Indian Journal of Geo Marine Sciences Vol. 46 (09), September 2017, pp. 1899-1907

Biology of Indian whiting, sihama (Forsskal) along the Ratnagiri coast

1Sawant P. P., 2Nirmale V. H., *3Metar S. Y., 4Bhosale B. P.4 & Chogale N.D.5

1, 2, 4 College of , Shirgaon, Ratnagiri. 415612., India 3.5 Marine Biological Research Station, Zadgaon, Ratnagiri. 415612, India

* [E.Mail : [email protected]]

Received 12 May 2015 ; revised 31 October 2016

The study found S. sihama to be an omnivore and having bottom feeding habit. formed the main food of the and included juvenile of crabs, mysids and appendages. Preference for crustaceans gradually increased with size. The fish has got a prolonged breeding season from June to February, with peak spawning activity during the period of September to December. Length at first maturity for females was found to be 167 mm. The average sex ratio of the males and females was found to be 1: 1.04 for the entire period of study. The fecundity of S. sihama ranged from 12023 to 122274 .

[Keywords: Sillago sihama, feeding, , spawning, fecundity, sex ratio, Ratnagiri]

Introduction Ratnagiri fish market at weekly interval and Fishes belonging to the family were brought to the laboratory for analysis. The are commonly known as lady fish present study is based on the total of 619 and/ or sand whitings. Eight species of lady fish/ individuals ranging in the size range from 90 to whitings are reported from India, viz Sillago 300 mm total length (TL) comprising of 263 sihama, S. vincenti, S. parvisquamis, S. males, 274 females and 82 indeterminants. The macrooolepis, S. argentifasciata, S. maculate, S. samples were collected for a period of one year chandropus and S. panijus1, 2. Of these, the from March 2013 to February 2014. Indian sand whiting, S. sihama occurs Qualitative analysis was done as per the commonly in the coastal waters of Ratnagiri. It procedure given by 5 and 6. Quantitative analysis is one of the highly priced fishes in coastal was carried out by using frequency of region of Maharashtra. In view of its economic occurrence method7. importance and culture possibilities, an attempt For calculating the gonado somatic was made to study the feeding and reproductive index, the weight of the individual fish was biology of Sillago sihama from Ratnagiri noted. The gonads were removed carefully and region. Knowledge on feeding and reproductive weighed on an electronic balance after biology which provide insight into feeding removing the excess moisture using a blotting habit, maturity size, spawning, reproductive paper. potential and recruitment will help in devising Sex ratio was calculated for different months appropriate management measures for the and size groups of the fish and was tested for . Similarly within the context of high equality using Chi - square test. culture potential of S. sihama in India3, 4 Maturity stages of S. sihama were understanding its biology is vital. classified as per8. The stages are I) Immature, II) Maturing, III) Mature, IV) Ripe and V) Spent. Material and Methods The fecundity was studied by examining S. sihama samples were collected from matured preserved . The fecundity was the Mirkarwada fish landing centre and the determined by the formula,

1900 INDIAN J. MAR. SCI., VOL. 46, NO. 09, SEPTEMBER 2017

TW and fish eggs also formed the part of the diet F = × number of ova counted in though for most of the months. In most fishes, in SW the sub-sample all months, a great part of the stomach content was constituted by digested and semi- digested Where, F = Fecundity, TW = Total weight of matter. While sand grains were also reported the , SW = Sub-sample weight from the fishes almost during all the months For the ova diameter studies, intra thereby indicating bottom feeding behaviour. ovarian eggs from anterior, middle and posterior It is seen from size wise analysis of diet regions of ovaries were taken. The progress of that the preference for crustaceans gradually growth of ova from one stage of maturity to increased with growth. Crustaceans were another was observed by using Motic Images recorded highest in the size group 215-224 mm Plus 2.0 Digital Microscopy Software. For (66.66%) and lowest in the size group 115-124 determining the length at first maturity (Lm), mm (7.69%). were found in high specimens with ovaries in stages III, IV and V percentage in size group of 215-224 mm. The of maturation were considered as mature and the size group 215-224 mm recorded highest proportion of such mature fish in each length percentage (33.33%) of fish, while the lowest group determined. The length, at which about was recorded in 135-144 mm (5%). Highest 50% of the fish are mature, has been taken as percentage of digested matter was recorded in the Lm. For histological study, the gonads were 95-104 mm (100%) and the lowest in 225-234 collected from individual fish and fixed in mm and 245-254 mm size group (25%). While Mossman’s fixative (10 ml formalin, 10 ml highest percentage of semi-digested matter was glacial acetic acid, 30 ml of 95% alcohol and 50 recorded in 295 -304 mm size group and lowest ml distilled water). in 205-214 size groups (20.00%). The Required gonad portion were taken and occurrence of sand grains was also recorded in processed using standard protocol and gut in size groups of 115-124 to 225-234 mm. embedded in paraffin wax. Sections were Month wise data shows that highest percentage stained with haematoxylene following the of empty stomachs were recorded in August procedure described by Weesner 9. followed by in October 33.33%, July 30%, November 16.36% and June 14.81%. The month Results and Discussion of April recorded highest percentage of full The details of qualitative and stomachs (25%). In March the percentage of ¾ quantitative analysis of stomach contents of stomachs (46.34%) were high followed by S. sihama during different months are February. In May, the percentage of ½ stomachs presented in Table 1. was high (48.83). Gut content analysis indicated that crustaceans Radhakrishnan9 observed that the polychaetes formed the main food of the species which are commonest organisms forming a very large included the juvenile of crabs, mysids and proportion of the food throughout the year. crustacean appendages. Polychaetes, fish scales

Table 1 -Average percentage composition of food items in the stomach of S. sihama from March 2013 to February 2014 Sr.N Months/ Crustaceans Polychaetes Fishes (scales, Sand Semi-digested Digested o food items eggs) matter matter 1. March 25 8.33 - 16.66 37.5 41.66 2. April 29.41 5.88 29.41 5.88 23.52 52.94 3. May 19.23 - 11.53 7.69 15.38 61.53 4. June 22.22 - 37.03 7.40 29.62 44.44 5. July 30 - - - 30 40 6. August 11.76 - 8.82 - 20.58 76.47 7. September 21.62 - 11.76 11.76 29.41 78.37 8. October 18.18 - 4.54 - 27.27 56.81 9. November 31.03 - 6.89 6.89 37.93 58.62 10. December 33.33 3.70 11.11 3.70 55.55 48.14 11. January 12.5 4.16 25 8.33 66.66 33.33 12. February 54.54 27.27 36.36 18.18 63.63 36.36 SAWANT et al.: BIOLOGY OF INDIAN SAND WHITING 1901

Table 2 -The gonadosomatic index of S .sihama February percentage of empty stomach was recorded high. During March 2013-February 2014 The gonado-somatic index (GSI) was Month GSI (%) ± SE t-test calculated for each individual and grouped into (p –value) Male Female sex and averaged for each month (Table 2). March 1.37±1.02 1.33±0.71 NS Higher GSI values for females were observed during months of September, October, April 0.38±0.02 2.16±0.25 NS December and January while for males GSI was May 0.41±0.07 1.54±0.18 0.0001 found to be higher in months of September, June 0.21±0.02 1.44±0.13 0.0001 October, November and December. There was July 0.94±0.36 0.42±0.10 NS Aug 0.35±0.04 1.82±0.24 0.0001 no significant difference between GSI values of Sep 1.16±0.23 2.69±0.58 NS male and female except May, June October and Oct 1.36±0.07 3.45±0.27 0.0001 December. Nov 1.57±0.33 1.75±0.17 NS SS- Significant, NS- Not significant According to Jayasankar 15, GSI value is high in Dec 1.67±0.24 1.98±0.16 0.0001 Jan 0.81±0.08 2.35±0.30 NS month of November for S. sihama from Gulf of 20 Feb 0.97±0.11 2.02±0.38 NS Mannar. Mirzaei et. al., observed that maximum GSI values were found during March Among crustaceans, and crabs were - May with highest GSI value in April (4.1) for commonly observed from Mandapam and females and 1.7 for males. There was no Rameshwaram Island. Rao and Sivani10 reported significant difference in GSI of male and female (p> 0.05) in the south coast of Iran for S. that S. sihama is omnivorous fish and the gut 16 content of this fish consisted of polychaetes, sihama. Krishnamurthy and Kaliyamurthy amphipods, crustacean larvae, diatoms and reported that the higher values of molluscs. Sand particles in traces were also gonadosomatic index were observed during observed in the guts indicating that this fish is a June-August and December-January from 11 Pulicat Lake for S. sihama. According to Reddy bottom feeder. Shamsan reported that 17 crustaceans and polychaetes form major food and Neelakantan the GSI values in both the sexes increased gradually from May to reach a items in the stomach, constituting 28.07% and 18 22.33% respectively of the food composition. peak during August. Vinod and Basavaraja Digested matter was also found in large reported that, GSI was higher during September quantities (19.91%) followed by sand grains and October in females whereas mature males (11.83%) fish (5.63%) molluscs (3.56%) and were observed during June, October November, nematodes (2.49%).According to Motlagh et.al., December and January. 12 diatoms were found to be the most preferable In the present study, data on sex ratio of food of plant origin where it occurred in more S. sihama showed that the average sex ratio of than 59.52% of the examined fish. the males and females was found to be 1: 1.04 Weerts et al., 13 noted that fishes less for the entire period of study (Table 3). Chi- than 60 mm standard length consumed primarily square test of significance revealed no planktonic prey mainly larvae and copepods, significant difference in proportion of males and while larger fishes feed on benthic crustaceans, females except during the months of June, 14 August and November, when the population had polychaetes and bivalves. Gowda et al, 15 reported that crustacean were preferred by fishes highernumber of males. Jayasankar , reported of total length 40-100 mm while in fishes larger that during most of the months, females out- than 100 mm diet mainly consisted of numbered males and overall sex ratio was 1.1:1 (female:male) of S. sihama from Gulf of polychaetes, crustaceans, fishes and 20 miscellaneous food items. Mannar. Khan et. al., reported the sex ratio of 11 male to female to be 1: 1.13. Krishnamurthy Shamsan observed that S. sihama fed actively 16 during pre-monsoon period (February –May). and Kaliyamurthy reported a preponderance of Percentage of full stomach was observed in males in the 161-240 mm size range and month of April and highest percentage of empty females in the 101 -120 mm and 261 -340 mm size groups. stomachs was found in month of June. In March 20 the percentage of quarter three stomachs Mirzaei et. al., reported overall sex ratio to be 1.2: 1 (Female : Male) from south (46.34%) were high followed by February. 11 According to Radhakrishnan9, feeding becomes coast of Iran. According to Shamsan, , the active from March to May. From September to ratio of males to females was found to be 1:1.17. 1902 INDIAN J. MAR. SCI., VOL. 46, NO. 09, SEPTEMBER 2017

Table 3- Sex ratio of Sillago sihama during March 2013- February 2014 Months Total Males Females Sex ratio Chi-square (M:F) Mar-13 26 10 16 1 : 1.6 1.38 NS Apr-13 21 11 10 1.1 : 1 0.04 NS May-13 58 31 27 1.14 : 1 0.26 NS Jun-13 35 25 10 2.5 : 1 6.42 SS July-13 16 5 11 1: 2.2 2.25 NS Aug-13 47 16 31 1: 1.93 4.78 SS Sep-13 62 26 36 1 : 1.38 1.7 NS Oct-13 50 20 30 1: 1.5 2 NS Nov-13 60 38 22 1.72 : 1 4.26 SS Dec-13 45 23 22 1.04 : 1 0.02 NS Jan-14 66 32 34 1: 1.06 0.06 NS Feb-14 51 26 25 1.04 : 1 0 NS

According to Vinod and Basavaraja18, during all the months of the year. The largest the results of sex ratio reveal that females eggs examined in September showed the nearly dominated over males throughout the period, ripe condition from Mandapam and expect in the months of October and December Rameshwaram Island. Shamsan11 reported that when the population had a slightly higher females of S. sihama in stage III with mature percentage of males from Mangalore waters. gonads appeared round the year except in March It was seen that in females, stage I 2004, while females with stage IV gonads were (immature) was observed in months of March, observed during period lasted from June to April May, June, August and February with high December and few were found in February. percentage in month of April (60.50%). Stage II Fishes with immature and maturing gonads were (maturing) was observed round the year except present all round the year which indicates a in December, with high percentage in March protracted breeding behaviour. Vinod and (49.73%). Stage III (mature) with mature Basavaraja18, reported that the maximum gonads appeared round the year except in March percentage of mature males of S. sihama (100%) and April and highest percentage of mature during the month of June, while highest female (stage III) were observed in month of percentage of mature females (87.5) was July (70.76%). Females with stage IV (ripe) recorded in the month of June, followed by May gonads were observed during period from May from Mangalore waters. to February with high percentage in month of Percentage occurrence of matured October (54.86%) and November (52.35%). individuals plotted against different size groups Spent individuals (stage V) were observed from in females and the same is given in Fig 1. The September till March with high percentage of size at which females become mature is spent ovaries was observed in month of estimated as 167 mm total length. February. From the maturity stages studied it is observed that females with ripe gonads are observed during August to February. Similarly mature gonads are noted during the months from July to December while maturing gonads are observed during March to May in higher percentage and less during June to February. It can be concluded that the S. sihama from Ratnagiri coast has got a prolonged spawning period and possibly spawning takes place more than two times in the season. The findings are substantiated by higher GSI values observed during the period. Radhakrishnan 9 reported that immature eggs occur in every adult female of S. sihama Fig 1-Length at first maturity in S. sihama

SAWANT et al.: BIOLOGY OF INDIAN SAND WHITING 1903

Jayasankar 15 reported that 50% females The size of ova ranged from 0.000- become mature at 170-179mm length group. 0.475 mm. In the stage I (immature ovary) the Males and females became mature at size of size of the ova ranged from 0.00- 0.125 mm 132-138 mm total length20. According to with mode value 0.100 mm. In stage II Shamsan11, both sexes became mature at the size (maturing ovary) the size of the ova ranged from group of 155-164mm total length. Size at first 0.126-0.250 mm with mode value 0.210 mm. In maturity varies according to the distinct stocks stage III (mature ovary) the size of ova ranged present in the different geographic regions. from 0.251- 0.350 mm with mode value 0.321 The absolute fecundity of S. sihama mm. In stage IV (ripe ovary) size of ova ranged ranged from 12023 to 122274 eggs per female from 0.351 to 0.450 mm with mode value 0.360 with an average of 32855 eggs. A positive mm while in stage V (spent ovary) size of ova correlation was found between fecundity and ranged from 0.005-0.125 mm with a modal total length, body weight and ovary weight. value of 0.008 ( Fig.2). Maximum ova in stage I There is wide variation in the estimated value of were observed in April which progresses to fecundity reported by different workers in S. stage II in May and move to stage III in the sihama. Reproductive potential vary in different months of June and July. Ova in maturity stages stocks of species found along the different of I to III are found in these months in regions. Similarly many factors influence appreciable numbers, while maximum ova are fecundity such as frequency of spawning, observed in the months of July, September and parental care, size, population density and December. It is seen that these ova progresses to most importantly environmental factors such as ripe stage in October, November and February temperature, salinity and availability of food. 21. indicating spawning takes place more than twice Jayasankar 15, observed the fecundity of during the spawning season extending from S. sihama vary from 6956 to 48373, showing August to February. This can be substantiated positive correlation with length, body weight from the month wise maturity stages observed and ovary weight. Khan et. al., 19 reported the and GSI values of females and males. mean fecundity of S. sihama to be 58781. Different workers have quoted varying Krishnamurthy and Kaliyamurthy 16 reported the values of ova diameters in different stages of average fecundity of S. sihama to be 156711 maturity. Jayasanker 15 stated that maturing and from Pulicat Lake. Palekar and Bal 22 reported immature groups of ova pass in succession to the fecundity of S. sihama between 16682 to advanced maturity stages and progress of fresh 166130 from Karwar waters. Radhakrishnan 9, batches of mature ova from immature stock studied the fecundity of S. sihama and found takes place. Palekar and Bal 22 reported that the that the ovaries of the fully mature specimens of ova attain maximum size at complete maturity contained on an average 14000 eggs from during August to October when spawning takes Mandapam and Rameshwaram Island. place, while majority of the ova are in maturing According to Shamsan 11 the total number of stage during major part of the year and apparent mature eggs varied from 11376 to 103695 and majority of immature ova during November, average fecundity of S. sihama was 42575 from marks the end of breeding activity. Goa waters while according to Vinod and Radhakrishnan 9 studied the size progression of Basavaraja18, the absolute fecundity of S. ova during the different months of the year. He sihama from Mangalore waters varied between stated that immature eggs occurred in every 24439 and 59372 eggs per female, while the adult female during all the months of the year relative fecundity was observed to be between while the largest eggs were found from 429953 and 866968 eggs per kg body weight of September to February thereby suggesting female. The logarithmic relationship between possible spawning season extending from fecundity and body length (L) is expressed by August to February. Shamsan 11 studied the size the formula as: Log F= 3.770+0.3060 Log L (r frequency distribution of oocytes in the stages I = 0.76); the logarithmic relationship between - V of maturity. He reported the presence of fecundity and body weight (W) is expressed by three distinct modes of ova in mature ovary the formula as: Log F= 2.324+1.1672 Log W ( r besides the immature stocks, indicating that S. = 0.39) while logarithmic relationship between sihama from Goa waters spawns thrice a year. fecundity and ovary weight (OW) is expressed Immature stage is observed in month of by the formula as Log F= 4.0265+1.2514 Log March and April. At immature stage oogenesis OW ( r = 0.92) changes from oogonia to primary oocytes and 1904 INDIAN J. MAR. SCI., VOL. 46, NO. 09, SEPTEMBER 2017 then secondary oocytes. The oogonia are small rounded cells with relatively clear zone of cytoplasm. Maturing stage is observed in month of May wherein gonads appear with visible nucleus and cytoplasmic layer are thick and transparent. Maturing testes are flat, leaf-like but slightly thick. They had spherical nucleus with distinguishable nuclear membrane. The follicles are observed to be containing spermatocytes, but no spermatozoa were seen. Mature stage observed in month of July and August. In mature stage ovaries are oblong, transparent with opaque eggs. At this stage their nuclei increase in size. Oocytes are surrounded by isolated layer of follicular epithelium. In case of testis spermatogonia, primary and secondary spermatocytes are detected at mature stage. Ripe stage is observed during the months of October, November and December. In ripe stage, the testis were observed with full the entire body cavity and flabby. The ovary during ripe stage occupies entire body cavity, a few large eggs are observed. The yolk granules and nucleus appear intermingled with cytoplasm. Spent stage was observed in February month.

In spent stage, the ripe ova were discharged from the ovary. Ovary is shrunken, with blood vessels and having a hollow appearance. Follicular walls are found to be breaking. In spent stage, testis are loose, the follicles collapsed, residual sperms and phagocytes are present, while in females the gonads are observed to be loose, follicles are collapsed, residual eggs and phagocytes are present (Fig. 3). Mirzaei et. al., 20, studied histology of S. sihama and reported that ovary consist of an ovarian wall and numerous developing oocytes within follicles, which were embedded in a mass of connective tissue while vesicle (vertical alveoli) and yolk granules stages were present during the year except June and July while maturation, Fig.2- Stagewise ova diameter trend in S. sihama hydration and ovulation stages were found from March to August. According to Vinod and The immature testis is characterised by Basavaraja 18, the ovary of S. sihama consists of the presence of seminiferous lobules, an ovarian wall and numerous developing spermatogonia and spermatocytes. The ripe oocytes within follicles which are embedded in testis shows the confluence of several a mass of connective tissue; the ovary is seminiferous lobules leading to the flow of composed of atretic oocytes (corpus atreticum) mature spermatozoa through the sperm duct. and corpus luteum (post-ovulatory follicle). The The spent testis depicts empty seminiferous immature ovary shows maximum percentage of lobules, some residual spermatozoa and oogonia apart from immature and maturing spermatogonia. The results of the histological oocytes whereas the mature ovary has maximum studies demonstrated the presence of oocyte at number of mature, ready-to-ooze, vitellogenic different maturity stages indicating S. sihama to oocytes and a few atretic oocytes. be a batch spawning fish. Goodall et al. 23 SAWANT et al.: BIOLOGY OF INDIAN SAND WHITING 1905

a A

b B

c C

d D

e E

Fig 3- Histological sections of ovary and testis

a - immature female b - maturing female A - immature male B - maturing male c - mature female d - ripe female E. spent female C - mature male D - ripe male E. spent male

1906 INDIAN J. MAR. SCI., VOL. 46, NO. 09, SEPTEMBER 2017 studied the histology of gonads of free and 8. Shamsan, E.F., Ecobiology and fisheries of an captive simmer whiting S. ciliata and found economical important estuarine fish Sillago sihama (Forsskal). Ph.D (Marine Science) Thesis that the captive females were non-reproductive, (Goa University), Dona-Paula, Goa., (2008) 1- reaching only the vitellogenic stage before the 230. eggs were resorbed by atresia. Histological and 9. Radhakrishnan, N., A Contribution to the biology histochemical changes accompanying pre- of Indian sand whiting Sillago sihama vitellogenic and vitellogenic phase of the (Forsskal).Indian J. Fish., 4(2) (1987) : 254- 283. oocyte development of S. sihama were 10. Rao, L. M. and Sivani, G., The food preferences 24 described by Jayasankar and Alagarswamy . of five commercially important fishes of They found that towards the end of Gosthani . Indian J. Fish., 43(2) (1996) : vitellogenesis, the oil droplets coalesce and 199-202. 11. Shamsan, E. F. and Ansari, Z. A., Studies on the yolk appears as a homogenous mass. From reproductive biology of Indian sand whiting. histological findings it can be inferred that peak Sillago sihama (Forsskal). Indian J. Mar Sci., spawning season of S. sihama along the 39(2009) : 280-284. Ratnagiri coast is from September to December 12. Motlagh, A., Hakimelahi.M., Ghodrati, M., thereby substantiating the results of ova- Vahabnezhad, A. and Taheri, A., Feeding habit and stomach content of Silver Sillago, Sillago diameter and GSI studies. sihama, in the northern Persian Gulf. Iranian J. Fish. Sci. 11(4) (2013) : 892-901. Conclusion 13. Weerts,S. P., Cyrus, D.P. and Forbes, A.T., The It is concluded that S. sihama is an omnivore diet of the juvenile Sillago sihama (Forsskal 1775) from three estuarine systems in KwaZula- mainly feeding on juveniles of crustaceans, Natal. Water SA, 23 (1) (1997): 95-100. crabs, mysids and crustacean appendages. The 14. Gowda, H. H.; Joseph, P. S. and Joseph, M. M. spawning season of the species is from June to Feeding Ecology of the Indian Sandwhiting, February with the peak activity during Sillago sihama (Forskal); in: The First Indian September to October like other estuarine Fisheries Forum, Proceedings; edited by Joseph, M. M.; Asian Fisheries Society, Indian Branch; fishes. (1988) pp 263-266. 15. Jayasankar, P. Sillaginid fishes of Palk and Acknowledgement Gulf of Mannar with an account on the maturation Authors are grateful to the authorities and spawning of Indian sand whiting, Sillago sihama (Forsskal).Indian J. Fish.,38(1990) :13- of Dr.B.S. Konkan Krishi Vidyapeeth, Dapoli, 25. Dist. Ratnagiri (Maharashtra) for providing 16. Krishnamurthy, K. N. and Kaliyamurthy, M. facilities to carry out this work. 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22. Palekar, V. C. and Bal, D. V. Studies on the changes in the gonads of summer whiting maturation and spawing of the Indian sand Sillago ciliata. J. Fish Biol., 30(1987) : 589-595. whiting Sillago sihama from Karwar waters, 24. Jayasankar, P. and Alagarswamy, K.Histological department of Zoology, Institute of science, and histochemical observations on the oocytes in Bombay. 54(1961) : 76-93. the sand whiting, Sillago sihama (Forsskal). 23. Goodall, J. A., Capra, M. F. and Blackshaw, A. Proc. Indian Nat. Sci. Acad., 60 (2) (1994) : 173- W. Quantitative histology and essential 182.