdel Razek). Peer review under responsibility of National Institute of Oceanography and Fisheries.

Introduction

Holothurians (sea cucumber) have been harvested for hundreds of years in many nations of the western Indian Ocean. An increasing demand to supply the global market, has led to unsustainable fishing and over-exploitation of natural stocks (Marshall et al., 2001; Lovatelli et al., 2004; Conand

1687-4285 © 2013 Production and hosting by Elsevier B.V. on behalf of National Institute of Oceanography and Fisheries. http://dx.doi.Org/10.1016/j.ejar.2013.06.002

and Muthiga, 2007; Conand, 2008) for this reason effective conservation measures, become necessary.

After the depletion of sea cucumber fisheries in other parts of the world, a small-scale sea cucumber fishery began in Egypt in 1998 on the southern part of Red Sea coast. By 2000, the sea cucumber fishery in Egypt had increased greatly as a result of the high demand for beche-de-mer and the high prices paid for it (Lawrence et al., 2004). Evidence from the study of Ahmed and Lawrence (2007) indicates that four years after the ban of the fishery in Egyptian Red Sea, sea cucumber, there is evidence that some commercial species are returning to some of the sites, but there is no evidence of stock recovery.

Holothuroid fauna of the Red Sea attracted attention of many investigators for many years ago. The various habitats of the Red Sea from Cherbonnier (1955) till Hassan (2001) recorded 98 holothuroid species, including the presence of the present studied species Bohadschia vitiensis. Omar (2006) in his biological and ecological studies of Red Sea holothurian species mentioned that B. vitiensis is one of the important three species in Hurghada area of Red Sea.

Maturation and population spawning periodicity of most commercial species in Egyptian Red Sea fisheries are badly known. Adopting an effective management plan such as aquaculture, sea ranching and restocking are measures to be taken as a direct solution to wild sea cucumber. The present study deals with gonad maturations, size at first sexual maturity

and determination of spawning periodicity of B. vitiensis which is one of these important sea cucumber species in Hurghada area of Red Sea, Egypt.

Materials and methods

Area of study and sampling

The Red Sea is located between Asia and Africa. In the north it splits from the Sinai Peninsula and stretches over 1000 miles south to join the Indian Ocean between Ethiopia and Yemen. The peninsula is bordered by the relatively shallow Gulf of Suez along its west side, and the much deeper Gulf of Aqaba along its east side. South wards, the partly very deep main body of the Red Sea extends down to its shallow and narrow exit to the Indian Ocean, at Bab El-Mandab.

The Egyptian coast of the Red Sea is approximately 1000 km extending from Suez at the entrance of the Gulf of Suez to Shalatein on the Sudanese border and west into the Gulf of Aqaba. The Red Sea is divided into 2 main sectors. The first sector starts from Taba to Sharm El-Sheikh on the Sinai Peninsula. The second sector passes from north Hurghada south to the Sudanese border and included a number of offshore islands Map 1.

■o > 60 -D C

a ¿0 o

*----• Female

o-o Hale / /' ji Pi

_ T / 1 /

- A / 1

I 1 1 l 1 1 1 • / / .

n' 1 1 1 ' 1 * i : i i i i i I i i i i i i i i i i

tr 1/1 «I

Average total length (cm) Figure 3 Size at first sexual maturity of B. vitiensis.

0 -I-,-,-T

% % <5 ,<5 % % <5 ,<5 ..<5 % % <5 ,<5 % % %

llWillllh-

V V V V T.L (cm)

Figure 2 Length frequency distribution of Bohadschia vitiensis populations during the period of study.

<Xt f<0

Females Males

Figure 4 Monthly variations in G.S.I. of females and males of B. vitiensis.

13 1.5"

i/i 1(1 -

Autumn

• •m X •

•• •:» i

Winter

t^h««^! X<

~i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i—i

Spring

19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42

Summer

-X-»-

19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 Total length (cm)

• male x female

Figure 5 Seasonal variation in G.S.I. of B. vitiensis.

Figure 6 (A and B) Size distribution of different maturity stages of male (Bohadschia vitiensis) in Red Sea.

Sampling sites

For the present study, three different sites in the shallow tidal flat of Hurghada, were chosen site (I): lies 4 km northern to the site of NIOF with water depth varying between 0.5 m at the low tide time and 1.50 m in the high tide time.

Site (II) is located in protected area from the intense wave action and deeper than site (I) directly facing the NIOF. The water depth in this site reaches to less than 60 cm at low tide time.

Site (III) is located 4 km to the south of NIOF, in this site, the holothurians species suffer from both the high turbidity and the tidal exposure with high temperature rates in the low tide time especially in summer season.

Sampling

Samples of about 10-15 individuals were randomly collected by SCUBA-divers of B. vitiensis collected monthly using quadrate transect (10 x 10 m) from each of the selected sites by hand through snorkeling in the intertidal areas.

A total of 447 individuals of B. vitiensis were collected through the period from March 2003 to February 2004. The distribution and abundance of the studied species were calculated by counting per 100 m2. Measurements were done after relaxation of sea cucumber in 2.5% MgCl2 (w/v) in a plastic container. This was found to avoid the error resulting from contraction and relaxation by the animal body, as reported by Sewell (1994, 1992).

■ Female • Male

Figure 7 Monthly distribution of tubule diameter of females and males of Bohadschia vitiensis.

' Female > Male

Figure 8 Monthly distribution of tubule length of females and males of Bohadschia vitiensis.

G.S.I. = g0nadwt x 100 Body wt

Macroscopic examination of gonad tubules

Gonad index

Total length (T.L) of the animal was measured, from mouth to anus, with a metric tape to the nearest 0.5 cm. Each individual was then weighed with to the nearest 0.01 g (Tw). The vertical part of each animal was dissected and the entire gonad was removed, including the germinal tubules, and then towel-dried and weighed to the nearest 0.01 g (G.W), the gonads either male or female were fixed in 7% buffered formalin for 24 h then rinsed in tap water and stored in 70% ethanol according to (Ramofafia et al., 2000). Following removal of the internal organs and excess of coelomic fluid, the gutted body weight (G.B.W) was determined to the nearest 0.01 g. The gonad index was subsequently calculated as the ratio between the fresh gonad weight and the fresh body weight according to the following formula (Conand, 1981, 1993; Ramofafia et al., 2001; Abdel Razek et al., 2005):

Maturity stages were established according to physical characteristics of the tubules (length, diameter, color and branching) we used the following maturity stages according to Abdel Razek et al. (2005): Stage I Immature, Stage II Maturing, Stage III Ripe and Stage IV spent.

The gonad of each animal was placed on a Petri dish and 5-10 tubules were randomly selected from the tubular base. The length and diameter of tubule was measured using an electronic caliper, to the nearest 0.01 mm (Hamel et al., 1993); the color was annotated. In females, the diameters of 50 oocyctes were also measured using an ocular micrometer during the active spawning period (May, June and July).

Size at first maturity

First sexual maturity was defined as the size (L50) at which the gonads of 50% of the individuals were mature. It was

Figure 9 Size frequency distribution of oocyte diameter of ripe individuals of Bohadschia vitiensis during the spawning season.

Map 1 Locations of sampling sites of Bohadschia vitiensis.

determined by plotting the percentage of individuals with ripe gonads against size classes (Conand 1981).

Results

Population structure

From a total of 172 B. vitiensis were examined, 31 (18%) did not show any visible gonad, 52 individuals (30%) as females and 89 (52%) as males. The ratio of males, females and unsexed individuals varied from month to month with dominance of males (Fig. 1). The size distribution of the sampled animals (Fig. 2) showed that the sizes ranged from 16.0 to 42.0 cm total length (individuals smaller than 16.0 cm and larger than 42 cm were absent). For peaks were noted at total lengths of 21.5, 25.5, 31.5 and 36.5 cm.

Size at first sexual maturity

It is well known that a certain minimal body size is necessary before an individual becomes sexually mature (Lawrence, 1987). The size at first sexual maturity (L50) of B. vitiensis in the present study was at 24.5 cm for males and 26.1 cm total lengths for males as shown in Fig. 3. This may suggest that, from that moment on, gonadal and somatic growth have to share the available energy of the individual. Fig. 6(A and B) describes the size distribution of the different maturity stages of both sexes.

Gonad index

Fig. 4 describes the monthly distribution of the gonado-so-matic index (G.S.I) of females and males of B. vitiensis, while Fig. 5 represents its seasonal distribution according to the animal total lengths. The maximum value of gonad indices for males and females were observed in June and July during summer season and the values increased with increasing the animal size. While during autumn (September, October and November) and winter (December, January and February) the gonads were slightly shrinking and the values of G.S.I. decreased. The values of G.S.I. started to increase gradually from May up to June and July as in Fig. 4 which indicates a clear correlation between increasing in weight of gonads and that in water temperature in the case of the present studied species.

Macroscopic analysis of gonad tubules and spawning periodicity

The macroscopic features of male and female maturity stages of gonads in B. vitiensis are shown in Plates 1 and 2 while the size distribution of maturity stages are shown in Fig. 6A and B. Gonad tubules mainly grew to maturing stage (II) during spring season from March as described in Table 1. In June and July the gonads in both sexes reached their ripe stage (III) with its maximum body and gonad weights and during their period of spawning they start to release their gametes.

From August-September most of the tubules were in spent stage (V) with a considerable parts of the tubule volume still with uncharged oocytes and sepermatozoa. In winter season, tubules more or less empty, having white color and transparent for both sexes.

The physical characteristics of gonad tubules, length and diameter followed the pattern similar to the seasonal changes of G.S.I. as in Figs. 7 and 8 and were highly correlated with the gonadal index. Tubule coloration changed throughout the year, depending on the stage of maturity as described in Table 1 and Plates 1 and 2.

In female gonads, the mean diameter of the oocytes increased when the gonads reach their ripe stage as in Fig. 9. The relatively large size with higher frequency of oocytes were observed during June as the peak of spawning time of B. vitiensis and followed by July which confirms all the previous results.

Discussion

The reproductive output of marine invertebrates has shown that they depend for their development on various factors, such as sex and size of the individual as well as ecological factors such as population density (Levitan et al., 1991; Muthiga et al., 2006). Although B. vitiensis is a common species in the Red Sea and the adjacent indo-pacific area, yet, data about its biology and reproduction are lacking. As a result, any attempt to compare the present results with other populations is difficult. Therefore, the present data were compared with those of other similar species of the Holothuria genus.

Holothuroid fauna of the Red Sea attracted attention of many investigators for many years ago. Identification of species and species lists had been made by some authors, although taxonomy of holothuroids was faced by many difficulties. The various habitats of the Red Sea during the period 1955-2001

Plate (2) female

Plates (1 and 2) Macroscopic features of male and female gonads (Bohadschia vitiensis). (A and E) Immature stage (1). (B and F) Maturing stage (2). (C and G) Ripe stage (3). (D and H) Spent stage (4).

[Cherbonnier (1955), Hassan (2001)] recorded 98 holothuroid species.

Table 1 Macroscopic characteristics of B. vitiensis gonads at each of the stages of sexual maturity.

Stage of maturity Sex Tubule characteristics Shape and color Macroscopic G.S.I. range

T.L (mm) range Diameter range morphology

I Immature stage $ 2.5 to 21 mm 0.2 to 1.0 mm Branched tubules, No oocytes empty 1.0 to 3.5 according

short, thick and tubules to gutted wt.

yellow-white in color

# 2.0 to 22.0 mm 0.2 to 0.9 mm Small branched 0.4 to 3.1 of gutted

tubules, thin, short wt

and yellow white in

II Maturing stage $ 15.0 to 50.0 mm 0.4 to 1.3 mm Long, thick and Presence of oocytes 7.5 to 16.7

branched tubules but without nucleus

ovary pale red in

# 18.0 to 66.0 mm 0.4 to 1.2 mm Long, thin, 0.8 to 0.9

branched and

creamy-white color

tubules

III Ripe stage $ 67.0 to 130 mm 1.9 to 2.5 mm Long, thick swollen Most oocytes were 28.2 to 39.7

and branched ripe, clearly visible

tubules, red in color nucleus, spherical

# 90.0 to 125 mm 1.5 to 2.0 mm Maximum volume oocytes with 16.2 to 27.2

of tubules, long, diameter 75-150

swelling with white micron numerous

beaded filaments spermatozoa

swimming from a

tubule section

IV Spent stage $ 19.0 to 350 mm 0.5 to 0.7 mm Presence of some Considerable part of 0.5 to 1.5

tubules more limp, tubules volume was

branches, more or still with

less empty with a undischarged

white and oocytes

transparent color

# 12.0 to 46.0 mm 0.3 to 0.9 mm Branched tubules, Some remaining 0.4 to 10.8

more or less empty, spermatozoa

white color and

transparent

According to Hellal et al. (2007), the genus Bohadschia was represented by the species B. vitinesis with other 4 species, which were found in gulf of Aquaba and north of the Red Sea. B. vitinesis and H. atra were abundant in a habitat rich in algae, sea grasses, heaving a sandy bottom in the Red Sea coast of Egypt (Abdel Razek et al., 2006). Hellal et al. (2007) reported that B. vitinesis was found with area of sand, mud, sea grass, dead and live coral.

In the present study B. vitinesis which is considered as a tropical species follows one single annual cycle, as the typical temperate sea cucumber species H. sanctor (Navarro et al., 2012). The maximum reproductive activity was observed in summer with a rest stage in late autumn and winter.

The lack of gonads during winter is due to the resorption of tubules after the spawning of gametes into the water column (Coand, 1993). While in case of sea cucumber H. atra collected from the same area of Red Sea, it was found that the ripe individuals were nearly found all over the year with high abundance in June and November for males and from June to December for females [Abdel Razek et al. (2005)]. The reproductive cycle of B. vitinesis is clearly related to sea water temperature.

Gametogenesis occurs when sea water temperature rises and spawning when the maximum sea water temperature is reached (June, July) while resorption takes place when sea water temperature are decreasing. Starr et al. (1990) reported about the synchronization of the spawning of echinoderms with phytoplankton availability as it is considered as an advantages adaptation.

Chao et al. (1995) in his study on some holothurian species suggested that their feeding mode is related to food resources and may influence the reproductive period. He added also that in the direct-developing dendrochirotida (suspension feeder) go-nad development occurs in cool months and gametes are released at the beginning of warm months with phytoplankton growth.

B. vitinesis in the present study had a size range 16.0 to 42.0 cm is consistent with other observations. H. hawaiiensis individuals inhabiting the same area of study had a size range 25.5 cm to 41.5 cm and H. atra from 9.5 cm to 28.5 cm according to Abdel Razek et al. (2006). These differences in sizes distribution may be a function of fishing pressure, depth from which the sample was taken together with environmental factors (Uthicke and Benzie, 1999) or substrate type (Mercier et al., 1999).

Gonadal growth in both sexes in B. vitinesis however, was highly correlated, indicating tight synchrony between males and females. Sexual synchrony has previously been reported in other sea cucumber including H. scabra (Ramofafia et al., 2003).

In the present study a shift in sex ratio towards males in B. vitinesis was observed. This shift in sex-ratio from unity towards significantly more males suggests a negative impact of fishing pressure. However further studies on the effects of fishing on population structure, growth and recruitment of this species are needed to support this finding. This same observation has been reported in H. scabra population under heavy fishing pressure in the Red Sea (Hassan, 2005). Reproductive success is partly dependent on the abundance and distribution of adults, and the availability of gametes of both sexes (Levit-an, 1991, 2005).

Sylvie Gaudron (2006) and other authors, have reported that there were two positions for spawning either up right or laying flat on a substratum with grass in the lagoon St. Gilles-les Bains, Indian Ocean.

Size at first maturity is commonly used in almost every fishery in the world to establish a minimum capture size, indicating the size from which 50% of the captured animals are mature and have already gone through a reproductive period. The size at first maturity (TL50) of B. vitinesis was 24.5 cm for males and 26.1 cm for females which is comparable to that of other species with similar maximum lengths (Navarro et al., 2012).

Gonad index method is a reliable method for tracking reproductive maturity in B. vitinesis (Keshavarz et al., 2012; Abdel Razek et al., 2005a). Gonad tubule length and diameter has also been shown to be correlated with sexual maturity in the studied species. Both indicated one spawning cycle during summer period with maximum activity during June and July.

The present study provides information on sexual maturity, reproductive seasonality, including tubules length that are useful for mariculture and management as well as potential signs that reflect the impacts of over fishing. Therefore, we encourage future studies on the reproduction of B. vitinesis to focus on the fecundity per size distribution, estimating the ideal size to capture to avoid overexploitation of the Red Sea commercial species.

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