Free Access
Issue
Ann. Limnol. - Int. J. Lim.
Volume 55, 2019
Article Number 8
Number of page(s) 9
DOI https://doi.org/10.1051/limn/2019007
Published online 30 April 2019

© EDP Sciences, 2019

1 Introduction

Toxabramis swinhonis Günther, 1873 (family Cyprinidae, subfamily Cultrinae), commonly known as thin sharpbelly, is a small pelagic and gregarious fish widely distributed in the Yangtze River, Yellow River and other freshwater bodies in China (Chen et al., 1998; Zheng, 1998). The species mainly feeds upon copepods, cladocerans and insect larvae (Xie et al., 2001; Zhang, 2005), whilst it is the common prey of many larger economic piscivorous fishes such as Siniperca chuatsi (Basilewsky, 1855), Culter alburnus (Basilewsky, 1855), Culetr dabryi dabryi (Bleeker, 1871) and Cultrichthys erythropterus (Basilewsky, 1855) (Anonymous, 1976; Yang et al., 2002; Zhang, 2005; Cui et al., 2013). Consequently, despite not being a fish of fishing interest, T. swinhonis is an important species in terms of ecological aspects and fisheries management as it is one of the main by-catch species in freshwater fishery in inland China and plays a key role in the energy flows of these hydro-ecosystems, linking zooplankton to higher trophic levels (Li et al., 1988; Ye et al., 2014). Further, recent studies have documented that T. swinhonis is gradually becoming the most abundant small fish species in many rivers, lakes and reservoirs of China, and this phenomenon exhibits a trend of further increasing (Ge et al., 2009; Li et al., 2018), questioning the sustainability of fisheries resources and fish biodiversity conservation in these water bodies.

Hence, it is the time that much more attentions should be paid on the biology, ecology and fisheries management of this species. However, as far as the authors are aware, the limited documented studies on the above-mentioned aspects of T. swinhonis mainly focused on its age, growth, mortality, feeding habits and community ecology (Li et al., 1988; Xie et al., 2001; Zhang, 2005; Ye et al., 2014, 2015). To date, researches on reproductive biology of this species are either unpublished or unavailable though reproductive traits are essential for fish population dynamics modeling, fish stock assessment and fisheries management (King and McFarlane, 2003; Tracey et al., 2007).

Therefore, the present study aimed at filling the research gap of the reproductive biology of T. swinhonis with a focus on quantifiable characteristics needed for fish population dynamics modeling, fish stock assessment and fisheries management: (1) sex ratio, (2) size and age at first maturity, (3) spawning season and pattern and (4) batch fecundity. Finally, the implications of our findings for freshwater fisheries management and fish biodiversity conservation in inland China are discussed.

2 Materials and methods

2.1 Study site

Biandantang (BDT) Lake (Fig. 1; 30°17′17.03″ N, 114°43′00.68″ E) is a typical shallow macrophytic lake, which locates on the south bank of the middle reach of the Yangtze River, Hubei Province, central China (Guan, 1995). The lake, with an area of 3.86 km2, is a sub-lake of the larger Baoan Lake (39.3 km2) and separated from the latter by a stone dyke with one boat passage (width about 5 m) allowing water exchange (Xie et al., 2000). Although this lake was historically interconnected with the mainstream of the Yangtze River by a channel, it is now an enclosed water body. Thus, the water level oscillation of this lake mainly depends on the local rainfall. Meanwhile, according to the annual investigation of the present study, the lake was slightly eutrophic (the modified Carlson's synthesis trophic state index TSIM (Σ) = 49.44) (Aizaki et al., 1981) and covered with large quantities of aquatic macrophytes such as Potamogeton crispus (Linn) and Nelumbo nucifera (Gaerth), accounting for more than 90% of the whole lake surface. More details about limnological traits of this lake during the study period can be found in Table 1.

thumbnail Fig. 1

Skeletons of Biandantang (BDT) Lake and larger Baoan Lake (topright). Black solid dots indicate the locations of sampling sites.

Table 1

Limnological characteristics of BDT Lake during October 2016 to September 2017.

2.2 Data collection and laboratorial procedures

T. swinhonis and limnological characteristics were collected monthly at six sites in the BDT Lake from October 2016 to September 2017 (Fig. 1). Fishes were captured using fixed multi-mesh gillnets (mesh size: 10–125 mm, 30 m long × 1.5 m high) modified from Appelberg (2000) (mesh size: 5–55 mm, 30 m long × 1.5 m high) between 17:30 and 5:30 of the next day (i.e., 12 h), while the environmental factors were measured with multi-water quality meter (YSI Professional Plus; Yellow Spring Instruments, Ohio, USA), water depth finder (model SpeedTech SM-5, USA), turbidimeter (Hach 2100Q Portable Turbidimeter, Loveland, CO, USA), Secchi disk and ultraviolet spectrophotometer.

For each catch and euthanized (MS-222) fish, total length (LT, nearest 0.01 mm), total weight (WT, nearest 0.01 g), gonadal weight (WG, nearest 0.01 g), eviscerated weight (WE, nearest 0.01 g), sex, age and gonad maturity stage were determined immediately in their fresh state. Meanwhile, two subsamples, approximated 0.05 g of each, taken at anterior, middle and posterior parts of every sample fish's gonad were weighed (nearest 0.01 g) and stored separately into two labeled plastic centrifuge tubes (10 ml) with one containing Bouin's fluid and another 10% formalin neutral buffered solution (Cuellar et al., 1996).

Tissue samples immersed in Bouin's solution were subsequently made into histological sections in the laboratory as the following procedure: washed with distilled water, dehydrated through increasing concentrations of ethyl alcohol, cleared in xylene, infiltrated in paraffin wax (García-Seoane et al., 2014), cut into 5–6 µm thick with a microtome and stained with hematoxylin and eosin (H&E) (Lillie, 1947). In contrast, hydrated oocytes taken from the mature ovaries (stages IV to VI, collected in spawning season) infiltrated in 10% formalin neutral buffered solution were first teased apart from the connective tissue, and then counted or measured.

Fish lengths (LT) and weights (WT, WG and WE) were measured by an electronic caliper and a precision electronic balance, respectively. Age estimation was based on scalimetry, and sexes and gonad maturity stages were determined by inspecting the appearance of the gonads (shape, color and opacity) and histological analysis (whenever needed). According to Mейен (1939), gonad development stages of freshwater fish included six phases: (I) immature, (II) quiescent, (III) ripening, (IV) ripeness, (V) reproduction and (VI) spent. All microphotographs were obtained using the Olympus BX53 (Olympus Corporation, Tokyo, Japan) fluorescence microscope and all the hydrated oocytes were counted or measured under a Leica camera (DFC295) connected with a microscope (Leica S8APO).

2.3 Data analysis

Sex ratio, expressed as female:male, was computed monthly, seasonally and annually. Deviations from the theoretical value 1:1 were statistically tested using Chi-square (χ 2) test (Zar, 1999). Meanwhile, comparison of the average LT between females and males was conducted by the Wilcoxon rank sum test.

Fish length and age at first maturity (i.e., A50 and L50, at which the probability of maturity is 50%) were estimated using specimens (125 females: 54.56–132.90 mm; 204 males: 61.76–131.94 mm) collected throughout the spawning season (April–August), von Bertalanffy growth model (VBGM) of T. swinhonis proposed by Ye et al. (2014) and the following maturity ogive (Prager et al., 1989): P = 100 × (1 + exp(−K (LT − LT50)))−1, where P represents the probability of being mature at size LT and K is the curvature of this sigmoid curve. In order to fit this maturity ogive, maturity was described in a binary configuration (0 = immature, stages I–III for both sexes; 1 = mature, stages IV–VI for both sexes) (Tracey et al., 2007) and maximum likelihood estimation method was used. Further, the differences in maturity ogives between sexes were detected using the multivariate Hotelling's T-squared test (Bernard, 1981).

The spawning season and pattern were determined by analyzing the monthly values of the gonadosomatic index (GSI = 100 × WG/WE) (Devlaming et al., 1982), relative percentages of gonad maturity stages and size distribution of the oocytes. One-way ANOVA with Tukey's HSD post-hoc was used to determine whether there were significant differences in GSI among different months (Zar, 1999). The relationships between spawning season and environmental factors (water temperature and rainfall) were determined graphically using the monthly relative percentages of the gonad maturity stages.

The hydrated oocytes (stages IV and V) were used to estimate the batch fecundity (FB) of T. swinhonis using the following gravimetric equation: FB = n × (WG/WGS), where WGS is the weight of the subsample used for eggs counted and n is the number of hydrated oocytes within the same subsample (Bagenal and Braum, 1978; Hunter et al., 1985). Further, relative fecundity was computed as fecundity divided by WE. The relationships between FB, and LT, WG, WT and age were analyzed using linear or non-linear regression and one-way ANOVA with Tukey's HSD post-hoc, respectively.

All statistics and graphics were performed in R 3.3.2 (R Core Development Team, 2018) using the “base” and “rgdal” (Bivand et al., 2018) packages. The significance level (α) was also set to 0.05 and all estimates were expressed as mean ± standard error (S.E.) in the current study unless otherwise stated.

3 Results

3.1 Size structure

A total of  783 T. swinhonis (368 females, 358 males and 57 unsexed) were captured. Males were dominant in the middle size classes (80–120 mm LT), whereas females were more abundant in other size classes (Fig. 2). Nevertheless, no significant difference was found in average LT between females and males (F: 104.09 ± 1.06 and M: 104.13 ± 0.63 mm; Wilcoxon rank sum test, P > 0.05).

thumbnail Fig. 2

Length frequency distributions of female (white) and male (gray) Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017. Histograms and boxplots (horizontal line within box: median; boundaries of box: 25% and 75% quantiles; bars: lower and upper inner fences; circles: outliers) are two different approaches used to characterize this information.

3.2 Sex ratio

The overall sex ratio of T. swinhonis was 1.03:1, not divergent significantly from the expected value 1:1 (Tab. 2; χ 2 = 0.14, P > 0.05). Nevertheless, sex ratio varied with seasons: 1.32:1 (skewness toward females) in the early stage of spawning season (March–April), while 0.46:1 (skewness towards males) in the later stage of the spawning season (July–August). More specifically, sex ratio skewed toward females in March, August, September, November and December, whereas it reversed and biased in favor of males in June, July and October (Tab. 2). No significant differences were observed among this value with the theoretic value 1:1 for the remaining months, i.e. January, February, April and May (Tab. 2; χ 2 = 0.07, 2.39, 0.12 and 0.09, respectively, all P > 0.05).

Table 2

Monthly variations of sex ratio for female to male (F/M) Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017 (P-values determined by χ 2-tests).

3.3 Size and age at first maturity

The relationships between mature probability of females and males T. swinhonis and their total lengths (LT) in BDT Lake were P = 100 × (1 + exp (–0.14 (LT − 84.47)))−1 (n = 124, pseudo-R 2 = 0.65) and P = 100 × (1 + exp (–0.12 (LT − 81.86)))−1 (n = 204, pseudo-R 2 = 0.43), respectively. According to these two maturity ogives and VBGM of T. swinhonis, the estimates of LT50 of females and males T. swinhonis were 84.47 mm (accounted for 57.39% of the largest LT of females captured) and 81.86 mm (accounted for 62.04% of the largest LT of males captured), respectively (Fig. 3). A50 of females and males T. swinhonis were 1.62 and 1.56 yr, respectively. Further, we observed a significant difference in LT50 and A50 between sexes (T 2 = 129.89 and 856.62, respectively, both P < 0.05).

thumbnail Fig. 3

Mean ± 95% C.I. logistic regression model for estimating the length at first maturity (LT50) of (a) female and (b) male Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017. Black solid dots indicate the observed points.

3.4 Spawning season and pattern

Monthly succession of the average GSI (Fig. 4) and the percentage of mature individual (Fig. 5) co-indicated that T. swinhonis was a spring-summer spawner, as both indicators increased significantly in March, peaked strongly in May, decreased sharply between June and August, then returned to quiescent period in September and maintained this state until next spawning cycle. Similarly, the relationships between abiotic variables and development of the gonad showed that the water temperature and rainfall may be two of main drivers of spawning activity, and suitable water temperatures for reproduction of T. swinhonis were 23–34 °C (Fig. 5). Furthermore, the histological analysis on the mature gonads of females and males (Fig. 6) combined with the distribution of egg size of one mature female (Fig. 7) collected from the spawning season proved that T. swinhonis was a multiple or fractional spawner (release of eggs at intervals, usually over several days or weeks) due to the fact that oocyte diameter had a bimodal distribution and all development stages of oocytes or spermatogonia co-occurred in one fully mature ovary or testis. Certainly, based on these facts, it should not be forgotten that the absolute fecundity of T. swinhonis estimated in this study is actually the batch fecundity (FB).

thumbnail Fig. 4

Monthly variations in the gonadosomatic index (GSI) of (a) female and (b) male Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017. Different letters mean that there existed a statistical significance (one-way ANOVA with Tukey's HSD post-hoc). Error bars mean standard errors (S.E.).

thumbnail Fig. 5

Monthly successions in the pattern of gonadal maturity stages in relation to abiotic factors [water temperature (red solid lines) and water depth (blue solid lines)] for female (a) and male (b) Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017.

thumbnail Fig. 6

Histological sections for ovary or testis of two mature Toxabramis swinhonis collected in spawning season. Two top figures [(a) and (b)] were ovary containing oogonia (O), perinuclear (P) oocytes, cortical alveolar (CA) oocytes, vitellogenic (V) oocytes, post-ovulatory follicles (POF), luminal cavity (Lc) and lipid vacuoles (Lv). Two bottom figures [(c) and (d)] were testis including spermatogonia (S), spermatocytes (Sc), spermatid (St), spermatozoa (Sz) and luminal cavity (Lc). Stages I to VI were gonadal development stages.

thumbnail Fig. 7

Frequency distribution and kernel density estimation (solid line) of oocyte (N = 15 786) diameters from a mature female (in stage IV) Toxabramis swinhonis collected in BDT Lake at May 2017.

3.5 Batch fecundity

Fecundity was estimated for 98 mature females collected in spawning season whose LT and WT ranged from 74.77 to 111.37 mm, and 1.65 to 4.36 g, respectively. The estimates of FB varied in a wide range from 2006 to 73 592 eggs per fish, with a mean value of 26 487.15 ± 2675.61 eggs per fish. Similarly, the estimates of relative FB also varied within a wide range from 421 to 3608 eggs/g, with a mean value of 1730.14 ± 174.77 eggs/g of fish body weight. Meanwhile, FB increased with increasing gonad weight (WG), eviscerated weight (WE), total length (LT) and age (Fig. 8). The best-fit regression equations were FB = 4392.00 + 15 314.00 WG (n = 98, R 2 = 0.75); FB = –3367.80 + 2038.40 WE (n = 98, R 2 = 0.68) and FB = 0.0002 LT 3.77 (n = 98, R 2 = 0.73), respectively.

thumbnail Fig. 8

Relationships between Toxabramis swinhonis batch fecundity and gonad weight (g), eviscerated weight (g), total length (mm) and age (year). Different colors in the boxes mean that there existed a statistical significance among different age groups (one-way ANOVA with Tukey's HSD post-hoc).

4 Discussion

Sex ratio is one of the most important parameters in population ecology and fisheries management as it can inform fisheries scientists and managers about population structure, reproductive potential and population dynamics (Raposo and Gurgel, 2001; Cao et al., 2009). In this study, the overall sex ratio of T. swinhonis in BDT Lake was 1.03:1, which corresponded well with most fish populations whose sex ratios show no difference from expected 1:1 (Nikolsky, 1963). However, similar with Abramis brama (Linnaeus, 1758), this ratio varied with time and size, females being dominant in the early stage of spawning season (March–April) and older size groups, while males dominated in the later stage (July–August) and smaller size groups (Zhang et al., 2017). According to Zhang et al. (2017), Türkmen et al. (2002) and Wang et al. (2013), a surplus of females in the early stage of spawning season and larger size groups, and a surplus of males in the later stage of spawning season and smaller size groups as observed here can be considered as a reproductive strategy of T. swinhonis to produce high number of fertilized eggs or offspring, so as to get an accelerated population growth (Nikolsky, 1963; Manorama and Ramanujam, 2017).

The size or age at first maturity (LT50 or A50) of one fish species can directly influence its reproductive potential in population level (Beacham, 1983), being thus crucial parameter for biodiversity conservation and management strategies (Cruz et al., 2000). In the present study, T. swinhonis got mature at the later period of their life history. Meanwhile, females matured later than males, which was similar with many other fish species such as A. brama and Raja undulate Lacepède, 1802 (Coelho and Erzini, 2006; Zhang et al., 2017). Many fishery scientists pointed out that this might be a reproductive tactic to guarantee the population growth as a larger body size often means a bigger abdominal cavity, a higher reproduction potential and a quicker speed to accumulate the fat for reproductive activities or recovery from the spawning behavior (Parker, 1992; Bisazza and Pilastro, 1997; Türkmen et al., 2002; Bromley, 2003; Wang et al., 2013).

Gonad development has been described for many teleost fish species to determine the spawning season and pattern (Shinkafi et al., 2011; Manorama and Ramanujam, 2017), which are very important for artificial propagation and fisheries management (Cao et al., 2009). The results obtained in this study indicated that T. swinhonis was also an asynchronous, multiple and spring-summer (i.e., May and June) spawner, like many other freshwater fishes in the temperate zone (Peter and Crim, 1979). According to Malison et al. (1994), such a reproductive pattern may be a reproductive strategy for the larval and young T. swinhonis to grow quickly and survive well based on the suitable water temperature and sufficient food availability.

Fecundity is one of the most important components of fishery biology as it has direct bearing on fish production, stock recruitment and stock management (Qadri et al., 2015). The batch fecundity (FB) and relative batch fecundity of T. swinhonis obtained from this study were 26 487.15 eggs and 1730.14 eggs/g of fish body weight, respectively, which were obviously higher than many other freshwater fishes such as Oxygymnocypris stewartii (Lloyd, 1908), A. brama and Peltobagrus fulvidraco (Richardson, 1846) (Cao et al., 2009; Huo et al., 2013; Zhang et al., 2017). Undoubtedly, this may be another reason why T. swinhonis has become the most dominant fish species in many shallow lakes of China.

Based on these results, what should be noted is that the reproduction characteristics of T. swinhonis can lead to its population explosion which has negative effect on fish-diversity of the lake, and it has been verified that, of our catch, T. swinhonis took up nearly 58% in number and 22% in weight, respectively (unpublished data). To control the population of T. swinhonis, a very feasible or simple way we suggest, is to catch them with discretion before their spawning season and process the catch into feed (such as fish meal) for aquaculture or stock farming, or even food for human, like fried fish for sale. Besides, to release fish who prey on T. swinhonis with discretion is considerable as well (Ye et al., 2006).

Overall, this paper is the first report about reproductive biology of T. swinhonis, thus comparisons cannot be conducted with either previous data for the same population in the BDT Lake or other populations of the same species elsewhere. Nevertheless, the inferences made herein can be used as the baseline information for future population modeling, fish stock assessment, fisheries management and comparison studies of T. swinhonis.

Acknowledgments

We are grateful to Mr. Lisheng Liu and Mr. Xinnian Chen for their assistance in the field sampling. We would also like to give our sincere appreciations to Qingwu Cai for his valuable comments and suggestions, leading to the huge improvement of the earlier manuscript of this paper. Many thanks should be given to the National Science and Technology Supporting Program of China (2012BAD25B08), the Earmarked Fund for China Agriculture Research System (CARS-45), the State Key Laboratory of Freshwater Ecology and Biotechnology (2014FBZ04), and the China Scholarship Council (CSC) for their financial support to this work.

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Cite this article as: Dong X, Grenouillet G, Ju T, Xiang T, Mai Z, Laffaille P, Lek S, Liu J. 2019. Reproductive biology of thin sharpbelly, Toxabramis swinhonis Günther, 1873 in a shallow lake (Biandantang Lake) along the middle reach of the Yangtze River basin (China): implications for fisheries management. Ann. Limnol. - Int. J. Lim. 55: 8

All Tables

Table 1

Limnological characteristics of BDT Lake during October 2016 to September 2017.

Table 2

Monthly variations of sex ratio for female to male (F/M) Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017 (P-values determined by χ 2-tests).

All Figures

thumbnail Fig. 1

Skeletons of Biandantang (BDT) Lake and larger Baoan Lake (topright). Black solid dots indicate the locations of sampling sites.

In the text
thumbnail Fig. 2

Length frequency distributions of female (white) and male (gray) Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017. Histograms and boxplots (horizontal line within box: median; boundaries of box: 25% and 75% quantiles; bars: lower and upper inner fences; circles: outliers) are two different approaches used to characterize this information.

In the text
thumbnail Fig. 3

Mean ± 95% C.I. logistic regression model for estimating the length at first maturity (LT50) of (a) female and (b) male Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017. Black solid dots indicate the observed points.

In the text
thumbnail Fig. 4

Monthly variations in the gonadosomatic index (GSI) of (a) female and (b) male Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017. Different letters mean that there existed a statistical significance (one-way ANOVA with Tukey's HSD post-hoc). Error bars mean standard errors (S.E.).

In the text
thumbnail Fig. 5

Monthly successions in the pattern of gonadal maturity stages in relation to abiotic factors [water temperature (red solid lines) and water depth (blue solid lines)] for female (a) and male (b) Toxabramis swinhonis collected in BDT Lake from October 2016 to September 2017.

In the text
thumbnail Fig. 6

Histological sections for ovary or testis of two mature Toxabramis swinhonis collected in spawning season. Two top figures [(a) and (b)] were ovary containing oogonia (O), perinuclear (P) oocytes, cortical alveolar (CA) oocytes, vitellogenic (V) oocytes, post-ovulatory follicles (POF), luminal cavity (Lc) and lipid vacuoles (Lv). Two bottom figures [(c) and (d)] were testis including spermatogonia (S), spermatocytes (Sc), spermatid (St), spermatozoa (Sz) and luminal cavity (Lc). Stages I to VI were gonadal development stages.

In the text
thumbnail Fig. 7

Frequency distribution and kernel density estimation (solid line) of oocyte (N = 15 786) diameters from a mature female (in stage IV) Toxabramis swinhonis collected in BDT Lake at May 2017.

In the text
thumbnail Fig. 8

Relationships between Toxabramis swinhonis batch fecundity and gonad weight (g), eviscerated weight (g), total length (mm) and age (year). Different colors in the boxes mean that there existed a statistical significance among different age groups (one-way ANOVA with Tukey's HSD post-hoc).

In the text

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