ANNALES · Ser. hist. nat. · 30 · 2020 · 2 201 received: 2020-09-06 DOI 10.19233/ASHN.2020.24 GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE) Fatiha DALOUCHE, Lotfi BENSAHLA-TALET, Sidi Mohamed El Amine ABI AYAD & Ahmed BENSAHLA-TALET Laboratoire Aquaculture et Bioremediation (AquaBior). University Oran1 Ahmed Benbella. Faculty of Natural Sciences and Life. Department of Biology. Oran-Algeria e-mail: btlotfi1977@gmail.com ABSTRACT Our study aims to investigate the reproductive cycle of Boops boops caught in Oran Bay. The samples were received monthly from commercial catches of coastal trawlers operating in this area from January 2016 to De- cember 2017. The overall sex ratio was in favor of females and the length frequency distribution according to sex revealed that females were predominant beyond 14 cm of total length, presuming the beginning of the sexual inversion already described for this Sparidae species. The spawning period was established based on the follow-up of the gonado-somatic index, and appeared to last from February to late June with a peak in the March-April period. Our findings can contribute to a better understanding of the reproductive cycle of this species and help adopt measures toward a more adequate stock management of the most abundant sparid that is landed daily in many Mediterranean and Algerian fisheries. Key words: Boops boops, reproductive cycle, spawning season, size at first maturity, Oran, Algeria SVILUPPO GONADALE DELLA BOGA, BOOPS BOOPS (LINNAEUS, 1758) NELLA BAIA DI ORANO (TELEOSTEI, SPARIDAE) SINTESI Lo studio si propone di indagare il ciclo riproduttivo degli esemplari di Boops boops catturati nella baia di Orano. I campioni mensili provenivano dalle catture commerciali dei pescherecci costieri operanti in quest’area, da gennaio 2016 a dicembre 2017. Il rapporto tra i sessi è risultato a favore delle femmine e la distribuzione della frequenza della lunghezza in base al sesso ha rivelato che le femmine erano predominanti oltre i 14 cm di lunghezza totale, presumendo l’inizio dell’inversione sessuale già descritta per questa specie di sparidi. Il periodo di riproduzione è stato stabilito sulla base del follow-up dell’indice gonado-somatico e sembra durare da febbraio a fine giugno, con un picco nel periodo marzo-aprile. Tali risultati possono contribuire a una migliore comprensione del ciclo riproduttivo di questa specie e aiutare ad adottare misure per una gestione più adeguata dello stock dello sparide più abbondante, che viene sbarcato quotidianamente in molte zone di pesca del Mediterraneo e dell’Algeria. Parole chiave: Boops boops, ciclo riproduttivo, stagione di deposizione delle uova, taglia alla prima maturità, Orano, Algeria ANNALES · Ser. hist. nat. · 30 · 2020 · 2 202 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 INTRODUCTION The bogue is a widespread species in the eastern Atlantic, found from Norway to Angola, including the Canary, Cape Verde, and Sao Tome-Principe Islands. It is common between the Bay of Biscay and Gibraltar, and in the Mediterranean and Black Seas (Bauchot & Hureau, 1986). This sparid can be found in the shelf or coastal pelagic zone on various bottoms (sand, mud, rocks and seaweeds). Gregarious and ascending to the surface mainly at night, the species is omnivorous, feeding mainly on crustaceans, as well as plank- tonophagous (Frimodt, 1995). In Algeria, the Sparidae family is of high com- mercial importance, with the bogue representing ~ 20 % of all demersal fish landed and 45 % of all sparid catches (D.P.R.H, 2016). B. boops is a demersal and semi-pelagic species typifying the daily landed fish in Oran Bay. It moves in aggregations, ascending to the surface mainly at night (Campillo,1992); in Oran Bay it is fished at depths ranging between 100 and 250 m (pers. obs.) and captured by line gear, with bottom trawls and purse seines. There is some published data on the biology of this species, focusing mainly on the weight-length rela- tionship (Gonçalves et al., 1997; Moutopoulos & Ster- giou et al., 2002; Özaydin & Taskavak, 2006; Kara & Bayhan, 2008; Karachle & Stergiou, 2008; Crec′hriou et al., 2013; Özvarol, 2014; Crec’hriou et al., 2015), fishing gear selectivity (Ayaz et al., 2009; Cengiz et al., 2013; Kumova et al., 2015; Eryaşar, 2017; Ilkyaz et al., 2017), feeding habits (Sánchez-Velasco & Norbis, 1997; El-Maremie & El-Mor, 2015), and biology and population dynamics (Anato & Ktari, 1983; Alegria Hernandez, 1989; Gordo, 1996; Allam, 2003; Khemiri et al., 2005; Manaşirli et al., 2006; Monteiro et al., 2006; El-Okda, 2008; Kara & Bayhan, 2008). Several biological studies on its reproductive cycle have also been conducted (Frau, 1966; Gordo 1995,1996; Cano Fortuna & Lizaso, 1996; El-Agamy et al., 2004; Monteiro et al., 2006; Kasalica et al., 2011; Bottari et al., 2014; Layachi et al., 2015; Taylan & Bayhan, 2015; Mobilia et al., 2016; Dobroslavić et al., 2017), but in relation to Algerian waters, the works are limited to Derbal & Kara, 2008 on feed- ing habits; Boubaiou, 2014 (morphometrics); Benina, 2015; Kherraz et al., 2016 (population dynamics), Ider et al., 2017 (otolithometry), and only works of Chali-Chabane (1988) in Algiers Bay, and Bensahla- Talet et al. (1990) and Kherraz (2011) in Oran Bay dealt with the reproductive cycle of this species. Therefore, the present study aims to estimate more precisely the reproduction parameters of this species to help comparative studies in the Mediterranean and propose measures to allow a renewal of the resources and improved management. MATERIAL AND METHODS Specimens of B. boops (n=7153; 3317 in 2016, and 3836 in 2017) were caught by trawlers operating in Oran Bay, located in northwestern Algerian coast (western Mediterranean Sea), between Pointe de l’Aiguille and Cape Falcon (35.95 °N-0.65 °E) (Fig. 1) at depths ranging between 100 and 250 m between January 2016 and December 2017. Samples were randomly collected from daily landed fish at the Oran fishery. At the laboratory, total length (TL), measured to the nearest millimeter with an ichthyometer (± 1 mm), total weight (TW), and gonad weight (GW), using a digital precision balance (± 0.01 g), were recorded for each individual. Sex ratio The sex ratio was calculated monthly throughout the study period according to individual sizes (1 cm class interval) and seasons using the formula below, while sexually indeterminate and immature individu- als were not taken into account: where: nF = number of females, nM = number of males. To detect statistically significant deviations from the expected 1:1 ratio, the chi-square (χ², P < 0.05) test was used (Sokal & Rohlf, 1987). Spawning period For the description of the sexual cycle of B. boops several approaches were used: Fig. 1: Map of the study area (Oran Bay). Sl. 1: Zemljevid obravnavanega območja (Oranski zaliv). ANNALES · Ser. hist. nat. · 30 · 2020 · 2 203 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 1 - The maturation scale was established following the Holden & Raitt (1974) macroscopic scale, while microscopic description was based on the Aboussouan & Lahaye (1979) scale with a slight modification to fit B. boops gonad development (Tab. 1). Both are based on the macroscopic aspect, relative dimensions and microscopic characteristics of the gonads (I: immature, II: resting, III: ripe, IV: ripe and running, V: spent). 2 - Between 10 and 30 specimens of B. boops were selected each month for histological examination of the sexual organs, which were placed in Bouin’s fixative solution for 48 h, dehydration was carried out by increasing concentrations of acetone/toluene, then fragments were embedded in paraffin wax. Gonads were sectioned with a microtome into 5-6 μm sections and stained with hematoxylin-eosin. 3 - Monthly evolution of the gonado-somatic (GSI) index was calculated as follows: where: GSI = gonado-somatic index, GW = gonad weight (g), TW = total weight (g). The nucleoplasmic ratio is considered to be closely related to the mitotic cellular cycle and to the functional phase of cells. It is also a good indicator of dynamic changes in cells (Bensahla-Talet et al., 2017). The nucleoplasmic ratio (NPR) is expressed mathematically as: where: Nd = nucleus diameter, Cd = total cell diameter. Size at first sexual maturity Size at first sexual maturity (Lm) was defined as the size class at which 50 % of the individuals are mature. Specimens were grouped into 1 cm size classes, and the proportion of mature and immature individuals was recorded. The total length at which 50 % of the specimens were mature was estimated by a logistic non-linear least-squares regression (King, 1995): where: P = percentage of mature individuals, a = slope of the curve or rate of increase in maturity, Lm = length at 50 % maturity, L = 1 cm length class. RESULTS In total, 3317 specimens of B. boops were col- lected in 2016, 1319 of which were males (39.76 %) Tab. 1: Sexual maturity scale (macro- and microscopic) of the Sparidae modified and used in this study to classify B. boops gonads, with a focus on female gonads (Bensahla-Talet et al., 2017). Tab. 1: Spolna zrelost (makro- in mikroskopska) predstavnikov iz družine Sparidae, prirejena za potrebe te študije za opredelitev gonad vrste B. boops, s posebnim poudarkom na samičjih gonadah (Bensahla-Talet et al., 2017). Level name Macroscopic Microscopic I Immature Very small and translucent ovaries. Very small testes; no signs of development. Oocytes are small arranged on ovigerous lamellae. The nucleus is relatively clear. II Resting Ovaries in recovering condition; Testes in recovering condition. Oocytes are small spherical (about 60 μm), no vitellus is found in their cytoplasm. The nucleus is relatively dense and large with a NPR at its maximum attaining 0.6. III Vitellogenesis (Maturing) Larger ovaries and eggs visible. Larger testes, not running. Vitellogensis initiate characterized by massive entry of small vitelline and lipidic vesicles. Zona radiata begin to thicken and appearance of granulosa formed of single cell layer. IV Ripening and Spawning Large transparent eggs that are released under moderate pressure. Sperm released by a light press on the abdomen. Oocytes attainted their maximal size (~500 μm). The nucleus migrates to the animal pole. The follicle includes a thick zona radiata. The cytoplasm is overload with vitellus and lipid vesicles conferring to the egg a hyaline aspect. V Post spawning Ovaries shrunken with few residual eggs, much slime and often redish. Testes small, slack testes and often redish; resting condition. Many atretic follicles are encountered corresponding to oocytes that have not attained their maturation or mature ones that were not emitted and which will degenerate. The cytoplasm is disorganized and cells undergo pycnosis. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 204 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 and 1998 were females (60.23 %), while in 2017, 3836 specimens were collected, 1798 males (46.87 %) and 2038 females (53.12 %). The length frequency distribution of the entire population is shown in Fig. 2a, b; the male length range was between 10 and 22.9 cm, the female between 12 and 24.9 cm. The overall female-male ratio was in favor of fe- males (F:M 1:1.51 in 2016 and F:M 1:1.13 in 2017) and was significantly different from the 1:1 ratio (χ2=138.99 and χ2 = 15.02 respectively > χ 2t 1,0.05 = 3.84). Sex ratios between males and females by size class were also significantly different from the 1:1 ratio (χ2observed > χ2t 1, 0.05 = 3.84) for most size classes, the difference was significant beyond the 14 cm length class in 2016, while in 2017, this difference was dis- tinguished beyond the 17 cm of total length, where females predominated. Males predominated in smaller size classes and females in larger ones (Fig. 2). Maturity stages Females with ripe gonads (stage III) and those with ripe and running gonads (stage IV) were observed (Fig. 3) in early winter and were dominant in the March-July period, thus highlighting the spawning period of B. boops in Oran Bay. Spent fish (stage V) were recorded from June to November with a maximum in August, while the remaining period of the year gonads in stage II were dominant, marking the sexual rest period of this Sparidae species. Nucleoplasmic ratio (NPR) The variation of the nucleoplasmic ratio according to maturity stages is presented in Fig. 3b, reflecting the changes that affect the oocytes. It appears that high values of this ratio are encountered in early oogenesis Fig. 2: A. Length frequency distribution of males and females of B. boops caught in Oran Bay. B. Monthly length frequency distribution of males and females of B. boops caught in Oran Bay. Sl. 2: A. Frekvenčna porazdelitev velikosti samcev in samic bukve (B. boops), ujete v Oranskem zalivu. B. Frekvenč- na porazdelitev velikosti samcev in samic bukve (B. boops) po različnih mesecih, ujetih v Oranskem zalivu. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 205 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 stages, attaining 0.51, and as the oocyte develops, this ratio tends to decrease, attaining its lowest value of 0.29 in stage IV, when the oocytes are ready to be emitted. Microscopic analysis As with the majority of teleost fish and especially sparids, the microscopic analysis of the gonads allowed us to describe the following stages in B. boops: Ovaries Immature period The oogonia representing the reserve batch are small round cells with a clear nucleus (Fig. 4a), vary- ing in size between 36 and 169 μm, and the NPR is at its maximum value of 0.51. Resting period At this stage (Fig. 4b) the oocytes are spherical (169-260 μm), some of them have already began their first cellular division and the cells are arranged as ovarian lamellae with a homogenous and transpar- ent cytoplasm, having numerous nucleoli mixed to a large nucleus containing dense chromatin, the NPR is at 0.46. Maturing period Previtellogenesis Oogonia undergo progressive increase in size reaching 205-390 μm (Fig. 4c, d) with an average NPR of 0.37. The maturation period is mainly char- acterized by: A- A clear central nucleus containing some super- numerary nucleoli distributed at the periphery. B- Thousands of cortical alveoli appearing to mark the beginning of the endogenous lipidic vitel- logenesis. C- The granulosa and zona radiata becoming vis- ible. The vitellogenesis period (pre-spawning) A rapid increase in the size of the oocytes is observed at this stage (416 μm), resulting from an intense entry of the protein yolk, also the vitelline globules are rounded and colored red with a mean diameter of 9.5 μm marking the exogenous vitello- genesis (Fig. 4e, f). Lipid (colorless) inclusions move massively around the nucleus (Fig. 4g, h) forming a central vacuole. The central cytoplasmic zone is filled and repels the cytoplasm at the periphery. The NPR de- creases to 0.38. The oocyte membrane is enveloped by a pro- tective thick membrane, zona radiata, measuring 10.16 μm. The whole is enveloped by the granulosa, formed by one layer of ovarian cells, and the fibrous theca (Fig. 4i). Ripening and spawning period The nucleus moves to the animal pole to initi- ate the first meiotic division (Fig. 4j). Egg release is imminent, cytoplasmic structures merge and give the mature egg a translucent appearance, hence the name hyaline oocyte (Fig. 4k, l); their diameter is max 500 μm (390-542 μm) with an average NPR of 0.29. Fig. 3: A. Maturity stages of B. boops females caught in Oran Bay (II: resting, III: maturing, IV: ripe and running, V: spent). B. Variation of the nucleoplasmic ratio (NPR) in relation to maturity stages of B. boops females. Sl. 3: A. Zrelostni stadiji samic bukev (B. boops) ujetih v Oranskem zalivu (II: počivajoči stadiji, III: dozorevajoči, IV: zreli, V: dokončani). B. Variacije v nukleoplazmičnem deležu (NPR) v odnosu na zrelostne stadije samic bukve (B. boops). ANNALES · Ser. hist. nat. · 30 · 2020 · 2 206 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 Fig. 4: O varian histological slides of B. boops fem ale gonads (a-m ) stained by hem atoxylin-eosin: (a) general view of an im m ature ovary × 100; (b) resting ovary with: advanced peri nucleolar oocytes (O II), a large nucleus and hom ogenous cytoplasm × 40; (c) previtellogenic ovogonia (O III) presenting a large nucleus surrounded by several lipoprotein vesicles × 250; (d) previtellogenic oogonia (O III) × 400; (e) early m aturing large oocytes with large translucent vitelline vesicles and a thin zona radiata (O III) × 250; (f) O III with a thick zona radiata and apparition of granulosa × 1000; (g) hydrated large oocytes (m ature) O IV with num erous vitelline globules and im portant lipid inclusions form ing a central vacuole × 100; (h) hydrated large oocytes (m ature) × 250; (i) m ature oocyte with a thick zona radiata, granulosa and fibrous theca × 1000; (j) hyaline oocyte with nucleus in the anim al pole × 100; (k) general view of ovary in spawning phase x 40; (l) hyaline oocyte ready to be released ×100; (m ) post-ovulatory follicle × 250. Fc: follicular cells; Gr: granulosa; Hc: hyaline cytoplasm ; Li: lipid inclusion; Lv: lipid vesicle; M : oocyte m em brane; N: nucleus; Nu: nucleoli; O : oocyte; O o: oogonia; Vg: vitelline globules; Zr: zona radiata of chorion; Pof: post-ovulatory follicle; Th: theca; Vv: vitelline vesicule; Zr: zona radiata. Sl. 4: Histološki rezi ovarija sam ic bukve (B. boops) (a-m ), obarvani z hem atoksilinom -eozinom : (a) pogled na nezrel ovarij × 100; (b) počivajoči ovarij z: razvitim i perinuklearnim i oocitam i (O II), veliko jedro in hom o- geno citoplazm o × 40; (c) previteligenska ovogonia (O III) z velikim jedrom , obdan s številnim i lipoproteinski vezikli × 250; (d) previteligenska ovogonia (O III) × 400; (e) zgodnje dozorevajoče velike oocite z velikim i prozornim i vitelinskim i vezikli in tanko “zona radiata”(O III) × 250; (f) O III z debelo “zona radiata” in pojavom “granulosa” × 1000; (g) hidratirane velike oocite (zrele) O IV s številnim i vitelinskim i globuli in pom em bni lipidni vključki, ki tvorijo centralno vakuolo × 100; (h) hidratirane velike oocite (zrele) × 250; (i) zrele oocite z debelim a “zona radiata” in “granulosa” ter fibrozna teka × 1000; (j) hialina oocita z jedrom v anim alnem polu × 100; (k) pogled na ovarij v fazi drstenja x 40; (l) hialina oocita tik pred sprostitvijo ×100; (m ) post-ovulatorni folikel × 250. Fc: folikularne celice; Gr: granulosa; Hc: hialina citoplazm a; Li: lipidni vključek; Lv: lipidni vezikel; M : m em brane oocite; N: jedro; Nu: nukleoli; O : oocita; O o: oogonija; Vg: vitelinski globuli; Zr: zona radiata pri horionu; Pof: post-ovulatorni folikel; Th: teka; Vv: vitelinski vezikel; Zr: zona radiata. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 207 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 Post spawning In the ovary, a fraction of unemitted mature oo- cytes enter atresia marking the end of the spawning season; the nucleus enters pycnosis and the yolk disintegrates into a compact cluster; the cytoplasm becomes disorganized; remaining in the ovary is only the reserve oogonia that will be used during the next spawning season (Fig. 4m). At the end of the spawning period, the fish enters the resting phase and the ovary reverts to its initial appearance, which can be recognized by the presence of ovigerous lamellae (Fig. 4a, b). Testes With regard to the spermatogenesis in male go- nads, the testes studied were mature at the same time as the ovaries. The testicles are formed of a multi- tude of oval ampoules separated by a connective tissue (Fig. 5). Seminiferous tubules are composed of isogenic cysts at different stages of maturation (Fig. 5a, b). At maturity, spermatids are transformed to spermatozoids, which move into the central lumen and from there into deferent ducts to be released via the genital opening. Hermaphrodite gonads B. boops exhibits a protogynous hermaphroditism already described (D’Ancona, 1949; Reinboth, 1962; Frau,1966; Girardin, 1981; Gordo, 1992; Massaro, 2012). During our sampling period, 90 individuals were her- maphrodites presenting the two sexes in the same gonad, the ovotestis. The histological analysis of ovotestis (Fig. 6) allowed us to examine germinal tissues for males and females, which co-exist (Fig. 6a, b, c). The female part is functional and represented by ovogonous cells and some oocytes I (OI) arranged in ovigerous lamellae. The male part is not yet active and is made up of spermatogonia arranged in isogenic cysts at the beginning of spermatogenesis. Sexual cycle and spawning period To determine the reproductive period of B. boops, the gonado-somatic index (GSI) was used, which was calculated from samples taken monthly. The GSI value began to rise from January and remained high until May, with a peak in April (3.75 in 2016, and 3.66 in 2017). The GSI then decreased from June and remained low until November, confirming the sexual rest period (Fig. 7), which is in accordance with our macroscopic observation on maturity stages of B. boops. Fig. 5: Spermatogenetic stages; (a) seminiferous tubule with isogenic cysts at different stages of maturation × 100; (b): mature testicle showing seminiferous tubules with lumen full of spermatozoa with their flagella × 1000. Fl: flagella; Lu: central lumen; Sp I: spermatocyte I; Sp II: spermatocyte II; Spz: spermatozoa; Std: spermatids; St: seminiferous tubule. Sl. 5: Stadiji spermatogeneze; (a) seminiferni tubuli z izogenimi cistami pri različnih zrelostnih stadijih × 100; (b): zreli testikli z vidnimi seminifornimi tubuli z lumnom, napolnjeni s semenčicami z bički × 1000. Fl: bički; Lu: centralni lumen; Sp I: spermatocita I; Sp II: spermatocita II; Spz: spermatozoj; Std: spermatide; St: seminiferni tubul. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 208 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 Size at first sexual maturity An analysis of shares of mature specimens (Fig. 8) showed that in Oran Bay, 50 % of B. boops females were mature at 14 cm of total length. DISCUSSION In Oran Bay, the overall female-male ratio was found in favor of females, an observation already made by Lamrini, 1998; Monteiro et al., 2006; Kher- raz, 2011; Kasalika et al., 2012; and Dobroslavić et al., 2017, while Bottari et al., 2014 found this ratio equally distributed in the southern Tyrrhenian Sea. The predominance of males in smaller length classes and females in larger classes is probably due to protogynic hermaphroditism already described for this species by D’Ancona, 1949; Reinboth, 1962; Frau, 1966; Gordo, 1995; Cano Fortuna & Sánchez Lizaso, 1996; Lamrini, 1998; Bottari et al., 2014. Specimens are first female and became progressively male, which is characterized by the development of Fig. 6: Section of hermaphrodite gonad of B. boops; (a) section of ovotestis × 100; (b) section of hermaphro- dite gonad showing a functioning female part and early development of a male part × 250; (c) spermatogonia × 1000. O: ovary; OI: oocyte I; Oo: oogonia; Sg: spermatogonia; T: testis. Sl. 6: Sekcija hermafroditske gonade pri bukvi (B. boops); (a) sekcija ovotestisa × 100; (b) sekcija hermafro- ditske gonade, ki kaže funkcionalni del samice in zgodnji razvoj moškega dela × 250; (c) spermatogonija × 1000. O: ovarij; OI: oocita I; Oo: oogonija; Sg: spermatogonija; T: testis. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 209 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 female organs or maturation of their products before the appearance of the corresponding male product. Evolution of the sex ratio in relation to length classes led us to establish that sexual inversion for this sparid occurs between 13 and 17 cm of total length, which is in accordance with observations made by other authors who studied the same species (Lamrini, 1998) (16 cm). Investigation of the reproduction period of B. boops following a longitudinal evolution showed that (Tab. 2), generally, this species has one long spawning season that extends from January to July. Our findings in western Algerian coasts showed that the spawning period of this Sparidae species extends from January to July, peaking in spring period, which was already reported for this same bay by Bensahla- Talet et al. (1990), and Kherraz (2011), and for the Gulf of Annaba by Derbal & Kara (2008). In central Algerian waters, this period seems to be shortened to 3 or 4 months, as reported for Al- giers Bay (Chali-Chabane, 1988) and Bousmail Bay (Dieuzeide et al., 1955; Benina, 2015). The same finding was previously observed in the Gulf of Lion (Girardin, 1981), the Thyrrhenian Sea (Bottari et al., 2014), in the Gulf of Tunis (Anato & Ktari, 1983), in Egyptian waters (Hassan, 1990), and in the Lebanese coasts (Mouneimne, 1978). The differences in the spawning period duration could be due to the inflow of Atlantic water through the Strait of Gibraltar, namely, regional differences in the time and duration of the spawning act of species in the Mediterranean basin can be related to biotic and abiotic factors, such as climate, hydro dynamism, temperatures, sa- linity, and food availability (Wootton, 1979; Pajuelo and Lorenzo, 2000; Mouine et al., 2007; Tsikliras et al., 2010). Gonçalves & Erzini, 2000, stated that the reproduction period is correspondingly much longer when environmental conditions are favorable. The upwellings and related zooplankton abundance can also affect many species reproduction (Parrish et al., 1981). With regard to the length at first sexual maturity (Tab. 2) in Algerian waters, Derbal et al. (2007) found females to be mature at 13.5 cm; in Algiers Bay this length was reported at 13.5 cm (Chali-Chabane, 1988) and 14.6 cm (Benina, 2015), in Oran Bay between 12 and 14 cm, like in some other studies in the Mediterranean. Gordo (1995) and Monteiro et al., (2006) reported that length to be between 13 and 15.22 cm in Portuguese waters, while in Span- ish waters Cano Fortuna & Sanchez Lizaso (1996) found it equal to 10.2 cm. In Italian coasts, Bottari et al. (2014) recorded it at 13.8 cm. In the Adriatic (Kasalica et al., 2011) this size was reported to be 11.5 cm TL. In Tunisian waters, the first sexual matu- rity was reached, by most of the population, at sizes between 14 and 18 cm. In Egyptian and Lebanese waters, this maturity was attained at 13 cm. Most studies found this length to be comprised between 12 and 14 cm in the Mediterranean, except Bounhiol & Pron (1916) and Kherraz (2011), while in Atlantic waters the bogue seems to reach maturity later, at 17 cm (Lamrini, 1998; Monteiro et al., 2006; Massaro, 2012), probably due to environmental conditions, which differ from one habitat to another. Environmental factors, such as temperature, salinity and food (Gonçalves & Erzini, 2000; Mou- topoulos & Stergiou, 2002; Karakulak et al., 2006; Bottari et al., 2014) are at the origin of the difference in size at first sexual maturity and in the spawning period between individuals of the same species from different geographic locations. Mortier (1992), Taupier-Letage & Millot (1998), Salas et al. (2001) consider the Algerian current as the most energetic in the Mediterranean basin, conferring to Algerian waters their relative richness. Fig. 7: Monthly changes in the gonado-somatic index of B. boops females caught in Oran Bay. Sl. 7: Mesečne spremembe v gonadosomatičnem indeksu pri samicah bukve (B. boops), ujete v Oranskem zalivu. Fig. 8: Sexual maturity for females of B. boops caught in Oran Bay. Sl. 8: Spolna zrelost pri samicah bukve (B. boops), ujete v Oranskem zalivu. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 210 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 Important upwellings, which enhance the develop- ment of plankton, the first link of the aquatic food web, are generated by the entrance of Atlantic waters via the Strait of Gibraltar. The MLS (Minimum Landing Size) set for B. boops at 15 cm of TL according to Algerian legislation (Ex- ecutive Decree no. 2004-86 of 26 Muharram 1425, corresponding to 18 March 2004) (J.O.R.A.D.P, 2004), seems to be inadequate, given that it is too close to the length at first sexual maturity, as has been established during our study (14 cm). It would be recommendable to increase this length and set it at 18 cm, thus giving the opportunity to young females to contribute to and ensure the renewal of the resource. CONCLUSIONS The results obtained in the present study shed light on the reproductive biology of B. boops in the western Algerian coast. The bogue is of commercial importance to local and national fisheries. The Tab. 2: Spawning season of B. boops in different areas. Tab. 2: Obdobje drstenja pri bukvi (B. boops) v različnih predelih. Region J F M A M J J A S O N D Lm50% Author Portugal Algarve 13-15 Gordo, 1995 Peniche Algarve 15.22 Monteiro et al., 2006 Morocco Gibraltar strait 15.40 Lamrini, 1998 Beni Ensar Port 13.30 Layachi et al., 2015 Spain Port of Castellon - Zuniga, 1967 Western Mediterranean 10.20 Cano Fortuna & Sanchez Lizaso, 1996 Canary island 17.90 Massaro, 2012 France Gulf of lion 10-20 Girardin, 1981 Algeria Algerian coasts 17.20 Bounhiol & Pron, 1916 Annaba Bay 13.50 Derbal et al., 2007 Algiers Bay 13.50 Chali-chabane, 1988 Bousmail Bay 14.60 Benina, 2015 - Dieuzeide et al., 1955 Oran Bay 17.10 Kherraz, 2011 11.70 Bensahla-Talet et al., 1990 13.30 Aoudjit, 2001 14.00 Present study Italy Gulf of Naples - Lo Bianco, 1909 Tyrrhenian Sea - Bini, 1968 13.80 Bottari et al., 2014 Tunisia Gulf of Tunis 14-18 Anato & Ktari, 1983 Croatia Adriatic Sea - Dobroslavić et al., 2017 Montenegro 11.50 Kasalica et al., 2011 Greece Central Mediterranean - Vidalis, 1950 Egypt Alexandria Bay - Hassan, 1990 13.00 El Agamy et al., 2004 Lebanon Libanian coasts 13.00 Mouneimne, 1978 ANNALES · Ser. hist. nat. · 30 · 2020 · 2 211 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 ban on trawl fishery from 1 May to the 1 August as per Algerian legislation (Executive Decree no. 03-481a of 4 Rabi‘ al-Awwal 1425, corresponding to 24 April 2004), aiming to protect the renewal of the resources, is from our viewpoint insufficient to insure the set objective. We suggest an increase of the minimum landing size and the establishment of two closed fishing seasons per year to allow the renewal of multiple spawning species in Oran Bay and protect juvenile and adult spawners from overfishing. ACKNOWLEDGEMENTS This paper is dedicated to the memory of Professor Ahmed BENSAHLA-TALET (December, 1st 1946 – July, 31th 2020) (Algeria). Part of the project was funded by MESRS-Algerian National Program of Research (CNEPRU Project code: D00L03UN310120150005). The authors want to thank AquaBior team for their precious help in collecting the specimens, and anonymous reviewers for their comments and sug- gestions that improved the manuscript. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 212 Fatiha DALOUCHE et al.: GONADAL DEVELOPMENT OF BOGUES, BOOPS BOOPS (LINNAEUS, 1758), FROM ORAN BAY (TELEOSTEI, SPARIDAE), 201–214 RAZVOJ GONAD PRI BUKVI, BOOPS BOOPS (LINNAEUS, 1758), IZ ORANSKEGA ZALIVA (TELEOSTEI, SPARIDAE) Fatiha DALOUCHE, Lotfi BENSAHLA-TALET, Sidi Mohamed El Amine ABI AYAD & Ahmed BENSAHLA-TALET Laboratoire Aquaculture et Bioremediation (AquaBior). University Oran1 Ahmed Benbella. Faculty of Natural Sciences and Life. Department of Biology. Oran-Algeria e-mail: btlotfi1977@gmail.com POVZETEK Avtorji poročajo o reproduktivnem ciklu primerkov bukve Boops boops, ujetih v Oranskem zalivu. Vzorce so z obravnavanega območja enkrat mesečno dostavili ribiči od januarja 2016 do decembra 2017. Spolni delež je bil v korist samic. Frekvenčna porazdelitev dolžine je pokazala, da so samice prevladovale pri dolžinah, večjih od 14 cm celotne dolžine, kar verjetno odraža začetek spolne inverzije, sicer že opisane pri tej vrsti špara. Obdobje drstenja, ki je bilo določeno na podlagi gonadosomatičnega indeksa, je bilo od februarja do poznega junija z vrhom v marcu in aprilu. Izsledki avtorjev prispevajo k boljšemu poznavanju razmnoževalnega cikla te vrste in bodo pomagali k pripravi ukrepov za primernejše upravljanje s staležem najbolj pogoste vrste špara, ki ga dnevno ribiči ulovijo v mnogih Sredozemskih državah in Alžiriji. Ključne besede: Boops boops, razmnoževalni cikel, sezone drstenja, velikost pri zrelosti, Oran, Alžirija REFERENCES Aboussouan, A. & J. Lahaye (1979): Les potentialités ichtyologiques. Fécondité et ichtyoplancton. Cybium, 3ème série (6), 29-46. (In French). Alegria Hernandez, V. (1989): Study on the age and growth of bogue Boops boops (L.) from the central Adriatic Sea. Cybium, 13(3), 281-288. Allam, S.M. (2003): Growth, mortality and yield per recruit of Bogue, Boops boops (L.), from the Egyptian Mediterranean waters off Alexandria. Mediterr. Mar. Sci. 4(1), 87-96. doi:10.12681/mms.244. 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