On lin e F irs t A rtic le Reproductive Biology of Mahseer ( Tor tambroides ) from Atu Suasah and Lawe Melang Rivers in Aceh Province to Support Sustainable Fisheries Management

Teuku Fadlon Haser1*, Muh. Saleh Nurdin2, Eddy Supriyono3, Deni Radona4, Fauziah Azmi1 , Kukuh Nirmala3, Widanarni3, Tri Heru Prihadi4, Tatag Budiardi3 and Riris Yuli Valentine5 1Faculty of Agriculture, Samudra University, Aceh 24354, Indonesia 2Faculty of Animal Husbandry and Fishery, Tadulako University, Palu 94148, Indonesia 3Faculty of Fisheries and Marine Sciences, IPB University, Bogor 16151, Indonesia 4Research Institute for Freshwater Aquaculture Research and Fisheries Extension, Bogor 16129, Indonesia 5Polytechnic of Marine and Fisheries, Kupang 85351, Indonesia Article Information Received 31 August 2020 Revised 29 September 2020 Accepted 29 October 2020 Available online 15 Februay 2021


INTRODUCTION
M ahseer (Tor tambroides) is the fish commonly found in freshwater system in the south, east and south east of Asia Continent. Their habitat is characterised by fast or slowing moving water with high water clarity, high dissolved oxygen content with a preference for sand and gravel as substrates (Khare et al., 2014;Ambili et al., 2014;Pinder et al., 2019). The fish are abundant in intact water, especially in tropical regions of Indonesia, Malaysia, Thailand and India (Yadav et al., 2012;Hoang et al., 2015). In particular, Mahseer are found in freshwater riverine systems in Aceh, where they are one of the fishes exploited by local residents.
Four mahseer species are found in Aceh, Tor soro, Tor tambra, Tor douronensis and Tor tambroides. Based on body size, Tor tambroides is the biggest mahseer of Indonesia (Haryono et al., 2009). Among the four species Tor tambra population is the most abundant (Maghfiriadi et al., 2019). Local people usually refer to this fish as kereuling or jurong. This fish is highly appreciated by locals for the delicacy of its meat (Muchlisin et al., 2015;Wibowo and Dwirastina, 2016). Mahseer also have cultural value and are used in many cultural ceremonies (Kristanto et al., 2007;Haryono, 2017). Mahseer are rare in Java Island, whilst in Kalimantan and Sumatera the populations of these fish are also reported to be declining due to overexploitation and ecosystem degradation, especially in places where the fish spawn (Haryono, 2006;Gupta et al., 2014;Sarkar et al., 2015;Roesma et al., 2017). Hence, management and conservation efforts are needed to sustain mahseer populations.
Information on reproductive biology is required O n l i n e

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to devise policies on management and conservation of mahseer but is still scarce. Previous studies have reported progress with respect to biological information on mahseer including taxonomy , growth performance (Muchlisin et al., 2016), morphology  and genetics (Arifin et al., 2015). However, there is a lack of information on aspects such as sex ratio, condition factor, fecundity and reproductive potential. Therefore, this study aimed to assess this gap through analysing and comparing these aspects of mahseer reproductive biology in Atu Suasah and Lawe Melang Rivers, in Aceh Province, Indonesia.

MATERIALS AND METHODS
The study was conducted from July to December 2019 in the Atu Suasah and Lawe Melang Rivers, Aceh Province, Indonesia (Fig. 1). Mahseer samples were obtained from fishermen who captured the fish using gillnet with mesh size 1.5-2.0 inch. On one trip, the fishermen usually operated gill nets 10-15 m in length. The nets were set up at upstream and at the downhill in each of the two rivers. One trip is equaled to 16 h of fishing activity counting when the operation of gillnet at 16.00 in the afternoon and the liftup of gillnet at 08.00 am. In total 146 mahseer specimens were collected, consisting of 74 fish from Atu Suasah and 72 from Lawe Melang River. The specimens collected were placed in a coolbox and transported to the Aquatic Resources Management Department of IPB University in Bogor for further analysis. The total length (mm) and weight (g) of each specimen were measured, and the sex was determined. Weight was obtained from digital scale with 0.1 g accuracy whilst total length was measured using ruler with 1 mm accuracy. Three parts of each eggs from anterior, middle, and posterior parts were subsampled to counted fecundity. The eggs subsamples were immersed in Gilson solution for 24 h to dissolved the outer membrane therefore makes it easier to count. Fecundity was estimated using a gravimetric method (Bagenal, 1968) by counting the eggs in the subsamples under a microscope.
Sex ratio was determined by dividing the number of male with the number of females. Chi-square (Zar, 2010) was used to estimate sex ratio difference between the two populations following formula: where O i is the observed value and Ei is the expected value of the i th variable.
The length-weight relationship was calculated using the equation in Le Cren (1951): where W is the weight (g) and L is the total length (mm); a is the intercept and b is the slope of the logtransformed regression of weight against length.
The relative condition factor (Wr) and Fulton condition factor (K) were used to evaluate condition factor of each individual. Relative condition factor was computed refer to Rypel and Richter (2008): where Wr is the relative condition factor, W is weight of the specimen and Ws is the predicted standard weight for that same fish as calculated from a composite of lengthweight regressions throughout the range of the species.
A value of the relative condition factor < 100 indicates low food availability while Wr > 100 suggests abundant or surplus food availability (Anderson and Neumann, 1996).
The Fulton condition factor was calculated using the following equation (Froese, 2006). CF is the Fulton condition factor; W is the weight (g of the specimen; L is the total length (mm) of the specimen; a and b are the constants from the length-weight regression model.
The average difference between male and female condition factor was obtained using the Mann-Whitney test (Wilks, 1995):

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Z is the statistics, U is the smallest value of U 1 and U 2 ; n 1 and n 2 are sample size.
Fecundity was estimated following gravimetric protocol with formula: where F is fecundity, Fs is the number of eggs counted in the gonad sub-sample, Wg is total gonad weight, and Ws is the weight of the gonad sub-sample.
The between-population difference in mahseer total fecundity was analysed using the t-test (Zar, 2010), where t was calculated using the equation: where x ̅ 1 is the mean fecundity of specimens sampled from population 1, x ̅ 2 is the mean fecundity of specimens sampled from population 2, S 1 2 is the sample variance from population 1, S 2 2 is the sample variance from population 2, n 1 and n 2 are the sample sizes of the two populations.
Reproductive potential was calculated using the following formula (Tuwo, 1993):
The length and weight relationship regression analysis showed that the four fish groups have a negative allometric (b<3) growth pattern (Table I). This indicates that these fish generally grow faster in length than in weight. The coefficient of determination shows that length explains a higher proportion of weight gain in female mahseer compared to males in both Atu Suasah River and Lawe Melang River.
The mean values and range of the Fulton condition factor were similar for male and female mahseer sampled from the Atu Suasah River (1.03±0.23, 1.04±0.30) and Lawe Melang River (1.02±0.30 and 1.06±0.27s) with mean values slightly greater than 1 (Fig. 2). The relative condition factor was greater than 100 for all groups. The Mann Whitney-test showed no significant difference (P>0.05) in either condition factor between male and female fish or between the two study sites. The results also suggest that male and female fish condition remained similar throughout the six month sampling period. Mahseer fecundity ranged from 3,600 to 5,466 eggs (average 4,476±911 eggs) in the Atu Suasah River and 2,433 to 4,203 eggs (average 3,212±631 eggs) in Lawe Melang River. The student t-test showed no significant between-site difference in fecundity (P>0.05). Mean reproductive potential was estimated at 10,444±4,404 in the Atu Suasah River and 4,818±3,870 in the Lawe Melang River (Table II).

DISCUSSION
Theoretically, a balanced sex ratio (1:1) is ideal to

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maintain a population (Ball and Rao, 1984). Studies on mahseer from several localities, report a female-biased sex ratio; e.g. a study on Tor putitora in India (Joshi et al., 2018), and a study in Kalimantan (Haryono, 2006) where the male to female sex ratio was 1:2. Bhatt et al. (2004) and Wibowo and Kaban (2014) found that male mahseer are mostly young fish while females are predominately adult fish. The proportion of young fish in the samples collected from the Atu Suasah and Lawe Melang Rivers was 57.14% from and 47.22%, respectively. Therefore, the balanced sex ratio of fish in this study related to the balance between young and adult fish in the samples collected such what had been found in Manna River and Tarusan River (Wibowo and Kaban, 2014). Mahseer are pelagic fish which swim actively due to their habitat in fast flowing foothills streams with highwater quality (Dinesh et al., 2010;Ambili et al., 2014;Raghavan et al., 2017). Actively swimming fish which live in fast flowing water usually have a value of b < 3 because more energy is allocated for swimming than for growth in terms of weight gain (Shukor et al., 2008;Muchlisin et al., 2010;. The same phenomenon was observed in the mahseer populations at both study sites. However, growth patterns of mahseer reported in previous studies are varied (Tabel III). Muchlisin et al. (2015) also found that Tor tambra in Nagan and Sikundo Rivers had an allometric negative growth pattern. Tor putitora found in their spawning ground (Himalayan foothills) in Pakistan also had an allometric negative growth pattern (Naeem et al., 2011). On the other hand, Ali et al. (2014) who also studied Tor putitora in four different locations in the Indian Himalayan report an isometric growth pattern. The variability in fish growth patterns is usually closely related to the environment, including the biological and geographical condition of the habitat (Froese, 2006;Pervais et al., 2012).
Aside from food availability, biotic and abiotic factors, age, and length (size class) can also affect the fish condition factor (Le Cren, 1951;Blackwell et al., 2000). The Fulton condition factor of male and female mahseer was relatively stable over the sampling period. The value of relative weight exceeded 100 which indicates good food availability for the fish in both rivers. Mahseer in Atu Suasah and Lawe Melang are considered as omnivores with a tendency towards being predominantly herbivorous. While the main food sources of these fish are aquatic plants and algae, they also occasionally prey on insects (Pervais et al., 2012;Nautiyal, 2014;Mohapatra et al., 2017). Sulastri et al. (1985) suggested that, apart from relying on videoreceptor capability in searching for food, mahseer also use their barbels as mechanoreceptors.
Fecundity is considered the most reliable indicator to estimate fish reproductive potential (Bhatt and Pandit, 2015;Achmad et al., 2020). The estimates of mahseer fecundity in this research fall within the range of mahseer fecundity reported from other studies (Table IV). The highest fecundity was found in the Nayar River population (India) (Nautiyal and Lal, 1985). The lowest fecundity was found in Manna River population, West Sumatera Indonesia (Wibowo and Kaban, 2014). The fecundity found in this study is lower than that of mahseer found in Barito (Haryono, 2006), but higher compared to that reported from the Manna River. These variabilities may happens due to variabilities of fish size among populations.

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Reproductive Biology of Mahseer (Tor tambroides) from Atu Suasah and Lawe Melang Rivers  Table IV shows that the fecundity of mahseer populations can be different even they come from the same or similar species within the genus Tor. Bagenal (1971) argued that length and weight of fish tend to increase linearly. Additionally, variability in fish mahseer fecundity can be affected by species, spawning pattern, and estimating techniques (gravimetry and volumetry) (Pathani, 1981;Johal and Negi, 2003).
Mahseer from the 610-700 mm length class contributed the most to overall egg production. This size class was also the most abundant (42.86% and 50% of the total number of females within the two river population samples). Female mahseer with a length more than 710-800 mm had the lowest fecundity and only comprised 16.67% of the females sampled from the populations. Therefore, this group appears to make a relatively low contribution to total egg production.
Mahseer exploitation in the Atu Suasah and Lawe Melang Rivers is highly intensive due to excessive demand for the fish. To protect the fish populations, spawning grounds of the fish must be determined and protected. Establishing a reservation area in each of the two rivers could improve larval production through protection for the source of new recruits. This approach could also affect fisher incomes therefore its implementation must be accompanied by education for the local fishermen.

CONCLUSION
There was no significant between-site difference in sex ratio, length and weight relationship, condition factor or fecundity between mahseer captured in the Atu Suasah and Lawe Melang Rivers. The sex ratio was balanced and the growth pattern was negative allometric. Fish condition factor remained stable throughout the sampling period. Mahseer from the length class 610 -700 mm made the largest contribution to total egg production. To improve new recruitment, priority should be given to the protection of mahseer spawning grounds by establishing a reservation (protected area) in order to maintain egg production.

Statement of conflict of interest
The authors have declared no conflict of interest.

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T.F. Haser et al.

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Reproductive Biology of Mahseer (Tor tambroides) from Atu Suasah and Lawe Melang Rivers