Study of Reproductive Traits of Spiny Eel, Mastacembelus armatus (Mastacembeliforms) from Kalinadi-A Tributary of the Ganges River Basin, India

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1 Research Paper Study of Reproductive Traits of Spiny Eel, Mastacembelus armatus (Mastacembeliforms) from Kalinadi-A Tributary of the Ganges River Basin, India M. Serajuddin 1 * and B.C. Pathak 2 1 Associate Professor, Department of Zoology, University of Lucknow, Lucknow , U.P., India 2 Department of Zoology, University of Lucknow, Lucknow , U.P., India * lu.fisheries@gmail.com Abstract The population of Mastacembelus armatus was slightly dominated by males. Sex ratio varied with size and change in season. Monthly fluctuations in gonadosomatic index were recorded and five stages of gonad maturity in both sexes were identified. Ova diameter revealed the release of only one batch of mature ova during the breeding season, which extended from late June to early September. The relative fecundity was 63 eggs cm -1 body length and 29 eggs g -1 body weight. Four predictors of fecundity, body length, body weight, and ovary length and ovary weight were evaluated and regression equations derived. Fish weight proved to be the most precise predictor of fecundity. Absolute fecundity varied between in the specimens of M. armatus ranging between cm in size. Keywords: Fecundity, Gonadosomatic Index, Sex Ratio 1. Introduction The spiny eel, Mastacembelus armatus is one of the most common species of teleosts found in Asia. Attaining a length up to 65 cm, the species M. armatus is the largest out of the four species of the genus Mastacembelus found in India. M. armatus is an economically important inland water fish, which is quite palatable as a table fish and is nutritious too (Talwar & Jhingran, 1991). Demand for the fish almost always exceeds supply, particularly in India and its neighbouring countries such as Pakistan, Sri-Lanka and Bangladesh, although the fish has also been reported in Myanmar, Thailand, Malaysia and Southern China. In northern and eastern India, the fish is very popular when sold alive. It occurs in a variety of freshwater habitats in the plains as well as in hills of India (Talwar & Jhingran, 1991). Despite its abundance, palatability and consumer appeal, no published information is available on the biology of M. armatus, except in the studies of Dutta (1989 and 1990), Serajuddin & Mustafa (1994) and Serajuddin et al (1998) on the feeding specialization and food and feeding habits of the species, Sikder & Das (1980) on the skin structure of M. armatus and Saxena et al (1979) on the cytological details of its oocytes. Serajuddin (2004) reported the intraspecific diversity of M. armatus. The karyotype of M. armatus was studied by Das & Khuda Bukhsh (2007). Reddy et al (2011) extracted some tapeworms were from M. armatus. Narejo et al (2002 and 2003) studied the reproductive biology and length-weight relationship of M. armatus in the year 2002 and 2003 respectively from Bangladesh. Pathak et al (2012) reported a comparative analysis of reproductive traits in a closely related species, Macrognathus pancalus from lentic and lotic ecosystems of Gangetic basin. A number of workers reported that the reproductive traits such as fecundity and size of egg can be influenced by food quantity (Bagenal, 1969), fishing pressure and the environmental conditions (De Silva, Available online at 145

2 1986; Legendre & Ecoutin, 1996 and Duponchelle, 1997). The study on the aspects of reproductive cycle of fish is scanty for most tropical and sub-tropical fish species. Sokolowska et al (2002) on ninespine stickleback (Pungitius pungitius) and Kocabas et al (2011) on brown trout, however, did some notable work on this aspect. In the present study, we studied the reproductive traits of M. armatus in order to determining their breeding cycle and reproductive potential. 2. Materials and Methods Monthly samples of fish were obtained for a period of 12 months from January to December Each sample comprising about fish were caught from Kalinadi, a tributary of the Ganga river system at Aligarth (27 30ˈ N, 78 4ˈ 26ˈˈ E) using cast and drag nets and brought to the laboratory packed in ice. Length, weight, sex, stage of gonad development, gonad length and gonad weight were recorded. Stage of maturity was determined following the scheme of classification suggested by Qayyum & Qasim (1964) for tropical and subtropical fishes. The extracted gonads were preserved in 5% formalin. Intra ovarian eggs were taken out and their diameter was measured with the help of an ocular micrometer using magnification of binocular dissecting microscope (Ernstleitz Gmbh Wetlar). Timing of spawning was determined using the Gonadosomatic Index (GSI): GSI= GW 100/BW Where: GW is the fresh Gonad Weight (g) to the nearest 0.01 g and BW is the Body Weight of fish (g) nearest to 1.0 g. Mean values of these indices were plotted monthly in order to indicate the duration and peak of spawning. The linear regression fecundity on total body length, body weight and ovary length and ovary weight were calculated based on matured ovaries (Stage IV). Ovaries were collected from May through August One ovary randomly selected from each pair was blotted dry and weighted on an electronic balance to the nearest 0.01 g. The sub-samples (10-20 mg) from anterior, middle and posterior regions of each ovary were taken and ova present in each subsamples were counted, and their average count was multiplied by total weight of the ovary for determining the absolute fecundity. Relative fecundities (number of ova in unit length and weight of the body and ovary) were also calculated. Chi square test was used to analyze the sex ratio. The coefficient of correlation r was used to estimated the quality of the linear regression and the strength of correlation between fecundity, body weight, body length (TL) and ovary length and ovary weight. 3. Results 3.1. Sex Ratio The sex ratio varied with season (Figure 1A).The male: female ratio ranged from 1:0.5 to 1:1.2, with the average value being 1:0.8. In all months except February and September, males maintained a marginal numerical superiority over the females. However, the chi square test showed no significant departure from the hypothetical 1:1 ratio. The sex ratio also varied with size (Figure 1B). Females were relatively less abundant in the higher size range ( mm), in which case the ratio was ranged between 1:0.5-1:0.9, with an average value of 1: Gonads, Sexual Maturation and Spawning Paired gonads elongate with ripening and extend towards the posterior half of the abdomen. Five maturity stages were recognised. The gonads showed a regular seasonal development with little overlap in different phases of maturation (Figure 2). Gonads developed in March and entered the ripening stage and subsequently got predominant during April and May. Less active gonads were found during the period of late September through February. In June, both sexes were completely ripe and encountered up to August. Maximum number of spent individuals was recorded during August and September. The cycle of maturation and depletion of gonads suggest a breeding season for M. armatus of three months (late June-early September) Gonadosomatic Index (GSI) In both sexes, high values of GSI were recorded during the period of May through July indicating full development of their gonads (Figure 3). GSI declined abruptly at the onset of spawning in the month of July, and subsequently spent specimens (Stage IV) were appeared in the sample collection of this month Ova Diameter Figure 4 illustrates the ova diameter frequencies of M. armatus from March to June. The model size of ova ranged between mm in the ripening stage (i.e. March-May). Fully developed and ripe eggs (diameter mm) were encountered during June-July. Ova sampled from different parts of the ripe ovary were almost of the same size. Available online at 146

3 Figure 1. Variations of Sex Ratio With: (A) Months, (B) Size Groups in M. armatus Figure 2. Seasonal Variations of Maturity Stages in M. armatus: (A) Male, (B) Female Figure 3. Gonadosomatic Index in M. armatus: (A) Male, (B) Female Available online at 147

4 3.5. Fecundity The reproductive potential of the fish was measured in term of fecundity. Fecundity increased with size and weight of the fish. Absolute fecundity varied between egg cm -1 in the specimens of M. armatus ranging from cm in size. Length-wise, the fecundity varied between egg cm -1 with an average of 63 egg cm -1 and weight wise, it varied between egg g -1 with an average of 29 egg g -1 of the body weight of the fish. Regression analysis indicated that the total length and weight could be used to predict fecundity of this spiny eel, but weight proved to be the best predictor of fecundity (r= ). Although in both cases significant correlation was noted (P<0.001). Ova per g of ovary-weight varied between , with an average of 64 egg g -1. Results of the relationship of fecundity with both ovary-length and ovary-weight are presented in Table 1. of one sex in the population of fish are segregation of sexes through various periods of the year, size differences, gear selectivity related to sex difference in morphology and physiological activity and differences either by natural or artificial mortality. However, the less abundance of females particularly in the higher size range of M. armatus in the present study can be related to the mortality due to spawning stress or the pressure of selective fishing for large size fish. Cyclic changes in the maturation, depletion of gonads, intra ovarian oocytes and GSI in M. armatus clearly indicated to breeding synchronous with the onset of monsoon. The high values of GSI in both sexes during May through July and low values from October to January may be due to high and low effects of photo-period and temperature respectively. These changes showed that physical parameters also influence the cyclic development of gonads. The condition of all the ova in an ovary being at Figure 4. Size Frequency Distribution of Oocytes of M. armatus Table 1. Regression Analysis of Fecundity Relations in M. armatus Parameters Logarithmic Regression Parabolic Regression Correlation Co-efficient r Significant (p value) Body length vs. Fecundity Log F = logl F= L Body weight vs. Fecundity Log F = logw F= W Ovary length vs. Fecundity Log F = logol F= L Ovary weight vs. Fecundity Log F = logow F= OW Discussion Several workers reported the high population of males for different fishes (Gowda & Shanbhogue, 1988 and Hoda & Qureshi, 1989). The reasons suggested for the dominance the same stage of development is indicative of the fact that the spawning in this fish takes place only once in a year. Qasim & Qayyum (1961) made similar observations in another spiny eel, Rhyncobdella aculeate collected from Aligarh, U.P., India. The breeding behaviour in M. Available online at 148

5 armatus also follows a pattern, which is common to most of the freshwater fishes living in plains of western Uttar Pradesh (India). Fecundity was found to be low in M. armatus due to large size of eggs ( mm). Karim & Hossain (1972) also reported the occurrence of low absolute fecundity (2013 eggs on an average) in a closely related species, Mastacembelus pancalus. As regards the relative fecundity the number of eggs per unit length exceeded the number of eggs per unit body weight. Some workers (Pathani, 1981 and Piska & Waghray, 1989) in different species of freshwater fishes obtained similar results. Fecundity is significantly correlated with length and weight of the fish as well as the length and weight of the ovary. A linear relationship was found to exist between fecundity and each one of these four characters. Combinations of two independent variables, length and weight, improved predictability only slightly, therefore, separate equations for fecundity were derived for length and weight. Comparison of the quantitative variation in fecundity with both variables of ovary revealed a marked increase in egg production with increase in ovary length. The seasonal fluctuation in the water level also influence the nutrient cycling, trophic interaction and energy cycling of aquatic environment which directly or indirectly influence the reproductive capability of fish as well as associated biota (Junk et al, 1989 and Santos et al, 2010). 5. Conclusion There was no significant departure of male:female ratio in the present study of M. armatus from the hypothetical 1:1. Cyclic changes in the maturation, depletion of gonads, intra ovarian oocytes and GSI in M. armatus clearly indicated to breeding synchronous with the onset of monsoon, and the fish spawn only once in a year which extended from late June to early September. Fecundity was found to be low in M. armatus due to large size of eggs. Acknowledgement The authors thank the Head of the Department of Zoology, Lucknow University, Lucknow for providing facility. References Bagenal, T.B. (1969) Relationship between egg size and fry survival in Brown Trout Salmo trutta L. Journal of Fish Biology, 1(4), pp Das, J.K., and Khuda-Bukhsh, A.R. (2007) GC-rich heterochromatin in silver stained nucleolar organizer regions (NORs) fluoresces with chromomycin A 3 (CMA 3 ) staining in three species of teleostean fishes (Pisces). Indian Journal of Experimental Biology, 45(5), pp De Silva, S.S. (1986) Reproductive biology of Oreochromis mossambicus populations of man-made lakes in Sri Lanka: a comparative study. Aquaculture Research, 17, pp Duponchelle, F. (1997) Reproduction du tilapia (Pisces, Cichlidae) Oreochromis niloticus (Linnaeus, 1758) dans les retenues artificielles de Cote d Ivoire: analyse comparative des modalities de production et approche experimentale de leur determinisme. Ph.D. Thesis, Rennes, Univerite de Bretagne Occidentale. Dutta, S.P.S. (1989/1990) Food and feeding ecology of Mastacembelus armatus (Lecep.) from Gadigarh stream, Jammu.Matsya, 15(16), pp Gowda, G., and Shanbhogue, S.L. (1988) On the reproductive biology of grey mullet, Valamugil seheli (Forskal) from Mangalore waters. Mahasagar, 21(2), pp Hoda, S.M.S., and Qureshi, N. (1989) Maturity, sex ratio, ova diameter and fecundity of mullet Liza klunzingeri Day from Karachi- Sind waters. Indian J. Fisheries, 36(3), pp Junk, W.J., Bayley, P.B., and Sparks, R.E. (1989) The flood pulse concept in river- Floodplain systems. In: Dodge, D.P. ed. Proceedings of the International Large River Symposium (LARS) September 14-21, 1986, Honey Harbour, Ontario, Canada. Can. Spec. Publ. Fish. Aquat. Sci Ottawa, Dept. of Fisheries and Oceans, pp Karim, M.A., and Hossain, A. (1972) Studies on the biology of Mastacembelus pancalus (spiny eel, Hamilton) in artificial ponds. Part II, sexual maturity and fecundity. Bangladesh J. Biol. Agric. Sci., 1(2), pp Kocabas, M., Kayim, M., Can, E., Kutluyer, F., and Aksu, O. (2011) The Reproductive traits of Native Brown Trout (Salmo trutta macrostigma T., 1954), Turkey. Journal of Animal and Veterinary Advances, 10(13), pp Legendre, M., and Ecoutin, J.M. (1996) Aspect of the reproductive strategy of Sarotherodon melanotheron, comparison between natural population (Ebre lagoon, Cote d Ivore) and different cultured populations. In: Pullin, R.S.V., Lazard, J., Legendre, M., Amon Kothias, J.B., and Pauly, D. eds. Proceeding of Third International Symposium on Tilapia in Aquaculture ICLARM, Manila, pp Narejo, N.T., Rahmatullah, S.M., and Rashid, M.M. (2002) Studies on the reproductive biology of freshwater Available online at 149

6 spiny eel, Mastacembalus armatus (Lacepede) reared in the cemented cisterns of BAU, Mymensingh, Bangladesh. Pakistan Journal of Biological Sciences, 5(7), pp Narejo, N.T., Rahmatullah, S.M., and Rashid, M.M. (2003) Length-weight relationship and relative condition factor (Kn) of freshwater spiny eel, Mastacembalus armatus (Lacepede) from Mymensingh, Bangladesh. Indian Journal of Fisheries, 50, pp Pathak, B.C., Ali, R., and Serajuddin, M. (2012) Comparative Analysis of Reproductive Traits in Barred Spiny Eel, Macrognathus pancalus (Hamilton, 1822) from Lotic and Lentic Ecosystems of Gangatic Basin, India. World Journal of Fish and Marine Sciences, 4(5), pp Pathani, S.S. (1981) Fecundity of Mahaseer Tor putitora (Ham.). Proceedings. Animal Sciences-Indian Academy of Sciences, 90(2), pp Serajuddin, M., Khan, A.A., and Mustafa, S. (1998) Food and feeding habits of the spiny eel, Mastacembelus armatus. Asian Fish. Sci., 11(3-4), pp Serajuddin, M. (2004) Intraspecific diversity of riverine populations of spiny eel, Mastacembelus armatus. Applied Fisheries and Aquaculture, 4, pp Sikder, S.K., and Das, A. (1980) Investigation on fish Mastacembelus armatus skin: Part 2, isolation and characterization of glycosaminoglycans (Mucopolysaccharides). Indian J. Chem., Sect. B, 19, pp Sokolowska, E., and Skora, K.E. (2002) Reproductive cycle and the related spatial and temporal distribution of the ninespine stickleback (Pungitius pungitius L.) in Puck Bay. Oceanologia, 44(4), pp Talwar, P.K., and Jhinggran, A.G. (1991) Inland Fishes of India and Adjacent Countries. vol. 1, New Delhi, Oxford & IBH Publishing Co. Piska, R.S., and Waghray, S. (1989) Fecundity of carp minnow Salmostoma bacaila (Ham.) Indian J. Fish., 36, pp Qasim, S.Z., and Qayyum, A. (1961) Spawning frequencies and breeding season of some freshwater fishes with special reference to those occurring in the plains of northern India. Indian J. Fish., 8, pp Qayyum, A., and Qasim, S.Z. (1964) Studies on the biology of freshwater fishes, Part I. Ophiocephalus punctatus (Bloch.). J. Bombay Nat. Hist. Soc., 61, pp Reddy, Y., Wankhede, H., Gedam, A., and Gaikwad, D. (2011) Some Ptychobothridaen tapeworm from freshwater fish Mastacembalus armatus at Aurangabad district (M.S.) India. International Multidisciplinary Research Journal, 1(8), pp Santos, R.N., Amadio, S., and Ferreia, E.J.G. (2010) Pattern of Energy allocation to reproduction in three Amazonian Fish species. Neotropical Ichthyology, 8, pp Saxena, O.P., Bhatia, H.K., and Chowdhery, V. (1979) Cytological study of oocytes of the fish, Mastacembelus armatus with particular reference to the localization of protein and nucleic acids. Matsya, 5, pp Serajuddin, M., and Mustafa, S. (1994) Feeding specialization in adult spiny eel, Mastacembelus armatus. Asian Fish. Sci., 7, pp Available online at 150

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