Evaluation of seminal plasma composition and ...

4 downloads 0 Views 678KB Size Report
Hussain MG, Obaidullah M, Rahman MM, Akhteruzzaman M,. Perschbacher P (1987) Hormone induced ovulation and spawning of Puntius gonionotus ...
Fish Physiol Biochem https://doi.org/10.1007/s10695-018-0539-4

Evaluation of seminal plasma composition and spermatozoa quality parameters of silver barb, Barbonymus gonionotus Bleeker, 1850 Ibrahim Rashid & Md Shakhawate Hossain & Mohammad Abdus Salam & S. M. Rafiquzzaman

Received: 27 February 2018 / Accepted: 5 July 2018 # Springer Nature B.V. 2018

Abstract Seminal composition and semen quality are the important determinants in assessing the reproductive performance of different fishes. This study was carried out to evaluate the seminal composition and sperm quality of Barbonymus gonionotus. The seminal plasma contained 17.2 ± 0.34 mmol/l, 20.9 ± 0.48 mmol/l, 0.72 ± 0.04 mmol/l, 3.8 ± 0.2 mmol/l, and 1.49 ± 0.02 g/dl of Na+, K+, Ca++, Mg++, and total protein, respectively. The physical spermatological parameters, such as sperm volume, sperm motility, motility duration, sperm density, osmolality, and pH values were 1.55 ± 0.15 ml, 89 ± 2%, 391.9 ± 8.5 s, 2.8 ± 0.2 × 10 10 /ml, 400.6 ± 5.1 mmol/kg, and 8.75 ± 0.10, respectively. In correlaIbrahim Rashid and Md Shakhawate Hossain contributed equally to this work. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10695-018-0539-4) contains supplementary material, which is available to authorized users. I. Rashid : M. S. Hossain (*) : S. M. Rafiquzzaman Department of Fisheries Biology and Aquatic Environment, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh e-mail: [email protected] M. S. Hossain Faculty of Fisheries and Protection of Waters, South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses, University of South Bohemia in České Budějovice, Zátiší 728/II, 389 25 Vodňany, Czech Republic M. A. Salam Department of Genetics and Fish Breeding, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh

tion matrix, the K+ (R2 = 0.39, P < 0.01) and Ca++ (R2 = 0.27, P < 0.05) ions and osmolality (R2 = 0.29, P < 0.05) showed significant positive correlations with sperm motility. Similarly, fertilization rate significantly influenced by sperm motility (R2 = 0.26, P < 0.05) and K+ (R2 = 0.30, P < 0.05) and Ca++ (R2 = 0.26, P < 0.05) ions. Also, osmolality significantly and negatively correlated with Mg++ (R2 = 0.33, P < 0.05) and sperm motility duration (R2 = 0.28, P < 0.05). Therefore, based on this results, it can be concluded that seminal plasma ions, K+ and Ca++ and osmolality are the key factors for the determination of sperm quality of silver barb, and these parameters could be considered during standardization of artificial fertilization or cryopreservation technique of silver barb spermatozoa. Keywords Spermatozoa motility . Plasma ion . Osmolality . Barbonymus gonionotus . Silver barb

Introduction Reliable production in aquaculture requires the control of the reproduction which, in turn, requires a good knowledge of sperm characteristics, including physical and biochemical parameters. Use of high-quality spermatozoa collected from captive broodstock has great importance to ensure the valuable offspring production in aquaculture (Hajirezaee et al. 2010). Therefore, assessment of individual variability or capacity to fertilize is necessary to understand the basic biochemical processes occurring during motility of spermatozoa and

Fish Physiol Biochem

fertilization to evaluate the reproductive capability of different fish (Sarvi et al. 2006; Hatef et al. 2009). Sperm volume, concentration and motility, as well as composition of the seminal plasma are most common parameters to assess spermatozoa quality in fish (Linhart et al. 2000; Alavi and Cosson 2006). The spermatozoa motility is a prerequisite factor determining fertilizing capacity of spermatozoa (Alavi et al. 2004). The spermatozoa motility is usually influenced by several factors, such as pH (Alavi and Cosson 2005), cations or osmolality (Alavi 2007), and dilution ratio (Alavi et al. 2004) in either aqueous environment or diluents (Alavi and Cosson 2006). The ions, such as Na+, K+, and Cl− not only create osmotic pressure but they are deeply involved in sperm movement triggering (Bozkurt et al. 2011). Mg++ has most often a minor role in the initiation of intracellular mechanisms of spermatozoa motility in teleost (Cosson et al. 1999). Assessment of seminal plasma is also important because, generally, spermatozoa are immotile in the testes (Morisawa and Morisawa 1986) and maintained in this condition by some physical or biochemical characteristics of seminal plasma. These would provide knowledge for the preparation of artificial plasma solution, which can be used for the dilution of semen for short-term storage or cryopreservation (Billard and Cosson 1992; Dreanno et al. 1998). Seminal plasma composition has been studied in rainbow trout and salmon as well as other salmonids (Hatef et al. 2007). However, few cyprinids, including Cyprinus carpio (Emri et al. 1998; Linhart et al. 2003a), Ctenopharyngodon idella (Khara et al. 2012), Tinca tinca (Linhart et al. 2003c), and Hypophthalmicthys molitrix (Rahman et al. 2011) received attention like acipenseridae (Linhart et al. 2003a, b, c; Alavi et al. 2004) and other marine fishes (Ciereszko et al. 2002) for analysis of seminal plasma composition. Regarding the compositional analysis, it has been well documented that fish seminal plasma composition and its physiological characteristics are important aspects of semen quality and have been found variable with the species (Alavi and Cosson 2006), even among the individuals of the same species (Piironen 1985). Silver barb, Barbonymus gonionotus, is a native species to Southeast Asia and is cultivated in freshwater ponds of Thailand, Indonesia, Vietnam, India, and Bangladesh (FAO 2016). It is a fast growing freshwater fish species having good nutritional value (Bogard et al. 2015). This species attains sexual maturity within a year

and also reaches a weight of 150–200 g within 5– 6 months, becomes ready for harvesting (Hussain et al. 1987). Although basic reproductive and life history information of silver barb is available (Liley and Tan 1985; Mondol et al. 2005; Bhuiyan et al. 2006; Jiwyam 2014); however, data on the effect of cations on the spermatozoa motility and fertilization capacity is rare. With this view, this present study aimed to analyze the chemical spermatological parameters, ionic contents (Na+, K+, Ca++, Mg++), and protein of seminal fluid as well as to show if there is any physiological relationship between the spermatozoa quality factors and plasma composition of silver barb.

Materials and methods Ethical statement No specific permissions were required for the locations and activities involved in this study. The study did not involve endangered or protected species. All experimental manipulations (rearing, capture, and measurements) were conducted according to the principles of the Ethical Committee of Bangabandhu Sehikh Mujibur Rahman Agricultural University, Bangladesh, and National Research Ethics Committee (NREC) of Bangladesh. This study also follows the rules for the Protection of Animals in Research of the University of South Bohemia, Faculty of Fisheries and Protection of Waters, Research Institute of Fish Culture and Hydrobiology, Vodňany, based on the EU harmonized animal welfare act of Czech Republic. The principles of laboratory animal care and the national laws 246/1992 and regulations on animal welfare were followed (Ref. number 22761/2009-17210). Broodstock care and collection of semen Premature adult (male and female) (mean weight, 19.1 ± 5.7 g) fishes were collected from Government hatchery, reared (average water temperature range during culture period, 24–34 °C) at stocking density of 3/m2 in the field complex pond (130 m2) and fed with a pelleted diet (protein—30%) (Hossen et al. 2017) for about 1 year. Thirty fishes (15 each sex, age: 1+ year) were selected randomly from the broodstock for use as semen and egg donors. Selected brood fishes were

Fish Physiol Biochem

conditioned by transferring them in a mechanically aerated, 500L flow-through tank system for about 6 h (~ 25 °C, room temperature) prior to hormone treatment. Commercially available ovaprim (Salmon Gonadotropin Releasing Hormone Analog 20 μg/ml −1 + domperidone 10 mg/ml−1) (Western Chemicals Inc., USA) were administered in the pectoral fin girdle of male fish as a dose of 0.25 ml ovaprim/kg−1 body weight and for female at 0.5 ml ovaprim/kg−1 body weight (Hossen et al. 2017). Each male was stripped once only after 6 h of injection, and the total amount of expressible milt was collected individually by gently pressing the abdomen. Much care was taken to avoid the contamination of semen with water, urine, blood, or fecal matter, and immediately kept in flake ice at about 4 °C in the ice box. Semen samples for all evaluation were processed instantly after gathering of semen from each male. Fish length and weight were also recorded using measuring board-scale and electric balance (ZSA 120, Scientech, USA) to estimate their possible correlations with all studied spermatozoa quality parameters.

activation to till the ceasing of last spermatozoa movement in that field. Measurement of sperm density Semen were diluted 1000 times through 0.3% NaCl. A hemocytometer counting chamber was used to determine spermatozoa density and expressed as the number of cells per milliliter. A droplet of the diluted milt was placed on a hemocytometer slide (depth 0.1 mm) with a cover slip (Marienfeld, Laudakonigshofen, Germany) and count using light microscopy (× 400, Olympus CK2, Tokyo, Japan). After 3– 5 min (to allow sperm sedimentation), the number of spermatozoa were counted in at least 5 large squares (area 0.04 mm2 each) of total 25 squares (one large square has 16 individual cells), and then, counted cells were calculated to estimate the sperm density using the following formula: No:of cells per ml ¼ ðnumber of cells  10; 000Þ =ðnumber of squares  dilutionÞ

Evaluation of semen volume, pH, and osmolality Sperm samples were collected into 20-ml calibrated glass tubes. Sperm pH was determined with a pH indicators strips (Merck, Germany) within 30 min of sampling. Osmolality of semen were determined using Vapro® vapor pressure osmometer (Model 5600, ELITechGroup Inc., USA). Each measurement for pH and osmolality were replicated in three times. Spermatozoa motility (%) and duration The motility (%) and duration (s) of spermatozoa in each sample were evaluated at room temperature (~ 25 °C) within the first hour following the semen collection. One microliter of milt was taken on a glass slide and about 10 μl activation solution (0.3% NaCl) (Hassan et al. 2013; Rahman et al. 2016) was added to activate the sperm. Motility observation was carried out under a prefocused inverted microscope (× 400, Olympus CK2, Tokyo, Japan). Only forward movements of spermatozoa were assessed as motile, whereas simply vibrating spermatozoa assessed as immobile. The counting process was repeated at least three times, and motility was expressed as percentage. Motility duration of spermatozoa was calculated using stopwatch from the start of forward movement of spermatozoa after 3–5 s of

Evaluation of seminal plasma composition Seminal plasma was collected after centrifugation of the semen at × 3370g for 10 min. Centrifugation was done twice to avoid possible contamination with spermatozoa, and supernatants were stored in vials at − 20 °C until the beginning of analysis. Levels of major cations (Na+, K+, Ca++, and Mg++) were determined according to Hatef et al. (2007). A total nitrogen content of semen was measured through the micro-Kjeldahl method (Layne 1957), and the total nitrogen percentage was converted into total protein by multiplying with the conversion factor 6.25. Fertilization trail of silver barb egg Eggs were collected from hormone induced female through stripping into a plastic bowl and divided into different batches according to our experimental design. Each batch contains approximately 1200 eggs. At least three batches of eggs were fertilized with fresh milt (30 μl) collected from each male at a ratio (egg:sperm) of approximate 1:500000 (Chew and Zulkafli 2012; Sarder et al. 2009). After mixing sperm, 5–10 ml of physiological saline (0.3% NaCl solution) was added to

Fish Physiol Biochem

the egg mass and mixed with hen feather. The fertilized eggs were washed carefully three to four times with tap water and transferred into marked incubation jars (radius 0.3 m, height 0.7 m, and volume 90 l) having continuous water flow (12–14 l min−1) for egg movement. All of the processes were done at room temperature about ~ 25 °C. After 6 h of fertilization, some eggs (approximate 150 eggs) were collected from all of the jars and observed visually. Fertilized eggs seem to be transparent, adhesive, and swollen, while unfertilized eggs smaller in size and opaque (Rahman et al. 2016). The progress of cell division was observed under microscope. Fertilization rate was estimated as follow the formula. Fertilization rate ð%Þ ¼ No:of fertilized eggs  100  total no of eggs ðfertilized and unfertilizedÞ

Statistical analysis Correlations between spermatological parameters and plasma composition were estimated using Pearson’s correlation test. Length and weight data were fitted in the exponential equation of Le Cren (1951) after log transfer to find a linear relationship and indicator of growth pattern, b value (Riedel et al. 2007). Condition factor (K) was determined using the formula as: K = 100 W/TL3, where W = weight and TL = total length (Ricker 1975). The spermatozoa motility was used as dependent and other observed parameters as independent variables and fits to linear regression. Statistical analyses were performed using SPSS16 for Windows statistical software package. Results are presented as means ± SEM. The significance level was set to P < 0.05.

Results Growth rate of brood fish The regression equation is expressed as Log W (male) = 2.678 and Log TL − 1.434, where b = 2.678 and a = −1.434 (Fig. 1). The condition factor (K) value ranges from 1.46 to 0.77 with mean 1.01 ± 0.13. The lengthweight regressions were found to be highly significant (P < 0.01) based on the coefficient of determination (R2 = 0.91).

Fig. 1 Logarithmic relationship between total length and body weight of B. gonionotus male

Spermatological parameters Sperm volume, sperm motility, motility duration, sperm density, osmolality, and pH values were 1.55 ± 0.15 ml, 89 ± 2%, 391.9 ± 8.5 s, 2.8 ± 0.2 × 1010/ml, 400.6 ± 5.1 mmol/kg, and 8.75 ± 0.10, respectively (Table 1). Length (cm) and weight (g) of fish were not significantly correlated with the volume of collected sperm (Table S1). Similarly, sperm volume and sperm density were not showed a significant correlation with the spermatozoa motility. On the other hand, the spermatozoa motility significantly and positively correlated with fertilizing ability (R2 = 0.26, P < 0.05) and osmolality of seminal plasma (R2 = 0.29, P < 0.05) (Fig. 2a, b), while osmolality negativity correlated with sperm motility duration (R2 = 0.28, P < 0.05). Table 1 Descriptive statistics of sampled fish, spermatozoa motility and seminal plasma characteristics in silver barb. N, number of individual used Parameters

N

Mean

SEM

Length (cm)

30

22.8

0.8

Weight (g)

30

160.1

19.1

Sperm volume (ml)

15

1.6

0.2

pH

15

8.8

0.1

Motility (%)

15

Sperm density (× 1010/ml)

15

2.8

0.2

Motility duration (sec)

15

391.9

8.5

K+ (mmol/l)

15

20.9

0.5

Na+ (mmol/l)

15

17.2

0.3

++

Mg

89

2

(mmol/l)

15

3.8

0.2

Ca++ (mmol/l)

15

0.72

0.04

Osmolality (mmol/kg)

15

400.6

Total protein (g/dl)

15

1.5

5.1 0.02

Fish Physiol Biochem

Fig. 2 The relationships between the spermatozoa motility and a osmolality, b fertilization rate of B. gonionotus

Fig. 3 The relationships between the spermatozoa motility and a K+, b Ca++ of B. gonionotus

Seminal plasma composition The ion content of seminal plasma Na+ and K+ was predominated in silver barb. The ranges of Mg++ and Ca++ were 2.5–5 and 0.5–1 mmol/l, respectively, and the total protein content ranged from 1.35 to 1.59 g/dl (Table 1). The K+ (R2 = 0.39, P < 0.01) and Ca++ (R2 = 0.27, P < 0.05) ions showed significant positive correlations with spermatozoa motility (Fig. 3a, b). No significant correlation was found between spermatozoa motility and other parameters of seminal plasma. Significant correlations were observed between K+ and Ca++ (R2 = 0.29, P < 0.05) and Mg++ and osmolality (R2 = 0.33, P < 0.05). The analysis also showed that K+ (R2 = 0.30, P < 0.05) and Ca++ (R2 = 0.26, P < 0.05) ion concentration of seminal plasma have significant positive influences on the fertilization rate (83.1 ± 7.2%) similar to the spermatozoa motility (Table S1).

Discussion This is the first report in determining the sperm quality of silver barb, although it has been considered as one of

the important aquaculture fish species. Firstly, we determined the growth condition of experimental fish and found that, the exponential value (b) in the lengthweight equation was 2.678, indicating negative allometric growth (length increase more than weight, b < 3), based on Bagenal and Tesch (1978) criteria of 3.0 and condition factor was > 1, which shows the wellbeing of fish (Wimberger 1992). Similarly, other studies have also been suggested that the value of “b” is usually almost 3 (Hossain and Sultana 2014); however, a variation in “b” value might be due to species variation, difference in environmental factors, sex variation, etc. (Joadder 2009; Hossain 2014). Based on the result obtained from growth studies, we have selected fish for evaluating the seminal composition and sperm quality parameters. It has been reported that motility of fish sperm is affected by osmolality of the external activating medium (Alavi and Cosson 2006) and activating solution (Morisawa and Suzuki 1980; Morisawa et al. 1983). Suspension of sperm in hypo-osmotic solution generates an osmotic gradient between the intracellular and extracellular medium to balance the osmolality on the both sides of the plasma

Fish Physiol Biochem

membrane through an influx of water and triggers motility. In this study, 80–98% sperm motility was observed through subjective method after activation with 0.3% NaCl concentrations and which was similar to other cyprinids (Billard et al. 1989, 1995; Linhart et al. 2003a; Alavi et al. 2010). However, motility duration was higher compared to other freshwater fish species (Alavi et al. 2010; Hassan et al. 2013). This might be due to in response to ATP content of sperm (Perchec et al. 1995). On the other hand, sperm motility also vary due to brood biological characters (i.e., age), rearing conditions, inducing agent, spawning season, post stripping factors, and ionic composition of seminal plasma (Hajirezaee et al. 2010, 2011). The present study showed that the sperm density of silver barb was close to Hypophthalmicthys molitrix (Rahman et al. 2011), however, higher compared with L. calbasu (Hassan et al. 2013) and salmonid fish (Hatef et al. 2007). Sperm density of silver barb did not significantly correlated with any measured parameters of spermatozoa, except only moderate positive relationship with sperm volume, fish weight, and fertilization rate. It can be assumed that with the growth of fish sperm concentration and semen volume increased, which in turn increased the chances of fertilization rate. These results coincide with the findings of Piros et al. (2002) and Vuthiphandchai and Zohar (1999). Sperm concentration might be also related to gonadal development and maturation, which depends on climate change (temperature), day food length food supply, and nutrition (Piros et al. 2002). In the present study, the significant positive correlation between fertilization capacity and sperm motility as found in silver barb is expected. The higher the sperm motility, the higher the possibility of fertilized egg. In agreement with our results, similar relationships were found in silver carp (Rahman et al. 2011; Hossain and Sarder 2009), grass carp (Sarder et al. 2010; Khara 2014), and Catla catla (Nandi et al. 2007). However, higher sperm concentration does not always provide higher motility and fertilization rate (Williot et al. 2000); therefore, it is not considered sensitive and specific method to measure fertilization capacity always (Rurangwa et al. 2004). The ionic composition of seminal plasma has a significant influence on sperm motility in fish. It is generally known that a higher K+ concentration inhibits sperm motility in salmonids (Morisawa and Suzuki 1980), but it increases sperm motility in carp (cyprinids) and clariids through changing osmotic

pressure between the seminal plasma and water (diluents) (Morisawa et al. 1983; Billard and Cosson 1992; Bozkurt et al. 2009a). In this study, the K+ concentration was lower than in common carp (70 mmol/l) (Morisawa et al. 1983); silver carp (46 mmol/l); bighead carp (48 mmol/l) (Rahman et al. 2011); and grass carp (45 mmol/l) (Khara 2014), but higher than perch (10 mmol/l) (Lahnsteiner et al. 1995) and Asian catfish (18 mmol/l) (Tan-Fermin et al. 1999). It is evident from this study that the percentage of motile sperm cells in silver barb semen has increased with the rise of K+ ion concentration. Morisawa et al. (1983) and Cosson et al. (1999) reported that higher K+ ions increase sperm velocity and motility in carp. This is due to potassium channels, which regulate hypo-osmotic shock through cell-signaling pathways for the mechanism of initiation of sperm motility in carp, perch, and salmonids (Krasznai et al. 2000). The observed Na+ content in seminal plasma of silver barb is lower than that of common carp (75 mmol/l) (Morisawa et al. 1983), grass carp (98 mmol/l) (Bozkurt et al. 2008), perch (124 mmol/l) (Lahnsteiner et al. 1995), and Asian catfish (18 mmol/l) (Tan-Fermin et al. 1999). Nevertheless, it is also noted that there is no significant phenomenon observed between Na+ and motility. Similar results also observed in Cyprinus carpio (Billard and Cosson 1992), grass carp (Bozkurt et al. 2008), and silver carp (Rahman et al. 2011), might be due to low sensitivity of cyprinid spermatozoa to Na+ (Alavi and Cosson 2006). Ca++ contribute significantly to the ionic composition of seminal plasma in fish milt (Alavi and Cosson 2006), while Mg++ role is not so significant (Cosson et al. 1999). Also, ultrastructural studies localized intracellular calcium stores in the different parts of the fish mature spermatozoa, including mid-piece and flagellum (Golpour et al. 2016, 2017). Preliminary results indicate that the intracellular Ca++ concentration increases when motility is initiated (Billard et al. 1989; Cosson et al. 1989; Boitano and Omoto 1991). In cyprinid sperm, cAMP (cyclic adenosine monophosphate) is not required, only elevated amount of a Ca2+ ion is necessary to reactivate demembranated sperm (Krasznai et al. 2000), and influx of extracellular Ca++ through specific channels leads to induction of Ca++ release from stores and initiates carp sperm motility through the calmodulin system (Krasznai et al. 2003). In this study, Ca++ ion concentration has a significant positive effect on spermatozoa motility like freshwater acclimated tilapia

Fish Physiol Biochem

spermatozoa, where Ca2+ ion plays a significant role in motility activation, although sperm can move without extracellular Ca2+ (Morita et al. 2003). The motility of Salmo trutta macrostigma spermatozoa was increasing when the Ca++ and Mg++ ion levels in seminal plasma were high (Bozkurt et al. 2011). However, in our study, Mg++ ion had no significant influence in sperm motility, only showed negative moderate correlation. Alavi et al. (2004) observed in Acipenser persicus, higher the Mg++ ion concentrations lower the sperm motility. Similarly in common carp, sperm motility decreases with the increase of Mg++ ion concentration due to inhibitory effect on spermatozoa (Bozkurt et al. 2009b). In addition to, seminal plasma osmotic pressure is also one of the important indicators of semen quality. Kruger et al. (1984) and Lahnsteiner et al. (1996) found statistically significant relationship between sperm motility and osmolality in C. carpio and A. alburnus, respectively. Lahnsteiner et al. (1996) also claimed that lower the osmolality, weaker the motility. All these mentioned findings coincide with our current study. It is also reported that plasma ions are significantly responsible for the osmolality of seminal plasma and viability of spermatozoa in sperm ducts (Kruger et al. 1984), and the control of the initiation of carp sperm motility in external hypotonic medium (Krasznai et al. 2000). However, there were no significant relationships observed between osmolality and ions, which significantly influence silver barb sperm motility in that study. Generally, in external medium or diluents cyprinids sperm motility initiated through efflux of K + and changes in external osmolality (Alavi and Cosson 2006). Therefore, we can speculate that silver sperm motility is regulated by ions more than osmolality similar to salmonids and other teleosts (Morisawa et al. 1983). Analysis of organic component of seminal plasma is an important criterion for evaluation of sperm quality (Billard et al. 1995). High level of protein might have a protective role in sperm motility, and it contains a number of key enzymes for the metabolic process (Kowalski et al. 2003). The total protein concentration of present study showed non-significant negative correlation with sperm motility. Lahnsteiner et al. (2004) affirmed that seminal plasma proteins prolong the viability of rainbow trout sperm, as measured by sperm motility. Seminal plasma of Persian sturgeon similar to other sturgeons is characterized by much lower protein concentration (Piros et al. 2002). Ciereszko (2008) also confirmed that

protein concentrations in the seminal plasma of most fish are much lower than in the other vertebrates. However, the specific role of protein in silver barb semen is unknown and warranted future study. On the other hand, spermatozoa motility and semen pH of silver barb did not showed any significant relationship like common carp (Emri et al. 1998) and grass carp (Bozkurt et al. 2008) though pH of seminal plasma indicates alkaline condition, which is best environment for fish sperm viability. This could be results of complex chemistry among the seminal plasma components. Therefore, Alavi and Cosson (2005) and Redondo-Müller et al. (1991) postulated that “Sperm motility is not pH dependent.” In sum, we can conclude that sperm motility of silver barb are significantly depends on the seminal plasma ions (K+, Ca++) and osmolality. As results of higher motility of silver barb spermatozoa contributes significantly in the achievement of higher fertilization rate, however, osmolality also largely relies on the ions of seminal fluid. Therefore, the results of the present study indicate that the ionic composition of seminal plasma is an important factor determining sperm quality in silver barb. Such information can contribute extensively to the improvement of management in reproduction under captive conditions, especially the efficacy of fertilization procedures and semen storage, including cryopreservation. Nevertheless, suitable activation solution of sperm motility of these species should be studied further. In addition to, determination of suitable biomarkers of spermatozoa quality evaluation would be an important aspect for future researches. Ultimately, it facilitates the design of specific probes for the genes responsible for sperm quality, fertilization success, and early indicators of embryonic development. Acknowledgements Authors would like to thank to Prof. Dr. GKM Mustafizur Rahman for his kind help during sample analysis and to Dr. Hamid Niksirat for his valuable guidelines during manuscript preparation.

Funding information This study is supported by the Research Management Committee (RMC) of Bangabandhu Sheikh Mujibur Rahaman Agricultural University (Grant No. UGC/RMC-55, Section-8) and the Ministry of Education, Youth and Sports of the Czech Republic—projects “CENAKVA” (No. CZ.1.05/2.1.00/ 01.0024), “CENAKVA II” (No. LO1205 under the NPU I program), and by the Grant Agency of University of South Bohemia (No. 017/2016/Z).

Fish Physiol Biochem

References Alavi SMH (2007) Fish spermatology: implications for aquaculture management. In: Alavi SMH, Cosson J, Coward K, Rafie G (eds) Fish spermatology. Alpha Science Ltd, Oxford, pp 397–460 Alavi SMH, Cosson J (2005) Sperm motility in fishes. I. Effects of temperature and pH: a review. Cell Biol Int 29:101–110 Alavi SMH, Cosson J (2006) Sperm motility in fishes.(II) effects of ions and osmolality: a review. Cell Biol Int 30:1–14 Alavi SMH, Cosson J, Karami M, Amiri BM, Akhoundzadeh MA (2004) Spermatozoa motility in the Persian sturgeon, Acipenser persicus: effects of pH, dilution rate, ions and osmolality. Reproduction 128:819–828 Alavi SMH, Jorfi E, Hatef A, Mortezavi SAS (2010) Sperm motility and seminal plasma characteristics in Barbus sharpeyi (Gunther, 1874). Aquac Res 41:e688–e694. https://doi.org/10.1111/j.1365-2109.2010.02600.x Bagenal TB, Tesch FW (1978) Age and growth. In: Bagenal TB (ed) Methods for assessment of fish production in fresh waters-3. Blackwell Scientific Publication, Oxford, pp 101– 136 Bhuiyan AS, Islam MK, Zaman T (2006) Induced spawning of Puntius gonionotus (Bleeker). J Biosci 14:121–125 Billard R, Cosson MP (1992) Some problems related to the assessment of sperm motility in freshwater fish. J Exp Zool 261:122–131 Billard R, Bieniarz K, Popek W, Epler P, Saad A (1989) Observations on a possible pheromonal stimulation of milt production in carp (Cyprinus carpio L.). Aquaculture 77: 387–392 Billard R, Cosson J, Perchec G, Linhart O (1995) Biology of sperm and artificial reproduction in carp. Aquaculture 129: 95–112 Bogard JR, Thilsted SH, Marks GC, Wahab MA, Hossain MAR, Jakobsen J, Stangoulis J (2015) Nutrient composition of important fish species in Bangladesh and potential contribution to recommended nutrient intakes. J Food Compos Anal 42:120–133 Boitano S, Omoto CK (1991) Membrane hyperpolarization activates trout sperm without an increase in intracellular pH. J Cell Sci 98:343–349 Bozkurt Y, Öğretmen F, Erçin U, Yιldιz Ü (2008) Seminal plasma composition and its relationship with physical spermatological parameters of Grass carp (Ctenopharyngodon idella) semen: with emphasis on sperm motility. Aquac Res 39:1666–1672 Bozkurt Y, Ogretmen F, Secer FS, Ercin U (2009a) Effects of seminal plasma composition on sperm motility in mirror carp (Cyprinus carpio). Isr J Aquacult Bamidgeh 61:307–314 Bozkurt Y, Ogretmen F, Secer FS, Ercin U (2009b) Relationship between seminal plasma composition and spermatological parameters in scaly carp (Cyprinus carpio). J Anim Vet Adv 8:2745–2749 Bozkurt Y, Öğretmen F, Kökçü Ö, Ercin U (2011) Relationships between seminal plasma composition and sperm quality parameters of the Salmo trutta macrostigma (Dumeril, 1858) semen: with emphasis on sperm motility. Czech J Anim Sci 56:355–364 Chew PC, Zulkafli AR (2012) Sperm cryopreservation of some freshwater fish species in Malaysia. In: Igor I, Katkov (eds)

Current Frontiers in cryopreservation. InTech. https://doi. org/10.5772/32243 Ciereszko A (2008) Chemical composition of seminal plasma and its physiological relationship with sperm motility, fertilizing capacity and cryopreservation success in fish. In: Alavi SMH, Cosson J, Coward R, Rafiee G (eds) Fish spermatology. Alpha Science, Oxford, pp 215–240 Ciereszko A, Dabrowski K, Toth GP, Christ SA, Glogowski J (2002) Factors affecting motility characteristics and fertilizing ability of sea lamprey spermatozoa. Trans Am Fish Soc 131:193–202 Cosson MP, Billard R, Letellier L (1989) Rise of internal Ca2+ accompanies the initiation of trout sperm motility. Cytoskeleton 14:424–434 Cosson J, Billard R, Cibert C, Dreanno C, Suquet M (1999) Ionic factors regulating the motility of fish sperm. In: Gagnon C (ed) The male gamete: from basic to clinical applications. Cache Rive Press, Vienna, pp 161–186 Dreanno C, Suquet M, Desbruyères E, Cosson J, Le Delliou H, Billard R (1998) Effect of urine on semen quality in turbot (Psetta maxima). Aquaculture 169:247–262 Emri M, Marian T, Tron L, Balkay L, Krasznai Z (1998) Temperature adaptation changes ion concentrations in spermatozoa and seminal plasma of common carp without affecting sperm motility. Aquaculture 167:85–94 FAO (2016) Species Fact Sheets: Puntius gonionotus (Bleeker, 1850). . Fisheries and Aquaculture Department. http://www. fao.org/fishery/species/2175/en Golpour A, Pšenička M, Niksirat H (2016) Ultrastructural localization of intracellular calcium during spermatogenesis of sterlet (Acipenser ruthenus). Microsc Microanal 22:1155– 1161 Golpour A, Pšenička M, Niksirat H (2017) Subcellular distribution of calcium during spermatogenesis of zebrafish, Danio rerio. J Morphol 278:1149–1159 Hajirezaee S, Amiri BM, Mirvaghefi A, Sheikh Ahmadi A (2010) Evaluation of semen quality of endangered Caspian brown trout (Salmo trutta caspius) in different times of spermiation during a spawning season. Czech J Anim Sci 55:445–455 Hajirezaee S, Mojazi Amiri B, Mehrpoosh M, Nazeri S, Niksirat H (2011) Gonadotropin releasing hormone-analogue (GnRHa) treatment improves the milt production and sperm motility of endangered Caspian brown trout, Salmo trutta caspius, over the course of a spawning season. Aquac Res 42:1789–1795 Hassan MM, Nahiduzzaman M, Al Mamun SN, Taher MA, Hossain MAR (2013) Fertilization by refrigerator stored sperm of the Indian major carp, Labeo calbasu (Hamilton, 1822). Aquac Res 45:150–158 Hatef A, Niksirat H, Amiri BM, Alavi SMH, Karami M (2007) Sperm density, seminal plasma composition and their physiological relationship in the endangered Caspian brown trout (Salmo trutta caspius). Aquac Res 38:1175–1181 Hatef A, Niksirat H, Alavi SMH (2009) Composition of ovarian fluid in endangered Caspian brown trout, Salmo trutta caspius, and its effects on spermatozoa motility and fertilizing ability compared to freshwater and a saline medium. Fish Physiol Biochem 35:695–700 Hossain MS (2014) Reproductive characteristics of Bele, Glossogobius giuris from Mithamoin Haor, Kissorgonj, Bangladesh. World J Fish Mar Sci 6:537–543

Fish Physiol Biochem Hossain MS, Sarder MRI (2009) Cryogenic freezing of silver carp spermatozoa for conservation of gene pool. Progress Agric 20:99–106 Hossain MS, Sultana N (2014) Morphometric characters and length-weight relationship of Bele,(Glossogobius giuris) from Mithamoin haor, Kissorgonj, Bangladesh. J Bangladesh Agricult Uni 12:389–395 Hossen B, Hossain MS, Rashid I, Hasan MN, Ethin R, Thapa H, Majumdar BC (2017) Effect of extenders and storage periods on motility and fertilization rate of Silver Barb, Barbonymus gonionotus (Bleeker, 1850) semen. Int J Agric Policy Res 5: 178–185 Hussain MG, Obaidullah M, Rahman MM, Akhteruzzaman M, Perschbacher P (1987) Hormone induced ovulation and spawning of Puntius gonionotus (Bleeker). Bangladesh J Fish 10:1–4 Jiwyam W (2014) Growth and feeding behaviour of Barbonymus gonionotus (Bleeker, 1850) and Hypsibarbus wetmorei (Smith, 1931) in added-substrate and no-added-substrate cages. Kasetsart Uni Fish Res Bull 38:28–37 Joadder AR (2009) Length Weight relationship and Condition Factor (Kn) of Gobi, Glossogobius giuris (Hamilton), from “Atrai River” in The Northern Part of Bangladesh. J Fish Int 4:1–4 Khara H (2014) Sperm characteristics in Grass carp, Ctenopharyngodon idella; effect of ions on spermatozoa motility and fertilization capacity. Iran J Fish Sci 13:354–364 Khara H, Shahrooz BN, Hadiseh D, Rahbar M, Ahmadnejad M, Khodadoost A (2012) The effect of cations on sperm motility performance and fertilizing ability of silver carp Hypophthalmichthys molitrix. Acta Vet 62:599–609 Kowalski R, Wojtczak M, Glogowski J, Ciereszko A (2003) Gelatinolytic and anti-trypsin activities in seminal plasma of common carp: relationship to blood, skin mucus and spermatozoa. Aquat Living Resour 16:438–444 Krasznai Z, Márián T, Izumi H, Damjanovich S, Balkay L, Trón L, Morisawa M (2000) Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp. Proc Natl Acad Sci 97:2052–2057 Krasznai Z, Morisawa M, Morisawa S, Krasznai ZT, Trón L, Gáspár R, Márián T (2003) Role of ion channels and membrane potential in the initiation of carp sperm motility. Aquat Living Resour 16:445–449 Kruger JDW, Smit G, Vuren J, Ferreira J (1984) Some chemical and physical characteristics of the semen of Cyprinus carpio L. and Oreochromis mossambicus (Peters). J Fish Biol 24:263–272 Lahnsteiner F, Berger B, Weismann T, Patzner R (1995) Fine structure and motility of spermatozoa and composition of the seminal plasma in the perch. J Fish Biol 47:492–508 Lahnsteiner F, Berger B, Weismann T, Patzner R (1996) Motility of spermatozoa of Alburnus alburnus (Cyprinidae) and its relationship to seminal plasma composition and sperm metabolism. Fish Physiol Biochem 15:167–179 Lahnsteiner F, Mansour N, Berger B (2004) Seminal plasma proteins prolong the viability of rainbow trout (Oncorynchus mykiss) spermatozoa. Theriogenology 62: 801–808 Layne E (1957) Spectrophotometric and turbidimetric methods for measuring protein. Methods Enzymol 3:447–454

Le Cren E (1951) The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 20:201–219 Liley NR, Tan ESP (1985) The induction of spawning behaviour in Puntius gonionotus (Bleeker) by treatment with prostaglandin PGF2α. J Fish Biol 26:491–502 Linhart O et al (2000) Spermiation of paddlefish (Polyodon spathula, Acipenseriformes) stimulated with injection of LHRH analogue and carp pituitary powder. Aquat Living Resour 13:455–460 Linhart O, Cosson J, Mims S, Rodina M, Gela D, Shelton W (2003a) Effects of ions on the motility of fresh and demembranate spermatozoa of common carp (Cyprinus carpio) and paddlefish (Polyodon spathula). Fish Physiol Biochem 28:203–205 Linhart O, Mims SD, Gomelsky B, Hiott AE, Shelton WL, Cosson J, Rodina M, Gela D, Bastl J (2003b) Ionic composition and osmolality of paddlefish (Polyodon spathula, Acipenseriformes) seminal fluid. Aquac Int 11:357–368 Linhart O, Rodina M, Bastl J, Cosson J (2003c) Urinary bladder, ionic composition of seminal fluid and urine with characterization of sperm motility in tench (Tinca tinca L.). J Appl Ichthyol 19:177–181 Mondol MR, Dewan S, Hossain M, Asaduzzaman M, Islam MA, Rozario UA (2005) Food and feeding habits of Puntius gonionotus (Thai Sarpunti) in rice field. Pak J Biol Sci 8: 386–395 Morisawa S, Morisawa M (1986) Acquisition of potential for sperm motility in rainbow trout and chum salmon. J Exp Biol 126:89–96 Morisawa M, Suzuki K (1980) Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science 210:1145–1147 Morisawa M, Suzuki K, Shimizu H, Morisawa S, Yasuda K (1983) Effects of osmolality and potassium on motility of spermatozoa from freshwater cyprinid fishes. J Exp Biol 107:95–103 Morita M, Takemura A, Okuno M (2003) Requirement of Ca2+ on activation of sperm motility in euryhaline tilapia Oreochromis mossambicus. J Exp Biol 206:913–921 Nandi S, Routray P, Gupta SD, Rath SC, Dasgupta S, Meher PK, Mukhopadhyay PK (2007) Reproductive performance of carp, Catla catla (Ham.), reared on a formulated diet with PUFA supplementation. J Appl Ichthyol 23:684–691 Perchec G, Jeulin C, Cosson J, Andre F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108:747–753 Piironen J (1985) Variation in the properties of milt from the Finnish landlocked salmon (Salmo salar m. sebago Girard) during a spawning season. Aquaculture 48:337–350 Piros B, Glogowski J, Kolman R, Rzemieniecki A, Domagala J, Horváth Á, Urbanyi B, Ciereszko A (2002) Biochemical characterization of Siberian sturgeon Acipenser baeri and sterlet Acipenser ruthenus milt plasma and spermatozoa. Fish Physiol Biochem 26:289–295 Rahman MM, Rahman MS, Hasan M (2011) Changes in sperm quality of silver (Hypophthalmichthys molitrix) and bighead carps (Hypophthalmichthys nobilis) during the spawning season. Asian Fisher Sci 24:413–425 Rahman MM, Ali MR, Sarder MRI, Mollah MFA, Khan NS (2016) Development of sperm cryopreservation protocol

Fish Physiol Biochem of endangered spiny eel, Mastacembelus armatus (Lacepede 1800) for ex-situ conservation. Cryobiology 73:316–323 Redondo-Müller C, Cosson MP, Cosson J, Billard R (1991) In vitro maturation of the potential for movement of carp spermatozoa. Mol Reprod Dev 29:259–270 Ricker WE (1975) Computation and interpretation of biological statistics of fish populations, vol 191. Department of the Environment Fisheries and Marine Service, Ottawa Riedel R, Caskey LM, Hurlbert SH (2007) Length-weight relations and growth rates of dominant fishes of the Salton Sea: implications for predation by fish-eating birds. Lake Reserv Manag 23:528–535 Rurangwa E, Kime DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28. https://doi.org/10.1016 /j.aquaculture.2003.12.006 Sarder MRI, Rahman F, Hossain MS, Samad MS (2009) Cryogenic freezing of silver barb (Barbonymus gonionotus) spermatozoa for gene pool conservation. Progress Agric 20: 117–124

Sarder MRI, Hossain MA, Hossain MS (2010) Cryofreezing of grass carp (Ctenopharyngodon idella) spermatozoa for ex situ conservation. Progress Agric 21:141–150 Sarvi K, Niksirat H, Amiri BM, Mirtorabi SM, Rafiee GR, Bakhtiyari M (2006) Cryopreservation of semen from the endangered Caspian brown trout (Salmo trutta caspius). Aquaculture 256:564–569 Tan-Fermin JD, Miura T, Adachi S, Yamauchi K (1999) Seminal plasma composition, sperm motility, and milt dilution in the Asian catfish Clarias macrocephalus (Gunther). Aquaculture 171:323–338 Vuthiphandchai V, Zohar Y (1999) Age-related sperm quality of captive striped bass Morone saxatilis. J World Aquac Soc 30: 65–72 Williot P, Kopeika EF, Goncharov BF (2000) Influence of testis state, temperature and delay in semen collection on spermatozoa motility in the cultured Siberian sturgeon (Acipenser baeri Brandt). Aquaculture 189:53–61. https://doi. org/10.1016/s0044-8486(00)00358-6 Wimberger PH (1992) Plasticity of fish body shape. The effects of diet, development, family and age in two species of Geophagus (Pisces: Cichlidae). Biol J Linn Soc 45:197–218