Indian Journal of Geo Marine Sciences Vol. 47 (07), July 2018, pp. 1478-1485

Age, growth and reproductive biology of Goldlined Seabream sarba (Pisces: ) in coastal waters of Pakistan

1Shabir Ali Amir, 2 Sher Khan Panhwar, 2Pirzada J. A. Siddiqui,* 3Fozia Khan, 2Shehnaz Rashid & 3Ye Zhenjiang 1Zoological Sciences Division, Pakistan Museum of Natural History, Islamabad, 44000, University, Pakistan 2Centre of Excellence in Marine Biology (CEMB), University of Karachi, Karachi, 75270, Pakistan 3Collage of Fisheries, Ocean University of China, Qingdao, 266003, China *[E.Mail: [email protected]]

Received 23 September 2016; revised 06 March 2017

For the examination of age, growth and reproductive aspects of R. sarba, 504 specimens were sampled from Karachi landing site (May 2010 - April 2011), ranging from 9.8 to 33.7 cm in standard length and 38.68 to 1164 g in weight. Standard length-weight relationship for combined sexes was estimated W=0.052*SL2.893 (R2=0.984). Age and growth were determined by sectioning and interpretation of otolith of 230 (15 to 20 in each month). Age was estimated from 0 – 7 years while the length-at-age data from combined sexes was fitted by von Bertalanffy model: SLt = 29.23 (1-e-0.115(t+1.3384)) (R2 = 0.94). The overall sex ratio was 1:1.4 males (43%) to females (57%), and significantly in favor of females. Gonadosomatic indices were high from November to February and the macroscopic examination and histology of gonads indicates that spawning occurred in winter to early spring with peak in January.

[Keywords: Rhabdosargus sarba, Age, Growth, Sexual maturity, Spawning season, Pakistan]

Introduction Age and growth studies of R. sarba from east and In its geographical distribution Goldlined seabream west coasts of Australia4,12 showed considerable difference (R. sarba) occurs in inshore, estuarine and coastal in maximum length, for example, 45 cm (east coast) waters throughout the Indo-West Pacific Pacific and 37.5 cm (west coast). Similarly, R. sarba attains including the Red Sea, East Africa, Madagascar, 68.3 cm at 16 years in South African waters7 and Japan, China, Australia and Pakistan1-7. This 30.0 cm at 8 years of age from Arabian Gulf9. The inhabits in near-shore coastal waters to a depth of gonadal developmental stages and maturation in 70 meters and uses estuaries as nursery areas whereas male Goldlined seabream from Oman has also been spawning occurs in the offshore waters. In small scale observed through histological examination of gonads8. fisheries, R. sarba is considered as an important The reproductive biology of R. sarba from other parts commercial species, reported landings during the of the world has also been variously reported, for year 2000 was 80t from the New South Wales4 example, in South Africa, Hong Kong, Oman this species while Mehanna5 reported its important fishery in the is considered as protandrous hermaphrodite8, 13, and 14 Arabian Sea coastal waters of Oman. R. sarba is also and from eastern and Western Australia as rudimentary popular among anglers in recreational fisheries. In hermaphrodite4,12. Goldlined seabream possess specialized fish market, the Goldline seabream has high demand gonads having testicular and ovarian zone separated by due to its white meat and naturally sweet and connective tissues called ovotestis12, 13. distinctive taste. It is considered to be a potential Despite the importance of biological aspects, no species for aquaculture, especially in the Asian published information is available on the fishery regions6. In recent years, Goldlined seabream have biology of R. sarba from Pakistan. The paucity of been successfully cultured in India, Japan and France7 information has led to this study focusing on: (a) while in the Gulf States of the Middle East it is determine of age and growth, and (b) assessment of considered a candidate species for aquaculture8 reproductive biology of R. Sarba with respect to Different aspects of biology, ecology and fisheries length-weight relationship data, age through sectioned of R. sarba has been in focused by several researchers4-11. otoliths and gonadal studies. AMIR et al.: AGE, GROWTH AND REPRODUCTIVE BIOLOGY OF R. SARBA 1479

Materials and Methods compare W-SL relationship for females and males Goldlined seabream (R. sarba) fishes were sampled (length and weight as independent and dependent from commercial fisher catches at Ibrahim Hyderi variables, respectively, and sex as a covariate). Chi- Fish landing site (24 47 04.61N, 67 08 26.19E), square (χ2) was used to test the proportion of observed Karachi (Fig. 1), which is located near Korangi Creek, males and females, whether it vary significantly form a part of a large creek systems of River Indus delta. the expected 1:1 sex ratios. The sex ratio was This site is popular for small scale fishing activities. estimated for each month and all size classes. The fishermen mostly use small fishing crafts locally The mean length-at-age data of R. sarba was fitted known as “Hori” (6-8 meters length overall) and by von Bertalanffy21 based on the following growth categorized as “Sail boat” according to Marine equations: L  L (1 ek(t t0 ) ) Where L = predicted t  t Fisheries Department of Pakistan. Some of these length at time t, L = mean asymptotic length, K = a small crafts have small engines. Hand-line, locally −1 known as “Dori", is the main fishing gear equipped growth rate parameter (y ), and t0 = the theoretical with small hooks (Mustad 12-20 no.) to target fishes age or time at which the fish length is zero. in the creek areas. Fishing is done in shallow coastal Results and creek waters at a depth of 3-15 meters. Around Rhabdosargus sarba ranging from 12.9- 43.6 cm in 20-50 fishing crafts participate in this type of fishing total length (TL) (9.8 to 33.7 cm in standard length where snappers, seabreams, sciaenids and grunts 15 (SL) obtained throughout 12 months sampling period dominate in their daily catches . from May 2010 to April 2011. Males (n=218) ranged The present study is based on 504 individuals of from 13.4 to 41.3 cm in TL and females (n=286) from R. sarba procured in the monthly collection from 12.9 to 43.6 cm TL. Length-classes (with standard May 2010 to April 2011. Fish were measured length) of different months are represented in Figure 2 (SL, TL, nearest to 0.1cm) and weighted (nearest to 0.1 g.) and sex ratios revealed from 504 fishes through and sexed (checking gonads). Gonads were weighed Chi-square (χ2) test are depicted in Table 1. (0.001g) and preserved for histological examination. The overall male to female ratio was 1:1.4 showing Total Length (TL) and Standard Length (SL) relationship 16 significant deviation from 1:1 Mendelian ratio (χ²=30, was established through linear regression analysis . df=1, P<0.05). The monthly distribution of sexes Least-squares regression was used to estimate the during the study period fluctuated significantly and parameters of the SL-W relationship by a function of b always in the favor of females except for June (where W=aSL . The length weight data were transformed males were 52%). The maximum female to male ratio logarithmically for linear line and the equation can be of 87% was recorded in November 2010 (χ² = 12.57; demonstrated as Log W= log a + b log SL. Whereas 17 Table 1 — Chi-square values for monthly male to female ratios analysis of covariance (ANCOVA) was used to recorded for R. sarba sampled during May 2010 to April 2011(n=504)

Fig. 1 — Ibrahim Hyderi fish landing site near Korangi Creek from where Rhabdosargus sarba specimens were procured on monthly basis. 1480 INDIAN J. MAR. SCI., VOL. 47, NO. 07, JULY 2018

Fig. 2 — Distribution of male and female R. sarba in size classes (standard lengths). A total of 504 fish were sampled during May-2010 to April-2011.

Table 2 — The observed age-length key for male and female R. sarba (n = 230) collected from May 2010 to April 2011. Size-classes (SL) O I II III IV V VI VII Total 8 - 11 16 1 17 12 - 15 40 41 10 1 92 16 - 19 2 31 36 10 79 20 - 23 1 9 11 3 3 27 24 - 27 2 3 2 1 8 28 - 31 3 1 1 5 32 – 35 1 1 2 Total 58 74 55 24 6 8 3 2 230 % ages 25.2 32.2 23.9 10 2.6 3.5 1.3 0.9 100

P <0.001) and 75% in January 2011 (χ² = 9; P <0.05). between SL/W for male and female were significantly During winter to early spring season (November to different (ANCOVA, (P< 0.0001) (Figure 3). SL/W March), R. sarba rarely appeared in commercial relationship for combined sexes was W=0.052*SL2.893 landings at Ibrahim Hyderi Fish landing site, and only (R2=0.984) (Figure 4a & b). The length-length 20 fishes were found in December. This low number relationship between total length and standard length of R. sarba from November to March may be due to were also highly significant with R2=0.996 (Table 3). migration in relatively deeper water for spawning All the sectioned otoliths were examined and purposes. It is also evident that 12-15 cm SL size class yielded useful estimates. The otolith showed distinct was dominated in the population. However, only two growth zones (translucent and opaque) (Figure 5). In individuals appear in 32-35 cm size-class having this study, the individuals having zero opaque zone, six and seven year ages, respectively (Table 2 and were 25.2% followed by 32.2% having one opaque Figure 2). The regression between standard length and zone, the latter dominated the population. The weight was significant (P < 0.0001). The relationship individuals having III, IV, V, VI, VII opaque zones

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Fig. 3 — Weight-Standard length (SL) relationship of female (red points, n=286) and male (blue points, n= 218) R. sarba collected during May-2010 to April-2011 (n = 504) in Pakistan waters.

Fig. 5 — . Photomicrographs showing thin sections of otoliths obtained from 0-7 years old R. sarba (14X magnification).

Fig. 4 — Length-weight relationship analysis through: a) least square regression b) natural logarithm transformed data for combined sexes of R. sarba procured during May-2010 to April- 2011.

Table 3 — Linear regression analysis between standard length (SL) and total length (TL) of R. sarba collected during May 2010 to April 2011. The regression equation is Y= a + bX. 2 Y X N a b r SL TL 504 0.41±0.04 0.77±0.001 0.99

TL SL 504 0.59±0.05 1.28±0.003 0.99 Fig. 6 —. a) von Bertalanffy growth curve and b)

estimated parameters and fitness parameters based on (R2) values were 10%, 2.6%, 3.5%, 1.3% and 0.9%, respectively for both sexes (n = 230) of R. sarba, collected from Pakistan (Table 2). The estimated age groups in R. sarba waters. ranged between 0 to 7 years (Figure 5). The translucent zone in the otoliths of R. sarba is formed were evaluated separately for males and females as during the period of greatest growth and it is usually shown in Figure7. GSI values for male R. sarba wider than the opaque ring, particularly during the showed that the males of this species attains maturity early life of fish (Figure5A–G). The type of zone during October and November and possibly functions forming on the edge of the otolith can be recorded up to late February. Maximum recorded value of from a series of samples taken throughout the year the GSI of the male R. sarba was 5.45 in November which confirms the zones are annual (Figure 5). 2010 for fish that had total length of 23.8 cm. The mean length-at-age data of combined males The maximum gonad weight of a male R. sarba was and females was fitted by von Bertalanffy growth 17.42 g in January and the total length of that fish was model: SLt = 29.23 (1-e-0.115(t+1.3384)) R2 = 0.94. Both 30.5 cm. The identical pattern of maturity of males males and females grew quickly and reached an throughout the year was followed by the females. average standard length of 11.1 cm SL after one Maximum GSI value of 8.21 was recorded for the year (Fig. 6). Monthly variations in GSIs for R. sarba total length of female fish of 19.8cm. 1482 INDIAN J. MAR. SCI., VOL. 47, NO. 07, JULY 2018

The maximum gonad weight of 45 g was recorded Gonads in this stage were more regularly found for female R. sarba in January 2011 for which the during the study period. The immature gonads were in total length was 43.6 cm with GSI value of 4. Mean higher proportion during April to June. Macroscopically values of GSI in percentage for each month are the ovaries in this phase were small, thin and strand- shown in Figure 7, which revealed the similar pattern like and had slightly transparent to yellowish appearance of maturity with functional and resting stages for in color with indistinct blood vessels. Only oogonia both males and females. The maximum value of and primary growth oocytes were visible, thickly GSI in both sexes was recorded during winter (from packed in the ovary (Figure 9a). Developing females November to February). were more abundant during May to October 2010 Macroscopic examination of gonads and observed ranging from 9-14cm. In developing phase, ovaries GSI trend throughout the year showed the existence were becoming large and mature, and have yellowish- of only one breeding season for R. sarba, which takes orange color. Blood vessels were also distinct and place in winter (late October to early March). During oocytes visible through ovary wall. Primary growth these months maximum number of ripe gonads and oocytes (PG), cortical alveolar (CA), vitellogenic highest values of GSIs were seen while resting stages (Vtg) oocytes and some atresia were present during (testes and ovaries) were observed in March-2011 developing phase. indicating the end of the reproductive season The mature and ripe stages were observed during (Figure 7). The maturity curves and estimated sizes September to February but highest percentage was at 50% maturity for combined sexes through logistic recorded in January. Ovaries were larger and curve model and showed SL50 of 14.8 cm (Figure 8). occupied two third of the abdominal cavity. Blood Following developmental stages were recognized vessels were protruding and oocytes were visible in female R. sarba on the basis of macroscopic and macroscopically. In spawning phase, abdominal histological characteristics. cavity of the running ripe fishes were swollen and oviduct were full of hydrated ova. Advance Vtg oocytes, postovulatory follicle complex (POF) and PG were visible (Figure 9b). The regressing females were first appeared in November and the highest percentage of spent gonads were observed in March. Ovaries in this phase were loose and leathery, POF and atresia (A) were present including some CA and Vtg oocytes (Figure 9c).

Fig. 7 —. Gonadosomatic indices (mean % GSI) calculated for male and female R. sarba collected during May-2010 to April- 2011(n=504). The number by sex per month is in the Fig. 2.

Fig. 9 —.Female-gonadal stages of R. sarba: a) immature stage showing full of primary growth oocytes (PGO); b) mature and running stage having vitelogenic oocytes (Vtg), postovulatory follicle (POF) and primary growth (PG) oocytes; c) regressing or Fig. 8 —. Model of logistic curve showing 50% maturity for spent stage with atresia (A), Vtg and POF; and d) regenerating or R. sarba (combined sexes, n = 504) in Pakistan waters. resting stage having PG and POF

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Gonads in regenerating stage, marked with small (Sz) were abundant while few spermatocytes (Sc) and ovaries and indistinct blood vessels, were commonly spermatids were also present (Figure 10b). observed during March to May. Ovarian wall was The regressing and regenerating gonads, marked by relatively thick as in immature gonads, and muscle with dull milky white color and much reduced in size bundle oogonia and PG oocytes were apparent (Figure and compactness, were observed during November to 9d). Following male gonadal development stages April with the highest percentages in March. Some were recognized in R. sarba on the basis of residual spermatozoa were present with follicle cells macroscopic and histological characteristics. and connective tissues. In regenerating phase testes During immature stage testes were small and again attain smaller size and thread-like appearance. thread like, indiscernible sex, and were transparent to Spermatocytes were absent whereas some residual white in color. Only connective tissue and some spermatozoa were occasionally present. Regressing spermatogonia were present. In the developing phase and regenerating stages are shown in Figure 10c and testes were relatively larger and identifiable because Sc, Sg, and few Sz are evident in Figure 10d. of creamy in color. Spermatogonia (Sg) and Histological examination of R. sarba gonads spermatocytes (Sc) were visible (Figure 10a). revealed the occurrence of special gonads called Testes in this phase were much larger and occupied ovotestis during their early developmental stages. The usually major portion of the abdominal cavity. Spermatozoa ovotestis gonads consist of tissue of both sexes, male and females eventually grow to either male or female. The figure 11a shows inactive ovarian tissue in a mature testis of male R. sarba while both immature testicular (T) and ovarian (O) tissues are apparent in a juvenile R. sarba (Figure 11b). In the present histological examination no any evidence/slides was encountered showing degeneration of functional gonads of one sex and progressing of other sex that can lead towards functional hermaphroditism.

Discussion Goldlined seabream demonstrated a typical growth pattern similar to other teleost fishes4, 7, 9. In Pakistani waters, R. Sarba appear to have only one breeding season through a year during late winter and early

Fig. 10 — Male-gonadal stages of R. sarba: a) immature stage spring season; peak spawning period is from having full of spermatogonia (Sg); b) mature and running stage November towards the end of February as apparent showing spermatocyte (Sc), spermatogonia (Sg) and spermatozoa from the year-round data (May 2010- April 2011) of (Sz); c) regressing or spent stage with Sc, Sg, and few Sz; d) Gonadosomatic indices. The low number of R. sarba regenerating or resting stage having Sc and Sg and very few Sz. appears in landing at fish landing site at Ibrahim Hyderi during the period from November to March may be attributed to the fact that adults of R. sarba move offshore into deeper waters for spawning and the coastal and estuarine habitat are used by this species as a nursery ground4,22,23. Similar spawning season of R. sarba has also been reported from Oman waters5, 8 (from late October up to early March) and from Pescadores6 (December to March). On the contrary, this species has been reported to spawns during late winter and spring (July-November) in 7 4 KwaZulu-Natal South African waters , and eastern Fig. 11 — a) Section of a mature testes having spermatogonia and western24 Australia. (Sg) and primary growth oocytes (Pg); b) Section through 25 immature portion of gonad showing parts of both testes (T) and Sadovy suggested that trends in GSIs may also ovary (O). provide an insight into spawning behavior of fish 1484 INDIAN J. MAR. SCI., VOL. 47, NO. 07, JULY 2018

species. However, in the present study such behavioral Panhwar32 described a comparative account of five study of R. sarba was not observed. The present study growth models applied on ten fish populations and revealed that the males and females of R. sarba from the selection of best model was based on the Pakistan waters mature at the length of about 15.0 cm Akaike information criterion (AIC) and Bayesian SL. This has also been confirmed through histological information criterion (BIC). This study reveals examination. In the Arabian Gulf (Qatar waters), the that although the growth of R. sarba and maximum size at maturity of R sarba was 18.0 cm TL9. Our size at age were in agreement but its spawning pattern findings are close to the study carried out in Arabian and season differs from those reported from other Gulf9. Another study from Oman waters shows that parts of its distribution. male R. sarba mature at the length of 19 cm (TL) while female matures at a greater length8, 26. 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