Reproductive biology of Etroplus suratensis (Bloch) from the Vembanad wetland system, Kerala

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1 Indian Journal of Geo-Marine Sciences Vol. 43(4), April 2014, pp Reproductive biology of Etroplus suratensis (Bloch) from the Vembanad wetland system, Kerala 1,2 L Bindu* & 2 K G Padmakumar 1,2 Kerala Agricultural University, Regional Agricultural Research Station, Kumarakom Kerala, India M S M College, Kayamkulam, Alappuzha, Pin , Kerala, India *[ bindukylm@gmail.com] Received 16 July 2012; revised 15 November 2012 In the present study, data on sex ratio, maturity, Gonadosomatic index, fecundity and oocyte distribution of the pearlspot, Etroplus suratensis, were evaluated. Samples were collected from the landings of Vembanad lake during Male-female ratio was found to be 1:0.8. Maximum GSI in male and female was 1.45 and 4.43 respectively. L 50 was 19.5 cm in case of males and 20.0 cm in case of females. Absolute fecundity, varied between 874 and 7554 with an average of Fish is an asynchronous spawner with different clutches of ova, varied between 0.25 to 2.75 mm. [Keywords: Etroplus suratensis, Biology, Fecundity, Asynchronous spawner] Introduction Popularly known as Karimeen, E. suratensis is widely distributed in almost all the brackish and freshwaters of peninsular India. It is essentially a brackish water fish that has become naturally acclimatized to freshwaters. It is an economically important food fish and is a delicacy that fetch a very high price. Owing to its omnivorous feeding habit, it is much suited to aquaculture (Bindu and Padmakumar, 2008). The fish breeds naturally in confined conditions and is ideally compatible for polyculture with both freshwater and brackish water fish and prawn species (Thampy, 1980). Information on the biological features of E.suratensis is indispensable for devising valid programs for its conservation. Biological characterization will also be of immense use for identifying the characteristic of the species that qualify them as candidates for aquaculture. Critical life history parameters linked to artificial breeding and culture, such as sex ratio, size at maturity, gonadosomatic index, fecundity and oocyte size-frequency profiles were monitored and biological information quantified. Rather than working on a hit and trial basis, these information were found essential * Present address of the corresponding author: not only for evolving captive breeding protocols but also for formulating sustainable conservation programs. Materials and Methods Monthly samples were collected from gill nets and scare line fishing during from the landings of Vembanad lake (Lat & N and Long & E), on the south west coast of India. Total length L T (cm) and total weight W T (g) were recorded. Gonads were separated and subsequently weighed to 0.1g and macroscopically analyzed for sex determination and maturity stages. In the absence of specific sexual dimorphism, sexes were determined by examining the gonads. A total of 626 fishes, comprising 351 males (L T cm) and 275 females (L T 8-30 cm), were examined. Difference in sex ratio between reproductive and non-reproductive period were compared by applying Pearson χ2 test. On the basis of the maturity stages observed, the ovarian cyclicity of E. suratensis could be divided into multiplication, growth, differentiation, maturity and depletion phases commonly identified as stage I- immature, stage II- maturing, stage III- mature and ripening, stage IV- ripe and stage V- spent. In females, the maturity stages could be demarcated on

2 BINDU & PADMAKUMAR: REPRODUCTIVE BIOLOGY OF ETROPLUS SURATENSIS 647 the basis of colour and relative size of the gonads with reference to the body size, ova diameter and the extent of yolk formation, whereas in males, it was based on the external appearance of the testis. The size at which 50% of the fishes reach maturity (L 50 ), was determined by grouping fishes in stages III and IV separately, into 2.5 cm size groups and their frequencies were scaled into percentages. In order to determine the prime spawning season of the species, gonadosomatic index (G.S.I.) was monitored round the year (n=610) and was estimated by using the formula GSI = (weight of the gonad/weight of the fish) 100. Preserved ovaries were used to estimate fecundity (F) and oocyte distribution. Fecundity was estimated by using the formula, F = (No. of oocyte in the sample/weight of the sample) weight of the ovary. For this, a total of 61 ovaries in the stage III and IV were collected from fishes ranging between 15.3 and 26.7 cm L T and 80 to 380 g W T. Simple regression analysis of the L T, W T and ovary weight on fecundity were carried out (Bailey, 1995). A small portion of the ovary was taken and the diameters of the intraovarian eggs were measured to the nearest 0.01mm using an ocular micrometer fitted to a CETI trinocular microscope. Oocyte diameter frequency of different stages of maturity, pattern of progression of ova during different months and the modes in size frequency distribution were also monitored. A total of 1940 ova from 86 ovaries were examined. The maximum oocyte diameter for mature females was obtained by averaging the measurements of at least 50 of the largest oocytes (Wu et al., 2001). For histological observations, small pieces of ovaries were fixed in Bouin s solution for 24 h and then immersed in 80% ethanol. After dehydration with a series of ethanol and benzene, they were embedded in paraffin and were serially sectioned at 3-4 µm thickness and stained with haematoxylin-eosin. Results E.suratensis is monogamous and identification of sexes is possible only during the breeding season. Ovaries were bilobed, left lobe was slightly smaller than the right. Testis was thin and tubular. Genital papillae of the female became reddish and broader and modified into an ovipositor while in male it became thin and pointed. Just prior to spawning, the males become deeply coloured and the colour bands become strongly marked with a greenish blue iridescence and pearly white spots. The rayed portions of the dorsal and anal fin also become slightly reddish. Male-female ratio in the whole population was found to be 1:0.8. A perceptible preponderance of males over females was noticed in the exploited catches. Males, the outnumbered sex, indicated a higher average size (L T 19.9 cm, W T 211g) than the females (L T 18.7 cm, W T 170 g). The sex ratio was found to fluctuate widely and in most of the months, males dominated the females (Table 1). In gill netting the ratio was 1:0.5 where as in scare line fishing, it was found to be 1:1.1. Chi-square(χ2) analysis indicated significant differences in sex ratio during January and October. Gonadosomatic Index (GSI) in E. suratensis varied between 0 and 1.45 in male and 0.01 and 4.43 in female. Fluctuations in GSI showed a bimodal pattern, high values during February-April and June-October indicating the occurrence of fully ripe fishes during these months (Table 2). Apparently, the trend was almost similar for both the sexes. Ovarian weight shows perceptible and rapid increase during April and June and this coincided with the increased incidence of fully ripe individuals. In males, GSI values were however, highest during June, followed by February and November. In E.suratensis, all the four stages of maturity were represented in varying proportions through out the year and the minimum size of mature specimen was 14.5 cm invariably, among both males and females. L 50 was 19.5 cm in case of males and 20.0 cm in case Month Table 1 Sex ratio of Etroplus suratensis in collections from Vembanad lake n Percentage of Ratio Male Female Male: Female January : February : March : April : May : June : July : August : September : October : * November : December : Total : * n= number of fishes, * Significant (P<0.05) χ2

3 648 INDIAN J. MAR. SCI., VOL. 43, NO. 4, APRIL 2014 Month Table 2 Gonadosomatic Index of Etroplus suratensis from Vembanad lake Male Female Range Mean + SD Range Mean + SD n = 610 January February March April May June July August September October November December n = total number of fishes of females. (Fig. 1). Evidently, size groups up to 12.5 cm were apparently immature or maturing types. Percentage of mature fishes were found to be higher in the size range, 17.6 cm to 35 cm. Mature males and females increased rapidly with size and beyond 27.6 cm, all specimens were found to be of the mature type. Macroscopic appearance of ovary also indicated that both immature and mature ones occurred round the year, and spent ovaries begin to appear from June to August. Apparently, the fish was found to attain maturity by the end of first year. Seasonal changes in the stages of maturity were perceptible in the histological investigations (Fig. 2). The absolute fecundity, varied from 874 (L T 19 cm, W T 180 g) to 7554 (L T 18.8 cm, W T 175 g) with an average of The fecundity indices in relation to various length groups in E. suratensis is given in Table 3. Relative fecundity or number of eggs produced per gram of body weight, varied from 4 to 51 with an average of 16. Number of eggs per kg body weight ranged between 3655 and with an average of The fecundity values were plotted against the respective L T, W T and ovary weight as a scatter diagram (Fig. 3). The diameter of intra ovarian eggs did not indicate any significant difference in size of ova in the anterior, middle or posterior parts of the ovary. Thus, it could be presumed that oocyte size frequency distribution with in the ovary is almost uniform in pearlspots. The size of the ova, however, was found to fluctuate widely between 0.25 to 2.75 mm. The distribution of ova in ovaries of different stages of maturity in E. suratensis is given in (Fig. 4). Fig. 1 Size at first maturity (L 50 ) of E.suratensis collected from Vembanad lake. (a) Male (b)female, n = number of fishes

4 BINDU & PADMAKUMAR: REPRODUCTIVE BIOLOGY OF ETROPLUS SURATENSIS 649 Fig. 2 Histological appearance of oocyte development in different stages of ovary. Perinucleolus (PE); Yolk vesicle (YS); Primary yolk stage (PYS); Tertiary yolk stage (TYS); and Ripe egg (RE). (Scale bar = 0.1 mm) In the immature stages, most of the oocytes were <1.0 mm, and in stage II, the maturing ova from among the immature stocks appear to get separated. As the ovary passes from stage II to stage III, size of the ova further increased and the second batch of ova got separated from the first. Both the batches of eggs, thus appeared apparently separated. In the ripe and gravid fishes, the oocyte size exhibited two distinct peaks at 2.5 mm and 1mm. The large yolked eggs (2.5 to 2.75 mm) comprised almost 49.5% of the total ova and they appeared separated out from the immature stock (0.75 to 1.75 mm) of eggs constituted 21%. In spent fishes, the mature eggs remained fully ovulated and all eggs (1.0 to 1.5 mm) that underwent final maturation appeared virtually released. The pattern of distribution of ova during different months is shown in (Fig. 5). Preponderance Table 3 Fecundity of Etroplus suratensis from the Vembanad lake (Mean values are given) Size Group (cm) n L T (cm) W T (g) Fecundity n= number of fishes of immature eggs in ovaries, in collections made during May-June and October-January was perceptible. It appears that maturation of ova begin in January-February when the ovary is characterized by fully mature ova. A second spawning season with maturation begins by June and again the modal size of

5 650 INDIAN J. MAR. SCI., VOL. 43, NO. 4, APRIL 2014 Fig. 3 Linear correlation of absolute fecundity with (a) fish length, (b) fish weight and (c) ovary weight in E.suratensis. r = correlation coefficient, n = number of females ova is reached by October. This second spawning season appears to be staggered and prolonged. Discussion Assessment of the breeding habits of E. suratensis, in different peninsular waters viz., Pulicat lake, Chilka lake, Kali estuary, Nethravathi-Gurpur estuary have been attempted by several workers (Prasadam, 1971; Jhingran and Natarajan,1969; Raju et al., 1987; Keshava et al.,1988). However, detailed reproductive biology with reference to the conservation management, has not been attempted. It is well known that even within a species and among populations surviving at different geographical locations, there occur major variations in life history patterns. Such variations in reproduction, growth and life history fitness traits are of crucial significance for assessing the long term variability of the fish species (Ponniah and Lal, 2000). Like other cichlids such as Oreochromis spp., Etroplus suratensis exhibits some degree of sexual dimorphism, males being larger than females of equivalent age. Variations in morphology of gonad is linked to the breeding habit of the fish (Billiard et al., 1982). Large testis and high GSI values are characteristic to species with sperm competition where as males that invest energy in parental care will have a small testis (Munro et al.,1990; Valdes et al., 2004). The tubular testis in E. suratensis also appear to be linked to their unique habit of parental care and monogamy. It is not possible to sort males and females until a pair is formed and ovipositor of the female becomes enlarged. It has been observed that in males the coloration and iridescence become more intense close to spawning. This peculiar coloration of the fish earned the popular name Green chromide to it. Apparently, this coloration enables the male partner to lure the gravid female to the spawning site and the colour patterns are identified to be good communication systems to ensure synchronization of courtship to signal the mate as regards the readiness to spawning activities (Mckaye et al., 1979). Similarly, it appears that the black belly of E.maculatus is a signal that invite its mate for spawning (Keenleyside, 1991). The significant variation in sex ratio, with preponderance of males in Vembanad waters is in conformity with the findings of Qasim (1966). However, Jayaprakash (1980) reported a sex ratio of 0.84:1.0 for the species in Veli lake and Keshava et al. (1988) reported 1:2.73 from the Nethravati Gurpur estuary of Karnataka, skewed in favor of females. Similar situation was observed in Pulicat lake and Mandovi estuary also (Prasadam, 1971; Vijayaraghavan et al.,1981). One sex in a population is apparently linked to sexual difference in growth rate; individuals with faster rate of growth is exposed to low predation and loss from population and this influences sex ratio (Qasim, 1966). Males that grow faster become mature at a smaller size and at an younger age. It is observed

6 BINDU & PADMAKUMAR: REPRODUCTIVE BIOLOGY OF ETROPLUS SURATENSIS 651 Fig. 4 Frequency distribution of oocyte diameter in different mature stages of E.suratensis. n = number of oocytes measured from each ovary that the sex which outnumber the other attain a much bigger size. This is apparently true for E. suratensis where the males invariably attain a higher size as compared to females. Pandian et al., (2001) observed that in many oviparous fishes where the duration of reproductive cycle is short and a single male can satisfy several females, the sex ratio is skewed in favor of females. This situation however do not hold good in case of E. suratensis which is characterized by biparental monogamy. The present observations support the view that sex ratio falls with growth and females are exposed greater mortality and shorter longevity as compared to males. This problem is crucial from the point of view of management of E. suratensis fisheries in Vembanad, where the trend is one of rapid decline. GSI is a reliable indicator on gonadal maturity; as naturally the weight of the gonad increases with maturity and when it spawns, there is a reduction in the weight of the gonad on account of the release of gametes (de Vlaming et al., 1982). Studies on the GSI in E. suratensis indicate that the fish spawns twice a year and this is also confirmed by gonadal studies with the occurrence of ripe individual in large numbers during these months. The G S I was perceptibly low in male E. suratensis as compared to females. The breeding season of E. suratensis in Vembanad lake is indicated to be synchronized with the cessation of monsoons and high tidal amplitudes (Thampy, 1980). In Veli lake, the peak breeding season of the fish has been indicated to be October to January and

7 652 INDIAN J. MAR. SCI., VOL. 43, NO. 4, APRIL 2014 Fig. 5 Monthly changes on the frequency distribution of oocyte diameter. n = number of oocytes measured during each month

8 BINDU & PADMAKUMAR: REPRODUCTIVE BIOLOGY OF ETROPLUS SURATENSIS 653 June to August (Jayaprakas and Nair, 1981). The peak breeding season observed in down stream locations in Vembanad near Poothotta in December with a second peak in June-July (Krishnan and Diwan, 1990). Apparently breeding is influenced by the salinity regime in brackish waters. The recrudescence of gonads appears to be synchronized by increased food availability, high primary productivity and favorable environmental conditions. Gonadal development has been observed to be rapid during post monsoon months. The high tidal amplitude during this period appear to provide suitable environmental conditions that trigger breeding. Evidently, in estuarine fishes the onset of spawning and recruitment is directly linked to the tidal rhythm. Knowledge of the minimum size at maturity is useful for regulating mesh size and to avoid recruitment over fishing. The fish has been reported to attain maturity at cm (Thampy, 1980; Raju et al., 1987) and cm (Jayaprakas and Nair, 1981). In culture ponds, the fish has been reported to become mature at a fairly small size of 10cm (Vijayaraghavan et al., 1981), as observed in tilapias (Pena-Mendoza et al., 2005). Fecundity of E. suratensis recorded in the present study is higher than earlier observations (Thampy, 1980; Vijayaraghavan et al., 1981; Keshava et al., 1988). All these observations indicate that the reproductive potential of E. suratensis is quite low in comparison to cultivable fishes like major carps. It is however higher than that of other cichlids like Oreochromis (Fawole and Arawomo, 2000; Pena-Mendoza et al., 2005). The range of fecundity observed in the study was found to be higher than that reported for the same species in the Veli lake (Jayaprakash et al.,1990). It is an adaptation to varying environmental conditions that work through the food supply (Wu et al., 2001). Various factors like food productivity, rainfall, salinity of water and genetic difference of the stock affect fecundity of fishes. Hence fecundity variations characteristically occur in different populations and even in same population in the same water body during different years. In the present study also, regression between fecundity and L T, W T and ovary weight indicated a direct proportional increase and the values were significant in case of ovary weight and fecundity. In general, the fecundity of a fish increases with the square of its length. Some authors have reported a still higher rate of fecundity increase and have reported it to be cube of its length (Bagenal,1957; Varghese, 1961). Apparently, relation between fecundity and length is linear. Allen (1951) observed a curvilinear relationship between fecundity and body weight. In the present study also the relationship between fecundity and ovary weight has been perceptible, the number of ova of the ovary weight. Apparently, the number of ova produced by the fish was closely related to the weight of the gonad and the correlation coefficient r was highest in this case as compared to all other relationships. Perrone and Zaret (1979) observed that egg size and fecundity are strongly correlated to parental care patterns. It appears that, a high degree of parental care is associated with fishes of low fecundity and in fishes like Tilapia, which show a high level of parental care, production of gametes is rather low. Moyle and Cech (2000) mentioned that naturally, the low fecundity in mouth brooding cichlids is linked to parents ensurance of the survival of the offsprings. Presence of two distinct group of ova sharply separated from each other confirms that the fish spawns more than once a year. As the oocyte development and spawning is found to occur at least two times, E. suratensis can be categorized as a multiple spawner that follows a lunar cycle, similar to observations reported by Harahap et al., (2001) in the spiny rabbit fish, Siganus spinus, that inhabit the Okinawan waters. In the context that several clutches of oocytes were observed in the ovary and the leading clutch consisted of oocytes at yolk and maturation stage, E. suratensis can be considered to belong to the asynchronous category (Wallace and Selman, 1981) and Winemiller (1989) considered them as equilibrium strategists as they show parental care and a non seasonal reproduction. Acknowledgement Authors are grateful to Vice Chancellor, Kerala Agricultural University for the facilities provided during the study period. References 1 Allen K R, The Horokiwi stream: A study of trout population, Fish Bull N Z Wellington, 10 (1951) Bagenal T B, Annual variation in fish fecundity, J Mar Biol Ass U K, 36 (1957) Bailey N T J, Statistical methods in Biology, The English University Press, London, (1995) 255 p.

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