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Journal of Fish Biology (2003) 62, 129^142 doi:10.1046/j.0022-1112.2003.00014.x, available online at http://www.blackwell-synergy.com

Reproductive cycles and spawning periods of two Lessepsian siganid fishes on the Lebanese coast M. B A R IC H E *†, M. H A RM E L I N -V I V I E N * A N D J.-P. Q U IG NA R D ‡ *Centre d’Oce¤anologie de Marseille, UMR CNRS 6540, Universite¤ de la Me¤diterrane¤e, Station Marine d’Endoume, 13007 Marseille, France and ‡Laboratoire d’Ichtyologie me¤diterrane¤enne, Case102, Universite¤ de Montpellier II, Place Euge'ne Bataillon, 34095 Montpellier Cedex 05, France (Received 25 March 2002, Accepted 4 November 2002) A total of 1048 specimens of Siganus rivulatus and Siganus luridus were collected from the Batrun area of the Mediterranean Sea from January 1999 to August 2000. The sex-ratio in both species did not differ significantly from 1: 1 between size classes or months. For S. rivulatus, the estimated mean length at first maturity (LT50) was 1325 mm for males and 1365 mm for females, and 1390 and 1420 mm, respectively, for male and female S. luridus. Spawning occurred in June in S. rivulatus and from May to July in S. luridus. High temperature in summer appeared to be a limiting factor in the gonadal development of both siganid species, which have reduced their breeding seasons on the # 2003 The Fisheries Society of the British Isles Lebanese coast compared to their native Red Sea. Key words: Lebanon; Mediterranean; reproduction; Siganus luridus; Siganus rivulatus.

INTRODUCTION Siganids are a relatively small family of herbivorous fishes widely distributed in the Indo-West Pacific (Woodland, 1983). Of the 30 species recognized by Woodland (1999), only half are restricted to coral reefs. The opening of the Suez Canal in 1869 linked the Red Sea to the Mediterranean Sea and resulted in the invasion of the eastern Mediterranean Sea by many marine species (Por, 1978; Boudouresque, 1999; Fishelson, 2000; Galil, 2000; Quignard & Tomasini, 2000). Por (1978) termed this invasion Lessepsian migration. To date, 56 Indo-Pacific fish species have been found in the Mediterranean Sea (Golani, 1999, 2000). Siganus rivulatus ForsskDl was first recorded in the Levant Basin in 1927 (Tortonese, 1970) while Siganus luridus (Ru«ppell) appeared suddenly in large numbers in 1956 (Ben-Tuvia, 1964). Both species have since established large populations in their new environment and can be considered amongst the most successful of Lessepsian fishes (George, 1972; Ben-Tuvia, 1985; Papaconstantinou, 1990). Siganids are economically important and relatively easy to rear and are thus considered suitable for aquaculture (Lam, 1974; Bryan & Madraisau, 1977; Juario et al., 1985;

†Author to whom correspondence should be addressed. Tel.: þ33 491041623; fax: þ33 491041635; email: [email protected]

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Hara et al., 1986). There have been attempts to breed and rear S. rivulatus and S. luridus (Ben-Tuvia et al., 1973; Popper et al., 1973, 1979; Popper & Gundermann, 1975). Some data on their reproduction are available for the Red Sea (Popper et al., 1979; Hashem, 1983; Amin, 1985a, b) and the eastern Mediterranean Sea (George, 1972; Mouneimne¤, 1978; Hussein, 1986; Saad & Sabour, 2001). Nevertheless, these papers present limited information on the reproductive cycle of both the Red and Mediterranean Sea populations. Success or failure in a new environment depends on the adaptability of the colonizer.To survive novel hydroclimatic factors, particularly a different water temperature range, an adjustment to the reproductive process is necessary. The present study investigates the reproductive parameters of the Mediterranean Sea populations of S. rivulatus and S. luridus on the Lebanese coast. It aims to describe: (1) the gonad developmental stages of these two species, (2) the timing and duration of their spawning activity, (3) the adult sex-ratio and (4) the size at first sexual maturity. Comparison of these data with previous information available in the literature will allow a better understanding of the biological adaptation of Red Sea siganids to the new environmental conditions encountered in the eastern Mediterranean Sea.

MATERIALS AND METHODS The study was carried out along the northern coast of Lebanon, in the Batrun area (from Batrun to 6 km north) (Fig.1), from January1999 to August 2000. Surface water temperature ( C) was recorded monthly, at mid-day (1000^1400 hours), in a small bay in Batrun throughout the study. Samples were collected weekly during the breeding season and monthly during the rest of the year. Samples of the two species (n ¼ 528 for S. rivulatus and n ¼ 520 for S. luridus) were selected randomly from catches of fishermen using trammel nets fishing between 8 and 15 m depth. Siganids were purchased early in the morning and transported immediately in crushed ice to the laboratory where they were analysed. Total length (LT) was measured to the nearer mm and total body mass (MT) to the nearer 001g. Fresh gonads were removed and visually inspected for size, colour, vascularization and the presence of milt and oocytes. Although general maturity stage tables exist (Laevastu, 1967; Holden & Raitt, 1974) and others specifically for siganid species (Al-Ghais, 1993; El-Sayed & Bary, 1994), none were suitable for the present observations. Therefore, ovary maturity was divided into five stages (I ^ V) and testis into four stages (I, II, III and V) (Table I). Gonads were weighed (MG) to the nearest 0001g after being fixed in 10% buffered formaldehyde. Since the sex of an individual could not be determined macroscopically before stage II, stage I fish were not considered in the sex-ratio.The sex-ratio (male : female) and size at first maturity were determined during the periods of gonadal development which occurred from May to June for S. rivulatus and from May to August for S. luridus. A 2 goodness-of-fittest was undertaken to compare the sex-ratios within the size groups at each sampling or within years, with a hypothesized sex-ratio of 1: 1. The length at which 50% of the fish were ‘mature’ (stage III for males and stages III and IV for females) was regarded as the size at first maturity (LT50). It can be calculated by fitting a logistic function to the proportion of sexually mature individuals bylength: P ¼ f1 þ e½rðLT LT50 Þ g1 (King,1995), where P is the proportion of mature fish and r the slope. Since there was no relationship between the values of y and x for S. rivulatus in the linear model {ln½(1 P)P1 ¼ rLT50 LT and plotting ln½(1 P)P1

against LT}, size at first maturity (LT50) for both species was calculated by fitting the logistic function P ¼ f1 þ e½rðL T L T50 Þ g1 using a nonlinear regression (Quasi-Newton estimation) with individuals classed into10 mm LT intervals. The gonado-somatic index (IG) is an indicator commonly used for depicting annual reproductive cycles in fishes (Crim & Glebe, 1990). It was calculated from IG ¼ 100 MG (MT MG )1 . #

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FIG.1. Map of the eastern Mediterranean and the northern Red Sea, showing the location of the Batrun area.

RESULTS MAT URI T Y STAGES

At the same maturity stage, ovaries and testes were similar in appearance and size for both the siganid species. A macroscopic description of each stage is given in Table I. Both undeveloped and juvenile gonads (stage I) were small, cylindrical and occupied a minute portion of the lower body cavity, located over the posterior part of the pelvic fins, and extending posteriorly. When developed, the left and right lobes are asymmetric. The left lobe is relatively flat and covers the entire left surface of the cavity. The right one is more rounded and elongated, pushing the gut upward. The temporal development of S. rivulatus and S. luridus gonadal maturity stages are given in Figs 2 and 3. SEX-RAT IO

Of all the S. rivulatus sexed (stage II and above) during the period May to June in 1999 and 2000 (n ¼177), 452% were mature females and 548% mature males. The sex-ratio of this species did not differ significantly from 1: 1 during May to June in either year (P ¼ 0764 for 1999 and P ¼ 0674 for 2000) or between the two years (P ¼ 0747) and was 1: 082. Similarly, in S. luridus during the period May #


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TABLE I. Macroscopic criteria used to classify the gonad maturity stages in Siganus rivulatus and Siganus luridus along the coast of Lebanon Classification

Macroscopic appearance

Stage I

Undeveloped

Sex cannot be determined macroscopically. Gonads relatively small (230 mm LT) for both species in the present study. The relatively small number of fishes caught at these sizes (seven S. rivulatus and eight S. luridus) might be the cause of the skewed ratio, or the result of a difference in growth or longevity between sexes. SIZ E AT M AT U RI T Y

In this study, the smallest reproducing S. rivulatus were a 126 mm LT female and a 127 mm LT male. The smallest reproducing individuals of S. luridus were a 135 mm LT female and a 125 mm LT male. Data on size at first maturity for S. rivulatus are rare and none exist for S. luridus. In the Mediterranean Sea, George (1972) found that gravid individuals occurred between 120 and 160 mm LT in S. rivulatus. The smallest sexually mature female S. rivulatus collected in the Mediterranean Sea were 148 mm LT (Mouneimne¤, 1978) and 150 mm LT (Hussein, 1986) and in the Red Sea 130 mm LT (Hashem, 1983). Saad & Sabour (2001) found LT50 to be equal to 1722 mm for females and 1785 mm for males along the Syrian coast (values were converted from standard length, LS, using the regression equation of Bilecenoglu & Kaya, 2002). These LT50 values were higher than found in this study for S. rivulatus (1325 and 1365 mm for males and females, respectively). SPAW N I NG SEAS ON

Various authors have reported a spawning season ranging from 2 to 7 months for the two siganids in the Red and Mediterranean Sea (Popper & Gundermann, 1975; Popper, 1979; Amin, 1985a; Hussein, 1986; Saad & Sabour, 2001) (Fig. 6). A second spawning in September (George, 1972) or an extension of the first spawning to November (Mouneimne¤, 1978) was suggested for S. rivulatus in the Mediterranean Sea as young-of-the-year were found in the autumn. Although differences in spawning intensity and duration may vary between years, defining a spawning season for a species should be based on a large number of specimens sampled regularly over a relatively long period and be coupled with physical factors (e.g. water temperature, salinity and luminosity). In the present study, a clear difference was observed in spawning season between the two species. On the Lebanese coast, all S. rivulatus spawned in June in both 1999 and 2000. In this species, gonads of both sexes were found at stage I from July to April. In contrast to what was previously reported (George, 1972; Mouneimne¤, 1978; Hussein, 1986), S. rivulatus did not spawn in the autumn, at least in 1999. #


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Red Sea

Golani (1990) Amin (1985a, b) Popper & Gundermann (1975)

Mediterranean Sea

Present study Saad & Sabour (2001) Golani (1990) Hussein (1986) Mouneimné (1978) Popper & Gundermann (1975) George (1972)

1

2

3

4

5

6

7

8

9

10

11

12

Month FIG. 6. Spawning seasons reported in the literature for Siganus rivulatus (&) and Siganus luridus (&) according to different geographical locations. - - -, a possible spawning period.

Siganus luridus spawned between May and July (Fig. 3) and fish with maturing gonads (stage III) were seen again in October and November without any observed spawning. Thus, on the Lebanese coast, S. luridus presented a well-defined spawning period in May to July and may have spawned again in the autumn if the environmental conditions had been suitable. Popper & Gundermann (1975), comparing the Red Sea population of these siganids with those in the Mediterranean Sea, noted that both the invaders shortened their spawning season in the new environment (Fig. 6). In Aqaba, S. rivulatus spawned from May to August and S. luridus from March to September. In Jeddah, Amin (1985a, b) reported that S. rivulatus spawned from March to September. The present results, which indicated a spawning season restricted to June for S. rivulatus and May to July for S. luridus, are consistent with a reduction in the duration of the spawning period in the Mediterranean Sea as reported by Popper & Gundermann (1975). Previous studies on the reproductive biology of siganid species have shown that water temperature plays a role in the determination of the timing and duration of spawning season (Lam & Soh, 1975; Popper et al., 1976; Amin, 1985a, b). In the eastern Mediterranean Sea, seawater temperature is higher in summer and lower in winter than in the Red Sea (Fig. 5). George (1972) noted that S. rivulatus spawning occurred when water temperature reached 27 C. In the present study, it appeared that both species spawned within the temperature range 24^29 C. During the warmest period (30^31 C) no ripening fishes were observed and all had spawned. In October, when water temperature decreased to 25 C, the second increase in the gonad development of S. luridus occurred. Probably no second spawning took place in 1999, because water temperature rapidly decreased between #


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November (24 C) and December (19 C). Popper & Gundermann (1975) did not observe any ripe fish in August (29 C) in the Mediterranean Sea populations while in the Gulf of Aqaba they were observed until August (S. rivulatus) and September (S. luridus), with a mean water temperature close to 27 C. In Jeddah, Amin (1985a) observed all S. rivulatus in spent condition by the time water temperature reached 30 C (July). From these observations and the present data, it is proposed that spawning in S. rivulatus and S. luridus occurs within a particular range of water temperatures. It appears that both the species may have been forced into curtailing the duration of their spawning season because seawater temperatures exceed those in their native Red Sea habitat during the latter part of their traditional breeding period. As spawning occurs with water temperatures ranging between 24 and 29 C, the Lessepsian siganids have reduced their spawning season in the Levant Basin to1month for S. rivulatus and 2 months for S. luridus. The authors wish to express their gratitude to the Universite¤ de la Me¤diterrane¤e (Marseille, France) and to the French ^ Lebanese C.E.D.R.E. Program for partially supporting this study. They also thank the Station Marine d’Endoume (Marseille, France), the Marine Station of Batrun (Lebanon), N. Navarro for his valuable help with statistics and M. Paul for correction of the English. The manuscript was improved by the criticisms of J.G. Harmelin and by the helpful comments of two anonymous referees.

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