Population Parameters of a Freshwater Clupeid , Corica soborna ( Hamilton , 1822 ) from the Ganges River , Northwestern Bangladesh

Dalia Khatun1, Md. Yeamin Hossain1,2*, Md. Firose Hossain3, Zannatul Mawa1, Md. Ataur Rahman1, Md. Rabiul Hasan1 Md. Akhtarul Islam1, Md. Ashekur Rahman1, Habib Ul Hassan4 and Sadicun Nahar Sikha1 1Department of Fisheries, Faculty of Fisheries, University of Rajshahi, Rajshahi 6205, Bangladesh 2Faculty of Fisheries, Kagoshima University, 4-50-20 Shimoarata, Kagoshima 8900056, Japan 3Department of Molecular and Functional Genomics, Interdisciplinary Center for Science Research, Shimane University, Matsue, Japan 4Department of Zoology (MRCC), University of Karachi, Karachi-75270, Pakistan


INTRODUCTION
T he Clupeidae is the main family of the order Clupeiformes, containing approximately 200 species in 54 genera (Froese and Pauly, 2014). It is considered as the most valuable food fish family in the world (Csirke, 2005), being represented mostly by herrings, sardines, anchovies and shads and their relatives (Royce, 1996). The Ganges River sprat, Corica soborna is a member of the family Clupeidae, one of the representative and abundant species in the Ganges River of Bangladesh,

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Thailand (Froese and Pauly, 2019;Talwar and Jhingran, 1991). This clupeid is a plankton feeder that mostly inhabits ponds and pools of creeks, rivers, and estuaries (Talwar and Jhingran, 1991;Rahman, 1989;Bhuiyan, 1964), sometimes also being found in Bay of Bengal (Kapoor et al., 2002). It is a highly popular food fish due to its taste and high content of protein and micronutrients (Hossain et al., 2009(Hossain et al., , 2017a, as well as having some medicinal value (Bhuiyan, 1964). However, this species has a small contribution in commercial fisheries probably because of its small size and is generally caught by smalland large-scale fishers as bycatch (Bhuiyan, 1964;Talwar and Jhingran, 1991). The conservation status of this species is categorized as least concern both in Bangladesh (IUCN Bangladesh, 2015) and elsewhere in South Asia (IUCN, 2018). Information on life-history traits of fish species is very crucial for the execution of appropriate management approaches for sustaining the indigenous fishes like C. soborna (Hossain et al., 2013a). Sex ratio (SR) and size structure (length-frequency distribution, LFD) reveals major information to evaluate reproductive prospective of fish populations (Vazzoler, 1996). The study of LFDs revealed the status of stock, breeding period, and ecology of riverine fishes (Ranjan et al., 2005). Such study also expresses the relations of the dynamic rates of growth, recruitment, and mortality (Neuman and Allen, 2001). Length-weight relationships (LWRs) and length-length relationships (LLRs) are valuable parameters for determining the well-being of individuals, and to differentiate different stocks within species (King, 2007). LWRs of fish species have significant implications for fishery assessments and estimates of fishery biomass and yield (Ricker, 1975;Martn-Smith, 1996;Garcia et al., 1998), as well as to prove data for aquatic ecosystem modeling (Christensen and Walters, 2004). Moreover, LWRs are fundamental for evaluating the life histories of fishes among diverse geographic localities (Le Cren, 1951;Hossain et al., 2009Hossain et al., , 2012aHossain et al., , 2016aAzad et al., 2018) and are also helpful for conservation and stock assessment (Ahmed et al., 2012;Hossain et al., 2013bHossain et al., , 2016bHossain et al., , 2017b. Additionally, LLRs are also important in fisheries management for comparative growth studies where one length type is preferred (Hossain et al., 2006(Hossain et al., , 2015aWang et al., 2015). Condition factors are valuable parameters to examine for differences among numerous stocks within species (King, 2007). Furthermore, relative weight (W R ) is one of the most renowned indices to ascertain the status of fishes in various water bodies (Rypel and Richter, 2008;Hossen et al., 2018). In addition, the form factor (a 3.0 ) can be used to determine whether the body shape of a certain population or species is significantly distinct from others (Froese, 2006). On the other hand, the status of fish stock and its management policies is often depends on the assessment of natural mortality (M W ) (Brodziak et al., 2011).
Although some studies have been done on C. soborna regarding LWRs (Hossain et al., 2017a); LWRs, LLRs, size at first sexual maturity, and fecundity (Hossain et al., 2008) and LWRs and condition factors (Kamal, 1982), to knowledge no studies have done on population used multimodels for this important fishery. Therefore, this study focused on the complete and comprehensive description on population parameters, including sex ratio (SR), lengthfrequency distributions (LFDs), length-weight (LWRs) and length-length relationships (LLRs), condition factors (allometric, K A ; Fultons, K F ; relative, K R ; relative weight, W R ), form factor (a 3.0 ), size at first sexual maturity (L m ), and natural mortality (M W ) of C. soborna using many specimens of different body sizes from the Ganges River in northwestern Bangladesh as sampled over a 1 year study period.

Fish measurement
Sex identification of fish was done by (i) morphometric and meristic traits and (ii) microscopic observation of the gonads. Before weighing, each individual was rinsed with water and kept exposed to air-dry it, although blotting paper was also used to eliminate excess moisture. For each individual, total (TL), fork (FL), and standard lengths (SL) were measured by a digital slide calipers to the closest 0.01 cm. Whole body weight (BW) were taken by an electronic balance to the nearest 0.01 g, precision.

Sex ratio (SR) and length-frequency distribution (LFDs)
The variation of sex-ratio from the anticipated 1:1 O n l i n e

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(male: female) value was determined by chi-square test. The length-frequency distribution for male and female C. soborna was made individually with 1cm intervals of TL. The normal-frequency distribution was fitted to the TL frequency distribution of C. soborna using a computer program (Microsoft Excel add insolver), based on Hasselblad′s maximum-likelihood method (Hasselblad, 1966).

Length-weight and length-length relationships (LWRs and LLRs)
The LWRs was calculated using the equation: W = a × L b , where, W is body weight (BW, g) and L is body length (cm). The parameters a and b were estimated by linear regression analyses based on natural logarithms: ln(W) = ln (a) + b ln(L). In addition, 95% confidence limits of a and b and the coefficient of determination (r 2 ) were estimated. Based on Froese (2006), all extreme outliers were excluded from the analyses. A t-test was used to confirm whether b values obtained in the linear regression were significantly different from the isometric value (b= 3), (Sokal and Rohlf, 1981). Furthermore, LLRs -including TL vs. SL, TL vs. FL, and SL vs. FL relationships-were estimated by linear regression (Hossain et al., 2006).

Condition factors
The allometric condition factor (K A ) was estimated using the equation of Tesch (1971): W/L b , where W is the body weight (g) and L is the TL (cm), and b is the LWR parameter. The Fultonʹs condition factor (K F ) was calculated using the equation of Fulton (1904): where W is the body weight (g) and L is the TL in cm. The scaling factor of 100 was used to bring the K F close to unit. Moreover, the relative condition factor (K R ) was calculated following the equation of Le Cren (1951): where W is the body weight (g), L is the TL (cm), and a and b are LWR parameters. For assessing the relative weight (W R ), the equation of Froese (2006): where W is the weight of a particular individual and W s is the predicted standard weight for the same individual as calculated by W s = a×L b . For the latter, a and b values are gained from the relationships between TL vs. BW.

Form factor (a 3.0 )
The a 3.0 of C. soborna was calculated using the equation of Froese (2006) as: a 3.0 = 10 log a -s (b-3) , where a and b are regression parameters of LWR, and s is the regression slope of ln a vs. b. We used a mean slope S = -1.358 for estimating a 3.0 because information on LWR is not available for this species to estimate the regression (S) of ln a vs. b.

Size at first sexual maturity (L m ) and natural mortality (M W )
L m was estimated by the equation of Binohlan and Froese (2009) as log (L m ) = −0.1189 + 0.9157 × log (L max ), where L max signifies maximum TL. M W was calculated using the model of Peterson and Wroblewski (1984) as M W = 1.92 year -1 *(W) -0.25 , where, M W = natural mortality at mass W, and W= a×L b , and a and b are regression parameters of LWR.

Statistical analysis
Statistical analyses were performed using GraphPad Prism 6.5 software. Homogeneity and normality of the data were tested prior to analysis. A 1-sample t-test was used to compare the mean relative weight (W R ) with 100 (Anderson and Neumann, 1996). In addition, the Spearman rank correlated body measurements (e.g., TL and BW) with condition factors (K A , K F , K R , and W R ). Furthermore, the LWRs between sexes were compared by the analysis of covariance (ANCOVA). All statistical analyses were considered significant at 5% (P < 0.05).

Sex ratio (SR) and length-frequency distributions (LFDs)
During the study, a total of 303 individuals of C. soborna were collected from the Ganges River, where 41.55% were males and 58.45% were females, hence the overall sex ratio differed statistically from the expected 1:1 ratio (df = 1, χ 2 = 4.06, P ˃ 0.05) ( Table I).
Descriptive statistics for length and weight measurements and their 95% confidence limit (CL) for C. soborna are demonstrated in Table II. Specimens ranged from 2.70cm to 5.00cm for TL and 0.22 to 1.08 g for BW, regardless of sex. LFDs revealed that the 3.99-4.49 cm TL size group was numerically dominant for both males and females, constituting 72% vs. 69% of the total population, respectively ( Fig. 1). There was a significant difference for LFD between sexes (Mann-Whitney U-Test, U= 9727, P = 0.027). But BW showed insignificant differences between males and females (Mann-Whitney U-test, U= 10726, P= 0.367).

Length-weight and length-length relationships (LWRs and LLRs)
Descriptive statistics and estimated parameters of length-weight relationships, sample sizes (n), regression parameters a and b of the LWRs, 95% confidence limits, and coefficients of determination (r 2 ) of C. soborna are given in Table III and Fig. 2. All LWRs were highly significant (P < 0.001), with all r 2 values ≥0.963. In addition, all LLRs were also highly significant (P < 0.001) with all r 2 values ≥ 0.971 (Table IV and

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Population Parameters of Corica soborna  M, male; F, female; C, combined sex; n, sample size; Min, minimum; Max, maximum; SD, standard deviation; CL, confidence limit for mean values; K A , allometric condition factor; K F, Fulton′s condition factor; K R, relative condition factor; W R , relative weight.

Condition factors
The K A values varied from 0.0107 -0.0134 (mean ± SD = 0.0117 ± 0.0005) for males and 0.0141 -0.0174 (mean ± SD = 0.0158 ± 0.0008) for females (Table V). According to the Mann-Whitney U-test, K A was significantly different between sexes (P < 0.0001). The K F ranged from 0.8573 -1.1177 (mean±SD= 0.9141±0.0403) for males and 0.8640 -1.1844 (mean±SD= 0.9696±0.0680) for females, respectively (Table V), and the U-test showed that K F was significantly different between genders (P < 0.0001). In addition, K R ranged from 0.9162 -1.446 (mean ± SD = 0.9993 ± 0.0406) for males and 0.8922 -1.0992 (mean ± SD = 1.0022 ± 0.0502) for females (Table V) and the U-test showed insignificant deviations between sexes (P = 0.7228) in our study area. Calculated W R for males were 91.623 to 114.460 (mean ± SD = 99.933 ± 4.055) and for females were 89.223 to 109.921(mean ± SD = 100.224 ± 5.017) ( Table V). According to Wilcoxon sign rank test, W R showed no significant differences from 100 for both males (P= 0.6137) and females (P=0.6185). The relationship between TL vs. W R is shown in Fig. 4, and the relationships of different condition factors (K A , K F , K R , and W R ) with TL and BW are shown in Table VI. From the above four condition factors, only K F has high significantly correlated with TL and BW (P < 0.001).

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D. Khatun et al.

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Form factor (a 3.0 ) The calculated a 3.0 values were 0.0067, 0.0050, and 0.0054 for males, females, and combined sexes of C. soborna, respectively, in the Ganges River (Table VII), such values indicate that this fish is fusiform in shape. We also calculated the a 3.0 of C. soborna from various South Asian studies using available literature to compare with our study (Table VII).

Size at first sexual maturity (L m )
The calculated L m values for males and females were 3.14 cm (95% CL = 2.63 -3.80 cm TL) vs. 3.32 cm TL (95% CL=2.77 -4.02 cm TL), respectively (Table  VII). Moreover, we calculated the L m of C. soborna from different South Asian studies in the available literature ( Fig. 5 and Table VII).

Natural mortality (M W )
M W for the population of C. soborna was estimated as 2.52 year -1 , irrespective of sex in the Ganges River, NW Bangladesh. However, M W was very high for specimens under 2.4 cm TL, but it declined for bigger fish (Fig. 6). The calculated M W for C. soborna in the Ganges River and other South Asian water-bodies are shown in Table VII.

DISCUSSION
Past information on population parameters of C. soborna is scant for Bangladesh and elsewhere in South Asia. However, Hossain et al. (2017a) carried out a brief study on LWR for this species from the Ganges River, NW Bangladesh. Nevertheless, a work has also been done on biological aspects of this species by Hossain et al. (2008) from the Mathabhanga River, southwestern Bangladesh. During the present study, 303 individuals were sampled to encompasses various body sizes (2.7-5.0 cm TL), as collected through different conventional fishing gears. We highlighted the population parameters of C. soborna comprising SR, LFDs, LWRs, LLRs, condition factors (K A , K F , K R and W R ), a 3.0 , L m , and M W from the Ganges River in NW Bangladesh. Variation of sex ratio from 1:1 is not expected for most aquatic (fish and shellfish) species, but some finfish and prawn populations may exhibit a strong bias in this ratio (Hossain et al., 2013b(Hossain et al., , 2016bKhatun et al., 2018). In our study, the sex ratio of male and female was 1:1.41 with female dominant over males. A similar finding was also reported by Hossain et al. (2008) from the Mathabhanga River, southwestern Bangladesh. During our study, the overall sex ratio varied significantly from the predictable 1:1 ratio (df = 1, χ 2 = 4.06, P < 0.05), whereas Hossain et al. (2008) observed no noticeable variation from the expected 1:1 ratio (df = 1, χ 2 = 0.07, P > 0.05) elsewhere in Bangladesh. Our LFDs showed a lack of C. soborna smaller than 2.7 cm in TL which might be attributed to inappropriate selection of fishing gears rather than their absence from the fishing ground; or else the fishermen did not go where smaller fish occurs (Hossain et al., 2015b(Hossain et al., , 2016b(Hossain et al., , 2017cHossen et al., 2016;Nawer et al., 2017). Hossain (2010a, b) made a similar hypothesis when studying small indigenous species from the Ganges River.
In our study, the observed maximum length of C. soborna was 5.0 cm TL irrespective of sex, which is higher than the reported value of (i) 2.70 cm (Sultana, 2012) from the Ganges River, Bangladesh (ii) 4.99 cm (Hossain et al., 2008) from the Mathabhanga River, Bangladesh (iii) 3.80 cm (Kamal, 1982) from the Ganga River, India, but lower than the maximum recorded length (TL= 5.3 cm) reported by Hossain et al. (2017a) from the Ganges River, NW Bangladesh. Information on maximum length is crucial for the estimation of asymptotic length and growth coefficient of fishes, as required for planning and management of fisheries resources (Hossain et al., 2012a(Hossain et al., , 2017dHossen et al., 2018;Khatun et al., 2019a).  , allometric condition factor; K F ; Fulton′s condition factor; K R , relative condition factor; W R , relative weight; M, male; F, female; C, combined sex; r S , Spearman rank-correlation values; CL, confidence limit; P, shows the level of significance; ns, not significant; * significant (P ≤ 0.005); ** highly significant (P ≤ 0.01); *** very highly significant (P ≤ 0.001) (Sokal and Rohlf,1981).

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Population Parameters of Corica soborna 9 The allometric coefficient (b) may fluctuate between 2 and 4, however, values stretching from 2.5-3.5 are more common for fishes (Froese, 2006). According to Tesch (1971), values of b close to 3 represent isometric growth and variations from 3 indicate allometric growth, either positively (> 3) or negatively (< 3) allometric. In our study, the b values of LWRs (TL vs. BW; FL vs. BW; SL vs. BW) were within the range of 2.81-2.82 for males and 2.59-2.70 for females, representing negative allometric growth (<3.00) for both sexes. A similar growth pattern was reported by Hossain et al. (2017a) (b = 2.71) for C. soborna from the Ganges River of Bangladesh. However, isometric growth was observed by Hossain and Afroze (1991) (b = 3.05) for combined sexes and Hossain et al. (2008) for males (b = 2.95) and females (b= 2.97) from the Mathabhanga River of SW Bangladesh, which is dissimilar to this study. Conversely, positive allometric growth was found by Kamal (1982) (b = 3.69) from the Ganga River, India, unlike our findings. However, this dissimilarity in growth pattern may results from numerous factors, including sex, physiology, maturation of gonads, habitat, seasonal influence, level of stomach plumpness, preservation methods and differences in the studied fish lengths (Hossain et al., 2013b(Hossain et al., , 2019Khatun et al., 2019b), which we did not study. All LLRs were highly correlated (P < 0.001), with all r 2 values ≥ 0.971 in our study. There are no prior studies dealing with LLRs to make comparisons.
We studied four condition factors (K A ; K F ; K R , and W R ) to assess the health and habitat condition of C. soborna in the Ganges River, although most of the study focused on a single condition factor. Among these condition factors, the Spearman rank correlation test found that K F was highly significant correlated with TL and BW than for other condition factors (Table V). Hence, K F can validly be used to evaluate the wellbeing of this species in the Ganges River and nearby water bodies. Moreover, the Wilcoxon signed-rank test showed that the W R revealed no remarkable differences from 100 for both males (P= 0.6137) and females (P=0.6185), suggesting a balanced habitat with plenty of food access compared to predator risk (Anderson and Neumann, 1996) for C. soborna in the Ganges River basin. This is the first study on this aspect, so comparison with other data is not possible.
The a 3.0 values were 0.0067 and 0.0050 for male and female C. soborna in the Ganges River, which indicated elongated body shapes. The a 3.0 helps to appraise variation of body shape among populations or species from others (Froese, 2006). There was no literature information on the form factor of this species, so our study will provide the foundation for future studies.
L m for males and females of C. soborna were 3.14 cm vs. 3.32 cm in TL, respectively. However, Hossain et al. (2008) reported L m as 4.44 cm TL for female C. soborna in the Mathabhanga River, SW Bangladesh, which is higher than observed for our study. This distinction may be result from differences in sample size, shrinkage in specimen body sizes from preservation in formalin, water temperature, population density, and food availability (Khatun et al., 2019a), which were not considered in our study. The natural mortality (M w ) for the population of C. soborna was assessed as 2.52 year -1 for combined sexes of C. soborna in the Ganges River, NW Bangladesh. This is the first study on natural mortality for this species, so comparisons are impossible with other literature. It would be useful to document the causes of fish mortality in our study area.

CONCLUSION
Our findings describe the population parameters of C. soborna including length-frequency distribution, growth pattern based on LWRs, best-suited condition factor, relative weight, form factor, size at first sexual maturity, and natural mortality in the Ganges River. The results should be an effective tool for fishery managers, fish biologists and conservationists to formulate prompt management and regulations for sustainability of existing stocks of this species in the Ganges River and other South Asian water-bodies.