Study of reproductive aspects of Trachurus trachurus (Linnaeus, 1758) from western coast of Algeria

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1 Indian Journal of Geo Marine Sciences Vol. 47 (12), December 2018, pp Study of reproductive aspects of Trachurus trachurus (Linnaeus, 1758) from western coast of Algeria Malika Gherram*; Ahmed BensahlaTalet; Fatiha Dalouche & Sidi Mohammed El Amine Abi Ayad Laboratoire d aquaculture et bioremediation (AQUABIOR) Département de Biotechnologie, Faculté des Sciences de la Nature et de la Vie, Université d Oran1 Ahmed Ben bella, BP 1524 El M naouer, Oran 31000, Algérie *[E. Mail : gherrammalika@gmail.com] Received 20 January 2017; revised 30 March 2017 In the present work, the reproductive study of the fish species Trachurus trachurus (Linnaeus, 1758) in Algeria, was investigated which is important for fishery resources and conservation management samples were collected from Oran Bay (Western coast of Algeria) between July 2010 and June This paper provides values of sizes at first sexual maturity (L50) that were estimated for males at cm and females cm, respectively. The spawning period for the population extends from January to May and the spawning peak occurs from January to March. However, the factor of condition (K) increased in summer during the sexual resting phase. This factor is weak in winter during the period of reproduction. Regarding the sex ratio, there was no significant difference in the number of males and females. [Keywords: Western coast of Algeria; Trachurus trachurus; Sex ratio; Length at first maturity; Spawning period]. Introduction Horse mackerel, Tarchurus trachurus (Linnaeus, 1758), is a major commercial fishery for the waters of the Mediterranean Sea, taxonomically, it belongs to the family of Carangidae. This family is represented by 200 species that are widely distributed in tropical, subtropical, moderate areas of all oceans and adjoining seas 1. This pelagic fish is very common in western coast of Algeria (Oran bay), however, few studies on reproduction aspect were carried out. Recently, in 2013, Gherram et al 2. have studied the fecundity of the horse mackerel (T. trachurus) of Algeria 2. This species is considered to be an undetermined spawner 3,4. The stocks of T. trachurus have been defined for management and assessment purposes and it is assumed that these form distinct spawning populations: the southern horse mackerel around the Iberian Peninsula; the western horse mackerel in the Norwegian Sea, northern North Sea, west and south of the British Isles, western and eastern English Channel and west of France. According to Ruckert et al 5, the latter stock is divided into a distinct northern and southern component. Horse mackerel is a fairly long-lived species, reaching a maximum age of well over 30 years 6. Therefore, an occasional strong year class can lead to high abundance of this species. In the case of the western horse mackerel, the extraordinary strong 1982 year-class created a substantial fishery in the northern areas, which continued for more than a decade. As a result, T. trachurus became an important commercial species in the 1980s, 90s and is now one of the three most important pelagic species. Another reason for this is the decrease of the availability of resources due to over-fishing and the subsequent increase of value of other species in the case of horse mackerel. Assigning maturity stages by macroscopical analysis has been the most common approach used so far to describe gonadal development 7. However, there has been no agreement on the use of common maturity scale for Lucio and Martin 8. Present study consists an original research of some reproductive characteristics of the Algerian horse mackerel, including maturation process, size at first maturity and timing of spawning during a one-year period (from July 2010 to June 2011). Materials and Methods The studied specimens were collected from commercial landings carried out between July 2010 and June 2011 at the port of Oran in western of

2 2470 INDIAN J. MAR. SCI., VOL. 47, NO. 12, DECEMBER 2018 Algeria (Fig. 1). A total of 1495 horse mackerel was sampled, among which 670 were females, 797 males and 28 undetermined. The sampling rate per month was related to fish availability. Each time, the specimens were sampled per class of size, measured to the nearest one centimeter. For each specimen, measurements included total length (Lt), total weight (W) and the gonads weight (G) to the nearest decigram; sex and stage of sexual maturity were also determined using the scale recommended by Fontana 9 ; it includes sex stages of sexual maturity for both sexes as follows: Stage I: Immature; Stage II: Immature or in resting phase; Stage III: pre-spawning; Stage IV: Mature and pre-spawning; Stage V: Post-spawning. Sex ratio of males and females is monthly calculated according to the following equation: Sex ratio = (F/M); F: number of females; M: number of males. This parameter was analyzed by 1 cm length class basis and it was calculated at peak spawning. Deviation from 1:1 null hypothesis was statistically tested by x 2 -test. The laying period is determined by two methods (1) Qualitative method: it is based on monthly changes of the percentage of macroscopic development of gonad stages. (2) Quantitative method: it is based on monthly changes of parameters related to sexual maturity, such as mean gonadosomatic index (GSI) and factor of condition (K). GSI is defined by J. Lahave 10 as follows: GSI= (G/W) x 100; G: gonad weight; W: total weight. However, factor of condition follows F. kartas, J.P, Quignard 11 : K= (W/Lt 3 ) x 100; W: total weight; Lt: total length. In addition, mean GSI and K were estimated by considering separately two size ranges, which were established in accordance with the length at first sexual maturity. Size at first sexual maturity was estimated in both sexes and for the species from the percentages of mature individuals (stages III, IV and V) occurring over the reproductive period (previously determined from monthly mean GSI 9. Excel (Microsoft Corporation, USA) and STATISTICA (version 10) were used for statistical analysis. Data are expressed as Mean ± SD. To assess the variation of the variables among samples, Fig. 1 Map showing sampling location Oran bay (Algerian western coast) N, W Fig. 2 Variation of the sex-ratio of T. trachurus with the size over the period July 2010-june a two-way analysis of variance (ANOVA) was performed. Microscopic examination of gonads Gonads were fixed in Bouin for 1 week, then they were passed through acetone baths and paraffin blocks were prepared. Tissues were sectioned into 5-7 μm thickness and then stained with Hematoxylin and Eosin for females and trichromatic hot coloration for males. Results and Discussion Annual sex ratios were not significantly different from the expected 1:1 ratio, during the period of peak spawning, females outnumber males. Sex ratio by size class shows a dominance of males in sizes ranging between 12 and 14 cm, except for the class of size

3 GHERRAM et al: REPRODUCTIVE ASPECTS OF TRACHURUS TRACHURUS cm, where males outnumbered females (Fig.2 and Table.1). In mean size ranging between 15 and 20 cm, males outnumbered females, except for size 22 cm, where females outnumbered males. During our study period (from July 2010 to June 2011), length at first maturity was estimated as cm for males and cm for females (Figs. 3 and 4). Length at full maturity no significant at differences were found in the L50 between sexes (Table.2). However, they fluctuate according to month in the both sexes. The evolution of mean RGS and RHS of males and females shows similar patterns. The mean Total M F F/M (%) M/F (%) Sex-ratio Χ values of gonadosomatic index gives three peaks in January, March, May and then dropped, reaching the lowest values in summer, as shown in fig. 6, the most important peak was observed in January which means the spawning season happens in winter The analysis of the seasonal patterns of the percentage of mature T. trachurus (stage IV and V) (Fig. 5 and Table 3) and mean gonadosomatic index (Fig.6) indicate the existence of a protected spawning season that extends from January to May with a maximal sexual activity between January to June. The factor of condition K shows similar patterns in both sexes, from 2010 to 2011, temporal trends of K shows a rather apparent seasonal cycle (Fig.7). The horse mackerel reached a higher condition from September to April, whereas the minimal values appeared in October and November. The percentage of mature individuals of T. trachurus per length are estimated during the spawning season. In our study, we notice that the Fig. 3 Maturity ogive and length at first maturity L 50 in males of T. trachurus over the period July 2010 to June Fig. 4 Maturity ogive and length at first maturity L50 in females of T. trachurus over the period July 2010 to June Table 2 Results of the analysis of variance (Test F, ANOVA) of the IGS, IHS and K indix of T. trachurus Males and Females according to the months of the Oran bay. F (sexe) F (Months) F (Sexe months) IGS 3,53 ns 4,33 ** 4,77 ** IHS 2,46 ns 0,83 ns 1,38 ns K 20,86 ** 15,78 ** 15,93 ** Fig. 5 Monthly percentages of macroscopic stages of maturity in females (a) and males (b) of T. trachurus over the period July 2010 to June 2011.

4 2472 INDIAN J. MAR. SCI., VOL. 47, NO. 12, DECEMBER 2018 Fig. 6 Monthly cycle of the gonadosomatic index, hepatosomatic index (mean±sd) in males and females of T. trachurus over the period July 2010 to June values of the length at first maturity estimated in Oran bay are similar than those observed in other areas (Table.4). At first glance, the inter-annual variability in length at maturity could be attributed to the differential growth of successive annual cohorts when facing different environmental conditions. As shown in Figs. 8 and 9, ovaries and testis histology and morphology was divided into five and four stages respectively. Both the macroscopic aspect (Table 3) of gonads and the seasonal variation of the mean GSI indicate that the reproductive period lasts from January to May. Our experimental results disagree with These results, we found that the reproduction period of T. trachurus is in winter. The maximum values of the mean GSI observed in T. trachurus (especially in females) were found to be low in relation to another species. Moreover, the mean GSI reached higher values in males than in Fig. 7 Monthly cycle of factor of condition (mean±sd) in males and females of T. trachurus over the period July 2010 to June females, contrary to what is considered the norm Macer 12 and Treasurer 13. The T. trachurus of the Algerian western coast has a maximal spawning rate in winter, however it is low in summer. In fact, small pelagic adopt a spawning strategy that aims at minimizing the losses by advection, the spawning fraction, which is inversely related to atresia, varies throughout the spawning period in the same year and among years. Spawning fraction reaches its highest values at the peak of spawning. As the GSI generally depends on the length and weight of the fish, the low values of GSI measured in this work probably result from the small size of scads. Furthermore, such low values of GSI, together with the fact that no post-ovulatory follicles were found in the ovaries, tends to confirm the Arneri and

5 GHERRAM et al: REPRODUCTIVE ASPECTS OF TRACHURUS TRACHURUS 2473 Table 3 Macroscopic descriptions of the gonad maturation stages of males and females T. trachurus Macroscopic observations Stage 1: Immature, GSI mean is (0.332±0.258) for males, GSI mean is (0.469±0.233) for females. Males Females Stage 2: Maturing or in resting phase; GSI mean from 0.462±0.140 for males, GSI mean from 1.155±1.003 for females. Stage 3: Mature GSI mean from 1.989±0.929 for males, GSI mean from 1.387±0.419 for females. Stage 4: Ripe and running GSI mean from 2.445±1.444 for males, GSI mean from 3.013±1.659 for females. Stage 5: Spent GSI mean from 4.029±1.187 for males, GSI mean from 4.205±3.852 for females. Stage 6: Resting GSI mean from 1.110±0.715 for males, GSI mean from 2.014±1.297 for females. Tangerini 14 hypothesis that the most northerly part of Upper Adriatic should be excluded from the reproductive area of T. mediterraneus. However, the presencee of mature specimens suggests that the periodic findings of pelagic eggs of the genus Trachurus trachurus, which appear in very small numbers every summer could result from occasional spawners, rather than from passive transport, especially considering the relatively rapid embryonic development (24-26 h) in this species 16.

6 2474 INDIAN J. MAR. SCI., VOL. 47, NO. 12, DECEMBER 2018 Oogonia or small primary oocytes in nest with primary Cortical alveolus (Endogenous vitellogenesis) G x 100 oocyte G x 100 Part of ovary containing early and late vitellogenic oocytes with densely stained (yolk bodies, exogenous vitellogenesis) G x 400 Stage showing a preovulatory follicle Fig. 8 Cross section of ovaries from female horse mackerel T. trachurus at different maturity stages of development, N: nucleus, Nu: nucleoli, Ca: cortical alveoli. Our observations about total length at sexual maturity (18cm) confirm those of Aeneri, Lucio and Martin 14 which showed the body condition factor of horse mackerel does not appear to change during the spawning season, this is due to the replacement of fat by water.

7 GHERRAM et al: REPRODUCTIVE ASPECTS OF TRACHURUS TRACHURUS 2475 Fig. 9 Cross section of gonad at different maturity stages of development Seminiferous lobule from male s horse mackerel T. trachurus showing various developmental stage: spermatogonia (A), spermatocyte (B), spermatids (C) and spermatozoa (D). Table 4 Summary of the available information on the values of sizes at first sexual maturity (L50) of horse mackerel in the NE Atlantic and the Mediterranean Sea. Author Sampling years Area Length at first maturity (cm) [18] North Sea and English Channel (FL) [13] North Sea and English Channel [19] North Sea [20] British and Celtic Seas 22.3 males 25.4 females [21] 1943 Bay of Biscay [8] Bay of Biscay 20.1 males 20.6 females [22] North/NW coast of Spain 21.1 [23] North/NW coast of Spain 20.9 males 21.9 females [24] Lisbon 19 (FL) [25] Western coast of Portugal (SL) 2 years [25] Southern coast of Portugal 16-19(SL) [26] Portuguese Coast 22.5 [27] North Africa 15 [28] North Africa [29] Catalonia (NW Mediterranean Sea) 15.5 [30] Catalonia (NW Mediterranean Sea) 16 [32] Aegean Sea years (1996) 22 [6] FL = fork length; SL = standard length. Conclusion T. trachurus of Oran bay is gonochoric species and presents a sex ratio without significant difference (p>0.05). The values of sizes at first sexual maturity (L50) were estimated for males at cm and females at cm, the evolution of meanrgs and RHS of

8 2476 INDIAN J. MAR. SCI., VOL. 47, NO. 12, DECEMBER 2018 both sexes shows similar patterns, the macroscopic and microscopic appearance arein agreement with the different indices determined in this stuy. The mean values of gonadosomatic index gives three peaks in January, March and May, the spawning season happens in winter, whereas it has a low spawning rate in summer. Acknowledgements The authors would like to thank the anonymous reviewers for their constructive comments that greatly improved the manuscript. References 1 Valkanov, Al., Marinov, H., Danov, H. and Vladev, P., Black Sea (collection) State Publishing house, Varna, (1978) Gherram M., BensahlaTalet A., Abi Ayad S- M E-A., Dalouche F., Fecundity and Distribution of Oocyte Diameters of Horse Mackerel Trachurus trachurus from Algerian Western Coast (Oran Bay), Journal of Life Sciences, USA. Vol. 7, No. (2013) Gordo, L.S., Martins, M.M, Aspecto morfo-histológico das gónadas de sarda Scomber scombrus L. 1758, da costa portuguesa. Elaboração de uma escala de maturaçãosexual. Bol. Inst. Nac. Invest. Pescas 14, (1986) Karlou-Riga, C., P.S. Economidis., Spawning frequency and batch fecundity of horse mackerel, Trachurus trachurus (L.), in the Saronikos Gulf (Greece). J. Appl. Ichthyol. 13(3): (1997) Rückert, C., Floeter, J., Temming, A., An estimate of horse mackerel biomass in the North Sea, ICES J. Mar. Sci. 59, (2002) Eltink, A.T.G.W., Kuiter, C., Validation of ageing techniques on otoliths of horse mackerel Trachurus (L.). ICES C.M. 1989/H:43, (1989)15. 7 Abaunza, P., L. Gordo, C. Karlou-riga, A. Murta, A.T.G.W. Eltink, M.T.G. Santamaría, C. Zimmermann, C. Hammer, P. Lucio, S.A. Iversen, J. Molloy and Gallo E.., Growth and reproduction of horse mackerel, Trachurus trachurus (Carangidae). Reviews in Fish Biology, Fisheries 13: (2003) Lucio P., Martin I., Biological aspects of horse mackerel (Trachurus trachurustrachurus trachurus L. 1758) in the Bay of Biscay in 1987, ICES Document CM 1989 /H 20 (1989) Fontana A., Étude de la maturité sexuelle des sardinelles Sardinella eba(val.) et de Sardinella aurita de la région de Pointe-Noire, Cah. ORSTOM, Ser. Oceanogr. 7 (2) (1969) Lahaye J., Les cycles sexuels chez les poissons marins, Oceanis 6 (7) (1980) ). 11 Kartas F., Quignard J.P., La fécondité des poissons téléostéens, Coll. Biol. MilieuxMarins, Masson, Paris, (1984) (121 p.). 12 Macer, C.T., The reproductive biology of the horse mackerel Trachurus trachurustrachurus trachurus(l.) in the North Sea, English Channel. J. Fish Biol. 6, (1974) Treasurer, J. W., Holliday, F. G. T., Some aspects of the reproductive biology of perch Percafluviatilis L. A histological description of the reproductive cycle. Journal of Fish Biology, 18: (1981) Arneri, E., Tangerini, P., Biological data, fromthe Pipeta expeditions, on Trachurus mediterraneus(steindachner) in the Adriatic Sea. CGPM Troisième consultation technique sur l évaluation des stocks dans l Adriatique, Fano, Annexe O : (1983) Mucchiut, G., Specchi, M., Prime osservazion isullacomparsa di uovapelagiche di Teleostei del Golfo di Trieste. Bollettinodella Società Adriatica di Scienze, LXXII : (1991) Pora, E., Le chinchard de la Mer Noire (Trachurus mediterraneus ponticus), étude monographique. Institutroumainde recherches marines, Constanta (Roumanie). (1979) Polonsky, A.S., Growth and age and maturation of the horse mackerel (Trachurus trachurus (Linné) in the north east Atlantic (1969). 18 Sahrhage, D., Ein Beitragzur Biologie des Stöckers (Trachurus trachurus (L.) in Ber. Dt. Wiss. Komm. Meeresforsch. 21, (1970) Kerstan, M., Age, growth, maturity, mortality estimates of horse mackerel (Trachurus trachurus) from the waters west of Great Britain, Irel, in ArchivfürFischerewissenschaft: (1985) Letaconnoux, R., Contribution à l études des espèces de genre Trachurus trachurus et spécialement du Trachurus trachurus (Linné, 1758) de la côte Belge. Mem. Off. Sci. Techn. PecheMarit. (1951) 15, Lozano Cabo, F., El jurel o chicharro (Trachurus trachurus, L.). Trab. Inst. Cienc. Nat. José de Acosta. 3, (1952) Abaunza, P., Fariña, A.C., Carrera, P., Geographic variations in sexual maturity of the horse mackerel, Trachurus trachurus (1995) Barraca, I.F., Quelques aspects de la biologie et de la pêche de chinchard, Trachurus trachurus(l.) de la côte Portugaise. Ntas (1964). 24 Arruda, L. M., Sexual maturation and growth of Trachurus trachurustrachurus trachurus(l.) along the Portugese coast. Investigacio npesquera, 48: (1984) Borges, M.F., Gordo, L.S., Spatial distribution by season and some biological parameters of horse mackerel (Trachurus trachurusixa). ICES C.M. 1991/H :54, (1991) Gail, R., État sexuel et croissance du saurel des côtes Atlantiques du Maroc (Trachurus trachurus (L.). Ann. Biol. C.I.E.M. 8, (1954) Sedletskaya, V.A., The dynamic of spawning in Trachurus trachurus L. by shores of north-west Africa. Trudy Atlant. NIRO. 41, (1971) Andreu, B., Rodriguez-Roda, J., La pescamarítimaen Castellón. Rendimentoporunidad de esfuerzo ( ) y consideraciones biometricas de la especies de interéscomercial. Publ. Inst. Biol. Apl. 8, (1951) Planas, A., Vives, F., Contribución al estudio del jurel(trachurus trachurusl.) delmediterráneo occidental (Sectores de Vinaroz e islascolumbretes). pinst.apl. biol. 13, (1953) Alegría-Hernández, V., Reproductive cycle and changes in condition of the horse mackerel Trachurus trachurus(l.) fromthe Adriatic Sea. ActaAdriat. 35, (1994) Karlou-Riga, C., Economidis, P.S., Ovarian atretic rates and sexual maturity of European horse mackerel, Trachurus trachurus(l.), in the Saronnikos Gulf (Greece). Fish. Bull. 94, (1996)

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