Life history traits of the Monsoon River prawn Macrobrachium malcolmsonii (Milne-Edwards, 1844) (Palaemonidae) in the Ganges (Padma) River, northwestern Bangladesh

Abstract

The Monsoon River prawn, Macrobrachium malcolmsonii (Milne-Edwards, 1844), is one of the dominant benthic species in the Ganges River. Our study describes some biological parameters including sex ratio, length–frequency distributions (LFD), length–weight relationships (LWR), and relative-condition (K_n ) factor of M. malcolmsonii in the lower part of the Ganges River, northwestern Bangladesh. A total of 502 specimens of the ranges 3.54–11.76 cm total length and 0.50–15.20 g body weight were analyzed in this study. Sampling was done using traditional fishing traps (Kara) during the period from March to October 2010. The overall sex ratio showed no significant differences from the expected value 1:1 (χ ² = 0.20, p = 0.157), and there was no significant difference in the LFD between the sexes (p = 0.460). The allometric coefficient b for the LWR indicated isometric growth (∼3.00) in males and negative allometric growth (<3.00) in females. K_n showed significant variation (p < 0.01) between the sexes, with better performance by females (1.027 ± 0.107) than males (0.968 ± 0.130). To our knowledge, this study presents the first comprehensive description of life-history traits for M. malcolmsonii from Bangladeshi waters. Our data should be useful for the sustainable management of this prawn fishery in the Ganges River basin of Bangladesh and neighboring countries.

Keywords:

• sex ratio
• length–weight relationship
• relative-condition factor
• Macrobrachium malcolmsonii
• Ganges River
• Bangladesh

Introduction

Palaemonid prawns are an important economic resource in the world's crustacean fishery industry as a major component of tropical and subtropical fisheries (Holthuis 1980; Mantelatto and Barbosa 2005). Over the last three decades, numerous studies around the world have been conducted on Palaemonidae prawn stocks to improve sustainable management of these resources (Pomeroy 1995). Sustainable management and exploitation of these resources, however, calls for a clear understanding of the fisheries’ biology (Carbonell et al. 2006; Aragón-Noriega and García-Juárez 2007; Hossain and Ohtomi 2008, 2010), including (i) avoidance of harvesting methods that destroy their benthic (Worm et al. 2006) and mangrove forest habitats (Stevenson 1997) and (ii) strategic use of marine reserves for finfish and shellfish recovery from overfishing and by-catch problems (Roberts et al. 2001). Several commercially important freshwater finfish and shellfish species, including Macrobrachium malcolmsonii, are fished by small-scale fishermen throughout the year in the Ganges River (Hossain 2010).

The freshwater prawn M. malcolmsonii is widely distributed throughout the Indian subcontinent, especially in the rivers draining into the Bay of Bengal. This species has a tremendous potential for culture in freshwater ponds and tanks. This second-largest, fast-growing prawn commonly occurs in the rivers of Bangladesh, India, and Pakistan, including the Ganges/Padma, Mahnanda, Hooghly, and Brahamputra River systems (Kanaujia 2003; Prasad 2005). Macrobrachium malcolmsonii is also abundant in the river Cauvery, a major perennial river of southern India (Selvakumar and Geraldine 2003).

Sex ratio and size structure constitute information basic to assessing reproductive potential and estimating stock size of populations (Vazzoler 1996). Departure from a 1:1 sex ratio is not expected for most aquatic (finfish and shellfish) species, although some finfish and prawn populations may show a strong bias in this ratio. Such differences could be from various causes, including thermal influences on sex determination (Conover and Kynard 1981), selective mortality by sex through differential predation, and divergent sexual behavior, growth rate, or longevity expectation (Schultz 1996).

Length–weight relationships (LWRs) are effective in fisheries management for both applied and basic research (Pitcher and Hart 1982) for several reasons. First, they allow conversion of length distributions into weights for biomass estimates (Poff et al. 1993; Gerritsen and McGrath 2007), a cost-effective alternative to direct, field-based weight measurements that can be time-consuming (Martin-Smith 1996; Koutrakis and Tsikliras 2003). Second, LWR parameters are important to assess fish-stock condition (Gonzalez Acosta et al. 2004). Indeed, an aquatic animal's condition reflects recent environmental (physicochemical and biotic) circumstances, as it fluctuates by interaction among feeding conditions, parasitic infections, and physiological factors (Le Cren 1951).

Life-history traits like sex ratio, length–frequency distribution (LFD), LWRs, and relative-condition factor (K_n ) are generally lesser known for tropical and subtropical prawns than finfish species (e.g., Harrison 2001; Ecoutin et al. 2005; Hossain et al. 2006, 2008, 2009; Hossain and Ahmed 2008). Although the Monsoon River prawn (M. malcolmsonii) is one of the dominant freshwater prawn species commercially important in the Ganges River, no previous biological information exists for it besides (i) Hossain and Rafik (1981) in the lower part of this Bangladeshi River and (ii) Shafi and Quddus (1975) elsewhere in Bangladesh. Hence, this article is the first complete and comprehensive description of the sex ratio, LFD, LWR, and K_n of M. malcolmsonii from the lower Ganges River, using a large number of specimens.

Methods

This study was conducted in the lower Ganges River, northwestern Bangladesh. The Ganges enters Bangladesh (where it is known as the Padma River) from India through the Rajshahi district (latitude 24° 22′ N; longitude 88° 35′ E; Figure 1). Monthly samples for M. malcolmsonii were collected during daytime from the fisherman catch landed at Rajshahi city (Jhaj ghat, Binodpur), Bangladesh from April to October 2010, as caught with traditional fishing traps (Kara).

Figure 1. Sampling site of the Ganges (Padma) River, northwestern Bangladesh, where the Monsoon River prawn M. malcolmsonii (Milne-Edwards, 1844) was captured during the period from March to October 2010.

The fresh samples were immediately placed on ice and fixed in 10% formalin upon arrival in the laboratory where all morphometric traits were examined. The fixed specimens were individually weighed, measured, and sexed. Total length (TL) was measured from the tip of the rostrum to the tip of the telson (FAO 1981) to the nearest 0.01 cm using digital slide calipers (Mitutoyo, CD-15PS) and whole body weight (BW) was measured on an electric balance (Shimadzu, EB-430DW) with 0.01 g accuracy. Sex was determined by the presence of an appendix masculinae on the second pleopod of males. The male:female ratio analysis was conducted on each size class of individuals captured during the study period. The total LFD for each gender was constructed using 1 cm intervals of TL.

The relationship between weight and length was calculated using the expression: BW = a × TL ^b , where a is the intercept of the regression and b the regression coefficient (slope). Parameters a and b of the LWR were estimated by linear-regression analysis based on natural logarithms: ln(BW) = ln(a) + [b × ln(TL)]. Additionally, 95% confidence limits of the parameters a and b and the statistical significance level of r ² (coefficient of determination) were estimated, the latter being a quality indicator of the linear regressions (cf. Scherrer 1984). To confirm whether b (slope) values were significantly different (p ≤ 0.05) from the isometric value of 3.0 (Tesch 1971), the equation of Sokal and Rohlf (1981) was applied: t_s  = (b − 3)/s_b , where t_s is the sample t-test value, b the slope, and s_b the standard error of b. We compared t_s and tabled critical values for b to determine statistical significance and to classify genders as showing isometric (b = 3) or allometric growth (negative allometry for b < 3 or positive allometry for b > 3). Extreme (obvious) outliers attributed to data error were omitted from this analysis.

The K_n for each individual was calculated via the equation of Le Cren (1951): K_n  = BW/a × TL ^b , where a and b are the LWR parameters.

Statistical analyses were performed using Microsoft® Excel Add-in DDXL, GraphPad Prism 5, and VassarStats (online at http://faculty.vassar.edu/lowry/VassarStats.html). Tests for normality of each group were conducted by visual assessment of histograms and box plots and confirmed by the Kolmogorov–Smirnov test. Where the normality assumption was not met, the Mann–Whitney U-test was used to compare the LFD and condition factor between genders. A Chi-square test helped to identify the sex-ratio divergence from the expected value of 1:1 (male:female). The parameters a and b of the LWR for both genders were compared by the analysis of covariance (ANCOVA). All statistical analyses were considered significant at 5% (p < 0.05).

Results

From the 502 specimens of M. malcolmsonii collected in the Ganges River during the study period (March to October 2010), 49% were males and 51% females; so, the overall sex ratio did not statistically differ from the expected 1:1 ratio (χ ² = 0.20, p = 0.157; Table 1). However, the variation in sex ratio with length class showed that females markedly dominated in the 4–5, 7–8, and 8–9 cm TL size groups, whereas males significantly dominated in the 5–6 cm range and above 10 cm TL.

Table 1. Numbers of males and females and sex ratio of M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh, during the period from March to October 2010.

TL class (cm)	Number of specimens			Sex ratio (male:female)	χ ^2(df = 1)	Significance
	Male	Female	Total
4.00–4.99	24	40	64	1:1.67	3.98	*
5.00–5.99	81	23	104	1:0.28	32.52	**
6.00–6.99	39	51	90	1:1.31	1.64	NS
7.00–7.99	25	71	96	1:2.80	21.53	**
8.00–8.99	17	36	53	1:2.14	7.04	**
9.00–9.99	22	28	50	1:1.27	0.72	NS
10.00–10.99	22	5	27	1:0.22	10.83	**
11.00–11.99	10	2	12	1:0.16	6.15	**
12.00–12.99	5	0	5	1:0.00	5.09	**
Overall	246	256	502	1:1.04	0.20	NS
Notes: NS, not significant.
*Denotes significant at 5% level (χ ^2 > χ ^2 1, 0.05 = 3.84), and ** denotes significant at 1% level (χ ^2 > χ ^2 1, 0.01 = 6.63).

Table 2 lists the descriptive statistics for length and weight measurements of the Monsoon River prawn. The LFD of M. malcolmsonii showed that the smallest and largest specimens were 3.54 cm and 11.76 cm TL, respectively, (Figure 2). The 5–6 cm size group was numerically dominant and constituted 33% of the male population, whereas females were dominated by the 7–8 cm size group that constituted 27% of its population. The Mann–Whitney U-test showed no significant differences in the LFD between sexes (Mann–Whitney U-test, p = 0.460). However, the results showed that BW of males (3.33 ± 3.12 g, range 0.60–15.20 g) was significantly higher (Mann–Whitney U-test, p < 0.001) than that for females (2.76 ± 1.95 g, range 0.50–10.70 g).

Figure 2. The T-LFD of male and female M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh, during the period from March to October 2010.

Table 2. Descriptive statistics on the length (cm) and weight (g) measurements of M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh, during the period from March to October 2010.

Sex (n)	Measurements	Minimum	Maximum	Mean ± SD	95% CL
Male (246)	TL	3.54	11.76	6.19 ± 2.17	5.83–6.55
	BW	0.60	15.20	3.33 ± 3.12	2.74–3.92
Female (256)	TL	3.60	10.20	6.14 ± 1.56	5.89–6.39
	BW	0.50	10.70	2.76 ± 1.95	2.45–3.07
Note: n, sample size; SD, standard deviation; and CL, confidence limit for mean values.

Sample sizes (n), regression parameters, and 95% confidence intervals for a and b of the LWR, coefficients of determination (r ²), and growth type of M. malcolmsonii are shown in Figures 3 and 4 and given in Table 3. The calculated allometric coefficient (b) indicated isometric growth in males (2.920 ≈ 3.00, p > 0.05), but negative allometry in females, as the latter t-test for b was significantly different from 3 (2.810 < 3.00, p < 0.01). The average-allometric b value for both sexes together was 2.865. All LWR relationships were highly significant (p < 0.01), with all r ² values exceeding 0.979. The ANCOVA revealed significant differences between genders for the intercepts (a) and slopes (b) of the regression lines (F = 5.03, p < 0.05; Figure 4).

Figure 3. Relationships between TL and BW of male and female M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh.

Figure 4. Natural-log relationships between TL (ln TL) and BW (ln BW) of male and female M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh.

Table 3. Descriptive statistics and estimated parameters for total-length and body-weight relationships (BW = a × TL ^b ) of M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh, during the period from March to October 2010.

Sex	n	Regression parameters		95% CL of a	95% CL of b	R ^2	ts
		a	b
Male	246	0.012	2.920	0.010–0.130	2.849–3.009	0.979	−2.23*
Female	256	0.014	2.810	0.013–0.016	2.748–2.872	0.981	6.03***
Notes: TL, total length; BW, body weight; a, intercept; b, slope; CL, confidence limit; r ^2, coefficient of determination; and t s, t-test value.
*Denotes significant at 5% level (ts  > t 0.05 = 1.96) and *** denotes significant at 0.1% level (ts  > t 0.001 = 3.29).

The relative-condition factors (K_n ) calculated for both genders are given in Table 4. Minimum and maximum K_n values across genders were 0.616 and 1.414, respectively, with an average of 1.015, suggesting that the stock was in good condition. But K_n showed significant variation (p < 0.01) between genders, with better performance by females (1.027 ± 0.107) than males (0.968 ± 0.130) based on overall means.

Table 4. Relative-condition factor (K_n  = W/a × L^b ) of M. malcolmsonii (Milne-Edwards, 1844) in the Ganges River, northwestern Bangladesh, during the period from March to October 2010.

Sex	n	Type	Relative condition factor (Kn )
			Min	Max	Mean ± SD	95% CL
Male	246	TL	0.616	1.242	0.968 ± 0.130	0.947–0.989
Female	256	TL	0.783	1.414	1.027 ± 0.107	0.957–1.097
Notes: n, sample size; TL, total length; Min, minimum; Max, maximum; SD, standard deviation; and CL, confidence limit for mean values.

Discussion

We sampled a large number of specimens of various body sizes via traditional fishing gear (traps). But it was not possible to catch prawns smaller than 2.95 cm TL during the sampling period, despite their presence, which is indicative of the selectivity of the fishing gear. Moreover, we recorded the maximum size of M. malcolmsonii in the Ganges River as 9.27 cm TL, which was noticeably smaller than the maximum value of 16.00 cm TL in the Meghna and Sitalakhya Rivers elsewhere in Bangladesh (Shafi and Quddus 1975). Our maximum weight for this prawn (15.20 g) was also lower than the maximum observed value of 65.0 g in two rivers studied by Shafi and Quddus (1975). For a tropical reservoir (Wyra) in India, Khan et al. (2009) estimated the asymptotic length of M. malcolmsonii as 20.30 cm TL, which is much larger than any Bangladeshi population. Hence, our size range (2.95–9.27 cm TL) for M. malcolmsonii and their preponderance at 4–6 cm TL reflects fast growth and recruitment into the fishery, with fishing harvests and natural mortality probably being high.

However, we did not catch M. malcolmsonii above 10.00 cm TL during the sampling period, which we attribute either to the absence of larger sized individuals in the population or fishing bias towards nursery habitats. In addition, Mossolin and Bueno (2003) and Fransozo et al. (2004), who studied congenerics (i.e., Macrobrachium olfersi and Macrobrachium iheringi, respectively), observed that males reached greater TL than females because of growth-rate differences between genders as with our study on M. malcolmsonii.

The calculated allometric coefficients (b values) based on the TL–BW relationship was 2.920 for males and 2.810 for females, which were within the limit (2.5–3.5) reported by Froese (2006) for most fin- and shellfishes. Hence, despite the presence of divergent prawn forms among species, b is close to 3.0, indicating that prawns generally grow isometrically (this study; Tesch 1971). Because LWRs with b values significantly different from 3.0 were often associated with narrow size ranges of specimens (Tesch 1971), such LWRs should be used only within these size ranges (and with caution for sample-size inadequacy).

LWR in prawn can be affected by several factors including habitat type, area, season, stomach fullness, gonad maturity, gender, health, preservation technique, and length ranges of collected specimens (Tesch 1971), most of which were not accounted for in this study. Because we collected prawns over an extended period of time, our data are not representative of any particular season, so should be treated only as mean-annual values for comparative purposes. However, BWs of M. malcolmsonii across sizes can be estimated from our LWRs, including asymptotic weights (W_∞ ) of 78.89 g in males and 66.10 g in females, as based on the asymptotic TL (L_∞ ) of 20.30 cm (without regard for gender) from the Wyra Reservoir, India (Khan et al. 2009).

Our results can be compared to other tropical and subtropical studies of shrimps. First, Shafi and Quddus (1975) recorded isometric growth for both male (b = 3.083) and female (b = 2.962) M. malcolmsonii, based on the carapace-length versus BW relationship in the Meghna and Sitalakhya Rivers, Bangladesh. Second, Anger and Moreira (1998) reported a higher b for males than females of Macrobrachium, opposite of Palaemon and Palaemonetes, among tropical caridean shrimps. Third, Ibrahim (1962) observed a slightly positive allometry for M. malcolmsonii in the river Godavari of India, whereas Khan et al. (2009) estimated this species’ b value as 2.907 from the TL–BW relationship but neither study separated males and females. In our study, sex-specific differences were observed, namely a higher slope for males than females, which is consistent with Shafi and Quddus’ (1975) study of the same species (M. malcolmsonii) and Anger and Moreira's (1998) study of one (out of three) caridean shrimps.

The mean relative-condition factor of M. malcolmsonii showed significant differences between genders in our study, likely indicating the presence of some ovigerous females. Similar sex-specific differences were reported by Deekae and Abowei (2010) for Macrobrachium macrobrachion in the Luubara Creek, Nigeria. Similarly, Ben-Abdullah et al. (2009) found that the condition factor of a penaeid shrimp (Metapenaeus monoceros) was constant during the pre-spawning period, decreased during spawning (reproduction), and was lowest immediately after it. Our lack of seasonally complete data for Monsoon River prawns or their available prey prevents us from examining K_n relative to spawning and food-production cycles. Unfortunately, other studies of M. malcolmsonii are not available to compare with our relative-condition factors. Besides seasonal changes in K_n via gonadal development, the LWR-based condition factor is an indicator of spatiotemporal changes in food reserves and thus an indicator of general prawn condition.

In conclusion, this study provides basic information on the sex ratio, LFD, LWR, and relative-condition factors of M. malcolmsonii from the Ganges River, which should be useful for the sustainable management of this prawn fishery in this river basin of northwestern Bangladesh and neighboring countries. Moreover, because no such information currently exists in the SealifeBase database for M. malcolmsonii, our results should contribute to this invaluable database. Yet, more detailed studies are needed to answer several questions about body-size range and the spawning periodicity of this prawn fishery.

Acknowledgments

The authors thank Md. Bor Jahan (local fisher, Rajshahi) for extending cooperation in collecting samples; the Chairman of the Department of Fisheries, University of Rajshahi, Bangladesh for providing laboratory facilities; the editor and anonymous referees for their useful and constructive comments; and the Japan Society for the Promotion of Science for providing research support.