DIFFERENCES IN GROWTH PERFORMANCE AND MEAT QUALITY BETWEEN MALE AND FEMALE NILE TILAPIA (OREOCHROMIS NILOTICUS)
The aim of this study was to compare the growth and meat quality of juvenile male and female Nile tilapia. The results of this work revealed that male Nile tilapia performed better than females in terms of growth and meat quality, particularly with regard to growth parameters and fatty acids. The profitability and efficiency of breeding could be increased by breeding males only. Thus, promoting sustainable aquaculture methods, such as early genetic sex determination, allows producers to focus on male tilapia, enabling them to improve production and market value.
1. Introduction
The three main species of farmed freshwater finfish are carp, tilapia, and salmonids. Of these, tilapia is the most frequently cultivated, accounting for 71% of the world’s total production (Ackman, 1989). This significant fish is farmed across 120 countries in both freshwater and brackish environments (FAO, 2020). The success of tilapia production is influenced by a variety of internal and external factors, including genetics, age, sex, water quality, and stocking density (Masoud et al., 2024, all of which directly affect growth performance and meat quality (El-Sayed,2006; Tuan et al., 2020). Notably, tilapia’s advantageous traits, such as high stocking density tolerance and adaptability to low-cost diets, facilitate its widespread farming.
However, despite these benefits, early breeding and the tendency for overpopulation in mixed-sex cultures pose significant challenges. This early maturation often diverts energy and nutrients from growth to reproduction, particularly affecting female tilapia. Consequently, farmers increasingly consider cultivating predominantly male tilapia or employing sex-reversal techniques to mitigate these issues (Maita et al., 1998).
The impact of rearing practices on tilapia growth and meat quality is pronounced when comparing same-sex and mixed-sex cultures. A study by Dawood (2020) highlighted that tilapia reared in same-sex environments exhibit more uniform growth patterns, reducing the occurrence of undersized or unsellable fish. While much research has examined why male tilapia tend to grow larger than females, fewer studies have explored the implications of same-sex rearing on growth performance and meat quality.
Comprehending the life cycle of tilapia is essential since every stage from the egg to the adult has an impact on quality and growth. The quality and temperature of the water have an impact on survival rates, with early stages being especially vulnerable. Optimal conditions result in healthier fish and increased productivity. The development of muscular bodies and quality meat in juvenile tilapia is mostly dependent on their nutrition and the density of their stockings ( El-Sayed, 2006; Abelti, 2017; Mekawy et al., 2014). A healthy diet promotes growth and improves the flavor and texture of meat. Male and female differences become significant when an individual reaches adulthood. While females tend to concentrate more on reproduction, males usually grow quicker and produce more meat. The quality and efficiency of meat production are impacted by this sexual dimorphism (Gonzalez and Garcia, 2010; Herrera, 2015; Kheirallah and El-Sayed, 2006; Li et al., 2015; Makkar et al., 2016).
The quality of tilapia meat encompasses several physical and chemical attributes, including color, moisture, fat cover, protein content, shelf life, and spoilage potential(El-Zaeem et al., 2012). Juvenile tilapia, known for their white, firm meat and delicate flavor, are appealing to consumers due to their nutritional value, which includes essential moisture, protein, and fatty acids (El-Zaeem et al., 2012) . However, it is worth noting that farmed fish sometimes exhibit lower-quality meat compared to their wild counterparts. Intrinsic factors such as race, age, and gender, along with environmental conditions like water quality, significantly influence meat quality (Biro et al., 2009). Studies have shown that male tilapia often have higher body weights and fillet yields, making them advantageous in aquaculture ( Herrera, 2015). Furthermore, maturation leads to distinct differences in fatty acid composition between the sexes. Larger, mature tilapia typically have softer meat with higher fat content compared to their leaner, younger counterparts (Doğan and Ertan, 2017; Mateen and Ahmed, 2015; Sambrook and Russell, 2015).
The rearing system also affects meat quality; for instance, recirculating aquaculture systems (RASs) provide more controlled conditions than traditional pond or cage culture, leading to more consistent meat quality [9,20]( Mekawy et al., 2014; DeLong et al., 2009). Conversely, outdoor and indoor pond cultures can introduce variability based on environmental factors and management practices.
By determining which sex grows faster or produces higher-quality meat, farmers can optimize resource distribution, such as feed and space, thereby enhancing overall productivity. Insights into the nutritional makeup and quality of meat from each sex can inform breeding strategies aimed at improving desirable traits, ensuring a superior product for consumers. These comparisons are essential for advancing tilapia farming practices, ultimately increasing both quality and output. Given the gaps in existing research, this study aims to investigate the differences in growth, blood serum profiles, meat quality, and amino and fatty acid compositions between male and female Nile tilapia reared separately.
2. Materials and Methods
2.1. Ethics Statement
These experiments were approved by the Bioethical Committee of the Freshwater Fisheries Research Centre (FFRC), Chinese Academy of Fishery Sciences (2013,863 BCE). The regulations for the handling and use of laboratory animals were followed at all times.
2.2. Experimental Fish
The juvenile Nile tilapia that was used in the experiment were raised in the Wuxi Fisheries College of Nanjing Agricultural University. The juveniles were obtained and randomly selected from pure brood stock genotypes of males (XY) and females (XX). The average weight and length (±SD) of the juveniles were 22.50 ± 0.31 g and 8.3 ± 0.12 cm, respectively. Before starting the sex determination procedure, the fish were acclimatized in an indoor tank (0.8 m3), monitored, and fed for satiation twice a day (9 a.m. and 4 p.m.) for 10 days to ensure that the fish were safe and in good health. Then, twenty experimental fish were taken randomly and used to conduct a sex determination experiment.
2.3. Sex Determination
The fish were placed in small tanks of 20 L each (two fish in the tank), connected to a closed filtered water cycle where the water temperature (26 ± 1 °C) and dissolved oxygen (≥6.5 mg/L) were controlled. The sex determination experiment was repeated several times in short order to accurately obtain the required fish (40 males, 40 females). The sex of both males and females was determined by extracting DNA from a small piece of caudal fin (0.5 × 0.5 cm) using the TIANamp Genomic DNA Kit (TIANGEN BIOTECH, BEIJING Co., Ltd., Beijing, China) following the manufacturer’s recommended protocol. Before starting the PCR test, a device (NANODROP LITE—Spectrophotometer—Thermo Scientific Co.—Wilmington, DE, USA) was used to gain the proper concentration of DNA purity optical density (OD) 1.9–2.1. The PCR was conducted with a total reaction volume of 25 μL containing 1 μL of DNA, 1 μL for each primer F and R (Forward and Reverse primers), 12.5 μL of Master Mix II, and 9.5 μL of RNase-free water. Afterwards, the tubes were placed in a microcentrifuge for 10 s and put into a PCR device (BIO-RAD T100TMThermal cycler—Singapore) as follows: initial denaturation (95 °C for 3 min), 35 cycles of denaturation (95 °C for 15 s), annealing (60 °C for 20 s), extension (72 °C for 5 min), and final extension (12 °C for 5 min). After that, agarose gel electrophoresis was conducted, whereby 1.6 g of agarose powder was weighed and placed in a small glass beaker, and then 80 mL (TBE solution) was added and heated in the microwave for 2 m, after which it was cooled in a water bath for 10 s. Then, 0.8 µL of super stain was added into the beaker and mixed with the solution, which was subsequently placed in the template that contained the comb inside it at one end, and finally, left for about 15–20 min until it cooled down and became a gelatinous solid so that the teeth of the comb left the gaps (wells) in which the DNA samples were placed. A suitable micropipette was used to put 0.4 µL DNA samples in the wells. The agarose gel was placed in an electrophoresis device (BIO-RAD, FW Version:1.29-Sn.017797, Singapore), and at one end of the plate, the gel contained gaps called wells, in which the samples were placed. The DNA marker (DL 2000) was placed in the first gap (wells) of the agarose gel to measure the size of the DNA fragments in the other wells. The power supply was set to 100 V for an hour and then the movement of dyed DNA molecules through the agarose gel could be seen. After electrophoresis was completed, a device ultraviolet UV Transilluminator (WD-9413C Gel Imaging Analyzer—Beijing, China) was used to examine the agarose gel using a wavelength of 300 nm to analyze the results.
2.4. Experimental Design
After completing the sex determination procedure and separating the males and females, the fish were transferred to the greenhouse, where the experiment was conducted. The initial weight and length of the fish were measured individually and the fish were placed in eight fiber tanks, each with a capacity of 200 L, connected to a recirculating aquaculture system (Zhongkehai Recirculation Aquaculture Systems Co., Ltd., Qingdao, China). The tanks were divided into two groups: four barrels were allocated to the females, and four barrels to the males. The stocking density of each tank was 10 fish. The experiment lasted 85 days, and all groups were subjected to the same experimental conditions in terms of water temperature (27 ± 1 °C), dissolved oxygen (>7 mg/L), pH (7.6 ± 0.2), feed quality, and daily feeding frequency (see Section 2.5).
2.5. Fish Feed
In this study, the fish were fed on floating feed; the feed used was manufactured by the company Liu Xinixin Tiansi Aquatic Feed Co., Ltd. (Jiaxing, China) according to the following specifications: the percentage of crude protein was ≥28, the percentage of fat was ≥4, the ash was ≤15, the humidity was ≤10%, phosphorous (1–3), lysine ≥ 1.5, and the diameters were 1.5, 2 and 3 mm and proportional to the stages of growth during 85 days of the experimental period. The fish were fed by hand at two time periods: 8:00–9:00 a.m. and 16:00–17:00 p.m. The feeding ratio is 5% of the calculated body weight based on FCR.
2.6. Sample Collections and Analyses of Growth Parameters
After 85 days of fish rearing, the fish were starved for 24 h to clean the intestines before sampling. Then, the fish in each tank were individually weighed by electronic scale to determine the final body weight (FBW), and the final body length (FBL) of both males and females was measured with a measuring plate to the nearest (0.1 cm). The growth performance parameters calculated are whereby FBL: final body length; FBW: final body weight; WGR: weight gain rate; SGR: specific growth rate; FCR: feed conversion ratio; GSI: Gonad Somatic Index; VSI: Viscesromatic Index; HIS: Hepatosomatic Index..
2.7. Meat Sample Collection
Three fish were chosen at random from each tank, one male and one female (n = 6). Using a sharp scalpel, meat samples were extracted from one side of the body starting from the vicinity of the head and ending at the tail. The samples of flesh weighed about 50 g and were sliced free of scales, skin, and spines. Male and female samples were separated using laboratory bags, and the samples were then stored in the freezer (−80 degrees) until usage.
2.8. Analysis of Meat Proximate Composition
2.8.1. Moisture Content
The typical standard drying temperature used for moisture content was 105 °C (221 °F) and the sample was dried at this temperature for 16–24 h. According to the AOAC [21], the moisture content was estimated using the oven drying method by weighing the sample both before and after the water was removed and using the following formula:
3. Results
3.1. Growth Performance Parameters
The growth performance parameters of juvenile male and female Nile tilapia reared in separate tanks at 85 days are summarized in Table 1.
Table 1. Growth performance parameters for male and female Nile tilapia.
Note: Data are means ± SD. The values in the different lowercase letters show significant differences between experimental groups within the same row (p < 0.05), whereby FBL: final body length; FBW: final body weight; WGR: weight gain rate; SGR: specific growth rate; FCR: feed conversion ratio; GSI: Gonad Somatic Index; VSI: Viscesromatic Index; HIS: Hepatosomatic Index.
3.2. Approximate Composition of Meat
The results of the approximate composition of meat indicate that there is no significant difference (p > 0.05) in the moisture and crude protein between male and female Nile tilapia. However, there are significant differences (p < 0.05) in crude fat and ash content between male and female Nile tilapia, as the results in Table 3 for fat are 1.30 ± 0.17%, 1 ± 0.10%, and ash content are 1.13 ± 0.05%, 0.76 ± 0.06%, for male and female, respectively, where the fat and ash contents in males are greater than females.
3.5. Profile of Amino Acids
In this study, 17 different types of amino acids were obtained in both male and female Nile tilapia. The results showed that there was no significant difference (p > 0.05) between males and females in the profile of essential amino acids (EAAs), while there was a low significant difference (p < 0.05) between males and females in muscle content of non-essential amino acids (NEAAs). The results of the total amino acid (TAA) profile were 15 ± 0.152% and 15.866 ± 0.120% for males and females, respectively, indicating that the TAA in females is slightly higher than in males, but the statistical study showed that there is no significant difference (p > 0.05) and no effect of sex on TAA profile.
3.6. Profile of Fatty Acids
The results of fatty acids are classified into saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs), polyunsaturated fatty acids (PUFAs), and total fatty acids (TFAs), where it can be seen that there is a significant difference (p < 0.05) in TFAs, SFAs, and PUFAs between males and females, where the results are 1.05 ± 0.045%, 0.628 ± 0.015% for TFAs, 0.381 ± 0.0143%, 0.224 ± 0.0026% for SFAs, and 0.337 ± 0.012%, 0.237 ± 0.007% for PUFAs for males and females, respectively, as males outperform the females. And the results showed that there was no significant difference (p > 0.05) between males and females in the content of MUFAs, where the results were 0.327 ± 0.0307%, and 0.167 ± 0.0114% for males and females, respectively. This indicates that MUFAs are slightly higher in males than in females, but the statistical study indicated that there is no effect of sex on the muscle content of MUFAs.
4. Discussion
4.1. The Growth Performance
In this study, males outperformed females in WGR and SGR; this indicates the efficiency of males in converting the bulk of their energy from digestive processes for physical growth mentioned that the majority of the metabolic energy in Nile tilapia males resulting from the consumption of the provided feed is directed towards growth and masculinization, whereas the majority of the metabolic energy in females is typically directed towards reproduction and egg formation, which results in slow growth. The FCR of male tilapia was lower than females (Table 1). This indicates the efficiency of males in converting feed and benefiting from it in weight gain compared with females. Moreover, Osibona reported that, despite eating the same number of feeds, males grow bigger and more rapidly than females due to their superior ability to convert food into energy. This result shows a significant correlation between growth and FCR, whereby faster-growing fish had a better lower FCR.
In this study, the GSI of females was higher than that of males, as the female gonads were fully mature and full of eggs. Fleming notes that female fish may invest 20–25% of their body weight in gonads before reproduction and require a great deal of energy to develop eggs, but male fish may invest only 3–9%. When the male gonads reach the ripe (running) stage, the fish’s ripe gonads mark a critical moment when energy is shifted towards successful reproduction. Therefore, the mature state of male gonads affects the quality of meat and causes changes in fat content, texture, flavor, appearance, and shelf life, all of which can affect consumer acceptance and marketability. In addition, there was a positive correlation between HSI and GSI during the development of the gonads, where raised HSI may help maintain the transport of nutrients to the developing ovary, increase GSI, and promote follicle. However, there was no significant difference in HSI between males and females, as the slightly elevated HSI in females may be due to changes in energy intake and homeostasis during ovarian development, ovulation, and reproductive processes.
4.2. Meat Quality (Approximate Composition)
4.2.1. Moisture Content
No significant difference in the moisture content of meat was found in both males and females, as shown in Table 3, and the results were low compared to many previous studies. Also, there was an inverse correlation between moisture and FBL in males, as shown in Figure 2, while a positive correlation was seen in females, as shown in Figure 3, at the significance level. This low moisture content in the meat plays a role in preserving the characteristics, quality, and taste of the meat. Olagunju stated that if the moisture content of the meat is greater than 80%, it is considered to be high in moisture, which makes fish meat and fish products more susceptible to microbial spoilage and oxidative decomposition of polyunsaturated fatty acids in addition to lowering the quality, safety, and shelf life of these products.
4.2.2. Crude Protein
There is no significant difference in crude protein in the composition of the meat between males and females. While the crude protein content of fish muscles ranges from 15% to 28%, some fish species can have values as low as 15% or as high as 28%. According to the results in Table 3, the protein content was greater than 15% for males and females; thus, the meat of Nile tilapia is a rich and high source of crude protein, as reported by Stancheva.
4.2.3. Crude Fat
In the current study, there is a significant difference between males and females in the content of crude fat, as shown in Table 3. The crude fat is higher in males compared to females, which causes it to be considered as lean fish according to the classification by Ackman, who reported that fish can be divided into four categories based on their crude fat content: lean fish (crude fat percentage < 2%), i.e., low-fat fish; the percentage of crude fat between (2 and 4%); medium fat (4% to 8%); and high fat (if the percentage of crude fat > 8%).
4.2.4. Ash Content
There is a significant difference in the ash content in the composition of the meat, which is higher in males than females. This indicates that the meat of males contains more minerals than females, since the percentage of ash reflects the amount of minerals in the sample. However, the percentage of ash is related to the breeding environment and the vital processes of the fish body. Also, there is a positive correlation between ash and moisture in males, as shown in Figure 2, while an inverse correlation is seen in females, as shown in Figure 3, at the significance level.
4.4. Profile of Amino Acids
Nile tilapia is regarded as a fish that is rich in essential amino acids. No significant difference between males and females in the TAAs was detected, as well as in the EAAs because proteins are the basic constituents of cells during the early stages of growth, differentiation, development, and sexual maturity, synthesized by both males and females in proportionate amounts. However, the number of amino acids in tilapia fluctuates based on a variety of factors, such as the habitat, the type and composition of the fish’s diet, the fish’s age, weight, and length [7]. The FAO and WHO reported that high-quality dietary protein not only contains a full range of essential amino acids, but these essential amino acids are also in appropriate proportions [50]. As determined by the WHO/FAO (2007), protein is considered to be of high quality when the ΣEAA/ΣTAA ratio is more than 40%, and the ΣEAA/ΣNEAA ratio is more than 60%. In this study, the ratio of ΣEAA/ΣTAA is 45.35% and 45.22% in males and females, respectively, and higher than 40%; and the ratio of ΣEAA/ΣNEAA is 83.33 and 82.86 in both males and females, respectively, and much higher than 60%. Thus, the protein in the meat of Nile tilapia is of high quality, and the protein quality of males is slightly higher than that of females based on this indicator.
4.4. Profile of Fatty Acids
In this study, there is a significant difference in the content of the muscles of males and females in each of the SFAs, PUFAs, and the TFAs that were determined, where the males outperformed the females. The difference in fatty acid composition in Nile tilapia is due to differences in stages of sexual maturity, vital processes, and metabolic processes between the sexes.
The fatty acids in the female fish’s fat are transmitted to the eggs during the growth and development of the gonads in the bloodstocks, and they play a significant role in determining the quantity and quality of the eggs. As reported by Abelti, palmitic acid as a major metabolite is not affected by diet in fish, and it is a dominant SFA in Nile tilapia and found in high concentrations in the adipose tissue; this is consistent with the results of the current study, but it is slightly higher in males than females.
In the current study, males had slightly higher levels of MUFAs in their muscles than females, but statistically, there was no significant difference between the sexes. This contrasts with the work of Abelti [8] which reported that females had slightly higher levels of MUFAs in their muscles than males, possibly because samples were collected during sexual maturity and before ovulation in this study, and females consumed more MUFAs than males during the process of ovarian development and formation of eggs. In this study, not all PUFAs, especially n-3 and n-6, were identified. Perhaps the reason for the low percentages was caused by the increased consumption by both males and females as PUFAs are of great importance in the growth, development, and sexual maturity of juvenile fish. There was a strong positive correlation between PUFAs and WGR in females, as shown in Figure 3, with the significance level, while the correlation was inverse in males, as shown in Figure 2, with the significance level. There is no effect of sex on muscle content of n-3 and n-6 PUFAs; perhaps the reason for this is due to their similar important role for both males and females during the stages of growth and development of the various organs of the body, in addition to the growth and development of the gonads.
5. Conclusions
In this research, male Nile tilapia fish perform better than female fish in terms of growth and flesh quality, especially when it comes to growth metrics and fatty acids. Farming profitability and efficiency could be increased by rearing males alone. Promoting sustainable aquaculture methods, such as early Genetic Sex Determination, enables producers to concentrate on male tilapia, improving output and market value.
Source : Sayouh, M.; Ali, M.; Li, Y.; Tao, Y.-F.; Lu, S.-Q.; Qiang, J. Differences in Growth Performance and Meat Quality between Male and Female Juvenile Nile Tilapia (Oreochromis niloticus) during Separate Rearing. Animals 2024, 14, 2954. https://doi.org/10.3390/ani14202954.
