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Effect of Garcinia kola seeds supplemented diet on growth performance and gonadal development of Oreochromis niloticus juveniles breed in ponds

Effect of Garcinia kola seeds supplemented diet on growth performance and gonadal development of... Background: Despite the favorable geo-climatic potential of Cameroon, the national production of tilapia remains low due to poor tilapia growth reported by fish farmers. One of the underlying reasons is the early female maturation at a very small size and precocious breeding in earthen ponds, resulting in overpopulation which leads to stunted growth and therefore to the production of unmarketable fish size. Studies have shown that dietary supplementation of G. kola enhanced growth in young Clarias gariepinus and Oreochromis niloticus. It was also reported that G. kola inhibited spawning in Tilapia adult females. Therefore, this study sought to assess the effects of Garcinia kola as growth promoter and inhibitor of gonadal development in young Oreochromis niloticus. Methods: A total of 108 juveniles weighing 13.32 ± 0.62 g were randomly distributed in 9 hapas of 12 fishes each (9 females and 3 males) and fed for 70 days with three isonitrogenous diets, 40% crude protein with increasing Garcinia kola supplementation levels of 0 (normal diet), 6% and 10% (experimental diets). Physico-chemical parameters of the water (temperature, dissolved oxygen, pH, nitrate, nitrite, ammonia, and transparency) were measured twice a week. Every 14 days, fish were harvested, counted, and weighed. At the end of the experiment, three fish of each sex per replicate were sacrificed and their gonad and liver collected and weighed. Data were statistically analyzed using one- way analysis of variance repeated measure followed by Newman-Keuls multiple tests. Results: The results showed that all physico-chemical parameters of the water were within the recommended values for Tilapia culture. Tilapia fed 6% Garcinia kola supplemented diet displayed higher final body weight in males (38.60 ± 3.50 g) and females (36.77 ± 3.62 g) compared to those receiving normal diet (36.23 ± 1.36 g and 25.87 ± 3.32 g; respectively to the final body weight in males and females). The gonadosomatic index and hepatosomatic index indicated no significant variation in males while in females, these were significantly low in the experimental fish compared to control fish. Conclusion: The results of this study demonstrated that supplementation of G. kola seeds in diets of young Tilapia improved growth performance and impaired gonadal development in females. Keywords: Oreochromis niloticus, Garcinia kola, Growth, Gonad development * Correspondence: epauka@yahoo.fr The University of Douala, Institute of Fisheries and Aquatic Sciences of Yabassi, P.O. Box: 7236, Douala, Cameroon Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 2 of 8 Background niloticus adult females; while in Tilapia fry, it was demon- In Africa, particularly in Cameroon, fish food represents strated that supplementation of G. kola can induce sex the primary source of animal protein. It offers better types conversion (Sulem-Yong et al. 2018;Tigoliet al. 2018). To of essential minerals, amino acids and is low in undesir- our knowledge, this study is the first on the effect of diet- able saturated fats (Hussain, 1986). To cope up with nutri- ary inclusion of G. kola on gonadal development in non- tional requirements of increasing population, aquaculture puber Oreochromis niloticus. Therefore, the present work is considered as the only possible solution to increase fish was undertaken to evaluate the effect of dietary supple- production. Tilapia being an important food fish world- mentation of Garcinia kola seed powder on growth per- wide, significant developments have been recorded during formances and gonadal development of Oreochromis the last three decades in its farming. About 85 countries niloticus juveniles. worldwide are involved in fish farming and about 98% of tilapia produced there are grown outside their original Methods habitats (Shelton, 2002). It provides one of the most im- Collection and acclimation of experimental fish portant sources of animal protein and income throughout The experiment was carried out in a small-scale private the world (Sosa et al. 2005). In some African countries farm located at Bomabom (LN: 3°41′0″–°46′30″ and LE: such as in Egypt, the culture of Nile tilapia (Oreochromis 1°7′30″–11°13′0″) in the central region of Cameroon. A niloticus) has increased dramatically in the last few years; total of 108 juveniles of Oreochromis niloticus were used; while in Cameroon the global production remains insig- each weighing 13.32 ± 0.62 g with an average length of nificant despite the natural potential of the country. One 8.76 ± 0.41 cm. They were randomly distributed in tripli- of the major drawbacks to tilapia culture is the early cate into 9 hapas (made up of mosquito net cloth with size female maturation at very small size (15–30 g) (Mair and 1′ ×1′ ×0.5′) of 12 juveniles each (9 females and 3 males). Little, 1991; Popma and Lovshin, 1995), and precocious The hapas suspended in an earthen pond (800 m )with breeding in earthen ponds resulting in overpopulation the help of four bamboo poles, one at each corner of the which often leads to stunted growth. Mair and Little cage. The hapas were suspended in the pond such that (1991) enumerated various methods and techniques avail- three-quarters of each hapa was submerged in water able for the control of prolific breeding in tilapia. How- whereas one-quarter remained outside. The roof of the ever, each technique or method has its own limitations. hapas was covered with mesh to stop the experimental Monosex culture of all-male populations, which exhibits fish from jumping out and to prevent natural predators faster growth rates and which is usually produced through (snakes, kingfishers, frogs) from getting in. The fish were androgenous hormone sex reversal, is the preferred op- then allowed to acclimatize for 4 days prior to the experi- tion, and is used extensively in the countries that produce ment. During the acclimation, the fish were fed with nor- large numbers of tilapia like China (Phelps, 2006). Consid- mal diet. ering the problem associated with the use of androgenous hormonal treatment, such as environmental and public Experimental diet formulation and preparation health concerns and the limitations of existing methods A balanced dietary ration formula was prepared to meet and techniques documented by Mair and Little (1991), the nutritional requirements of Nile tilapia according to there is a need to explore other technologies to control NRC (2011) (Table 1). Three isonitrogenous diets were undesirable tilapia recruitment in ponds using natural prepared: an unenriched control diet plus two test diets. reproduction inhibitors found in plants to enhance better The test diets were supplemented with 6% and 10% Gar- growth and improved flesh (Jegede, 2010). Garcinia kola cinia kola at the expense of maize meal. In preparing ex- commonly called Bitter kola belongs to the family Clusia- perimental diets, the dried ingredients were ground into ceae. It is a multipurpose tree indigenous to West and fine particles. After weighing and mixing manually for Central Africa (Manourová et al. 2019). The seed of G. 10 min, the preparations were moistened with warm −1 kola is traditionally served to visitors for entertainment; it water (400 ml kg ) and mixed for another 20 min. Dur- is also chewed by men as an aphrodisiac or used to pre- ing the mixing, palm oil was added slowly along with vent or relieve colic disorders or cure head or suppressed warm water to achieve a proper consistency. The result- cough (Madubunyi, 2010). Previous studies on rats and ing mixture was then passed through a meat extruder to poultry have shown that inclusion of G. kola seeds in pow- obtain a 2-mm pellet. The “spaghetti-like” strands were der and methanolic extracts form improved their growth sun-dried and stored in airtight containers prior to use. performance (Oluyemi et al. 2007). Moreover, studies on The chemical composition of the test diets was analyzed Oreochromis niloticus have shown that dietary supplemen- by standard methods (AOAC, 1990). Moisture was ana- tation of G. kola seeds powder promotes the growth per- lyzed by drying the sample in an air convection oven at formance. It was also shown that dietary supplementation 105 °C overnight. Crude protein was analyzed by the of G. kola seeds powder inhibits spawning in Oreochromis Kjeldahl method after acid digestion (% crude protein = Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 3 of 8 Table 1 Formulations and proximate composition of and 10%, respectively. Fish were hand-fed four times per experimental diets (g/100 g dry weight) day (08:00 a.m., 11:00 a.m., 14:00 p.m. and 17:00 p.m. re- Ingredients Normal Normal diets Normal diets spectively) at a rate of 5% of their body weight per day. diet + G. kola (6%) + G. kola 10% Feeding rates were adjusted every 14 days for 70 days Fish meal 26 26 26 based on the weight gain of each group of fish per 14 days. Garcinia kola meal // 6 10 Physico-chemical parameters of the water in each hapa such as temperature was measured using a maximum- Soybean cake 23 23 23 minimum thermometer; dissolved oxygen (O ) was deter- Cottonseed cake 22 22 22 mined using JBL Test Kits, pH, nitrate (NO ), nitrite Maize meal 10 4 0 (NO ), and ammonia (NH ) were measured twice a week 2 3 Wheat bran 10 10 10 before feeding using test strips (JBL Easy Test 6in1) while Palm oil 4 4 4 transparency was monitored using a Secchi disk (Table 2). Premix 5 5 5 Data collection Total 100 100 100 Growth performances, feed utilization, and somatic indi- Proximate composition (%) ces were assessed by determination of weight gain Protein 40.47 40.03 39.73 (WG), specific growth rate (SGR), feed intake (FI), con- Lipid 13.23 13.14 13.12 dition factor (K), feed conversion ratio (FCR), protein ef- Ash 12.75 12.71 12.68 ficiency ratio (PER), survival rate (SR), hepatosomatic Moisture 7.74 8.04 7.94 index (HSI), and gonadosomatic index (GSI). Calcula- tions were carried out using the following formulae: Dry matter 92.26 91.96 92.06 weight gain (g) = final weight–initial weight; specific Energy (kcal/100 g) 420.63 418.17 417.20 growth rate (%/day) = 100 (lnW2–lnW1)/T, where W1 and W2 are the initial and final weight, respectively, and % nitrogen × 6.25) while crude lipid was determined by T is the number of days in the experimental period; sur- extraction with petroleum ether using the Soxhlet vival rate (%) = final number of fish × 100/initial number method. The ash content in the diet was analyzed by of fish; condition factor = 100 (weight/length ); feed in- combustion of samples in a muffle furnace at 550 °C for take = total dry feed/number of fish; feed conversion ra- 12 h (Table 1). tio (FCR) = feed intake/live weight gain; protein efficiency ratio (PER) = live weight gain/protein fed, Experimental design where protein fed = % protein in diet × total diet con- Mixed-sex Nile tilapia O. niloticus were used in the feed- sumed/100; HSI = 100 (liver weight/body weight); GSI = ing trial. At the initiation of the experiment, individual 100 (gonad weight/body weight). weight and length of all fishes per treatment were mea- sured for determination of both initial weight and length. Statistical analysis The acclimatized juveniles were randomly distributed in All results were expressed as mean ± SD. Data were sta- three replicates in 9 hapas each at a stocking density of 12 tistically analyzed using one-way analysis of variance fish per hapas (9 females and three males). In the first trip- (ANOVA-1) repeated measure followed by Newman- licate, fish were fed with normal diet to serve as controls Keuls multiple tests with n = 3 replicates. Differences while in the second and third triplicates, they were fed were considered significant when P < 0.05. All statistics with the Garcinia kola supplemented diet at rates of 6% were carried out using GraphPad Prism version 6.0. Table 2 water quality parameters (Mean ± SD) during 70 days of the experimental period Parameters Rearing period (daRearing period (days) 0 1428 4256 70 Temperature (°C) 28.10 ± 0.35 28.10 ± 1.10 28.71 ± 0.70 28.1 ± 0.80 28.71 ± 0.70 27.96 ± 0.70 Dissolved oxygen (mg/l) 5.56 ± 0.25 5.46 ± 0.35 5.56 ± 0.32 5.55 ± 0.28 5.55 ± 0.38 5.55 ± 0.37 pH 7.20 ± 0.03 7.34 ± 0.10 7.35 ± 0.10 7.36 ± 0.10 7.22 ± 0.20 7.17 ± 0.20 Transparency (cm) 36.60 ± 4.44 36.61 ± 3.70 37.23 ± 3.40 37.23 ± 4.00 38.85 ± 4.10 36.28 ± 2.20 Ammonia (mg/l) 0.58 ± 0.02 0.50 ± 0.05 0.50 ± 0.05 0.50 ± 0.00 0.50 ± 0.08 0.50 ± 0.02 Nitrite (mg/l) 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 Nitrate (mg/l) 0.12 ± 0.01 0.12 ± 0.01 0.12 ± 0.02 0.12 ± 0.05 0.12 ± 0.05 0.12 ± 0.05 Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 4 of 8 Results Body weights and organs measurements of sexually Growth performances mature Oreochromis niloticus Growth performances of O. niloticus juveniles fed The average body weights, hepatosomatic index, and with different diet in terms of weight gain and gonadosomatic index per treatments in both males and specific growth rate are presented in Fig. 1.The females were computed and were presented in Figs. 2 weight gain recorded during fish sampling showed an and 3. In males, the mean values of body weight (Fig. 2), increase with respect to time but not according to hepatosomatic index (Fig. 3a), and gonadosomatic index the G. kola supplementation rate (Fig. 1a). Feed sup- (Fig. 3b) among the different groups were not signifi- plemented with G. kola at 6% induced in O. niloticus cantly different. After 70 days of experiment, the mean juveniles the highest values of weight gain as from body weights of 36.77 ± 3.62 g obtained in females fed the fourteenth day of the experiment up to the end. with 6% G. kola supplemented diet was significantly (p < At the end of sampling, fish fed with diet supple- 0.05) high compared to the control group (25.87 ± 3.32 mented with 6% of G. kola presented a weight gain g) and groups fed with 10% G. kola supplemented diet of 19.46 ± 1.31 g, which was significantly (p <0.05) (26.33 ± 3.34 g) (Fig. 2). Moreover, feeding the female O. higher by 17.68% and 32.58% compared to that in niloticus with a diet supplemented with G. kola signifi- fish fed with the normal diet (16.02 ± 1.55 g) and diet cantly (p < 0.05) decreased both hepatosomatic index supplemented with 10% G. kola (13.12 ± 1.58 g) re- and gonadosomatic index compared to the control spectively (Fig. 1a). Observation on specific growth group (Fig. 3a, b). rate showed significant (p < 0.05) increase in fish re- ceiving a diet containing G. kola at 6% compared to Discussion fish fed with both the normal diet and diet supple- Fish is one of the most appreciated foodstuff worldwide mented with 10% G. kola during the first two rearing and particularly in most of the African countries like periods (Fig. 1b). Cameroon. However, despite the increase in production of cultured fish from some countries, production from some other countries including Cameroon has not im- Survival and feeding efficiency proved yet; statistics show that the supply of fish in The results presented in Table 3 illustrate the survival Cameroon comes to 43% of fishing (22% of inland fish- rate and feeding efficiency in term of condition factor, eries, 21% of sea fisheries), 56.8% of imports and only feed intake, protein intake, feed conversion ratio, and 0.1% of fish farming, that is 1000 t/year (FAO, 2009; protein efficiency ratio on the 70th day of the experi- Ndah et al. 2011). One of the reasons for low aquacul- ment. No mortality was recorded during the culture ture production has been attributed to feeding quality. period. Similarly, no significant variation in condition Research is currently focused on improving the quality factor and feed conversion ratio was observed among of fish feed through replacement or addition of appro- the different groups during the study. However, for priate ingredients that encourage faster fish growth. the feed intake, Protein intake and Protein efficiency, Tropical forests contain many tree species that have sup- significant differences were obtained only in fish fed plied edible fruits for centuries. It has been previously diet supplemented with G. kola at 6% compared to reported in many research works that different plant that receiving diet supplemented with G. kola at 10%. additives can enhance growth in some fish species such Fig. 1 Effects of diet supplementation with Garcinia kola seeds on mean weight gain (a) and specific growth rate (b)of Oreochromis niloticus juveniles. Mean on the same rearing period carrying the same superscript are not significantly different at p < 0.05 Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 5 of 8 Table 3 Survival and feed utilization of Oreochromis niloticus juveniles fed with different quantities of Garcinia kola supplemented diets for 70 days Parameter Normal diet Normal diet + G. kola (6%) Normal diet + G. kola (10%) Initial number 36 36 36 Final number 36 36 36 a a a Survival rate (%) 100 100 100 Initial biomass (g) 159.86 ± 8.71 158.15 ± 6.87 161.72 ± 16.94 Final biomass (g) 352.13 ± 27.28 391.63 ± 13.66 319.18 ± 16.94 Initial weight (g) 13.32 ± 0.72 13.18 ± 0.57 13.48 ± 0.78 Final weight (g) 29.34 ± 2.27 32.64 ± 1.13 26.60 ± 1.41 Final length (cm) 11.35 ± 0.41 12.35 ± 0.10 11.30 ± 0.19 a a a Condition factor 2.00 ± 0.10 1.73 ± 0.04 1.84 ± 0.03 ab a b Feed intake (g/fish) 69.94 ± 4.68 73.81 ± 2.60 63.35 ± 2.68 ab a b Protein intake (g/fish) 28.00 ± 1.08 29.56 ± 0.60 25.37 ± 0.62 a a a Feed conversion ratio 4.39 ± 0.30 3.80 ± 0.10 4.87 ± 0.37 ab a b Protein efficiency ratio 0.57 ± 0.03 0.66 ± 0.01 0.52 ± 0.04 Values are mean ± standard deviation of 3 replications containing 12 fish per replicate. Values on the same row carrying the same letter are not significantly different at p < 0.05 as Oreochromis niloticus (Kareem et al. 2016, Hassan et among the treatment means were not significant. Previ- al. 2018). Results from the present study indicate that ous studies revealed that G. kola seed powder supple- there was an increase in the growth of the fish fed with mented in animal diets also promoted growth and feed different rate of dietary supplementation with G. kola conversion efficiency in Clarias gariepinus juveniles seed. However, the highest growth response was ob- (Adeniji et al. 2018)and Oreochromis niloticus adults served in the fish fed with G. kola seed supplemented (Sulem-Yong et al. 2018). The proximate and phyto- −1 meal at a level of 60 g kg , indicating that the G. kola chemicals analysis of G. kola seeds revealed that it is rich seed meal supplementation could have enhanced nutri- in nutrients such as, vitamins, minerals, phytochemicals ent utilization, which is reflected in improved weight but low in anti-nutrients content, indicating that it could gain, specific growth rate, feed intake, feed conversion be used as supplements in feed manufacturing (Adesuyi ratio, and protein efficiency ratio. In general, relatively et al. 2012; Mazi et al. 2013; Onyekwelu et al. 2015). high feed conversion ratio values were obtained in all According to Onyekwelu et al. (2015), the low anti- treatments, but the best occurred in fish fed with 60 g nutrients content in G. kola indicates that its consump- −1 kg G. kola seed meal inclusion even though differences tion would not pose nutritional or health problems. Moreover, the low protein content observed in the G. kola seeds can be indicative that the growth response observed in fish fed with G. kola supplemented diet might not be attributed to its nutritional value but mostly to its bioactive compounds. Diab et al. (2008) re- ported that O. niloticus fingerlings fed with medicinal plants supplemented diets exhibited faster growth than those fed with the control diet. According to Kim et al. (1998) unknown factors in various medicinal herbs might lead to favorable results in fish growth trials. Phy- tochemicals such as phenolic compounds and flavonoids are known as non-nutritive plant chemicals that have protective or disease preventive properties. They are present naturally in seeds, flowers, fruits, vegetables, nuts, and bark of a variety of plants that interplay with nutrients and dietary fiber to protect them (Mazur, Fig. 2 Mean weight of male and female Oreochromis niloticus fed 2000). Phytochemicals analysis of G. kola seeds revealed Garcinia kola during 70 days. Different letters indicate significant the presence of phenols and flavonoids in appreciable differences at p < 0.05 amounts (Onyekwelu et al. 2015). It has been established Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 6 of 8 Fig. 3 Hepatosomatic index (a) and gonadosomatic index (b) of male and female Oreochromis niloticus fed Garcinia kola after 70 days. Different letters indicate significant differences at p < 0.05 that phenols and flavonoids possess many properties maturity at a later age and at a higher weight than that which makes them vital to both plants and animals. raised in culture ponds. For instance, it is established Some of these properties are their antioxidant potential that in several natural lakes in East Africa, O. niloticus that protects cells against oxidative damage, anti- matures at about 10 to 12 months at a size of 350 to microbial properties, and physiological activities. Sim 500 g. The same population in farm or culture ponds, and Nurestri, 2010) also reported that fruits with high under conditions of near-maximum growth, will reach phenolic contents generally show stronger antioxidant sexual maturity at an age of 5 to 6 months and 150 to activities. Thus, the results of the present findings may 200 g (Popma and Lovshin, 1995). Under poor condi- be due to the presence of bioflavonoids in G. kola that tions of rural fish breeding, farmed tilapias often reach would have stimulated growth in both the males and fe- sexual maturity in 3 to 6 months at a size of 15–20 g and males’ experimental O. niloticus juveniles, certainly by spawn before they reach marketable size (Mair and Lit- improving feed intake and feed utilization. In addition, tle, 1991). The results of this study showed that all the bioflavonoids are known as plant chemicals with estro- fish presented a size above 20 g with the highest size genic activity, and studies have shown that estrogen pro- above 35 g in both males and females O. niloticus fed motes growth in common carp (Kocour et al. 2005). As with G. kola at 6% inclusion rate in the diet. Accord- aforementioned above, phytochemical studies of Garci- ingly, the fish used in the present study would have nia kola seeds have revealed relatively low levels of anti- reached their first sexual maturity. Results on GSI and nutritional compounds such as tannin, oxalate, phytate, HSI in males revealed no statistically significant changes and trypsin inhibitor (Omeh et al. 2014, Dah- between treatments; while in females, the GSI and HSI Nouvlessounon et al. 2015). However, the increase in indices of the experimental groups were significantly dietary supplementation of G. kola is naturally followed lower than those obtained in normal females. Similar re- by that of the above-mentioned anti-nutritional compo- sults were also obtained by Kareem et al. (2016) during nents. Thus, the low growth in O. niloticus juveniles fed their study on the effects of some dietary crude plant ex- with dietary supplementation of G. kola seeds at 10% tracts on the growth and gonadal maturity of Nile tilapia compared to that at 6% might be probably attributed to (Oreochromis niloticus) and their resistance to Strepto- the increased in anti-nutritional components level in the coccus agalactiae infection and by Ramírez et al. (2017) diet, which would have reduced the secretion of bile and while studying the effect of Passiflora incarnata (L) ex- the activity of digestive enzymes as describe by Kaur and tract on gonadal maturation in young Tilapia (Oreochro- Shah (2017). mis sp). This could indicate that dietary inclusion of G. The first sexual maturity in fish is strongly related to kola seeds powder in addition to its effects as growth size. According to Gnoumou et al. (2018), size at first promoter in both males and females’ Oreochromis niloti- sexual maturity in O. niloticus depends on the environ- cus, might also exert its physiological effects on the fe- mental conditions in which the fish grows. Thus, when male’s reproductive system by delaying or inhibiting conditions are favorable, the size at first maturity in- gonadal maturation. As it is known, early sexual matur- creases while it decreases when conditions are unfavor- ity in Tilapia culture is a well-recognized problem which able. Under natural conditions, tilapia reaches sexual results in inbreeding in overstocked fish ponds, reduced Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 7 of 8 production, and farmed stocks of generally low quality throughout the study, coupled with experimental fish’sap- (Kumar et al. 2018). The low value of the gonadosomatic parent good health observed through the results on both index obtained in O. niloticus females fed G. kola supple- the growth and feed utilization. mentation compared to the control group indicates a slowing of the development of the ovaries whose conse- Conclusion quence would be a delay in sexual maturity. This shows The results of this study show that supplementation of G. that the use of G. kola as a feed additive would be benefi- kola seeds powder at 6% in diets of Oreochromis niloticus cial to the Tilapia farmer. This could help to reduce the juveniles induced the best effect on growth performances. production cost and even the time the fish farmer use dur- However, on the gonadal development, dietary supple- ing pond management. These effects might be related mentation of G. kola irrespective to the level of inclusion, once more to the presence of bioactive compounds such highly inhibited gonadal development in Oreochromis as flavonoids, known as one of the main classes of phy- niloticus females; suggesting that for a sustainable devel- toestrogens present in a variety of plants (Mazur, 2000). opment in Tilapia culture, G. kola seeds could be used as According to Patisaul and Jefferson (2010), the US Envir- growth-promoting agent and also control prolific breeding onmental Protection Agency (EPA) described “phytoestro- through its capacity to inhibit ovary development. gens as naturally occurring plant compounds that are Acknowledgements structurally and/or functionally similar to mammalian es- The authors sincerely thank Mr. Nkamegni Noupeu Roger, manager of a trogens and their active metabolites.” These compounds private fish farm in Bomabom Village, Cameroon, for providing the technical infrastructure to carry out this study. have the capacity to alter the structure or function(s) of the endocrine system and cause adverse effects including Authors’ contributions the timing of puberty, capacity to produce viable and fer- PN contributed to the study design, data analysis, and writing of the manuscript. JA contributed to the study design and sample collection. NPN tile offspring, sex-specific behavior, premature reproduct- drafted the manuscript. METT helped in the study design. All authors ive senescence, and compromise fertility. According to reviewed, edited, and approved the manuscript for submission. Cheshenko et al. (2008), phytoestrogens might act by inhi- Funding biting steroidogenic enzymes through competitive inhib- This work did not receive any grant. It was funded by the authors of the ition with natural substrates for a particular enzyme. They manuscript. are also able not only to bind to respective receptors, but Availability of data and materials also to directly interact with aromatase CYP19, possibly All datasets generated during and/or analyzed during the current study are leading to inhibition of this enzyme involved in the syn- available from the authors on reasonable request. thesis of 17ß-estradiol, thereby affecting reproductive Ethics approval and consent to participate health of the fish. Not applicable Oreochromis niloticus being one of the famous species reared in Cameroon, its growth, metabolism, and Consent for publication Not applicable reproduction are greatly influenced by the water quality parameters of the culture environment. Water quality is Competing interests the most important limiting factor in pond fish produc- The authors declare that they have no competing interests. tion as its quality directly affects feed efficiency, growth Author details rates, the fish’s health, and survival, as well as the fish re- 1 The University of Douala, Institute of Fisheries and Aquatic Sciences of productive cycle. Any changes in the fish environment Yabassi, P.O. Box: 7236, Douala, Cameroon. College of Technology, The University of Bamenda, P.O. Box 39, Bambili, Bamenda, Cameroon. add stress to the fish and the higher and faster the changes, the greater the stress. So, the maintenance of the Received: 23 January 2019 Accepted: 4 September 2019 physico-chemical parameters within the acceptable limits are very essential for getting maximum yield in a fish pond References (Bhatnagar and Dev, 2013). The water quality parameters Adeniji AR, Osifeso OO, Abiodun W, Yusuff KO, Agidigbi OR. 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Effect of Garcinia kola seeds supplemented diet on growth performance and gonadal development of Oreochromis niloticus juveniles breed in ponds

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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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Abstract

Background: Despite the favorable geo-climatic potential of Cameroon, the national production of tilapia remains low due to poor tilapia growth reported by fish farmers. One of the underlying reasons is the early female maturation at a very small size and precocious breeding in earthen ponds, resulting in overpopulation which leads to stunted growth and therefore to the production of unmarketable fish size. Studies have shown that dietary supplementation of G. kola enhanced growth in young Clarias gariepinus and Oreochromis niloticus. It was also reported that G. kola inhibited spawning in Tilapia adult females. Therefore, this study sought to assess the effects of Garcinia kola as growth promoter and inhibitor of gonadal development in young Oreochromis niloticus. Methods: A total of 108 juveniles weighing 13.32 ± 0.62 g were randomly distributed in 9 hapas of 12 fishes each (9 females and 3 males) and fed for 70 days with three isonitrogenous diets, 40% crude protein with increasing Garcinia kola supplementation levels of 0 (normal diet), 6% and 10% (experimental diets). Physico-chemical parameters of the water (temperature, dissolved oxygen, pH, nitrate, nitrite, ammonia, and transparency) were measured twice a week. Every 14 days, fish were harvested, counted, and weighed. At the end of the experiment, three fish of each sex per replicate were sacrificed and their gonad and liver collected and weighed. Data were statistically analyzed using one- way analysis of variance repeated measure followed by Newman-Keuls multiple tests. Results: The results showed that all physico-chemical parameters of the water were within the recommended values for Tilapia culture. Tilapia fed 6% Garcinia kola supplemented diet displayed higher final body weight in males (38.60 ± 3.50 g) and females (36.77 ± 3.62 g) compared to those receiving normal diet (36.23 ± 1.36 g and 25.87 ± 3.32 g; respectively to the final body weight in males and females). The gonadosomatic index and hepatosomatic index indicated no significant variation in males while in females, these were significantly low in the experimental fish compared to control fish. Conclusion: The results of this study demonstrated that supplementation of G. kola seeds in diets of young Tilapia improved growth performance and impaired gonadal development in females. Keywords: Oreochromis niloticus, Garcinia kola, Growth, Gonad development * Correspondence: epauka@yahoo.fr The University of Douala, Institute of Fisheries and Aquatic Sciences of Yabassi, P.O. Box: 7236, Douala, Cameroon Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 2 of 8 Background niloticus adult females; while in Tilapia fry, it was demon- In Africa, particularly in Cameroon, fish food represents strated that supplementation of G. kola can induce sex the primary source of animal protein. It offers better types conversion (Sulem-Yong et al. 2018;Tigoliet al. 2018). To of essential minerals, amino acids and is low in undesir- our knowledge, this study is the first on the effect of diet- able saturated fats (Hussain, 1986). To cope up with nutri- ary inclusion of G. kola on gonadal development in non- tional requirements of increasing population, aquaculture puber Oreochromis niloticus. Therefore, the present work is considered as the only possible solution to increase fish was undertaken to evaluate the effect of dietary supple- production. Tilapia being an important food fish world- mentation of Garcinia kola seed powder on growth per- wide, significant developments have been recorded during formances and gonadal development of Oreochromis the last three decades in its farming. About 85 countries niloticus juveniles. worldwide are involved in fish farming and about 98% of tilapia produced there are grown outside their original Methods habitats (Shelton, 2002). It provides one of the most im- Collection and acclimation of experimental fish portant sources of animal protein and income throughout The experiment was carried out in a small-scale private the world (Sosa et al. 2005). In some African countries farm located at Bomabom (LN: 3°41′0″–°46′30″ and LE: such as in Egypt, the culture of Nile tilapia (Oreochromis 1°7′30″–11°13′0″) in the central region of Cameroon. A niloticus) has increased dramatically in the last few years; total of 108 juveniles of Oreochromis niloticus were used; while in Cameroon the global production remains insig- each weighing 13.32 ± 0.62 g with an average length of nificant despite the natural potential of the country. One 8.76 ± 0.41 cm. They were randomly distributed in tripli- of the major drawbacks to tilapia culture is the early cate into 9 hapas (made up of mosquito net cloth with size female maturation at very small size (15–30 g) (Mair and 1′ ×1′ ×0.5′) of 12 juveniles each (9 females and 3 males). Little, 1991; Popma and Lovshin, 1995), and precocious The hapas suspended in an earthen pond (800 m )with breeding in earthen ponds resulting in overpopulation the help of four bamboo poles, one at each corner of the which often leads to stunted growth. Mair and Little cage. The hapas were suspended in the pond such that (1991) enumerated various methods and techniques avail- three-quarters of each hapa was submerged in water able for the control of prolific breeding in tilapia. How- whereas one-quarter remained outside. The roof of the ever, each technique or method has its own limitations. hapas was covered with mesh to stop the experimental Monosex culture of all-male populations, which exhibits fish from jumping out and to prevent natural predators faster growth rates and which is usually produced through (snakes, kingfishers, frogs) from getting in. The fish were androgenous hormone sex reversal, is the preferred op- then allowed to acclimatize for 4 days prior to the experi- tion, and is used extensively in the countries that produce ment. During the acclimation, the fish were fed with nor- large numbers of tilapia like China (Phelps, 2006). Consid- mal diet. ering the problem associated with the use of androgenous hormonal treatment, such as environmental and public Experimental diet formulation and preparation health concerns and the limitations of existing methods A balanced dietary ration formula was prepared to meet and techniques documented by Mair and Little (1991), the nutritional requirements of Nile tilapia according to there is a need to explore other technologies to control NRC (2011) (Table 1). Three isonitrogenous diets were undesirable tilapia recruitment in ponds using natural prepared: an unenriched control diet plus two test diets. reproduction inhibitors found in plants to enhance better The test diets were supplemented with 6% and 10% Gar- growth and improved flesh (Jegede, 2010). Garcinia kola cinia kola at the expense of maize meal. In preparing ex- commonly called Bitter kola belongs to the family Clusia- perimental diets, the dried ingredients were ground into ceae. It is a multipurpose tree indigenous to West and fine particles. After weighing and mixing manually for Central Africa (Manourová et al. 2019). The seed of G. 10 min, the preparations were moistened with warm −1 kola is traditionally served to visitors for entertainment; it water (400 ml kg ) and mixed for another 20 min. Dur- is also chewed by men as an aphrodisiac or used to pre- ing the mixing, palm oil was added slowly along with vent or relieve colic disorders or cure head or suppressed warm water to achieve a proper consistency. The result- cough (Madubunyi, 2010). Previous studies on rats and ing mixture was then passed through a meat extruder to poultry have shown that inclusion of G. kola seeds in pow- obtain a 2-mm pellet. The “spaghetti-like” strands were der and methanolic extracts form improved their growth sun-dried and stored in airtight containers prior to use. performance (Oluyemi et al. 2007). Moreover, studies on The chemical composition of the test diets was analyzed Oreochromis niloticus have shown that dietary supplemen- by standard methods (AOAC, 1990). Moisture was ana- tation of G. kola seeds powder promotes the growth per- lyzed by drying the sample in an air convection oven at formance. It was also shown that dietary supplementation 105 °C overnight. Crude protein was analyzed by the of G. kola seeds powder inhibits spawning in Oreochromis Kjeldahl method after acid digestion (% crude protein = Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 3 of 8 Table 1 Formulations and proximate composition of and 10%, respectively. Fish were hand-fed four times per experimental diets (g/100 g dry weight) day (08:00 a.m., 11:00 a.m., 14:00 p.m. and 17:00 p.m. re- Ingredients Normal Normal diets Normal diets spectively) at a rate of 5% of their body weight per day. diet + G. kola (6%) + G. kola 10% Feeding rates were adjusted every 14 days for 70 days Fish meal 26 26 26 based on the weight gain of each group of fish per 14 days. Garcinia kola meal // 6 10 Physico-chemical parameters of the water in each hapa such as temperature was measured using a maximum- Soybean cake 23 23 23 minimum thermometer; dissolved oxygen (O ) was deter- Cottonseed cake 22 22 22 mined using JBL Test Kits, pH, nitrate (NO ), nitrite Maize meal 10 4 0 (NO ), and ammonia (NH ) were measured twice a week 2 3 Wheat bran 10 10 10 before feeding using test strips (JBL Easy Test 6in1) while Palm oil 4 4 4 transparency was monitored using a Secchi disk (Table 2). Premix 5 5 5 Data collection Total 100 100 100 Growth performances, feed utilization, and somatic indi- Proximate composition (%) ces were assessed by determination of weight gain Protein 40.47 40.03 39.73 (WG), specific growth rate (SGR), feed intake (FI), con- Lipid 13.23 13.14 13.12 dition factor (K), feed conversion ratio (FCR), protein ef- Ash 12.75 12.71 12.68 ficiency ratio (PER), survival rate (SR), hepatosomatic Moisture 7.74 8.04 7.94 index (HSI), and gonadosomatic index (GSI). Calcula- tions were carried out using the following formulae: Dry matter 92.26 91.96 92.06 weight gain (g) = final weight–initial weight; specific Energy (kcal/100 g) 420.63 418.17 417.20 growth rate (%/day) = 100 (lnW2–lnW1)/T, where W1 and W2 are the initial and final weight, respectively, and % nitrogen × 6.25) while crude lipid was determined by T is the number of days in the experimental period; sur- extraction with petroleum ether using the Soxhlet vival rate (%) = final number of fish × 100/initial number method. The ash content in the diet was analyzed by of fish; condition factor = 100 (weight/length ); feed in- combustion of samples in a muffle furnace at 550 °C for take = total dry feed/number of fish; feed conversion ra- 12 h (Table 1). tio (FCR) = feed intake/live weight gain; protein efficiency ratio (PER) = live weight gain/protein fed, Experimental design where protein fed = % protein in diet × total diet con- Mixed-sex Nile tilapia O. niloticus were used in the feed- sumed/100; HSI = 100 (liver weight/body weight); GSI = ing trial. At the initiation of the experiment, individual 100 (gonad weight/body weight). weight and length of all fishes per treatment were mea- sured for determination of both initial weight and length. Statistical analysis The acclimatized juveniles were randomly distributed in All results were expressed as mean ± SD. Data were sta- three replicates in 9 hapas each at a stocking density of 12 tistically analyzed using one-way analysis of variance fish per hapas (9 females and three males). In the first trip- (ANOVA-1) repeated measure followed by Newman- licate, fish were fed with normal diet to serve as controls Keuls multiple tests with n = 3 replicates. Differences while in the second and third triplicates, they were fed were considered significant when P < 0.05. All statistics with the Garcinia kola supplemented diet at rates of 6% were carried out using GraphPad Prism version 6.0. Table 2 water quality parameters (Mean ± SD) during 70 days of the experimental period Parameters Rearing period (daRearing period (days) 0 1428 4256 70 Temperature (°C) 28.10 ± 0.35 28.10 ± 1.10 28.71 ± 0.70 28.1 ± 0.80 28.71 ± 0.70 27.96 ± 0.70 Dissolved oxygen (mg/l) 5.56 ± 0.25 5.46 ± 0.35 5.56 ± 0.32 5.55 ± 0.28 5.55 ± 0.38 5.55 ± 0.37 pH 7.20 ± 0.03 7.34 ± 0.10 7.35 ± 0.10 7.36 ± 0.10 7.22 ± 0.20 7.17 ± 0.20 Transparency (cm) 36.60 ± 4.44 36.61 ± 3.70 37.23 ± 3.40 37.23 ± 4.00 38.85 ± 4.10 36.28 ± 2.20 Ammonia (mg/l) 0.58 ± 0.02 0.50 ± 0.05 0.50 ± 0.05 0.50 ± 0.00 0.50 ± 0.08 0.50 ± 0.02 Nitrite (mg/l) 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 0.03 ± 0.00 Nitrate (mg/l) 0.12 ± 0.01 0.12 ± 0.01 0.12 ± 0.02 0.12 ± 0.05 0.12 ± 0.05 0.12 ± 0.05 Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 4 of 8 Results Body weights and organs measurements of sexually Growth performances mature Oreochromis niloticus Growth performances of O. niloticus juveniles fed The average body weights, hepatosomatic index, and with different diet in terms of weight gain and gonadosomatic index per treatments in both males and specific growth rate are presented in Fig. 1.The females were computed and were presented in Figs. 2 weight gain recorded during fish sampling showed an and 3. In males, the mean values of body weight (Fig. 2), increase with respect to time but not according to hepatosomatic index (Fig. 3a), and gonadosomatic index the G. kola supplementation rate (Fig. 1a). Feed sup- (Fig. 3b) among the different groups were not signifi- plemented with G. kola at 6% induced in O. niloticus cantly different. After 70 days of experiment, the mean juveniles the highest values of weight gain as from body weights of 36.77 ± 3.62 g obtained in females fed the fourteenth day of the experiment up to the end. with 6% G. kola supplemented diet was significantly (p < At the end of sampling, fish fed with diet supple- 0.05) high compared to the control group (25.87 ± 3.32 mented with 6% of G. kola presented a weight gain g) and groups fed with 10% G. kola supplemented diet of 19.46 ± 1.31 g, which was significantly (p <0.05) (26.33 ± 3.34 g) (Fig. 2). Moreover, feeding the female O. higher by 17.68% and 32.58% compared to that in niloticus with a diet supplemented with G. kola signifi- fish fed with the normal diet (16.02 ± 1.55 g) and diet cantly (p < 0.05) decreased both hepatosomatic index supplemented with 10% G. kola (13.12 ± 1.58 g) re- and gonadosomatic index compared to the control spectively (Fig. 1a). Observation on specific growth group (Fig. 3a, b). rate showed significant (p < 0.05) increase in fish re- ceiving a diet containing G. kola at 6% compared to Discussion fish fed with both the normal diet and diet supple- Fish is one of the most appreciated foodstuff worldwide mented with 10% G. kola during the first two rearing and particularly in most of the African countries like periods (Fig. 1b). Cameroon. However, despite the increase in production of cultured fish from some countries, production from some other countries including Cameroon has not im- Survival and feeding efficiency proved yet; statistics show that the supply of fish in The results presented in Table 3 illustrate the survival Cameroon comes to 43% of fishing (22% of inland fish- rate and feeding efficiency in term of condition factor, eries, 21% of sea fisheries), 56.8% of imports and only feed intake, protein intake, feed conversion ratio, and 0.1% of fish farming, that is 1000 t/year (FAO, 2009; protein efficiency ratio on the 70th day of the experi- Ndah et al. 2011). One of the reasons for low aquacul- ment. No mortality was recorded during the culture ture production has been attributed to feeding quality. period. Similarly, no significant variation in condition Research is currently focused on improving the quality factor and feed conversion ratio was observed among of fish feed through replacement or addition of appro- the different groups during the study. However, for priate ingredients that encourage faster fish growth. the feed intake, Protein intake and Protein efficiency, Tropical forests contain many tree species that have sup- significant differences were obtained only in fish fed plied edible fruits for centuries. It has been previously diet supplemented with G. kola at 6% compared to reported in many research works that different plant that receiving diet supplemented with G. kola at 10%. additives can enhance growth in some fish species such Fig. 1 Effects of diet supplementation with Garcinia kola seeds on mean weight gain (a) and specific growth rate (b)of Oreochromis niloticus juveniles. Mean on the same rearing period carrying the same superscript are not significantly different at p < 0.05 Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 5 of 8 Table 3 Survival and feed utilization of Oreochromis niloticus juveniles fed with different quantities of Garcinia kola supplemented diets for 70 days Parameter Normal diet Normal diet + G. kola (6%) Normal diet + G. kola (10%) Initial number 36 36 36 Final number 36 36 36 a a a Survival rate (%) 100 100 100 Initial biomass (g) 159.86 ± 8.71 158.15 ± 6.87 161.72 ± 16.94 Final biomass (g) 352.13 ± 27.28 391.63 ± 13.66 319.18 ± 16.94 Initial weight (g) 13.32 ± 0.72 13.18 ± 0.57 13.48 ± 0.78 Final weight (g) 29.34 ± 2.27 32.64 ± 1.13 26.60 ± 1.41 Final length (cm) 11.35 ± 0.41 12.35 ± 0.10 11.30 ± 0.19 a a a Condition factor 2.00 ± 0.10 1.73 ± 0.04 1.84 ± 0.03 ab a b Feed intake (g/fish) 69.94 ± 4.68 73.81 ± 2.60 63.35 ± 2.68 ab a b Protein intake (g/fish) 28.00 ± 1.08 29.56 ± 0.60 25.37 ± 0.62 a a a Feed conversion ratio 4.39 ± 0.30 3.80 ± 0.10 4.87 ± 0.37 ab a b Protein efficiency ratio 0.57 ± 0.03 0.66 ± 0.01 0.52 ± 0.04 Values are mean ± standard deviation of 3 replications containing 12 fish per replicate. Values on the same row carrying the same letter are not significantly different at p < 0.05 as Oreochromis niloticus (Kareem et al. 2016, Hassan et among the treatment means were not significant. Previ- al. 2018). Results from the present study indicate that ous studies revealed that G. kola seed powder supple- there was an increase in the growth of the fish fed with mented in animal diets also promoted growth and feed different rate of dietary supplementation with G. kola conversion efficiency in Clarias gariepinus juveniles seed. However, the highest growth response was ob- (Adeniji et al. 2018)and Oreochromis niloticus adults served in the fish fed with G. kola seed supplemented (Sulem-Yong et al. 2018). The proximate and phyto- −1 meal at a level of 60 g kg , indicating that the G. kola chemicals analysis of G. kola seeds revealed that it is rich seed meal supplementation could have enhanced nutri- in nutrients such as, vitamins, minerals, phytochemicals ent utilization, which is reflected in improved weight but low in anti-nutrients content, indicating that it could gain, specific growth rate, feed intake, feed conversion be used as supplements in feed manufacturing (Adesuyi ratio, and protein efficiency ratio. In general, relatively et al. 2012; Mazi et al. 2013; Onyekwelu et al. 2015). high feed conversion ratio values were obtained in all According to Onyekwelu et al. (2015), the low anti- treatments, but the best occurred in fish fed with 60 g nutrients content in G. kola indicates that its consump- −1 kg G. kola seed meal inclusion even though differences tion would not pose nutritional or health problems. Moreover, the low protein content observed in the G. kola seeds can be indicative that the growth response observed in fish fed with G. kola supplemented diet might not be attributed to its nutritional value but mostly to its bioactive compounds. Diab et al. (2008) re- ported that O. niloticus fingerlings fed with medicinal plants supplemented diets exhibited faster growth than those fed with the control diet. According to Kim et al. (1998) unknown factors in various medicinal herbs might lead to favorable results in fish growth trials. Phy- tochemicals such as phenolic compounds and flavonoids are known as non-nutritive plant chemicals that have protective or disease preventive properties. They are present naturally in seeds, flowers, fruits, vegetables, nuts, and bark of a variety of plants that interplay with nutrients and dietary fiber to protect them (Mazur, Fig. 2 Mean weight of male and female Oreochromis niloticus fed 2000). Phytochemicals analysis of G. kola seeds revealed Garcinia kola during 70 days. Different letters indicate significant the presence of phenols and flavonoids in appreciable differences at p < 0.05 amounts (Onyekwelu et al. 2015). It has been established Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 6 of 8 Fig. 3 Hepatosomatic index (a) and gonadosomatic index (b) of male and female Oreochromis niloticus fed Garcinia kola after 70 days. Different letters indicate significant differences at p < 0.05 that phenols and flavonoids possess many properties maturity at a later age and at a higher weight than that which makes them vital to both plants and animals. raised in culture ponds. For instance, it is established Some of these properties are their antioxidant potential that in several natural lakes in East Africa, O. niloticus that protects cells against oxidative damage, anti- matures at about 10 to 12 months at a size of 350 to microbial properties, and physiological activities. Sim 500 g. The same population in farm or culture ponds, and Nurestri, 2010) also reported that fruits with high under conditions of near-maximum growth, will reach phenolic contents generally show stronger antioxidant sexual maturity at an age of 5 to 6 months and 150 to activities. Thus, the results of the present findings may 200 g (Popma and Lovshin, 1995). Under poor condi- be due to the presence of bioflavonoids in G. kola that tions of rural fish breeding, farmed tilapias often reach would have stimulated growth in both the males and fe- sexual maturity in 3 to 6 months at a size of 15–20 g and males’ experimental O. niloticus juveniles, certainly by spawn before they reach marketable size (Mair and Lit- improving feed intake and feed utilization. In addition, tle, 1991). The results of this study showed that all the bioflavonoids are known as plant chemicals with estro- fish presented a size above 20 g with the highest size genic activity, and studies have shown that estrogen pro- above 35 g in both males and females O. niloticus fed motes growth in common carp (Kocour et al. 2005). As with G. kola at 6% inclusion rate in the diet. Accord- aforementioned above, phytochemical studies of Garci- ingly, the fish used in the present study would have nia kola seeds have revealed relatively low levels of anti- reached their first sexual maturity. Results on GSI and nutritional compounds such as tannin, oxalate, phytate, HSI in males revealed no statistically significant changes and trypsin inhibitor (Omeh et al. 2014, Dah- between treatments; while in females, the GSI and HSI Nouvlessounon et al. 2015). However, the increase in indices of the experimental groups were significantly dietary supplementation of G. kola is naturally followed lower than those obtained in normal females. Similar re- by that of the above-mentioned anti-nutritional compo- sults were also obtained by Kareem et al. (2016) during nents. Thus, the low growth in O. niloticus juveniles fed their study on the effects of some dietary crude plant ex- with dietary supplementation of G. kola seeds at 10% tracts on the growth and gonadal maturity of Nile tilapia compared to that at 6% might be probably attributed to (Oreochromis niloticus) and their resistance to Strepto- the increased in anti-nutritional components level in the coccus agalactiae infection and by Ramírez et al. (2017) diet, which would have reduced the secretion of bile and while studying the effect of Passiflora incarnata (L) ex- the activity of digestive enzymes as describe by Kaur and tract on gonadal maturation in young Tilapia (Oreochro- Shah (2017). mis sp). This could indicate that dietary inclusion of G. The first sexual maturity in fish is strongly related to kola seeds powder in addition to its effects as growth size. According to Gnoumou et al. (2018), size at first promoter in both males and females’ Oreochromis niloti- sexual maturity in O. niloticus depends on the environ- cus, might also exert its physiological effects on the fe- mental conditions in which the fish grows. Thus, when male’s reproductive system by delaying or inhibiting conditions are favorable, the size at first maturity in- gonadal maturation. As it is known, early sexual matur- creases while it decreases when conditions are unfavor- ity in Tilapia culture is a well-recognized problem which able. Under natural conditions, tilapia reaches sexual results in inbreeding in overstocked fish ponds, reduced Nyadjeu et al. Fisheries and Aquatic Sciences (2019) 22:20 Page 7 of 8 production, and farmed stocks of generally low quality throughout the study, coupled with experimental fish’sap- (Kumar et al. 2018). The low value of the gonadosomatic parent good health observed through the results on both index obtained in O. niloticus females fed G. kola supple- the growth and feed utilization. mentation compared to the control group indicates a slowing of the development of the ovaries whose conse- Conclusion quence would be a delay in sexual maturity. This shows The results of this study show that supplementation of G. that the use of G. kola as a feed additive would be benefi- kola seeds powder at 6% in diets of Oreochromis niloticus cial to the Tilapia farmer. This could help to reduce the juveniles induced the best effect on growth performances. production cost and even the time the fish farmer use dur- However, on the gonadal development, dietary supple- ing pond management. These effects might be related mentation of G. kola irrespective to the level of inclusion, once more to the presence of bioactive compounds such highly inhibited gonadal development in Oreochromis as flavonoids, known as one of the main classes of phy- niloticus females; suggesting that for a sustainable devel- toestrogens present in a variety of plants (Mazur, 2000). opment in Tilapia culture, G. kola seeds could be used as According to Patisaul and Jefferson (2010), the US Envir- growth-promoting agent and also control prolific breeding onmental Protection Agency (EPA) described “phytoestro- through its capacity to inhibit ovary development. gens as naturally occurring plant compounds that are Acknowledgements structurally and/or functionally similar to mammalian es- The authors sincerely thank Mr. Nkamegni Noupeu Roger, manager of a trogens and their active metabolites.” These compounds private fish farm in Bomabom Village, Cameroon, for providing the technical infrastructure to carry out this study. have the capacity to alter the structure or function(s) of the endocrine system and cause adverse effects including Authors’ contributions the timing of puberty, capacity to produce viable and fer- PN contributed to the study design, data analysis, and writing of the manuscript. JA contributed to the study design and sample collection. NPN tile offspring, sex-specific behavior, premature reproduct- drafted the manuscript. METT helped in the study design. All authors ive senescence, and compromise fertility. According to reviewed, edited, and approved the manuscript for submission. Cheshenko et al. (2008), phytoestrogens might act by inhi- Funding biting steroidogenic enzymes through competitive inhib- This work did not receive any grant. It was funded by the authors of the ition with natural substrates for a particular enzyme. They manuscript. are also able not only to bind to respective receptors, but Availability of data and materials also to directly interact with aromatase CYP19, possibly All datasets generated during and/or analyzed during the current study are leading to inhibition of this enzyme involved in the syn- available from the authors on reasonable request. thesis of 17ß-estradiol, thereby affecting reproductive Ethics approval and consent to participate health of the fish. Not applicable Oreochromis niloticus being one of the famous species reared in Cameroon, its growth, metabolism, and Consent for publication Not applicable reproduction are greatly influenced by the water quality parameters of the culture environment. Water quality is Competing interests the most important limiting factor in pond fish produc- The authors declare that they have no competing interests. tion as its quality directly affects feed efficiency, growth Author details rates, the fish’s health, and survival, as well as the fish re- 1 The University of Douala, Institute of Fisheries and Aquatic Sciences of productive cycle. Any changes in the fish environment Yabassi, P.O. Box: 7236, Douala, Cameroon. College of Technology, The University of Bamenda, P.O. Box 39, Bambili, Bamenda, Cameroon. add stress to the fish and the higher and faster the changes, the greater the stress. So, the maintenance of the Received: 23 January 2019 Accepted: 4 September 2019 physico-chemical parameters within the acceptable limits are very essential for getting maximum yield in a fish pond References (Bhatnagar and Dev, 2013). The water quality parameters Adeniji AR, Osifeso OO, Abiodun W, Yusuff KO, Agidigbi OR. 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