Effectiveness of Sargassum Meal As Feed Additive on Growth Performance of Nile Tilapia, Oreochromis Niloticus

Aquacult. Sci. 66（1），25－31（2018）

Effectiveness of Sargassum meal as feed additive on growth performance of Nile tilapia, Oreochromis niloticus

1,2 1,＊ 3 Fittrie Meyllianawaty PRATIWY , Jun KOHBARA and A. B. SUSANTO

Abstract: The present work was carried out to assess the effects of Sargassum meal (SM) on the growth performance of Nile tilapia Oreochromis niloticus. Three different 32% iso-proteinous diets were prepared by replacing rice bran with inclusion of SM of 0% (T1), 4% (T2), and 8% (T3) and fed to replicate trials of individual males, individual females, and mixed sex tilapia. The results showed that the highest values of feed efficiency (FE) and specific growth rate (SGR) in each rearing condition were observed in T3. There were significant differences (P < 0.05) of FE and SGR for the individual male and mixed sex experiment trials between T1 and T3, however, there were no significant differences for individual female trials. The results of the length-weight relationship showed that there were significant differences (P < 0.05) between individual males and individual females according to the condition factor which showed a positive allometric (b > 3) exponential growth in individual males, while the individual female trials showed a negative allometric (b < 3) growth pattern at each level of SM inclusion. It is concluded that 8% SM produced the best results for growth performance in Nile tilapia.

Key words: Nile tilapia; Sargassum; Feed additive; Growth

Recently, seaweeds have been recognized as disease resistance. For example, the enhance- a good resource of minerals, vitamins, carbo- ment of growth performance by dietary sup- hydrates and some amino-acids (Dawczynski plementation with algae was reported in red et al. 2007; Kendel et al. 2015). In addition, sea bream Pagrus major (Yone et al. 1986), seaweeds have got attention not only as food Japanese flounder Paralichthys olivaceus (Xu et resources with benefits for human health but al. 1993; Ragaza at al. 2013) and rainbow trout also as additives for diets of domestic animals Oncorhynchus mykiss (Sommer et al. 1992). including culture fish and aquatic inverte- Sargassum is a brown seaweed genus in the brates. For example, it has been reported that class Phaeophyceae, which grows abundantly seaweeds contain effective radical scavengers, in coastal sea areas all over the world from inhibitors of lipid peroxidation and to be capa- temperate to tropical regions (Zemke-White ble of enhancing immune response and disease and Ohno 1999). In Indonesia, species of this resistance for giant tiger prawn Penaeus mono- genus are found growing along Indonesian don (Immanuel et al. 2012). In the case of fish, coasts. Therefore, it can be anticipated that the seaweeds are also receiving more attention for addition of Sargassum to fish diets may enhance use in intensive aquaculture due to their effects the growth or health condition of culture fish of improvement of growth, lipid metabolism and enabling the effective utilization of this seaweed

Received 28 August 2017; Accepted 15 January 2018. 1 Laboratory of Fish Physiology, Graduate School of Bioresources, Mie University, Tsu, Mie 514-8507, Japan. 2 Graduate Program of Environmental Studies, Universitas Padjadjaran, Bandung 40132, Indonesia. 3 Faculty of Fisheries and Marine Science, Diponegoro University, Semarang, 50275, Indonesia. ＊Corresponding author: Tel, (+81)59-231-9534; Fax, (+81)59-231-9540; E-mail, [email protected] (J. Kohbara). 26 F. M. Pratiwy, J. Kohbara and A. B. Susanto in Indonesia. content as an ordinary supplemental ingredi- Nile tilapia (Oreochromis niloticus) is one of ent for Nile tilapia feeds. Each experimental the most important aquaculture species espe- diet was mixed and shaped as pellets of 3mm cially in South East Asia, Africa, South America in diameter and 3-4 mm in length. The shaped and China. Several species of tilapia are cul- pellets were dried at 60°C then subsequently tured commercially, Nile tilapia is the predomi- stored at 4°C until use. nant cultured species and its global production reached nearly 3,670,000 tons in 2014 (FAO Proximate analyses 2017). The gross production of Nile tilapia The proximate analyses of the finely ground increases year by year because of the strong Sargassum powder and experimental diets worldwide demand for this freshwater fish for were carried out according to procedures human consumption. In Indonesia, Nile tilapia described in the Official Methods of Analysis is also one of the most important culture fish, of AOAC International 17th edition (AOAC however the effects of inclusion of Sargassum 2003). Chemical compositions were analyzed at in tilapia diet have not been examined yet. It the Nutrition Laboratory of Faculty of Animal may enhance the growth performance since Husbandry, Padjadjaran University, analy- Nile tilapia is an omnivorous grazer which con- sis of moisture was measured by drying to a sumes plant materials in nature. The present constant weight in an oven at 105°C, analysis work aimed to investigate the effects of dried of crude protein was carried out by Kjehdahl Sargassum as a supplement in diets on growth method, analysis of lipid content was carried performance of Nile tilapia. out by Soxhlet method using extraction with petroleum ether, analysis of crude fiber was Materials and Methods measured by peroxide extraction method, and ash content was measured by mineralization of Seaweed Collection the sample at temperature 600°C for 2 hours. Sargassum spp. was collected manually from Nitrogen-free extract represents the soluble car- Tidung Island, Kepulauan Seribu, Indonesia. bohydrate of the feed, such as starch and sugar. Epiphytes were thoroughly removed from the fresh thalli, rinsed on the spot with seawater, Experimental animal and trial conditions and then placed in plastic bags. In the labora- The experimental fish, Nile tilapia tory of Aquatic Products Technology, Bogor Oreochromis niloticus were obtained from a Agricultural University, the seaweed samples substream of the Nikko River, Kanie town, were washed again with distilled water and then Aichi Prefecture, Japan. They were acclima- dried in fresh air under sunlight. They were tized for one month in an outdoor concrete ground by using a hammer mill. A sample of tank of the Experimental Fish Tank Facility 1 kg of finely ground Sargassum was used for of the Graduate School of Bioresources, Mie the experimental diets. University and they were fed with commercial diets. After being kept in an outdoor concrete Experimental diets tank, they were moved and maintained in an Three different iso-proteinous diets were pre- indoor room. They were divided into three pared with different levels of Sargassum meal types of experimental rearing condition; indi- (SM) including a diet (T1) without Sargassum vidual males, individual females, and a mixed as a control. SM was added to the formulated sex group. Prior to each experiment, they were experimental diets at 0% (T1), 4% (T2), and 8% anesthetized with 0.01% ethyl m-aminobenzoate (T3). All the feeds were formulated to meet the methansulfonate (Sigma-Aldrich) to measure 32% protein requirement. Based on an equality the initial body weight. In both individual male of percentage protein content, SM were added and female trial replicates, fish were sexed to replace rice bran which has a similar protein by visual analysis of the genital papilla. In the Effect of Sargassum on growth of Nile tilapia 27 mixed sex group trial replicates, it was diffi- Survival Rate (%) = (Total number of alive fish/ cult to differentiate sex by genital papillae, fish total number of fish)×100 were sacrificed to determine sex at the end of Feed Efficiency (%) = [50×(final mean weight the experiment. The body weight (average± －initial mean weight)×(initial number of fish SD) for the individual male trials was 78.3± + final number of fish)]/dry weight of feed 10.0 g, individual female trials was 71.4±5.1 g, delivered and the mixed sex group trials was 17.3±1.8 g. The reason that the size of the fish in the mixed Specific Growth Rate (%) = 100×[ln (final mean group trials is smaller than that of the individual weight)－ln (initial mean weight)]/days male and female experiments is because of hier- archy which specifically occurs in Nile tilapia Condition Factor (K): mean weight/total 3 whereby large fish dominate leading to a hier- length ×100 archical size structure of the population. This b W = aL : the form of a linear model where W = is the reason why the larger male and female body weight of samples in g, L = body length of trials were carried out individually since hier- the sample in cm, a = constant (intercept), b = archy may induces some negative influence on constant (slope of regression line), r = correla- the growth performance in group trials using tion coefficient. the larger size of Nile tilapia. Each trial group was separately reared in a 100 l volume poly- As the statistical analyses, all growth data ethylene cylinder tank for about three weeks. were subjected to the Wilcoxon-Mann-Whitney Males and females were reared as single fish test to determine if each parameter was signifi- per tank and the mixed group reared as 10 fish cantly different using SPSS software. per tank with variation among replicates. Each of the three experimental diets was randomly Results assigned to five different replication tanks for males, three replication tanks for females, and Proximate Analyses of Sargassum Meal two replication tanks for the mixed sex group The proximate composition of the experimen- and the rearing period ranged 24-26 days. Fish tal feeds is shown in Table 1. The total crude were hand-fed three times a day with a feeding rate of 2-3% of BW based on the results of the self-feeding experiment (Pratiwy et al. 2017). Table 1. The ingredient and proximate composition of the experimental diets (g/kg dry matter) The experimental pellets were consumed within Ingredients T1 T2 T3 a day and no food waste was observed on the Fish meal 320 320 320 bottom of the experimental tanks. Each group Soybean meal 320 320 320 was supplied with 6-7 l/min of filtered and aer- Sargassum meal 0 40 80 ated water. Temperature was monitored during Tapioca 70 70 70 the entire experiment and maintained at 26°C. Rice bran 130 90 50 Corn meal 130 130 130 At the end of the experiment, fish were weighed Fish oil 10 10 10 to obtain the final body weight. Premix1 17.5 17.5 17.5 Choline chloride 2.5 2.5 2.5 Data analysis Chemical composition The growth performance of experimental fish Crude protein 320.7 321.8 323.0 was evaluated by determining the survival rate Crude lipid 62.5 61.3 60.1 Nitrogen-free extract 446.6 441.9 437.3 (SR), feed efficiency (FE) and specific growth Ash 129.5 128.0 126.5 rate (SGR) and condition factor (K). Fish were Crude fiber 20.7 26.9 33.2 selected from each experimental tank and mea- 1Containing antibiotic (zinc bacitracin), amino acid (methionine sured after the rearing periods. The formulae and lysine), 6 essential minerals and 12 essential vitamins. Premix AQUAVITA, packed by Indosco, Co. Ltd., Surabaya, used are as follows: Indonesia. 28 F. M. Pratiwy, J. Kohbara and A. B. Susanto protein in each treatment was similar (320.7- Growth Performance and Condition Factor 323.0 g/kg dry matter) also total crude lipid The results of growth performance of Nile was within a range 60.1-62.5 g/kg dry matter. tilapia fed various levels of SM are shown in Sargassum powder meal was made from Table 3. There was no mortality recorded whole thalli of Sargassum spp. After being during the 24-26 days feeding trial. The high- ground to Sargassum powder, the proximate est SGR and FE were obtained from T3 in all analyses showed that it contained 11.77% crude rearing conditions, and SGR and FE in T2 protein, 0.21% crude lipid, and 20.33% crude were lower than those fish in T3. Specifically, fiber (Table 2). SGR and FE of male Nile tilapia in the individual rearing condition treatment ranged 1.39- Table 2. Proximate composition of Sargassum meal 2.12%/day and 63.55-106.81%, respectively. powder ingredient used in the experimental diet Fish in the mixed sex of Nile tilapia in the Proximate composition % group rearing condition treatment ranged 2.16- Moisture 12.13 3.48%/day and 67.89-127.11%, respectively. Crude protein 11.77 SGR and FE of fish in T2 were significantly (P Crude lipid 0.21 Crude fiber 20.33 < 0.05) greater than fish in T1 but not different Ash 15.42 with fish in T3 from both male and mixed sex Nitrogen-free extract 40.14 rearing conditions. On the contrary, SGR and *1 Nitrogen-free extract represents the soluble carbohydrate FE of female Nile tilapia in the individual rear- of the feed, such as starch and sugar. Crude fiber represents insoluble carbohydrate. ing condition were not significantly (P > 0.05)

Table 3. Growth performance of Nile tilapia fed diets supplemented with different levels of (SM) in different types of rearing condition1 Treatments Survival rate (%) Feed Efficiency (%) Specific Growth Rate (%fish/day) Male Nile tilapia T1 100a 63.55 ± 12.61a 1.39 ± 0.37a reared individually T2 100a 87.02 ± 18.73ab 1.79 ± 0.50ab (n=5) T3 100a 106.81 ± 20.85b 2.12 ± 0.58b Female Nile tilapia T1 100a 60.40 ± 16.65 1.07 ± 0.25 reared individually T2 100a 68.57 ± 25.18 1.19 ± 0.38 (n=3) T3 100a 89.46 ± 14.29 1.52 ± 0.19 Mixed sex of Nile tilapia T1 100a 67.89 ± 5.80a 2.16 ± 0.16a In group rearing condition T2 100a 100.88 ± 5.83ab 2.94 ± 0.15ab (n=2) T3 100a 127.11 ± 14.39b 3.48 ± 0.32b 1Each value is the mean ± S.E.M. of data from replicate groups. Within a column of each rearing condition, means with different letters indicate a significant difference (P < 0.05).

Table 4. The length-weight relationship of male and female Nile tilapia fed on SM (mean±SD) Average Average Average of Average Final Condition Slope Treatments Initial Weight Initial Final W=aLb r2 Weight (g) Factor (K) (b) (g) Length (cm) Length (cm) Individual Male Tilapia (n=5) T1 78.5±10.1 105.5±14.0 15.9±0.2 18.2±0.6 2.106L3.277 0.982 1.76±0.03a 3.277 T2 78.9±11.8 117.8±13.4 16.0±0.5 18.3±0.6 1.7514L3.028 0.901 1.92±0.06b 3.028 T3 77.4±10.5 124.2±19.5 16.1±0.5 18.7±0.6 2.835L3.869 0.972 1.89±0.07b 3.869 Individual Female Tilapia (n=3) T1 72.4±5.3 91.0±13.0 16.2±0.5 17.3±0.8 1.695L2.952 0.9942 1.76±0.02a 2.952 T2 71.9±5.1 92.9±15.5 15.8±0.4 16.7±0.9 1.527L2.856 0.9119 1.98±0.10b 2.856 T3 69.9±6.6 96.3±15.1 15.7±0.7 17.3±1.2 0.829L2.262 0.9160 1.85±0.10ab 2.262 W = aLb : The form of a linear model where W = body weight of samples in g, L = body length of the sample in cm, a = constant (intercept), b = constant (slope of regression line), r=correlation coefficient. Effect of Sargassum on growth of Nile tilapia 29 different within levels of feeding trial with range the digestive tract and retarding of the transpor- 1.07-1.52%/day and 60.40-89.46%, respectively. tation speed might lead to improved efficiency Nevertheless, the highest results of SGR and of nutrient absorption. Rioux and Turgeon FE for all trials (individual male, individual (2015) stated that seaweeds contained a high female, and mixed) were observed in T3. level of polysaccharides which may accelerate The length-weight relationships for individ- the gastrointestinal digestion with the results ual types of rearing condition were analyzed of high feed conversion ratio. These functions to observe any differences in the effect of SM might work more efficiently in Nile tilapia levels in diets on the growth pattern of male which has no stomach but a long digestive tract. and female Nile tilapia (Table 4). The condi- Thus, in our present study, the increasing of tion factor (K) of male Nile tilapia fed by SM SM up to 8% in diets could increase the growth diets showed significantly (P < 0.05) greater performance of Nile tilapia. A similar result values than by the T1. In female fish, although was reported in Japanese flounder that inclu- K values in fish fed SM were greater than T1, sion of 6% of Sargassum fulvellum in test diet there was no significant difference between T1 improved the growth performance (Ragaza et and T3. The K values of all experimental fish al. 2013). However, by adding more SM might was above 1.0 (1.76-1.98). The length-weight produce a negative impact with lower growth relationship which was determined by the value rates. Sargassum ilicifolium has been used of the exponent “b” showed that the growth pat- as a supplemental inclusion for rainbow trout tern of male Nile tilapia is positively allometric diet and a 7.5% inclusion showed the highest (b > 3) and female is negatively allometric (b < 3). growth rate, feed efficiency and survival rate, however, a 10% inclusion produced negative Discussion effects on these indexes (Zamannejad et al. 2016). There is a variant response depending The utility of seaweeds in fish diets has been on the species of seaweed such as Ulva pertusa increasing. Previous studies have revealed that which could improve growth performance of fish diets containing a small amount of sea- yellowtail Seriola quinqueradiata in 3% inclu- weeds could increase the growth performance sion but gave negative effects at over 6% inclu- of a variety of cultured fish (Nakagawa and sion (Hamauzu and Yamanaka 1997). Similar Montgomery 2007; Roy et al. 2011), including with a plant-based supplement which contain Sargassum (Ragaza et al. 2013; Serrano et al. anti-nutritional compounds such as protease 2015). Our results showed that 8% inclusion of inhibitors, phytates, glucosinolates, saponins, SM showed the best results for SGR, FE, and tannins, and lectins reported by Francis et al. K for individual and the group rearing condi- (2001), a non-amylaceous carbohydrates in sea- tions. From the five experimental male fish in weeds also may lead to give a negative effect on the individual rearing condition and two mixed fish performance (Davies et al. 1997; Costa et sex fish replicates in the group rearing condi- al. 2013). Thus, seaweed use as a supplemental tion, the highest SGR values were observed in inclusion for culture fish diets should be done T3. In the individual female rearing condition, in a careful manner. each treatment with three experimental fish, The present study demonstrated that whole although no significant difference was found thalli of Sargassum form an effective suplement among the treatments, there seems to be a ten- for Nile tilapia at least at 4% without negative dency that the growth performance tended to effects and 8% level inclusion of SM gave the be improved if the quantity of SM was increased best results for growth performance. In addi- (Table 3). The amount of crude fiber in T3 was tion, the results showed that the inclusion of 1.6 times greater than that in T1. Matanjun et al. SM could produce a different effect on the (2009) reported that crude fiber decrease the growth pattern between male and female Nile transportation speed of the consumed food in tilapia. The length-weight relationship was 30 F. M. Pratiwy, J. Kohbara and A. B. Susanto established using the equation W=aLb. The Costa, M. M., S. T. L. Oliveira, R. E. Balen, G. Bueno mean value of slope b in male trials showed Junior, L. T. Baldan, L. C. R. Silva and L. D. Santos (2013) Brown seaweed meal to Nile tilapia fingerlings. values higher than 3.0 and in female trials Arch. Zootec., 62, 101-109. showed values lower than 3.0. When b is more Dan, N. C. and D. C. Little (2000) The culture perfor- than 3.0, the fish shows positive allometric mance of monosex and mixed-sex new-season or the increase in weight is faster than the and overwintered fry in three strains of Nile tilapia (Oreochromis niloticus) in northern Vietnam. increase in length, and if b is less than 3.0, the Aquaculture, 184, 221-231. fish shows negative allometric growth or the Davies, S. J., M. T. Brown and M. Camilleri (1997) growth of length is faster than that of weight Preliminary assessment of the seaweed Porphyra (Weatherley and Gill 1987). However, this purpurea in artificial diets for thicklipped grey mullet (Chelon labrows). Aquaculture, 152, 249-258. value is slightly higher than the mean value of Dawczynski, C., R. Schubert and G. Jahreis (2007) Amino Nile tilapia (b=2.908) in natural conditions as acids, fatty acids, and dietary fiber in edible seaweed described by Britton and Harper (2008). The products. Food Chem., 103, 891-899. variation of b values depends on water quality FAO (2017) Food and Agriculture Organization of the United Nations. Cultured Aquatic Species Information and food ability sample size and length range Programme, Oreochromis niloticus (Linnaeus, 1758). (Mommsen 1998). The mean K values for Nile Retrieved from http://www.fao.org/fishery/cultured- tilapia fed with SM in this study were higher species/Oreochromis_niloticus/en, accessed on 15 than 1.0 for males and females, respectively. May 2017. Francis, G., H. P. S. Makkar and K. Becker (2001) This suggested that the fish were in a good Antinutritional factors present in plant-derived alter- health condition during the experimental period nate fish feed ingredients and their effects in fish. (Ighwela et al. 2011). Faster growth of male Aquaculture, 199, 197-227. Nile tilapia than that of female is considered Hamauzu, K. and M. Yamanaka (1997) Usefulness of the meal of a sterile mutant of Ulva pertusa as a feed sup- to be related to the lack of energy expenditure plement for cultured yellowtail. Suisanzoshoku, 45, on egg production by females (Dan and Little 357-363 (in Japanese with English abstract). 2000) and this is also true in the case of the Ighwela, K. A., A. B. Ahmed and A. B. Abol-Munafi (2011) experiments using SM included diet. Based on Condition factor as an indicator of growth and feeding intensity of Nile tilapia fingerlings (Oreochromis niloti- the growth performance results, selection and cus) feed on different levels of maltose. 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ホンダワラ属海藻の飼料添加がナイルティラピアの成長に与える効果

Fittrie Meyllianawaty PRATIWY・神原淳・A. B. SUSANTO

飼料中の米糠をホンダワラ属海藻粉末で 0%, 4%, 8%と段階的に置き換えた 3 種類の飼料をナイルティラピアに給餌し，成長に与えるホンダワラの添加効果を雌雄個体別飼育および集団飼育に分けて検討した。雄個体飼育群および集団飼育群においては，8%添加区が飼料転換効率および日間成長率において最も高く0%添加区との間に有意差がみられた。一方，雌個体飼育群においては，数値的には高添加区が好成績であったが，試験区間での有意差はみられなかった。肥満度では，雄は添加率が 4%より高くなると 0%区と比較して有意に増大し，成長曲線の傾きも大きくホンダワラの添加効果は高いと判断されたが，雌への添加効果は雄ほど効果的ではなかった。以上から，ホンダワラの飼料への添加はナイルティラピアの成長促進に有効である可能性が示唆された。