Relationship between seminal plasma composition and sperm quality parameters of the catfish Pseudoplatystoma reticulatum

Malbelys Padilla Sanchez1,2 , Laís Pedroso Borges1,2, Stella Indira Rocha Lobato1,2, Laicia Carneiro-Leite1,2, Rodrigo Yutaka Dichoff Kasai3, Cristiéle da Silva Ribeiro4, Rosicleire Veríssimo-Silveira1,2 and Alexandre Ninhaus-Silveira1,2

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Abstract​


EN

Sperm quality is a fundamental parameter for the effective reproduction of fish in captivity and the development of reproductive techniques, such as semen cryopreservation. This study aimed to determine the composition of the seminal plasma of Pseudoplatystoma reticulatum and analyze the relationships between plasma components and sperm characteristics. Nine males were induced to spermiation with carp pituitary extract in the reproductive period of the species (November and December/2019). Semen characteristics were evaluated: subjective sperm motility, motility, duration, released sperm volume, sperm concentration, pH, osmolality, and seminal plasma composition, including levels of calcium, chloride, sodium, magnesium, potassium, glucose, fructosamine, triglycerides, and total protein. To determine the relationship between seminal plasma components and sperm motility parameters, a principal component analysis (PCA) was performed. The seminal plasma of P. reticulatum is composed mainly of the Na+ ion and organic components such as protein and glucose. Through PCA, it was observed that sperm motility had a strong positive correlation with motility time, sperm concentration, and total protein and a negative correlation with osmolality and fructosamine.

Keywords: Ionic composition, Fish reproduction, PCA, Siluriformes, Sperm characteristics.

PT

A qualidade espermática é parâmetro fundamental para a reprodução eficaz de peixes em cativeiro e para o desenvolvimento de técnicas reprodutivas, como a criopreservação de sêmen. Este estudo teve como objetivo determinar a composição do plasma seminal de Pseudoplatystoma reticulatum e analisar as relações entre os componentes do plasma seminal e as características espermáticas. Nove machos foram induzidos à espermiação com extrato de hipófise de carpa no período reprodutivo da espécie (novembro e dezembro/2019). As características do sêmen foram avaliadas: motilidade espermática subjetiva, motilidade, duração, volume espermático liberado, concentração espermática, pH, osmolalidade e composição do plasma seminal, incluindo níveis de cálcio, cloreto, sódio, magnésio, potássio, glicose, frutosamina, triglicerídeos e proteína total. Para determinar a relação entre os componentes do plasma seminal e os parâmetros de motilidade espermática, foi realizada uma análise de componentes principais (PCA). O plasma seminal de P. reticulatum é composto principalmente pelo íon Na+ e componentes orgânicos como proteínas e glicose. Através da PCA, observou-se que a motilidade espermática apresentou forte correlação positiva com tempo de motilidade, concentração espermática e proteína total e correlação negativa com osmolalidade e frutosamina.

Palavras-chave: Composição iônica, Característica espermática, PCA, Reprodução de peixes, Siluriformes.

Introduction​


Brazil is the country with the greatest powers in the world for the development of fish farming due to its climate and diversity of species. The growth in recent years in the aquaculture sector has contributed to the decrease in fish catches in the natural environment (FAO, 2020). With the increase in the production of fish in captivity, it becomes necessary to develop effective protocols that optimize artificial reproduction. In this sense, it is fundamental to obtain biological and technical knowledge that allows the evaluation of the reproductive parameters of the fish, allowing the development of biotechnology that will make it possible to optimize the reproduction in captivity of these species, such as protocols for manipulation and storage of gametes.

The use of high-quality gametes from both males and females is an essential prerequisite to achieving high fertilization success and hatching, both for aquaculture and scientific purposes (Bozkurt et al., 2008; Yoshida, Asturiano, 2020). In the evaluation of fish semen quality, one of the most important criteria used in the literature is sperm motility, generally expressed as the percentage and duration of sperm motility after activation. (Lahnsteiner et al., 1996; Gallego, Asturiano, 2018).

Seminal plasma has a unique species-specific composition, containing substances that support sperm cells (Ciereszko et al., 2011). In addition, it plays an important physiological role in sperm maturation, having a biochemical composition that supports and protects the viability, motility, and fertilizing capacity of sperm, creating an ideal environment for their storage (Ciereszko, 2008; Bozkurt et al., 2011).

In fish, unlike other vertebrates, seminal plasma is composed mainly of mineral compounds (Na+, K+, Mg2+ and Ca+), being characterized by low concentrations of proteins, as well as other organic substances, such as hormones and pheromones, cholesterol, glycerol, vitamins, free amino acids, sugars, citric acid and lipids (Linhart et al., 1991; Ciereszko et al., 2000; Cosson, 2004). The determination of seminal plasma composition has a great influence on the biological quality of the semen. It can help to understand the design requirements to prepare the appropriate artificial seminal plasma solutions (Ciereszko, 2008).

Knowledge of the relationships between seminal characteristics and the chemical composition of sperm is a prerequisite for successfully assessing the reproductive capacity of different fish species (Ciereszko et al., 2011; Hussain et al., 2018). Also, these would provide knowledge for the preparation of artificial plasma solutions, which can be used for the dilution of semen for short-term storage or cryopreservation (Billard, Cosson, 1992).

In the last years, the interest of researchers in studies on seminal plasma in fish has been growing, especially in publications that somehow cover correlations between seminal plasma components and sperm motility. However, descriptions of plasma components and possible relationships between sperm motility parameters in species of neotropical fishes need further investigation. And, referring to fish species belonging to the Siluriformes order, some works related to this theme can be highlighted in species such as Clarias gariepinus (Burchell, 1822) (Steyn, van Vuren, 1986), Clarias macrocephalus Günther, 1864 (Tan-Fermin et al., 1999) and Rhamdia quelen (Quoy & Gaimard, 1824) (Borges et al., 2005), however, they are still very few.

The catfish species Pseudoplatystoma reticulatum Eigenmann & Eigenmann, 1889, popularly known as “Surubim cachara” (Silva et al., 2015) is among the species of Brazilian ichthyofauna that stand out with potential for fish farming. In the literature, no previous published works are describing the composition of seminal plasma and its relationship with sperm physical parameters. As it is a species that has high commercial value as it has characteristics that meet the fish consumer market (Kubitza, 1998). Its natural populations can be affected over time as a result of indiscriminate capture, as well as the destruction of their natural habitats.

Thus, it is essential to have in-depth knowledge of the seminal characteristics of the species, thus generating basic knowledge for future cryopreservation studies that could help to maintain the genetic viability of their populations. Given the above, the present study aimed to characterize the composition of seminal plasma and determine the relationships between its components and the characteristics of the semen of P. reticulatum in captivity.

Material and methods


Fish handling. Nine adult males of P. reticulatum (Fig. 1.) from the breeding stock of the company Piraí Fish-farming, located in Terenos, Mato Grosso do Sul, Brazil (20°25’05”S 55°17’11”W) were used for the development of the present work. The experiments were carried out between the late spring and early summer (November and December) of 2019, corresponding to the peak of the species’ reproductive season.

No vouchers of the target species were deposited in a scientific collection, since they were all adults belonging to the breeding stock, and there were no juveniles at the station that could be sent as vouchers. At the end of this experiment, the specimens were released into their natural environment, the Miranda River, in the upper Paraguai River basin.

FIGURE 1| Adult male specimen of Pseudoplatystoma reticulatum, belonging to the Piraí fish farming, Terenos, Mato Grosso do Sul, Brazil.

Sperm collection and analysis of seminal characteristics. After capturing the specimens of P. reticulatum in the excavated ponds, they were placed in a concrete tank for hormonal induction and semen collection. Adult breeders have an average body mass of 2.5 kg and were identified with microchips. The animals were hormonally induced by applying a single dose of carp pituitary extract at 3 mg/kg of fish. The semen was collected after 232 hours/degree (t = 8 h; T = 29 ºC) by gentle abdominal pressing and stored in graduated sterilized falcon tubes and kept in a styrofoam box at approximately 4 degrees until analysis. The semen obtained from each specimen, color, and seminal volume (Sem. Vol.) was determined, considering the maximum volume obtained via abdominal massage until the beginning of the presence of blood, avoiding contamination with urine, feces, and blood. Subjective sperm motility (Mot) was determined under light microscopy based on the scale proposed by Fribourgh (1966). Sperm was activated with 0.45% NaCl in a proportion of 1:10 (semen: activator). Motility duration (Mot.tm) was measured from sperm activation to observation of only 10% of motile sperm. The pH of fresh semen was measured using a pHmeter (Checker®). For osmolality (Osm), the semen was centrifuged at 3000 rpm for 15 min, the supernatant was removed and analyzed in a cryo-osmometer (OSMOMAT® model 030, Berlin, Germany). To determine the sperm concentration (Conc), the semen was diluted in formalin-saline solution at a proportion of 1:1000 (semen: solution), and the count was performed in a Neubauer hemocytometer chamber, the results were obtained according (Kavamoto et al., 1985).

Analysis of seminal plasma components. To obtain seminal plasma, the semen was centrifuged at 3000 g for 15 min. After centrifugation, the supernatant was transferred to sterile polyethylene tubes, properly identified, and stored in an ultra-freezer at -80 °C until biochemical analysis. Aliquots were thawed at room temperature (~25 ºC) for biochemical measurements of seminal plasma. The concentrations of calcium (Ca+), chlorides (Cl), sodium (Na+), magnesium (Mg2+), potassium (K+), glucose (Glic), fructosamine (Frut), triglycerides (Trig), and total proteins (Tot. pro). The tests were performed using commercial kits (LABTEST® Diagnostica S.A.), following the instructions for each analysis (Leite et al., 2018). All analyzes were determined using a SpectraMax Plus 384 spectrophotometer.

Statistical analysis. Data on sperm characteristics and respective components of seminal plasma were presented through a descriptive analysis expressed as mean ± SEM (Standard Error of the Mean). To determine the relationships between seminal plasma components and sperm characteristics of the species, a Principal Component Analysis (PCA) was performed to reduce the redundancy of the observed variables and identify patterns in the dataset. First, the data were standardized, allowing variables measured on different measurement units to be compared. The first two eigenvectors with the highest percentage of accumulated variance were considered to construct the PCA graph. For this analysis, six copies of the total analyzed were used. All analyzes were performed using the R Software, “FactoMineR” (R Development Core Team, 2020).

Results​


Sperm characteristics of Pseudoplatystoma reticulatum. Spermatological parameters of the sperm of P. reticulatum were found rather variable and they are shown in Tab. 1. The parameters of osmolality, motility, and motility time were where the greatest variability was found, with pH and concentration being the least variable.

TABLE 1 | Sperm characteristics of Pseudoplatystoma reticulatum (n = 9). Minimum, maximum, and mean values. SEM = Standard error of the mean.


Variable

Minimum

Maximum

Mean

SEM

Seminal volume (mL)

2.90

12.00

7.80

1.04

Sperm motility (%)

70.00

95.00

86.25

3.09

Time motility (s)

75.00

112.00

89.25

3.92

Concentration (spz.109/mL)

12.70

18.10

15.71

0.72

pH

7.33

8.00

7.75

0.08

Osmolality (mOsm/kg)

173.66

276.00

211.62

11.01


Seminal plasma composition of Pseudoplatystoma reticulatum. The results of the analysis of the seminal plasma are shown in Tab. 2. The seminal plasma of P. reticulatum is mainly composed of the Na+ ion, followed by the Cl, Ca+ and K+ ions, while the Mg2+ ion showed the lowest values. Within the organic components, total protein and glucose stood out; on the other hand, fructosamine and triglycerides had low values.

TABLE 2 | Seminal plasma components of Pseudoplatystoma reticulatum (n = 6). Minimum, maximum,
and mean values. Standard error of the mean (SEM), Calcium (Ca+), Chlorides (Cl), Sodium (Na+), Magnesium (Mg2+), Potassium (K+), Glucose (Glic), Fructosamine (Frut), Triglycerides (Trig), and Total proteins (Tot. Pro).


Variable

Min

Max

Mean

SEM

Ca+ (mg/dL)

7.94

26.42

12.67

2.15

Cl(mM/L)

2.83

4.95

4.24

0.25

Na+ (mM/L)

108.78

140.97

124.87

3.81

Mg²+ (mEq/L)

0.36

2.14

1.15

0.24

K+ (mM/L)

0.01

6.09

3.15

0.75

Glic (mg/dL)

124.11

365.24

205.67

39.63

Frut (µmol/L)

23.93

131.63

64.75

15.67

Trig (mg/dL)

1.86

11.60

4.97

1.24

Tot. Pro (g/dL)

0.00

0.85

0.39

0.12


Correlation between seminal plasma components and seminal characteristics of Pseudoplatystoma reticulatum. In the principal component analysis (PCA) to determine the possible relationships between the seminal plasma components and the sperm characteristics of this species, the first two components were chosen: the first component (PC1) explained 47.1% of the data variance and the second component (PC2) explained 21.42%, totaling 68.52% of the total variation of the data (Fig. 2).

FIGURE 2| Representation of the first two axes obtained by PCA analyzing the relationships between the components of the seminal plasma and the sperm characteristics of Pseudoplatystoma reticulatum (n = 6). Motilidade total (Mot), Tempo de motilidade (Mot. tm), Concentração (Conc) Calcium (Ca+), Chlorides (Cl), Sodium (Na+), Magnesium (Mg2+), Potassium (K+), Glucose (Glic), Fructosamine (Frut), Triglycerides (Trig) and Total proteins (Tot.pro).

The first two axes are obtained through the PCA and represented in Fig. 2, which can be observed in the colors from light blue to orange that indicate the percentage of contribution in the explained variance, with light blue for the lowest value and orange for the highest percentage. The graph shows a cluster between variables such as Mot, Mot.tm, and Conc, indicating a strong positive correlation between them and Sem.vol and Tot.pro. On the other hand, Frut and Osm had a high positive correlation, but a negative relationship with Mot, Mot.tm, Conc, Tot.pt, and pH. The Cl, Ca+, Trig, Sem.Vol, and Tot.pro variables had a strong positive correlation with pH, while this variable had a strong negative correlation with K+, which in turn had a positive correlation with Osm and Frut. The variables Glic, Na+ and Mg2+ contributed little to the variance of the analyzed data, but the Na+ and Mg2+ had a strong negative correlation between them.

Discussion​


Seminal plasma is an important component of fish semen, playing a vital role in sperm metabolism, function, survival, and motility (Mojica-Rodríguez, Cruz-Casallas, 2005; Navarro et al., 2019). Numerous components of seminal plasma are directly linked to these functions. This study to determine the main plasmatic components of P. reticulatum semen and its relationship with parameters of seminal quality is unprecedented and will serve as a basis for studies of the reproductive aspects of other fish species, in addition to providing important information for the development of extenders, extender immobilizers, and cryoprotective solutions.

The data obtained in the evaluation of the characteristics of the physical parameters of the species were variable among the individuals. Variations in seminal characteristics are related to physiological variations of the specimens, linked to their genetics and how they react to the “environmental conditions” to which they are subjected. Semen quality, particularly in aquaculture species, depends on several external factors, such as feeding regime, feed quality, temperature, and male reproductive season (Bozkurt et al., 2008).

The seminal plasma in fish, in contrast to that of other vertebrates, is characterized by low concentrations of proteins and other organic substances, containing mainly mineral compounds such as Na+, K+, Ca+, and Mg2+ (Ciereszko, 2008). In the present study, the seminal plasma was composed of Na+ ions like that reported for Clarias macrocephalus (Tan-Fermin et al., 1999).

Usually in seminal plasma sodium concentrations are 10 times higher than potassium concentrations (Tan-Fermin et al., 1999). In membrane permeability processes, ions play a fundamental role, according to the variation of their concentrations in the extra-and intracellular medium, some theses involucred inhibitory effects on the initiation of sperm motility. The increase in Na+ may be related to the high secretory activity in the sperm ducts (Lahnsteiner et al., 1993), for P. reticulatum it seems to be one of the fundamental ions in the maintenance of seminal plasma function. For other species of the order Siluriformes, similar concentrations to those obtained in this work were observed, i.e., Clarias gariepinus 125.25±9.80 (Steyn, van Vuren, 1986); Clarias macrocephalus Günther, 1864 164.4±0.6 (Tan-Fermin et al., 1999), Rhamdia quelen 153.7±2.4 (Borges et al., 2005), but the deference may be due to differences in feeding conditions, age, environ-mental factors within the same species due to their reproductive processes. The Na+ ion can act directly on the osmotic balance, motility, morphology, and metabolism of sperm (Rodríguez et al., 2013).

Potassium (K+) presented low concentration values in the present study, compared to other freshwater species, such as Hypophthalmichthys molitrix (Valenciennes, 1844), Clarias macrocephalus (Tan-Fermin et al., 1999; Rahman et al., 2011). It has been reported that low concentrations of K+ in seminal plasma may be associated with a high percentage of motility and better seminal quality in salmonids (Billard, Cosson, 1992). It has also been documented that in several species of the order Siluriformes, K+ levels are generally low, but this variability is species-specific and not always low rates of this ion are related to low sperm quality since depending on the concentrations of the other ions which can also influence the motility mechanisms (Dziewulska, 2020).

Ca+ and Mg2+ ions contribute significantly to the composition of fish sperm seminal plasma. These cations are effective as antagonists of the inhibitory effect of K+ on the motility of the Na+ ion (Billard, Cosson, 1992). In this study, the values of Ca+ and Mg2+ were similar to those compared with other Siluriformes species (Tan-Fermin et al., 1999; Borges et al., 2005).

The concentration of glucose in the seminal plasma has a primordial function for the protection of spermatozoa, providing high energy during the process of spermiogenesis, as well as in sperm motility. Different sperm glucose concentrations may indicate differences in sperm metabolic energy from numerous fish species (Hussain et al., 2018). In the present study, glucose showed a high concentration in seminal plasma, which coincides with what was detected for other fish species (Lahnsteiner et al., 1995), which may suggest that P. reticulatum spermatozoa also have a need for higher amounts of energy for its functions, compared to a species of the same genus, Pseudoplatystoma metaense Buitrago-Suárez & Burr, 2007, for which (Ramírez-Merlano et al., 2011). In turn, the presence in seminal plasma of glucose and high levels of fructosamine, which is described as a glycated protein that is not commonly investigated in seminal plasma of animals, may indicate the inefficient use of glucose by the organism (Armbruster, 1987). In humans, high fructosamine levels may indicate infertility (Tomaszewski et al., 1992). However, it is also known that fructosamine is consumed by superoxide dismutase (SOD), indirectly used to determine the activity of this antioxidant enzyme in the seminal plasma of dogs (Lopes et al., 2011). Considering this information, together with the data obtained from the PCA analysis in this study, we can consider that fructosamine has a negative correlation with the parameters of sperm motility.

The PCA is an interesting tool, as it is a type of exploratory analysis that can help in understanding the results obtainedresenting positive correlations between motility mainly with the concentration and motility time corresponding to that reported for freshwater species such as Rhamdia quelen, Salmo trutta Linnaeus, 1758, Barbus grypus (Heckel, 1843)(Borges et al., 2005; Bozkurt et al., 2011; Güllü et al., 2015).

However, in the particular case of motility and concentration, negative correlations have already been reported for species such as Prochilodus lineatus (Valenciennes, 1837) (Viveiros et al., 2019), Oncorynchus mykiss (Walbaum, 1792) (Ciereszko, Dabrowski, 1994), Cyprinus carpio Linnaeus, 1758 (Bozkurt et al., 2009). It can be considered that a higher sperm concentration is not always related to a higher motility and fertilization rate (Williot et al., 2000). It is understood that sperm concentration is species-specific and may be related to gonadal development and maturation, which in turn will depend on changes in temperature, nutritional quality, enzymatic activity, and age, which varies between individuals (Piros et al., 2002; Shaliutina-Kolešová et al., 2020).

Total proteins also play an important role in energy allocation in sperm, which may be the cause of a positive relationship with motility in the present study. Lahnsteiner et al. (2004) report that proteins in seminal plasma prolong sperm viability in O. mykiss. Lipids in seminal plasma are also used by spermatozoa as energy reserves while they remain in the spermatic ducts, and the synthesis of triglycerides may be a response to distinct physiological changes during artificial sperm storage (Lahnsteiner et al., 1993).

In the present study, triglycerides did not directly link with motility but showed a positive correlation with pH, Cl, and Ca+. Specific physiological relationships between these variables should be studied in more detail in the future, however, Lahnsteiner et al. (1998) reported that low triglyceride concentrations may indicate inadequate energy sources, which may reduce motility rates and fertilizing capacity in O. mykiss. Cl and Ca+ ions also showed no apparent relationship with motility in the present study.

The pH was not correlated with motility in this study. However, other authors have reported the effects of pH on sperm motility in several fish species, suggesting its importance in seminal plasma characteristics and membrane potential as well as motility (Billard, Cosson, 1988; Gallego et al., 2014; Baradaran et al., 2019; Pérez et al., 2020; Silva Pinheiro et al., 2020). According to previous studies, during the passage of sperm from the testis to the spermatic duct, an increase in external pH may be responsible for the acquisition of motility in some salmonid fish (Morisawa, Morisawa, 1986, 1988) and, therefore, the pH of the seminal fluid can also affect the final maturation of sperm (Lahnsteiner et al., 1998).

Several authors have reported the importance of the Na+ ion in the beginning of sperm motility. For this reason, it is widespread to observe activating solutions that contain Na+, i.e., for Esox lucius Linnaeus, 1758 (Hadi-Alavi et al., 2009) Prochilodus lineatus (Viveiros et al., 2009), Brycon insignis (Orfão et al., 2011), P. lineatus and Brycon orbignyanus (Valenciennes, 1850) (Viveiros et al., 2019). In the present study, sodium contributed little to the variance of the data, but it also had a trend in the graph very close to motility, so it could be positively related to this variable.

Knowledge of the physical and chemical constituents of sperm and seminal plasma is a prerequisite for success in assessing the reproductive capacity of different fish species. It is important to emphasize that the composition of seminal plasma can vary not only according to the characteristics of each species but also due to other external factors such as age, reproductive period, nutrition, and many others.

The seminal plasma of P. reticulatum has the predominant ions and sugars in its composition, Na+ and glucose, respectively, in addition to proteins. When applying PCA to the data, we observe positive relationships between motility and the parameters of motility time, sperm concentration, total protein, and negative relationships with osmolality and fructosamine. These data can serve as a basis for creating diluting or cryoprotectant solutions in the sperm cryopreservation protocols of the species.

Acknowledgments​


We would like to thank Piraí Piscicultura for providing the experimental fish. Special thanks to Dr. Juan F. Asturiano, Professor at the Polytechnic University of Valencia, for the final review of this work. This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/PROEX N°88887.302629/2018–00), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq N°200452/2022–3), the Brazilian fostering agencies Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP N°2020/15020–0).

References​


Armbruster DA. Fructosamine: structure, analysis, and clinical usefulness. Clin Chem. 1987; 33(12):2153–63. https://doi.org/10.1093/clinchem/33.12.2153

Baradaran NS, Noori A, Bahmani M, Yazdani SMA, Akbarzadeh A. Effects of seminal plasma ionic content, pH and osmolality on spermatozoa motility in bester (Female Huso huso × Male Acipenser ruthenus) sturgeon. Iran J Fish Sci. 2019; 18(3):395–404. https://doi.org/10.22092/ijfs.2019.118198

Billard R, Cosson MP. Sperm motility in rainbow trout, Parasalmo mykiss; effect of pH and temperature. In: B. Breton, Y. Zohar, editors. Reproduction in fish. Basic and applied aspects in endocrinology and genetics, 1988. p.161–67.

Billard R, Cosson MP. Some problems related to the assessment of sperm motility in freshwater fish. J Exp Zool. 1992; 261(2):122–31. https://doi.org/10.1002/jez.1402610203

Borges A, Siqueira DR, Jurinitz DF, Zanini R, Amaral F, Grillo LM et al. Biochemical composition of seminal plasma and annual variations in semen characteristics of jundiá Rhamdia quelen (Quoy and Gaimard, Pimelodidae). Fish Physiol Biochem. 2005; 31(1):45–53. https://doi.org/10.1007/s10695-005-4742-8

Bozkurt Y, Öǧretmen F, Erçin U, Yildiz Ü. Seminal plasma composition and its relationship with physical spermatological parameters of Grass carp (Ctenopharyngodon idella) semen: with emphasis on sperm motility. Aquac Res. 2008; 39(15):1666–72. https://doi.org/10.1111/j.1365-2109.2008.02041.x

Bozkurt Y, Öğretmen F, Kökçü Ö, Erçin U. 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. 2011; 56(8):355–64. https://doi.org/10.17221/2394-CJAS

Bozkurt Y, Ogretmen F, Secer FS, Ercin U. Effects of seminal plasma composition on sperm motility in mirror carp (Cyprinus carpio). Isr J Aquac Bamidgeh. 2009; 61(4):307–14. https://doi.org/10.46989/001c.20570

Ciereszko A. 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, editors. Fish spermatology. Oxford: Alpha Science Ltd; 2008; p.215–40.

Ciereszko A, Dabrowski K. Relationship between biochemical constituents of fish semen and fertility: the effect of short-term storage. Fish Physiol Biochem. 1994; 12(5):357–67. https://doi.org/10.1007/BF00004300

Ciereszko A, Glogowski J, Dabrowski K. Biochemical characteristics of seminal plasma and spermatozoa of freshwater fishes. In: Tiersch TR, Green CC, editors. Cryopreservation in Aquatic Species. 2nd Edition. World Aquaculture Society, Baton Rouge, Louisiana: 2011; p.46–79.

Ciereszko A, Ottobre JS, Glogowski J. Effects of season and breed on sperm acrosin activity and semen quality of boars. Anim Reprod Sci. 2000; 64(1–2):89–96. https://doi.org/10.1016/S0378-4320(00)00194-9

Cosson J. The ionic and osmotic factors controlling motility of fish spermatozoa. Aquac Int. 2004; 12(1):69–85. https://doi.org/10.1023/B:AQUI.0000017189.44263.bc

Dziewulska K. Effect of pH, osmolality and ion concentration on spermatozoa motility and composition parameters of sperm and seminal plasma in pikeperch (Sander lucioperca L.). Aquaculture. 2020; 520:735004. https://doi.org/10.1016/j.aquaculture.2020.735004

Food and Agriculture Organization of the United Nations (FAO). The state of world fisheries and aquaculture 2020. Sustainability in action. 2020; 35: 1–244. https://doi.org/https://doi.org/10.4060/ca9229en

Fribourgh JH. The application of a differential staining method to low-temperature studies on goldfish spermatozoa. Prog Fish Cult. 1966; 28(4):227–31. https://doi.org/10.1577/1548-8640(1966)28[227:TAOADS]2.0.CO;2

Gallego V, Asturiano JF. Sperm motility in fish: technical applications and perspectives through CASA-Mot systems. Reprod Fertil Dev. 2018; 30(6):820–32. https://doi.org/10.1071/RD17460

Gallego V, Martínez-Pastor F, Mazzeo I, Peñaranda DS, Herráez MP, Asturiano JF et al. Intracellular changes in Ca2+, K+ and pH after sperm motility activation in the European eel (Anguilla anguilla): preliminary results. Aquaculture. 2014; 418–419:155–58. https://doi.org/10.1016/j.aquaculture.2013.10.022

Güllü K, İnanan BE, Öğretmen F, Gölbaşı S, Yilmaz F. Effects of seminal plasma properties on percentage and duration of shabut (Barbus grypus Heckel, 1843) sperm motility. Isr J Aquac Bamidgeh. 2015; 67:1–09. https://doi.org/10.46989/001c.20700

Hadi-Alavi SM, Rodina M, Viveiros ATM, Cosson J, Gela D, Boryshpolets S et al. Effects of osmolality on sperm morphology, motility and flagellar wave parameters in Northern pike (Esox lucius L.). Theriogenology. 2009; 72(1):32–43. https://doi.org/10.1016/j.theriogenology.2009.01.015

Hussain S, Masood I, Balkhi H, Kashmir J, Farooz I, Bhat A et al. Biochemical composition of the seminal plasma of Schizothorax niger in response to different doses of synthetic breeding hormone WOVA-FH. J Entomol Zool Stud. 2018; 6(6):1033–37.

Kavamoto ET, Tocumaru M, Silva RAPS, Campos BES. Variações morfológicas e contagem diferencial das células leucocitárias do “Cascudo” Plecostomus albopuncatus (Regan, 1980), no desenvolvimento gonadal. Bol Inst Pesca. 1985; 12(2):15–23.

Kubitza F, Campos JL, Brum JA. Produção intensiva no Projeto Pacu Ltda. e Agropeixe Ltda. Panorama de Aqüicultura. 1998; 8:41–49.

Lahnsteiner F, Berger B, Weismann T, Patzner R. Fine structure and motility of spermatozoa and composition of the seminal plasma in the perch. J Fish Biol. 1995; 47(3):492–508. https://doi.org/10.1111/j.1095-8649.1995.tb01917.x

Lahnsteiner F, Berger B, Weismann T, Patzner RA. Determination of semen quality of the rainbow trout, Oncorhynchus mykiss, by sperm motility, seminal plasma parameters, and spermatozoal metabolism. Aquac. 1998; 163(1–2):163–81. https://doi.org/10.1016/S0044-8486(98)00243-9

Lahnsteiner F, Mansour N, Berger B. Seminal plasma proteins prolong the viability of rainbow trout (Oncorynchus mykiss) spermatozoa. Theriogenology. 2004; 62(5):801–08. https://doi.org/10.1016/j.theriogenology.2003.12.001

Lahnsteiner F, Patzner RA, Weismann T. Energy resources of spermatozoa of the rainbow trout Oncorhynchus mykiss (Pisces, Teleostei). Reprod Nutr Dev. 1993; 33(4):349–60. https://doi.org/10.1051/rnd:19930404

Lahnsteiner F, Weismann T, Patzner R. Cryopreservation of semen of the grayling (Thymallus thymallus) and the danube salmon (Hucho hucho). Aquaculture. 1996; 144(1–3):265–74. https://doi.org/10.1016/S0044-8486(96)01308-7

Leite JS, Oliveira-Araújo MS, Almeida-Monteiro PS, Campello CC, Campos ACN, Salmito-Vanderley CSB. Seasonal variation in seminal quality in Brazilian bocachico (Teleostei, Characiformes). Rev Caatinga. 2018; 31(3):759–66. https://doi.org/10.1590/1983-21252018v31n326rc

Linhart O, Schleta V, Slavik T. Fish sperm composition and biochemistry. Bull Inst Zool Acad Sin. 1991; 16:285–311.

Lopes BV, Monteiro GA, Ovídio PP, Jordão Júnior AA, Lopes MD. Avaliação do estresse oxidativo no plasma seminal de cães férteis e subférteis após suplementação oral com vitamina C e E. Vet Zoo. 2011; 18(3):452–61.

Mojica-Rodríguez JE, Cruz-Casallas PE. Ensayos preliminares sobre crioconservación de semen de bagre rayado (Pseudoplatystoma fasciatum Linnaeus, 1766). Orinoquia. 2005; 9(2):28–37. https://doi.org/10.22579/20112629.145

Morisawa S, Morisawa M. Acquisition of potential for sperm motility in rainbow trout and chum salmon. J Exp Biol. 1986; 126(1):89–96. https://doi.org/10.1242/jeb.126.1.89

Morisawa S, Morisawa M. Induction of potential for sperm motility by bicarbonate and pH in rainbow trout and chum salmon. J Exp Biol. 1988; 136(1):13–22. https://doi.org/10.1242/jeb.136.1.13

Navarro RD, Lemos JV, Ribeiro MT. Quality of semen in the reproductive cycle of cachara (Pseudoplatystoma fasciatum) raised in captivity. Acta Sci Biol Sci. 2019; 41(1):1–06. https://doi.org/10.4025/actascibiolsci.v41i1.46517

Orfão LH, Nascimento AF, Corrêa FM, Cosson J, Viveiros ATM. Extender composition, osmolality and cryoprotectant effects on the motility of sperm in the Brazilian endangered species Brycon opalinus (Characiformes). Aquaculture. 2011; 311(1–4):241–47. https://doi.org/10.1016/j.aquaculture.2010.11.041

Pérez L, Gallego V, Asturiano JF. Intracellular pH regulation and sperm motility in the European eel. Theriogenology. 2020; 145:48–58. https://doi.org/10.1016/j.theriogenology.2020.01.026

Piros B, Glogowski J, Kolman R, Rzemieniecki A, Domagala J, Horváth A et al. Biochemical characterization of Siberian sturgeon Acipenser baeri and sterlet Acipenser ruthenus milt plasma and spermatozoa. Fish Physiol Biochem. 2002; 26(3):289–95. https://doi.org/10.1023/A:1026280218957

R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. Available from: https://www.r-project.org/

Rahman MM, Rahman MS, Hossain A, Hasan M. Seminal plasma composition and their physiological relationship with spermatozoa motility in silver carp Hypophthalmichthys molitrix. W J Fish Mar Sci. 2011; 3(3):194–200.

Ramírez-Merlano J, Medina-Robles V, Cruz-Casallas P. Variación estacional de las características seminales del bagre rayado Pseudoplatystoma metaense (Teleostei, Pimelodidae). Rev MVZ Cordoba. 2011; 16(1):2336–48. https://doi.org/10.21897/rmvz.292

Rodríguez AL, Rijsselaere T, Beek J, Vyt P, van Soom A, Maes D. Boar seminal plasma components and their relation with semen quality. Syst Biol Reprod Med. 2013; 59(1):5–12. https://doi.org/10.3109/19396368.2012.725120

Shaliutina-Kolešová A, Ashtiani S, Xian M, Nian R. Seminal plasma fractions can protect common carp (Cyprinus carpio) sperm during cryopreservation. Fish Physiol Biochem. 2020:1461–68. https://doi.org/10.1007/s10695-020-00805-9

Silva AP, Lima AF, Lundstedt LM. A pesca e a aquicultura de surubins no Brasil: Panorama e considerações para a sustentabilidade. Palmas: Embrapa Pesca e Aquicultura; 2015.

Silva Pinheiro JP, Assis CB, Sanches EA, Moreira RG. Aluminum, at an environmental concentration, associated with acidic pH and high water temperature, causes impairment of sperm quality in the freshwater teleost Astyanax altiparanae (Teleostei: Characidae). Environ Pollut. 2020; 262:114252. https://doi.org/10.1016/j.envpol.2020.114252

Steyn GJ, van Vuren JHJ. The role of the blood-testis barrier in the chemical composition of the seminal plasma of the freshwater teleost Clarias gariepinus. Comp Biochem Physiol A Physiol. 1986; 83(3):421–25. https://doi.org/10.1016/0300-9629(86)90126-X

Tan-Fermin JD, Miura T, Adachi S, Yamauchi K. Seminal plasma composition, sperm motility, and milt dilution in the Asian catfish Clarias macrocephalus (Gunther). Aquaculture. 1999; 171(3–4):323–38. https://doi.org/10.1016/S0044-8486(98)00402-5

Tomaszewski L, Konarska L, Janczewski Z, Skarzyńska E, Lebioda K, Hryckiewicz L. Fructosamine in human and bovine semen. Life Sci. 1992; 50(3):181–85. https://doi.org/10.1016/0024-3205(92)90270-Y

Viveiros ATM, Chiacchio IM, Almeida ILG, Leal MC. Seminal plasma features of Prochilodus lineatus and Brycon orbignyanus throughout two consecutives spawning seasons. Mol Reprod Dev. 2019; 86(7):776–85. https://doi.org/10.1002/mrd.23170

Viveiros ATM, Orfão LH, Maria AN, Allaman IB. A simple, inexpensive and successful freezing method for curimba Prochilodus lineatus (Characiformes) semen. Anim Reprod Sci. 2009; 112(3–4):293–300. https://doi.org/10.1016/j.anireprosci.2008.04.025

Williot P, Kopeika EF, Goncharov BF. Influence of testis state, temperature and delay in semen collection on spermatozoa motility in the cultured Siberian sturgeon (Acipenser baeri Brandt). Aquaculture. 2000; 189(1–2):53–61. https://doi.org/10.1016/S0044-8486(00)00358-6

Yoshida M, Asturiano JF, editors. Reproduction in aquatic animals: from basic biology to aquaculture technology. Singapore: Springer; 2020.

Authors


Malbelys Padilla Sanchez1,2 , Laís Pedroso Borges1,2, Stella Indira Rocha Lobato1,2, Laicia Carneiro-Leite1,2, Rodrigo Yutaka Dichoff Kasai3, Cristiéle da Silva Ribeiro4, Rosicleire Veríssimo-Silveira1,2 and Alexandre Ninhaus-Silveira1,2

[1]    Pós-Graduação em Ciências Biológicas, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP, Av. Rubião Jr., s/n, 18618-970 Botucatu, SP, Brazil. (MPS) malbelys.padilla@unesp.br (corresponding author), (LPB) lais_borges27@hotmail.com, (SIRL) stellaindira1@hotmail.com, (LCL) laicialeite@hotmail.com.

[2]    Laboratório de Ictiologia Neotropical (LINEO), Departamento de Biologia e Zootecnia, Faculdade de Engenharia, Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP, Av. Brasil, 56, 15085-000 Ilha Solteira, SP, Brazil. (RVS) rosicleire.verissimo@unesp.br, (ANS) alexandre.ninhaus@unesp.br.

[3]    Piraí Piscicultura, BR-262, km 424, 79190-000 Terenos, MS, Brazil. (RYDK) rodrigokasai@hotmail.com.

[4]    Laboratório de Estudos em Fisiologia (LEFISA), Departamento de Biologia e Zootecnia, Faculdade de Engenharia, Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP, Av. Brasil, 56, 15085-000 Ilha Solteira, SP, Brazil. (CSR) cristiele@gmail.com.

Authors’ Contribution


Malbelys Padilla Sanchez: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing-original draft, Writing-review and editing.

Laís Pedroso Borges: Investigation, Methodology.

Stella Indira Rocha Lobato: Investigation, Methodology.

Laícia Carneiro-Leite: Data curation, Methodology.

Rodrigo Yutaka Dichoff Kasai: Investigation, Methodology, Resources.

Cristiéle da Silva Ribeiro: Data curation, Methodology.

Rosicleire Verissimo-Silveira: Funding acquisition, Investigation, Project administration, Resources.

Alexandre Ninhaus-Silveira: Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Writing-review and editing.

Ethical Statement​


All procedures used with the animals for the development of this experiment follow the standards approved by the Ethics Committee for the Use of Animals (CEUA-FEIS/UNESP 04/2021).

Competing Interests


The author declares no competing interests.

How to cite this article


Sanchez MP, Borges LP, Lobato SIR, Carneiro-Leite L, Kasai RYD, Ribeiro CS, Verissimo-Silveira R, Ninhaus-Silveira A. Relationship between seminal plasma composition and sperm quality parameters of the catfish Pseudoplatystoma reticulatum. Neotrop Ichthyol. 2024; 22(2):e230109. https://doi.org/10.1590/1982-0224-2023-0109


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Accepted June 3, 2024 by Bernardo Baldisserotto

Submitted October 16, 2023

Epub July 22, 2024