Academia.eduAcademia.edu
Aquaculture Reports 18 (2020) 100436 Contents lists available at ScienceDirect Aquaculture Reports journal homepage: www.elsevier.com/locate/aqrep Feeding strategy induces compensatory growth in Heros severus fingerlings, an Amazonian ornamental fish T Leonnan Carlos Carvalho de Oliveiraa,1, Lucas Gabriel Baltazar Costaa,1, Bruno José Corecha Fernandes Eirasa,1, Marcos Ferreira Braboa,1, Galileu Crovatto Verasb,1, Lorena Batista de Mouraa,1, Ana Lúcia Salaroc,1, Daniel Abreu Vasconcelos Campeloa,*,1 a Federal University of Pará, Department of Fisheries Engineering, Alameda Leandro Ribeiro s/nº, 68600-000, Bragança, PA, Brazil Federal University of Minas Gerais, Department of Veterinary Medicine, Av. Presidente Antônio Carlos 6627, 31270-901, Belo Horizonte, MG, Brazil c Federal University of Viçosa, Department of Animal Biology, Av. Ph Rolphs s/n, 36570-900, Viçosa, MG, Brazil b A R T I C LE I N FO A B S T R A C T Keywords: Cichlid Feeding strategy Growth performance Production costs The aim of the present study was to evaluate the compensatory growth of severum (Heros severus) fingerlings fed inert diet for 30 days, after 13 days of larviculture at different feeding rates. The production cost with Artemia nauplii was also evaluated. For that purpose, a growth trial was performed with 400 severum post-larvae, distributed in twenty aquaria (1 L) at density of 20 post-larvae L−1. The experiment was conducted in a completely randomized design with five treatments and four replicates. For 10 days, the post-larvae received Artemia nauplii at different feeding rates: 100, 150, 200, 250 and 300 nauplii post-larvae−1 day−1. Subsequently, three days of food transition to an inert diet was performed. After this period, the severum stocking density was halved and the fish received inert diet for 30 days. The post-larvae fed with 200 Artemia nauplii post-larvae−1 day−1 presented the best results of final length, length gain and specific growth rate for length. On the other hand, postlarvae fed with 300 nauplii post-larvae−1 day−1 presented the highest results for final weight, weight gain and specific growth rate for weight. The average cost of using Artemia nauplii incresed directly with the increasing amount of nauplii supplied. The fingerlings presented best results of final weight and final length when received 250 nauplii post-larvae−1 day−1 during the larviculture. The weight gain of fingerlings did not differ for fish initially fed with 150–300 Artemia nauplii post-larvae−1 day−1, proving that the fingerlings expressed partial compensatory growth. The specific growth rate for length and weight were higher in fingerlings initially fed with 100 Artemia nauplii post-larvae−1 day−1, however, the survival rate was lower in fingerlings fed that amount of Artemia nauplii. Therefore, it is recommended 150 Artemia nauplii post-larvae−1 day−1 during the larviculture of severum to induce partial compensatory growth and reduce cost. 1. Introduction tank culture systems and inert diets, being able to easily spawning in captivity (Favero et al., 2010; Alishahi et al., 2014). Although it expresses territorialism during reproductive periods, it is peaceful during the growth phase (Stawikowski and Werner, 1998; Campelo et al., 2019). In the aquaculture production chain, larviculture is the most important and critical step of captive rearing (Zuanon et al., 2011; Abe et al., 2019). Fish in the post-larval stage have a developing gastrointestinal tract and short bowel length (Portella and Dabrowski, 2008; Xie et al., 2011), and so do not adequately assimilate inert foods Ornamental fish farming can be a lucrative activity, mainly due to the high individual trade value that many species reach in national and international markets (Anjos et al., 2009; Fujimoto et al., 2014; Araújo et al., 2017). Severum (Heros severus) stands-out among fish species with potential for ornamental market. It is a native fish of the Amazon Basin (Mora et al., 2007), where it occurs in lentic waters with pH ranging 5.0–6.5 and temperature ranging 24–32 °C (Abe et al., 2016). The specie is described with bright yellowish color, good adaptation to Corresponding author. E-mail addresses: leonnanoliveira96@gmail.com (L.C.C.d. Oliveira), lucasbcosta1@icloud.com (L.G.B. Costa), bruno_eiras@hotmail.com (B.J.C.F. Eiras), mbrabo@ufpa.br (M.F. Brabo), galiveras@hotmail.com (G.C. Veras), lorena.moura@ufra.edu.br (L.B. de Moura), salaro@ufv.br (A.L. Salaro), danielvc@ufpa.br (D. Abreu Vasconcelos Campelo). 1 All authors have contributed significantly and are in agreement with the content of the manuscript. ⁎ https://doi.org/10.1016/j.aqrep.2020.100436 Received 30 September 2019; Received in revised form 30 June 2020; Accepted 31 July 2020 2352-5134/ © 2020 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). Aquaculture Reports 18 (2020) 100436 L.C.C.d. Oliveira, et al. concentration based on preliminary salinity studies for severum postlarvae (Unpublished results). All aquariums had an individual aeration system and the laboratory was maintained under photoperiod of approximately 12/12 h light/dark as recommended by Veras et al. (2016b). The experiment was conducted in a completely randomized design with five treatments and four replications. Initially, during the first 10 days, the post-larvae received Artemia nauplii at different feeding rates: 100, 150, 200, 250 and 300 Artemia nauplii post-larvae−1 day−1, as proposed by Abe et al. (2016). After this period, the feeding transition was performed; a period of three days in which the post-larvae were fed with Artemia nauplii and an inert diet (Campelo et al., 2019), the supply of nauplii from each treatment during the feeding transition was halved: 50, 75, 100, 125 and 150 Artemia nauplii post-larvae−1 day−1. Subsequently, an inert diet was provided ad libidum for the fish of all treatments, for a 30-day period. The stocking density in this phase was halved, leaving approximately 10 post-larvae L−1. Water salinity was maintained at 3 g L−1 throughout all 43 days of experimental period, as for the feeding frequency of four times a day, with three-hour intervals between meals, at times of 8:00, 11:00, 14:00 and 17:00 h. One hour after the last feeding, partial changes of 50 % of the water volume were performed by siphonation of the aquaria, to ensure the maintenance of water quality. During the post-larvae feed trial (13 days) no Artemia nauplii surplus was observed, indicating that the living food provided were consumed by the fish. (Pedreira et al., 2008; Diemer et al., 2012). Thus, the use of living organisms to feed post-larval fish has been recommended for several species because it increases survival and growth rates over that for inert diets (Schütz et al., 2008; Diemer et al., 2012; Fosse et al., 2013). However, the use of living organisms as feed generally makes larviculture the most-costly phase of fish farming (Zuanon et al., 2011; Veras et al., 2016a), due to the required continuous production and high cost of such organisms (Kodama et al., 2011; Sanches et al., 2013). Artemia nauplii stand-out among live foods for aquaculture because of their ease production in the laboratory and their nutritional characteristics, which enhance fish survival and growth (Silva and Mendes, 2006; Kestemont et al., 2007). However, since Artemia nauplii are marine organisms they experience high mortality rates in freshwater (Portella et al., 2000; Beux and Zaniboni-Filho, 2006), which directly influences post-larval consumption since dead nauplii have low attractiveness and their decomposition degrades water quality (Beux and Zaniboni-Filho, 2006; Santos et al., 2015a). Thus, an alternative to improve the use of Artemia nauplii to feed freshwater fish is to perform larviculture in salinized water (Luz and Santos, 2008; Jomori et al., 2013). This type of management has shown good results for larviculture of some species of fish (Jomori et al., 2012, 2013), and contributes to fish welfare and health (Salaro et al., 2012). In addition to salinization, promoting compensatory growth can also serve as a strategy for optimizing the use of Artemia nauplii by fish while reducing production costs (Ituassú et al., 2004). Compensatory growth is a physiological phase of accelerated growth when favorable conditions are restored after a period of growth depression. It is commonly observed in fish, and can reduce variance in size by causing convergence of individual growth trajectories (Ali et al., 2003). Compensatory growth can be classified according to the degree of the recovery response during the post-restriction feeding phase as: partial compensation, when restricted animals do not reach the same size as unrestricted animals but have high growth rates; full compensation, when restricted animals reach the same size as unrestricted animals; overcompensation, when restricted animals are larger than unrestricted animals; and no compensation, when animals show a resume growing at a rate similar that of size reached at the end of the deprivation period (Ali et al., 2003). Abe et al. (2016) found the best feeding rates for post-larval severum to be 250 Artemia nauplii post-larvae−1 day−1 distributed among four daily meals. Thus, the aim of the present study was to evaluate if compensatory growth of severum fingerlings can be used as a strategy to reduce this previously indicated amount of Artemia nauplii and, consequently, reduce production costs associated with this feed source. Therefore, post-larval severum were fed with Artemia nauplii at different feeding rates to evaluate the resulting compensatory growth by severum fingerlings. The production costs with Artemia nauplii were also evaluated. 2.2. Artemia hatching Artemia nauplii were obtained daily after incubation of 5 g L−1 cysts in salinized water at a concentration of 35 g L−1. The containers for the hatching of the cysts (2 L) were kept under artificial illumination for 24 h and constant aeration. After hatching, aeration was withdrawn and the living nauplii were collected from the suspension of unhatched cysts by siphoning. Artemia nauplii were then filtered through a 120 μm mesh and washed twice with running freshwater to remove impurities, reduce salinity and ensure food quality. Then, the hatched nauplii were transferred to a 200 mL of water and the density was estimated by collecting a volume of 0.5 mL, for determined the mean value of nauplii. The counting of the nauplii was performed out in triplicate with the aid of petri dish under stereomicroscope (QUIMIS Q714Z-2) with increase of 40×. After estimating nauplii density, the volume of Artemia nauplii to be supplied in each treatment was calculated. 2.3. Experimental diet The experimental diet used was formulated to contain 42 % of crude protein and 4.200 kcal kg−1 of gross energy (Table 1). After diet formulation, 25 % of warm water (50 °C) was added to the ingredients compound and then pelletized in conventional meat grinder (G. PANIZ, MCR-22, SP, Brazil) and then dried for 12 h by oven-drying at 45 °C (QUIMIS, SP, Brazil). Before being fed to the fish, the diet was ground so that the size of the pellets (approximately 1.5 mm) suited the postlarvae mouth opening. 2. Materials and methods The experiment was approved by the Ethics Committee for the Use of Animals of the Federal University of Pará, CEUA/UFPA (Approval number: 7656100517) and conducted at the Laboratory of Ornamental Fish, of the Faculty of Fisheries Engineering, Institute for Coastal Studies, Federal University of Pará, Bragança Campus, Pará State, Brazil. 2.4. Water parameters Monitoring dissolved oxygen concentrations (6.55 ± 0.35 mg L−1), pH (7.09 ± 0.10), temperature (27.36 ± 0.05 °C), total ammonia concentration (0.03 ± 0.02 mg L−1) and electrical conductivity of water (4.73 ± 0.27 μS cm−1), were performed using a multiparameter probe (HORIBA U-50). All analyzes were performed every three days at the morning time and remained constant. 2.1. Fish and culture conditions A total of 400 severum (Heros severus) post-larvae with seven days after hatching and initial weight and length of 1.95 ± 0.4 mg and 5.85 ± 0.3 mm (mean ± standard deviation) respectively, were used. The fish post-larvae were randomly distributed in 20 aquariums with a useful volume of 1 L of water, at a density of 20 post-larvae L−1. The aquariums were maintained with 3 g L−1 of salinity water, defined 2.5. Growth performance and production cost with Artemia nauplii At the beginning of the experiment, due to the small size and 2 Aquaculture Reports 18 (2020) 100436 L.C.C.d. Oliveira, et al. number of fish per experimental unit) *100 (Furuya et al., 1998), and survival rate (SR) SR = (final post-larvae number/initial post-larvae number) *100. The production cost with Artemia nauplii was also evaluated after the initial 13 days of feed trial. The calculated cost considered 280 thousand of Artemia cysts per gram of commercial product, nauplii hatching rate of 85 %, value of US$ 44.00 per kilogram of cysts, the amount of Artemia nauplii used for a thousand fish larviculture and the survival rates of the severum post-larvae during the first 13 days (Mankiw, 2020). The price of Artemia cysts kilogram was determined based on the values found in the Amazon region, where the experiment was conducted. The fish that remained in each experimental unit, after 30 days of feeding with inert diet ad libidum only, were counted, weighed and measured to determine the same growth performance parameters and verify if compensatory growth has occurred. Table 1 Percentage and chemical composition values of the experimental diet. Ingredient g kg−1 Soybean meal Fish meal Corn meal Wheat bran Soybean oil Dicalcium phosphate Mineral and vitamin mixa DL-methionine BHTb 200.0 560.0 90.0 70.0 56.0 15.0 5.0 3.8 0.2 Chemical compositionc Crude protein (%) Total lipid (%) Gross fiber (%) Gross energy (kcal. kg−1) 42.0 11.0 1.5 4200.0 2.6. Statistical analysis a Assurance levels per kilogram of product: vitamin A, 1,200,000 IU; vitamin D3, 200,000 IU; vitamin E, 12,000 mg; vitamin K3, 2400 mg; vitamin B1, 4800 mg; vitamin B2, 4800 mg; vitamin B6, 4000 mg; vitamin B12, 4800 mg; folic acid, 1200 mg; calcium pantothenate, 12,000 mg; vitamin C, 48,000 mg; biotin, 48 mg; choline, 65,000 mg; niacin, 24,000 mg; Fe, 10,000 mg; Cu, 6000 mg; Mg, 4000 mg; Zn, 6000 mg; I, 20 mg; Co, 2 mg; Se, 20 mg (Guabi Animal Nutrition, Brazil). b Butylated hydroxytoluene (BHT) (ISOFAR Ind., Brazil). c Performed in accordance with AOAC (AOAC, 2000). Statistical analysis of the data was subjected to the Lilliefors test, to verify the normality of errors, and to the Bartlett test, to verify the homogeneity of variances. Afterwards, one-way analysis of variance (ANOVA) at 5 % significance was performed. Then, in the values that presented significant difference (P < 0.05), Tukey test was used at 5 % of significance. All statistical analyses were performed with SPSS (SPSS Inc., Chicago, IL, USA, version 23.0). 3. Results fragility of the fish post-larvae, a sample of 80 individuals (20 % of the batch) were weighed on precision scale (GEHAKA AG200; 0.0001 g accuracy; SP, Brazil) and measured with the aid of digital caliper (PANTEC-150; 0.01 mm; SP, Brazil) to estimate initial mean of weight and length. After 10 days of Artemia nauplii supply and three days of food transition, the biometry of 10 fish per experimental unit was performed to determine the growth performance parameters: Final length (FL), length gain (LG) LG = final length - initial length, final weight (FW), weight gain (WG) WG = final weight - initial weight, specific growth rate for length (SGR(L)) and weight (SGR(W)) being SGR(L) = ((ln final length - ln initial length)/number of experiment days) *100 and (SGR(W)) = ((ln final weight - ln initial weight)/number of experiment days) *100 (Lugert et al., 2014), uniformity of the batch for length (LU) and weight (WU) being LU = (number of fish with length varying ± 20 % from the average in each experimental unit/total number of fish per experimental unit) *100 and WU = (number of fish with weight varying ± 20 % from the average in each experimental unit/total Post-larval severum fed with 300 Artemia nauplii post-larvae−1 day−1 had the highest final length, length gain and length-specific growth rate (P < 0.05), although the value did not differ from postlarval severum fed with 250 and 200 nauplii post-larvae−1 day−1. Batch uniformity for length showed no significant differences among treatments (P > 0.05) (Table 2). Post-larval severum fed with 300 nauplii post-larvae−1 day−1 also had the highest final weight, weight gain and weight-specific growth rate, while those that received 100 nauplii post-larvae−1 day−1 had the lowest values (P < 0.05). Batch uniformity for weight and survival rate showed no significant differences among treatments (P > 0.05) (Table 2). As expected, the average cost of using Artemia nauplii incresed directly with the increasing amount of nauplii supplied to post-larval severum (P < 0.05). The production cost (US$) with Artemia nauplii after 13 days were 0.19 ± 0.1, 0.33 ± 0.1, 0.46 ± 0.1, 0.57 ± 0.1 and 0.65 ± 0.1, for the post-larval submitted to feeding rates of 100, 150, 200, 250 and 300 Artemia nauplii post-larvae−1 day−1, respectively. Table 2 Growth performance (mean ± SD) of post-larval severum (Heros severus) after 13 days submitted to different feeding rates. Performance indices FL (mm) SGR(L) (% day−1) LG (mm) LU (%) FW (mg) SGR(W) (% day−1) WG (mg) WU (%) SR (%) Feeding rates (Artemia nauplii post-larvae−1 day−1) 100 150 200 250 300 P value 7.3 ± 0.6c 1.4 ± 0.5c 1.4 ± 0.6c 67.5 ± 10.3 6.0 ± 0.3d 7.5 ± 0.3d 4.0 ± 0.3d 100.0 ± 0.0 86.3 ± 8.9 9.0 ± 0.3b 2.9 ± 0.2b 3.1 ± 0.3b 64.4 ± 8.8 9.9 ± 0.8c 10.8 ± 0.6c 8.0 ± 0.8c 95.0 ± 7.5 92.5 ± 3.8 10.0 ± 0.3a 3.5 ± 0.1a 4.03 ± 0.2a 68.2 ± 11.9 12.0 ± 1.2bc 12.1 ± 0.6bc 10.1 ± 1.2bc 97.5 ± 3.8 95.0 ± 5.0 10.4 ± 0.2a 3.8 ± 0.1a 4.5 ± 0.2a 66.7 ± 17.7 14.2 ± 1.2b 13.2 ± 0.6b 12.2 ± 1.2b 100.0 ± 0.0 95.0 ± 7.5 10.6 ± 0.2a 4.0 ± 0.1a 4.8 ± 0.2a 80.0 ± 6.7 16.7 ± 0.7a 14.3 ± 0.3a 14.8 ± 0.7a 100.0 ± 0.0 90.0 ± 10.0 0.0001 0.0001 0.0001 0.3342 0.0001 0.0001 0.0001 0.3423 0.3677 P value determined by Analysis of Variance (ANOVA). Mean values in the same line, with different letters, are significantly different by Tukey test at 5 % probability. (n = 4). Final length (FL); Specific growth rate for length (SGR(L)); Length gain (LG); Length uniformity (LU); Final weight (FW); Specific growth rate for weight (SGR(W)); Weight gain (WG); Weight uniformity (WU); Survival rate (SR). 3 Aquaculture Reports 18 (2020) 100436 L.C.C.d. Oliveira, et al. Table 3 Growth performance (mean ± SD) of severum (Heros severus) fingerlings fed inert diet for 30 days, after larviculture at different feeding rates. Performance indices FL (mm) SGR(L) (% day−1) LG (mm) LU (%) FW (mg) SGR(W) (% day−1) WG (mg) WU (%) SR (%) IDC (g) Initial feeding rates (Artemia nauplii post-larvae−1 day−1) 100 150 200 250 300 P value 13.1 ± 0.2c 2.0 ± 0.3a 5.9 ± 0.5 91.3 ± 4.4 38.0 ± 3.0c 6.2 ± 0.4a 34.1 ± 1.5b 38.4 ± 1.8 85.0 ± 7.5b 4.9 ± 0.1 14.1 ± 0.3b 1.5 ± 0.2b 5.1 ± 0.6 97.5 ± 3.8 46.7 ± 2.3b 5.2 ± 0.5b 36.7 ± 3.2ab 41.5 ± 1.4 97.5 ± 3.8a 4.8 ± 0.2 14.3 ± 0.7b 1.2 ± 0.1b 5.0 ± 0.2 89.7 ± 5.3 50.0 ± 7.8b 4.7 ± 0.4b 38.0 ± 6.9ab 47.5 ± 3.9 96.7 ± 3.3a 4.9 ± 0.2 15.5 ± 0.5a 1.3 ± 0.1b 5.1 ± 0.3 97.2 ± 4.2 58.1 ± 3.0ab 4.7 ± 0.2b 43.9 ± 2.4ab 56.2 ± 2.1 96.7 ± 3.3a 4.7 ± 0.1 15.9 ± 0.2a 1.3 ± 0.1b 5.2 ± 0.2 97.5 ± 3.8 63.8 ± 1.9a 4.5 ± 0.1b 46.0 ± 1.6a 50.9 ± 3.2 100.0 ± 0.0a 5.0 ± 0.1 0.0001 0.0007 0.2216 0.2253 0.0003 0.0006 0.0266 0.1046 0.0205 0.1307 P value determined by Analysis of Variance (ANOVA). Mean values in the same line, with different letters, are significantly different by Tukey test at 5 % probability. (n = 4). Final length (FL); Specific growth rate for length (SGR(L)); Length gain (LG); Length uniformity (LU); Final weight (FW); Specific growth rate for weight (SGR(W)); Weight gain (WG); Weight uniformity (WU); Survival rate (SR); Inert diet consumption (IDC). Abe et al. (2016) found the best feeding rates for post-larval severum to be 250 Artemia nauplii post-larvae−1 day−1. In the present study, however, the fingerlings that initially received 150 or 250 nauplii post-larvae−1 day-1 did not differ significantly in weight and length gain, but the production cost was 42.11 % less for 150 nauplii postlarvae−1 day−1. The compensatory growth observed for severum can be used to increase production efficiency, since it is possible to initially feed fish with less Artemia and achieve a satisfactory growth rate after 30 days of feeding with inert diet. The type of compensatory growth observed for severum fingerlings is classified, according to Ali et al. (2003), as partial compensatory growth. Partial compensatory growth occurs when fish exhibit high growth rates after leaving a food restriction period, but do not reach the same final size as individuals fed at higher rates. Kojima et al. (2015) reports that despite possible tissue changes and growth retardation, dietary restriction does not compromise the ability of some fish species to grow when they return to normal dietary conditions, depending on the time and restriction the animals have undergone. This accelerated growth can occur due to several compensation mechanisms, such as increased food consumption, improved nutrient utilization or reduction in metabolic costs after the restriction period (O’Connor et al., 2000). Since no differences were found in inert diet intake, it is likely that compensatory growth occurred due to the better utilization of dietary nutrients. The partial compensatory growth found here for severum fingerlings is recurrent among fish species. Juvenile Nile tilapia (Oreochromis niloticus) submitted to five feed intervals exhibited a trend toward higher growth rates with greater feed restriction, except for the most deprived fish (Gao et al., 2015). Partial compensatory growth was also observed for the dolphin cichlid (Cyrtocara moorii), an ornamental fish submitted to different starvation periods (Yilmaz et al., 2018). Full compensatory growth was found for juvenile matrinxã (Brycon amazonicus) and tambaqui (Colossoma macropomum) submitted to different periods of food deprivation (Urbinati et al., 2014; Santos et al., 2018). On the other hand, other studies did not observe compensatory growth after a food deprivation period (Ferreira and Nuñer, 2015; Herrera et al., 2016). Despite several studies, the exact mechanisms that enable compensatory growth are not well-understood (Urbinati et al., 2014), especially for fish. It should also be emphasized that several factors can influence growth after a period of food deprivation, such as the biology of the species (Ali et al., 2003; Ye et al., 2016) and the phase of life (Vainikka et al., 2012). In the present study, animals that received the lowest feeding rate during larviculture had the lowest survival rate. Moreover, despite the low weight uniformity of fingerlings initially fed with the lower amount of Artemia nauplii post-larvae−1 day−1, it did differ significantly from Supplying 100 nauplii post-larvae−1 day−1 cost 70.77 % less than supplying 300 nauplii post-larvae−1 day−1. The average cost was also 49.23 %, 29.23 % and 12.31 % lower than that for 300 nauplii postlarvae−1 day−1 when 150, 200 and 250 nauplii post-larvae−1 day−1 were used, respectively. The final weight and final length of fingerlings followed the same trend observed for larviculture. The lowest values was observed for fingerlings fed 100 nauplii post-larvae−1 day−1 during the first 10 days (P < 0.05). However, the specific growth rates for length and weight were higher for the same fingerlings (P < 0.05). Moreover, fingerling length gain showed no differences and weight gain did not differ significantly among fish fed with 150, 200, 250 and 300 nauplii postlarvae−1 day−1 (P > 0.05). These results demonstrate an accelerated growth by fingerlings initial fed with 150 nauplii post-larvae−1 day−1, indicating that the severum fingerlings express partial compensatory growth (Table 3). The different initial feeding rates had no effect on the uniformity of fingerling length and weight (P > 0.05). Fish that received the lowest feeding rate during larviculture had the lowest survival rate (P < 0.05). Average consumption did not differ among treatments (Table 3), with an overall average of 4.84 ± 0.1 g of inert diet (P > 0.05). 4. Discussion Optimal food management should be developed to improve feed utilization by fish and reduce production costs (Abe et al., 2016). In this sense, it is very important to define ideal feeding rates for each species in each phase of their life in aquaculture. In the present study, the best results for body length and weight development were for post-larval severum fed at 200 and 300 Artemia nauplii post-larvae−1 day−1, respectively. These values are close to the best feeding rate found by Abe et al. (2016) for post-larval severum, which suggests an optimal feeding rate for severum fed with Artemia nauplii. On the other hand, a depression in growth was observed for post-larval severum fed 100 and 150 nauplii post-larvae−1 day−1, suggesting partial feed deprivation. In the present study, post-larval survival and uniformity were not affected by the different feeding rates tested. According to Pereira et al. (2016), the longer that Artemia nauplii are supplied, the greater the possibility of reducing fish uniformity, mainly due to the establishment of dominance among post-larval fish. The present work used 13 days of larviculture, which may have contributed to high uniformity of fish. Furthermore, the movement and distribution of Artemia nauplii in the water column made this food very attractive to the post-larval fish (Diemer et al., 2010), since Artemia nauplii experience higher survival and movement in salinized water, which in turn improves fish consumption and, consequently, batch uniformity and survival rate. 4 Aquaculture Reports 18 (2020) 100436 L.C.C.d. Oliveira, et al. that fish that received high initial feeding rates. It is also notable that the fish of all treatments exhibited high uniformity for length. A lack of standardization in fish weight does not directly affect ornamental fish marketing, since length uniformity of batches is more important for ornamental fish because it facilitates handling in the production system and outlets for marketing (Veras et al., 2016b). Furthermore, the use of smaller amounts of Artemia nauplii post-larvae−1 day−1 reduces the production costs of using living food. It is also important to note that ornamental fish species are sold per unit and not per weight (Abe et al., 2016; Selvatici et al., 2017), and so smaller fish can have market value (Fujimoto et al., 2014). Inducing compensatory growth in fish can be a strategy to reduce production costs. Moreover, it can be used to maintain or even improve fish growth rates after supplying a reduced amount of live food (Santos et al., 2015b). Such growth compensation can have important applications in aquaculture, because it optimizes the supply, consumption and utilization of food by animals (Santos et al., 2018), and thus improves the efficiency of larviculture by reducing the production costs associated with the living food. Ali, M., Nicieza, A., Wootton, R.J., 2003. Compensatory growth in fishes: a response to growth depression. Fish Fish. 4 (2), 147–190. https://doi.org/10.1046/j.1467-2979. 2003.00120.x. Alishahi, M., Karamifar, M., Mesbah, M., Zarei, M., 2014. Hemato-immunological responses of Heros severus fed diets supplemented with different levels of Dunaliella salina. Fish Physiol. Biochem. 40 (1), 57–65. https://doi.org/10.1007/s10695-0139823-5. Anjos, H.D.B., Amorim, R.M.S., Siqueira, J.A., Anjos, C.R., 2009. Exportação de peixes ornamentais do estado do Amazonas, bacia amazônica, Brasil. Bol. Inst. Pesca. 35 (2), 259–274. AOAC - Association of Official Analytical Chemists, 2000. Official Methods of Analysis, 17th ed. Gaithersburg, MD, USA. Araújo, J.G., Santos, M.A.S., Rebello, F.K., Isaac, V.J., 2017. Cadeia comercial de peixes ornamentais do rio Xingu, Pará, Brasil. Bol. Inst. Pesca. 43 (2), 297–307. https://doi. org/10.20950/1678-2305.2017v43n2p297. Beux, L.F., Zaniboni-Filho, E., 2006. Influência da baixa salinidade na sobrevivência de náuplios de Artemia sp. Bol. Inst. Pesca. 32 (1), 73–77. Campelo, D.A.V., Silva, I.C.E., Marques, M.H.C., Eiras, B.J.C.F., Brabo, M.F., De Moura, L.B., Veras, G.C., 2019. Estratégias alimentares na larvicultura do peixe ornamental amazônico acará severo (Heros severus) (Heckel, 1840). Arq. Bras. Med. Vet. Zootec. 71 (5), 1601–1608. Diemer, O., Neu, D.H., Sary, C., Feiden, A., Boscolo, W.R., Signor, A.A., 2010. Manejo alimentar na larvicultura do mandi-pintado (Pimelodus britskii). Rev. Bras. Saúde Prod. An. 11 (3), 903–908. Diemer, O., Neu, D.H., Sary, C., Finkler, J.K., Boscolo, W.R., Feiden, A., 2012. Artemia sp. na alimentação de larvas de jundiá (Rhamdia quelen). Ciênc. Anim. Bras. 13 (2), 175–179. https://doi.org/10.5216/cab.v13i2.9011. Favero, J.M.D., Pompeu, P.D.S., Prado-Valladares, A.C., 2010. Biologia reprodutiva de Heros efasciatus Heckel, 1840 (Pisces, Cichlidae) na Reserva de Desenvolvimento Sustentável Amanã-AM, visando seu manejo sustentável. Acta Amaz. 40 (2), 373–380. https://doi.org/10.1590/S0044-59672010000200015. Ferreira, L.S.B.P., Nuñer, A.P.O., 2015. Food deprivation and compensatory growth in juvenile piava, Leporinus obtusidens. Bol. Inst. Pesca. 41 (3), 471–478. Fosse, P.J., Mattos, D.C., Cardoso, L.D., Motta, J.H.S., Jasper, A.P.S., Radael, M.C., Andrade, D.R., Vidal Júnior, M.V., 2013. Estratégia de coalimentação na sobrevivência e no crescimento de larvas de Betta splendens durante a transição alimentar. Arq. Bras. Med. Vet. Zootec. 65 (6), 1801–1807. https://doi.org/10.1590/ S0102-09352013000600030. Fujimoto, R.Y., Santos, R.F.B., Maria, A.N., 2014. Densidade de Estocagem e Manejo Alimentar na Criação de Acarás-bandeira. Embrapa: Comunicado técnico. 145, 3–10. Furuya, W.M., Souza, S.R., Furuya, V.R.B., Hayashi, C., Ribeiro, R.P., 1998. Dietas peletizada e extrusada para machos revertidos de tilápias do Nilo (Oreochromis niloticus) na fase de terminação. Cienc. Rural 28 (3), 483–487. https://doi.org/10.1590/ S0103-84781998000300022. Gao, Y., Wang, Z., Hur, J., Lee, J.Y., 2015. Body composition and compensatory growth in Nile tilapia Oreochromis niloticus under different feeding intervals. Chin. J. Oceanol. Limnol. 33 (4), 945–956. https://doi.org/10.1007/s00343-015-4246-z. Herrera, L.A., Silva, F.D.C., Santos, A.P.D., Sousa, O.M.D., Sanches, E.G., 2016. Compensatory growth and food deprivation in common snook growth performance. Pesq. Agropec. Bras. 51 (6), 776–779. https://doi.org/10.1590/S0100204X2016000600010. Ituassú, D.R., Dos Santos, G.R.S., Roubach, R., Pereira-Filho, M., 2004. Desenvolvimento de tambaqui submetido a períodos de privação alimentar. Pesq. Agropec. Bras. 39 (12), 1199–1203. https://doi.org/10.1590/S0100-204X2004001200006. Jomori, R.K., Luz, R.K., Portella, M.C., 2012. Effect of salinity on larval rearing of pacu, Piaractus mesopotamicus, a freshwater species. J. World Aquacult. Soc. 43 (3), 423–432. https://doi.org/10.1111/j.1749-7345.2012.00570.x. Jomori, R.K., Luz, R.K., Takata, R., Fabregat, T.E.H.P., Portella, M.C., 2013. Água levemente salinizada aumenta a eficiência da larvicultura de peixes neotropicais. Pesq. Agropec. Bras. 48 (8), 809–815. https://doi.org/10.1590/S0100204X2013000800001. Kestemont, P., Xueliang, X., Hamza, N., Maboudou, J., Imorou Toko, I., 2007. Effect of weaning age and diet on pikeperch larviculture. Aquaculture. 264 (1–4), 197–204. https://doi.org/10.1016/j.aquaculture.2006.12.034. Kodama, G., Annunciação, W.F., Sanches, E.G., Gomes, C.H.A.M., Tsuzuki, M.Y., 2011. Viabilidade econômica do cultivo do peixe palhaço, Amphiprion ocellaris, em sistema de recirculação. Bol. Inst. Pesca. 37 (1), 61–72. Kojima, J.T., Leitão, N.J., Menossi, O.C.C., Freitas, T.M., Dal-Pai Silva, M., Portella, M.C., 2015. Short periods of food restriction do not affect growth, survival or muscle development on pacu larvae. Aquaculture 436, 137–142. https://doi.org/10.1016/j. aquaculture.2014.11.004. Lugert, V., Thaller, G., Tetens, J., Schulz, C., Krieter, J., 2014. A review on fish growth calculation: multiple functions in fish production and their specific application. Rev. Aquacult. 8 (1), 30–42. https://doi.org/10.1111/raq.12071. Luz, R.K., Santos, J.C.E., 2008. Densidade de estocagem e salinidade da água na larvicultura do pacamã. Pesq. Agropec. Bras. 43 (7), 903–909. https://doi.org/10.1590/ S0100-204X2008000700015. Mankiw, N.G., 2020. In: octave (Ed.), Principles of Microeconomics. Cengage Learning, Stamford. Mora, J.C., Urueña, F.R., Landines, M.A., Sanabria, A.I., 2007. Cíclidos. In: Parra, M.A.L., Ochoa, A.I.S., Daza, P.V. (Eds.), Producción de peces ornamentales en Colombia. Produmedios, Bogotá, pp. 63–88. O’Connor, K.I., Taylor, A.C., Metcalf, N.B., 2000. The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon. J. Fish Biol. 57 (1), 41–51. https://doi.org/10.1111/j.1095-8649.2000.tb00774.x. Pedreira, M.M., Santos, J.C.E., Sampaio, E.V., Pereira, F.N., Silva, J.L., 2008. Efeito do 5. Conclusion The induction of a compensatory growth by severum fingerling through low feeding rates during larviculture proved to be an efficient feed strategy. Thus, the feeding rate of 150 Artemia nauplii postlarvae−1 day−1 is indicated for initial feed of post-larval severum (Heros severus), once it induce partial compensatory growth and reducing the production cost with Artemia nauplii. CRediT authorship contribution statement Leonnan Carlos Carvalho de Oliveira: Investigation, Resources, Data curation, Writing - original draft. Lucas Gabriel Baltazar Costa: Investigation, Resources, Data curation. Bruno José Corecha Fernandes Eiras: Investigation, Resources, Data curation, Supervision. Marcos Ferreira Brabo: Conceptualization, Methodology, Writing original draft, Supervision. Galileu Crovatto Veras: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing. Lorena Batista de Moura: Conceptualization, Methodology, Writing - original draft, Writing - review & editing, Supervision. Ana Lúcia Salaro: Conceptualization, Methodology, Writing - review & editing. Daniel Abreu Vasconcelos Campelo: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing, Supervision, Project administration. Declaration of Competing Interest The authors report no declarations of interest. Acknowlegments The present study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brasília, DF, Brazil, and the Pró-reitoria de Pesquisa e Pós-graduação of Universidade Federal do Pará (PROPESP/UFPA), Belém, PA, Brazil. References Abe, H.A., Dias, J.A.R., Reis, R.G.A., Sousa, N.C., Ramos, F.M., Fujimoto, R.Y., 2016. Manejo alimentar e densidade de estocagem na larvicultura do peixe ornamental amazônico Heros severus. Bol. Inst. Pesca. 42 (3), 514–522. https://doi.org/10. 20950/1678-2305.2016v42n3p514. Abe, H.A., Dias, J.A.R., Sousa, N.C., Couto, M.V.S., Reis, R.G.A., Paixão, P.E.G., Fujimoto, R.Y., 2019. Growth of Amazon ornamental fish Nannostomus beckfordi larvae (Steindachner, 1876) submitted to different stocking densities and feeding management in captivity conditions. Aquac. Res. 50 (8), 2276–2280. https://doi.org/10. 1111/are.14108. 5 Aquaculture Reports 18 (2020) 100436 L.C.C.d. Oliveira, et al. Silva, A.P., Mendes, P.P., 2006. Influência de duas dietas na qualidade de água dos tanques berçário, utilizados no cultivo de camarão marinho Litopenaeus vannamei (Boone, 1931). Acta Sci. Anim. Sci. 28 (1), 105–111. https://doi.org/10.4025/ actascianimsci.v28i1.670. Stawikowski, R., Werner, U., 1998. Die Buntbarsche Amerikas, band 1. Verlag Eugen Ulmer, Stuttgart, Germany. Urbinati, E.C., Sarmiento, S.J., Takahashi, L.S., 2014. Short-term cycles of feed deprivation and refeeding promote full compensatory growth in the Amazon fish matrinxã (Brycon amazonicus). Aquaculture 433, 430–433. https://doi.org/10.1016/j. aquaculture.2014.06.030. Vainikka, A., Huusko, R., Hyvärinen, P., Korhonen, P.K., Laaksonen, T., Koskela, J., Vielma, J., Hirvonen, H., Salminen, M., 2012. Food restriction prior to release reduces precocious maturity and improves migration tendency of Atlantic salmon (Salmo salar) smolts. Can. J. Fish. Aquat. Sci. 69 (12), 1981–1993. https://doi.org/10. 1139/f2012-119. Veras, G.C., Soares, L.M.O., Brabo, M.F., Paixão, D.J.M.R., Dias, B.C.B., Alves, A.X., Murgas, L.D.S., Campelo, D.A.V., 2016a. Fotoperíodo e frequência alimentar na larvicultura do acará-bandeira Pterophyllum scalare. Arch. Zootec. 65 (252), 581–584. https://doi.org/10.21071/az.v65i252.1930. Veras, G.C., Paixão, D.J.M.R., Brabo, M.F., Soares, L.M.O., Sales, A.D., 2016b. Influence of photoperiod on growth, uniformity, and survival of larvae of the Amazonian ornamental Heros severus (Heckel, 1840). R. Bras. Zootec. 45 (7), 422–426. https://doi. org/10.1590/S1806-92902016000700010. Xie, F., Ai, Q., Mai, K., Xu, W., Ma, H., 2011. The optimal feeding frequency of large yellow croaker (Pseudosciaena crocea, Richardson) larvae. Aquaculture. 311 (1–4), 162–167. https://doi.org/10.1016/j.aquaculture.2010.12.005. Ye, J.D., Chen, J.C., Wang, K., 2016. Growth performance and body composition in response to dietary protein and lipid levels in Nile tilapia (Oreochromis niloticus Linnaeus, 1758) subjected to normal and temporally restricted feeding regimes. J. Appl. Ichthyol. 32 (2), 332–338. https://doi.org/10.1111/jai.13004. Yilmaz, E., Arik, R.O., Ari, B., Yilmaz, A., Gok, A., 2018. The investigation of the effects of different feeding strategies on the growth of dolphin cichlid (Cyrtocara moori Boulenger, 1902) fish. Aquac. Res. 49 (9), 3004–3010. https://doi.org/10.1111/are. 13761. Zuanon, J.A.S., Salaro, A.L., Furuya, W.M., 2011. Produção e nutrição de peixes ornamentais. R. Bras. Zootec. 40 (Esp) 165-17. tamanho da presa e do acréscimo de ração na larvicultura de pacamã. R. Bras. Zootec. 37 (7), 1144–1150. https://doi.org/10.1590/S1516-35982008000700002. Pereira, S.L., Gonçalves Junior, L.P., Azevedo, R.V., Matielo, M.D., Selvatici, P.D.C., Amorim, I.R., Mendonça, P.P., 2016. Diferentes estratégias alimentares na larvicultura do acará-bandeira (Peterolophyllum scalare, Cichlidae). Acta Amaz. 46 (1), 91–98. https://doi.org/10.1590/1809-4392201500472. Portella, M.C., Dabrowski, K., 2008. Diets, physiology, biochemistry and digestive tract development of freshwater fish larvae. In: Cyrino, J.E.P., Bureau, D.P., Kapoor, B.G. (Eds.), Feeding and Digestive Functions of Fishes. Science Publishers, Enfield, pp. 227–279. Portella, M.C., Verani, J.R., Cestarolli, M.A., 2000. Use of live and artificial diets enriched with several fatty acid sources to feed Prochilodus scrofa larvae and fingerlings. 1. Effects on survival and growth rates. J. Aquac. Trop. 15 (1), 45–58. Salaro, A.L., Campelo, D.A.V., Pontes, M.D., Tavares, M.M., Zuanon, J.A.S., Luz, R.K., 2012. Saline water for juvenile giant trahira during feed training. R. Bras. Zootec. 41 (6), 1342–1345. https://doi.org/10.1590/S1516-35982012000600004. Sanches, E.G., Tosta, G.A.M., Souza-Filho, J.J., 2013. Viabilidade econômica da produção de formas jovens de bijupirá (Rachycentron canadum). Bol. Inst. Pesca. 39 (1), 15–26. Santos, J.C.E., Correia, E.S., Luz, R.K., 2015a. Effect of daily Artemia nauplii concentrations during juvenile production of lophiosilurus alexandri. Bol. Inst. Pesca. 41 (Esp), 771–776. https://doi.org/10.20950/1678-2305.2015v41nep771. Santos, E.L., Souza, A.P.L., Pontes, E.C., Gonzaga, L.S., Ferreira, A.J.S., 2015b. Folha de amendoeira (Terminalia catappa) como aditivo promotor de crescimento em rações para alevinos de Tilápia do Nilo (Oreochromis niloticus). Rev. Agrotec. 36 (1), 190–196. Santos, E.L., Soares, A.C.L., Tenório, O.L.D., Soares, E.C., Silva, T.J., Gusmão Júnior, L.F., Santos, E.L., 2018. Desempenho de tambaquis (Colossoma macropomum) submetidos a restrição alimentar e a realimentação em tanques-rede. Arq. Bras. Med. Vet. Zootec. 70 (3), 931–938. https://doi.org/10.1590/1678-4162-9891. Schütz, J.H., Weingartner, M., Zaniboni-Filho, E., Nuñer, A.P.O., 2008. Crescimento e sobrevivência de larvas de suruvi Steindachneridion scriptum nos primeiros dias de vida: influência de diferentes alimentos e fotoperíodos. Bol. Inst. Pesca. 34 (3), 443–451. Selvatici, P.D.C., Valério Júnior, J.F., Farias, W.M., Santos, B.D., Mendonça, P.P., 2017. Manejo alimentar de juvenis de acará bandeira (Pterophyllum scalare). Nutr. Rev. Eletrôn. 14 (1), 4919–4927. 6