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Influence of guava residue on tambaqui growth performance

ABSTRACT.

Fruit residues represent alternative ingredients that can be included in diets of tambaqui, Colossoma macropomum. This study evaluated the growth performance of tambaqui fed diets containing different levels of guava agroindustrial residue. The experiment was based on a completely randomised design, with 105 fish randomly distributed in 15 plastic 60 L-1 boxes with a water recirculation system. Feeding was carried out to apparent satiety for 45 days, using diets with 0, 50, 100, 150 and 200 g kg-1 inclusion of guava residue. Biometrics were performed every 15 days. Quadratic effect (p < 0.05) was observed for daily feed intake and apparent feed conversion, with optimum levels of 4.86 and 6.05% inclusion of guava residue, respectively. There was no significant difference (p > 0.05) in relation to final weight, weight gain, specific growth rate, hepato-somatic index, survival rate and protein efficiency rate by the dietary treatments. The inclusion of up to 150 g kg-1 of the guava agroindustrial residue in the feed did not compromise the performance of tambaqui juveniles.

Keywords:
agroindustrial residues; Psidium guajava; fish nutrition; Colossoma macropomum

Introduction

Tambaqui, Colossoma macropomum, is a fish species native to the Amazon region with an omnivorous/fruity diet with potential for fish farming due to its rusticity, tolerance to low concentrations of dissolved oxygen in the water, rapid growth and ease of handling (Acuña & Rangel, 2009Acuña, J. J. A., & Rangel, J. L. H. (2009). Efectos del extracto hipofisiario de carpa común y el análogo de la GNRH sobre la maduración final del oocito y el desove de la cachama negra (Colossoma macropomum). Revista Científica, 19(5), 486 - 494. ; Dairiki & Silva, 2011Dairiki, J. K., & Silva, T. B. A. (2011). Revisão de literatura: exigências nutricionais do tambaqui - compilação de trabalhos, formulação de ração adequada e desafios futuros (Documentos, 91. M.I. N° 4/2011). Manaus, AM: Embrapa Amazônia Ocidental. ; Santos et al., 2013Santos, M. Q. C., Lima, M. C., Santos, L., Pereira‑Filho, M., Ono, E. A., & Affonso, E. G. (2013). Feeding strategies and energy to protein ratio on tambaqui performance and physiology. Pesquisa Agropecuária Brasileira, 48(8), 955-961. DOI: https://doi.org/10.1590/S0100-204X2013000800021
https://doi.org/https://doi.org/10.1590/...
; Ribeiro et al., 2016Ribeiro, F. M., Freitas, P. V. D. X., Santos, E. O., Sousa, R. M., Carvalho, T. A., Almeida, E. M., ... Costa, A. C. (2016). Alimentação e nutrição de Pirapitinga (Piaractus brachypomums) e Tambaqui (Colossoma macropomum). Publicações em Medicina Veterinária e Zootecnia, 10(12), 873-882. ). In Brazil, tambaqui is the second most cultivated species with a production of approximately 101 thousand tons in 2019, occurring mainly in the north and northeast regions of the country (Instituto Brasileiro de Geografia e Estatística [IBGE], 2020Instituto Brasileiro de Geografia e Estatística [IBGE]. (2020). Produção da pecuária municipal 2019. Brasilia, DF: IBGE. ).

Fish feed can represent 70% of the production costs of fish farming, due to the use of expensive traditional ingredients of high economic value in the composition of the rations, making it necessary to search for alternative ingredients. One option is to substitute with fruit residues from agroindustry (Silva, Pereira-Filho, Cavero, & Pereira, 2007Silva, J. A. M., Pereira-Filho, M., Cavero, B. A. S., & Pereira, M. I. O. (2007). Digestibilidade aparente dos nutrientes e energia de ração suplementada com enzimas digestivas exógenas para juvenis de tambaqui (Colosssoma macropomum Cuvier, 1818). Acta Amazônica, 37(1), 157-164. DOI: https://doi.org/10.1590/S0044-59672007000100021
https://doi.org/https://doi.org/10.1590/...
; Santos, Ludke, Barbosa, Rabello, & Ludke, 2009Santos, E. L., Ludke, M. C. M., Barbosa, J. M., Rabello, C. B. V., & Ludke, J. V. (2009). Digestibilidade aparente do farelo de coco e resíduo de goiaba pela tilápia do Nilo (Oreochromis niloticus). Revista Caatinga, 22(2), 175-180. ; Souza et al., 2013Souza, R. C., Melo, J. F. B., Nogueira-Filho, R. M., Campeche, D. F. B., & Figueiredo, R. A. C. R. (2013). Influência da farinha de manga no crescimento e composição corporal da tilápia do Nilo. Archivos de Zootecnia, 62(238), 217-225. DOI: https://dx.doi.org/10.4321/S0004-05922013000200007
https://doi.org/https://dx.doi.org/10.43...
).

The fruit processing industries are of great importance in the generation of waste, especially those that work with the production of fruit juices and pulps, generating bagasse, peel and seed. The residue of fruits such as orange, apple, mango and papaya, have soluble carbohydrates (fructose, glucose and sucrose), crude fiber (cellulose), proteins and vitamins, being an alternative for animal feed (Mirabella, Castellani, & Sala, 2014Mirabella, N., Castellani, V., & Sala, S. (2014). Current options for the valorization of food manufacturing waste: a review. Journal of Cleaner Production, 65(1), 28-41. DOI: http://dx.doi.org/10.1016/j.jclepro.2013.10.051
https://doi.org/http://dx.doi.org/10.101...
). Fruits like Ziziphus jujube demonstrated potential useful effects of on skin mucosal immunity in carps fingerlings (Hoseinifar et al., 2019Hoseinifar, S. H., Zou, H. K., Doan, H. V., Harikrishnan, R., Yousefi, M., Paknejad, H., & Ahmadifar, E. (2019). Can dietary jujube (Ziziphus jujubaMill.) fruit extract alter cutaneous mucosal immunity, immune related genes expression in skin and growth performance of common carp (Cyprinus carpio)? Fish & Shellfish Immunology, 94(1), 705-710. DOI: https://doi.org/10.1016/j.fsi.2019.09.016
https://doi.org/https://doi.org/10.1016/...
).

According to previous studies, the chemical composition of the guava residue varies between 0.17% starch, 2-11% protein, 3-7% moisture, 11-14% lipids, 1-2% ash and 63.94% crude fiber (Uchôa-Thomaz et al., 2014Uchôa-Thomaz, A. M. A., Sousa E. C., Carioca J. O. B., De Morais, S. M., De Lima, A., Martins, C. G., ... Rodrigues, L. L. (2014) Chemical composition, fatty acid profile and bioactive compounds of guava seeds (P. guajava L.). Food Science Technology, 34(3), 485-492. DOI: https://doi.org/10.1590/1678-457x.6339
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), which can be used with an alternative ingredient in the formulation of feed for omnivorous fish (Silva et al., 2009Silva, E. P., Silva, D. A. T., Rabello, B. V. C., Lima, R. B., Lima, M. B., & Ludke, J. V. (2009). Composição físico-química e valores energéticos dos resíduos de goiaba e tomate para frangos de corte de crescimento lento. Revista Brasileira de Zootecnia, 38(6), 1051-1058. DOI: https://doi.org/10.1590/S1516-35982009000600012
https://doi.org/https://doi.org/10.1590/...
).

Previous studies have demonstrated the viability of using fruit residues in the formulation of diets for tambaqui, providing a satisfactory zootechnical performance. Plantains and pupunha have been shown as energy sources for this species and can replace wheat bran in a proportion of 30% (Lochmann et al., 2009Lochmann, R., Chen, R., Chu-Koo, F. W., Camargo, W. N., Kohler, C. C., & Kasper, C. (2009). Effects of carbohydrate-rich alternative feedstuffs on growth, survival, body composition, hematology, and nonspecific immune response of black pacu, Colossoma macropomum, and red pacu, Piaractus brachypomus. Journal of the World Aquaculture Society, 40(1), 33-44. DOI: https://doi.org/10.1111/j.1749-7345.2008.00232.x
https://doi.org/https://doi.org/10.1111/...
). The babassu by-product contains approximately 20% crude protein, 4.6% lipid and 18% crude fiber, and can partially replace soybean meal and ground corn in the tambaqui diet (Lopes et al., 2010Lopes, J. M., Pascoal, L. A. F., Silva-Filho, F. P., Santos, I. B., Watanabe, P. H., Araújo, D. M., ... Oliveira, P. S. (2010). Farelo de babaçu em dietas para tambaqui. Revista Brasileira de Saúde e Produção Animal, 11(2), 519- 526. ). The substitution of soybean meal by coconut meal did not compromise the weight gain, daily feed consumption, feed conversion and specific growth rate of this species (Lemos, Guimarães, & Miranda, 2011Lemos, M. V. A., Guimarães, I. G., & Miranda, E. C. (2011). Farelo de coco em dietas para o tambaqui (Colossoma macropomum). Revista Brasileira de Saúde e Produção Animal, 12(1), 188-198. ). Mango flour represented a source of carbohydrates, replacing up to 50% soy bran and fish meal in diets for tambaqui (Bezerra, Souza, Melo, & Campeche, 2014Bezerra, S. K., Souza, R. C., Melo, J. F. B., & Campeche, D. F. B. (2014). Crescimento de tambaqui alimentado com diferentes níveis de farinha de manga e proteína na ração. Archivos de Zootecnia, 63(244), 587-598. DOI: https://doi.org/10.4321/S0004-05922014000400003
https://doi.org/https://doi.org/10.4321/...
). Tambaquis showed satisfactory digestibility and zootechnical performance when fed diets containing 8% banana meal to replace corn bran (Silva et al., 2020Silva, A. F., Copatti, C. E., Oliveira, E. P., Bonfá, H. C., Melo, F. V. S. T., Camargo, A. C. S., & Melo, J. F. B. (2020). Effects of whole banana meal inclusion as replacement for corn meal on digestibility, growth performance, haematological and biochemical variables in practical diets for tambaqui juveniles (Colossoma macropomum). Aquaculture Reports, 17(1), 1- 8. DOI: https://doi.org/10.1016/j.aqrep.2020.100307
https://doi.org/https://doi.org/10.1016/...
). Further studies on the inclusion of fruit residues in the diet of this species are still necessary.

The objective in this study was to evaluate the performance of tambaqui fed diets containing different levels of guava agroindustrial residue from fruit pulp production.

Material and methods

Processing of guava residue

The study was approved by the Ethics Committee of the Universidade Federal Sergipe - UFS (CEUA/CEPAP-UFS 02/2017). The experiment was based on a completely randomised design, consisting of 5 treatments and 3 replicates. The treatments comprised one control diet and four experimental diets, containing 0, 50, 100, 150 and 200 g kg-1 inclusion of guava agroindustrial residue.

The guava residue from pulp production, basically consisting of seeds and pulp, was donated by an industry (Pomar do Brasil) located in the city of Aracaju, Brazil. The residue was sent to the LANCOA- DEPAQ, UFS, Brazil. The residue was frozen at -18°C, dehydrated in a forced air circulation oven at 55°C for 48h and minced in a willey-type knife mill to obtain the meal with 1-mm granulometry. A sample of the meal was collected for determination of the proximate composition (Table 1).

Table 1
Proximate composition: crude energy (CE), dry matter (DM), neutral detergent fibers (NDF), total carbohydrate (TCHO), ethereal extract (EE), crude protein (CP) and ashes (ASH) of the guava residue (% dry matter).

Formulation of diets

The diets were formulated to meet the nutritional requirements of tambaqui according to Oliveira, Miranda, and Correa (2012Oliveira, A. C. B., Miranda, E. C., & Correa, R. (2012). Exigências nutricionais e alimentação do tambaqui. In D. M. Fracalossi, & J. E. P. Cyrino, Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira (p. 3-63). Florianópolis, SC: Gráfica e Editora Copiart Ltda. ). The guava residue meal was included in the feed at 0, 50, 100, 150 and 200 g kg-1 The guave residue was homogenised with the other ingredients with the addition of water at 65°C. The homogeneous material was processed in an electric grinder to form pellets and dried in a forced circulation air oven at 55°C for 24h to produce the experimental diets. Five isoproteic (310 g kg-1 crude protein) and isoenergetic rations (3700 kcal kg-1 crude energy) were formulated according to the fish feed formulation sheet, described in Table 2.

Nutritional analysis

Analyses of proximate composition of guava residue, experimental rations and fish were carried out at the LANA-DZO, UFS, Brazil. The levels of different components were determined as follows: dry matter (DM) by greenhouse dehydration; ash (ASH) by muffle incineration; crude protein (CP) by Kjeldahl and ethereal extract (EE) by Weende. Neutral detergent fibre content (NDF) was determined in guava residue (Silva & Queiroz, 2005Silva, D. J., & Queiroz, A. C. (2005). Análise de alimentos: métodos químicos e biológicos. Viçosa, MG.: UFV. ).

Total carbohydrate content (TCHO) was obtained by difference, decreasing by 100% the sum of ASH, CP and EE. Crude energy (CE) was calculated from the approximate centesimal conversion fator of Atwater (Núcleo de Estudos e pesquisas em Alimentação [Nepa], 2011Núcleo de Estudos e pesquisas em Alimentação [Nepa]. (2011). Tabela brasileira de composição de alimentos - TACO. Campinas, SP: NEPA; Unicamp. ).

Table 2
Formulation and proximate composition of the experimental diets containing 0, 50, 100, 150 and 200 g kg-1 inclusion of guava agroindustrial residue.

Growth performance experiment

Juvenile tambaqui, C. Macropomum, were acquired from CODEVASF 5th Fisheries Station and were subjected to 9 days of acclimatisation and 13 days of treatment with enrofloxacin, malachite green and common salt. The fish were kept in two polyethylene tanks with a capacity of 500 L and fed commercial diets containing 320 g kg-1 crude protein, 60 g kg-1 ethereal extract, 120 g kg-1 mineral matter and 4447 kcal kg-1 crude energy.

During the acclimation period, the fish were subjected to initial biometry with 7 individuals per experimental unit. Mean weight and standard deviation was 6.09 ± 0.39 g and mean length was 7.22 ± 0.20 cm. The experimental units consisted of 15 rectangular plastic boxes (60-L capacity) which were individually aerated, with filtration through a water recirculation system fitted with a biofilter, and thermostatically heat-controlled.

The concentrations of dissolved oxygen (mg L-1), temperature (ºC) and pH were measured daily using a multiparameter (Hanna, HI 9829, Portugal). Concentrations of total ammonia (ppm) and nitrite (ppm) were determined twice a week by colorimetry (Alfakit, Camboriú, Brazil). The following values were obtained: dissolved oxygen 4.77 ± 0.15 mg L-1; pH 5.41 ± 0.11; temperature 29.90 ± 0.27°C; total ammonia 0.25 ± 0.13 ppm and nitrite 0.75 ± 0.54 ppm.

Feed was offered at 9:00 am and 3:00 pm until the apparent satiety; the weight of the consumed ration was recorded. Biometrics were performed every 15 days using an ichthyometer and digital scales. The experiment was completed after a period of 45 days. Fish were subjected to euthanasia by immersdion in an ice bath, followed by section of the spinal cord. Fish were dissected and the livers collected for weighing.

Growth performance parameters were determined in the fish by Fracalossi, Rodrigues, Silva, and Cyrino (2012Fracalossi, D. M., Rodrigues, A. P. O., Silva, T. S. C. E., & Cyrino, J. E. P. (2012). Técnicas experimentais em nutrição de peixes. In D. M. Fracalossi, & J. E. P. Cyrino, Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira (p. 3-63). Florianópolis, SC: Gráfica e Editora Copiart Ltda. ) for weight gain (WG), apparent feed convertion (FC), specific growth rate (SGR), hepatic-somatic index (HSI), survival rate (SR), protein efficiency rate (PER) and Costa-Bomfim, Silva, Bezerra, Druzian, and Cavalli (2017Costa-Bomfim, C. N., Silva, A. V., Bezerra, R. S., Druzian, J. I., & Cavalli, R. O. (2017). Growth, feed efficiency and body composition of juvenile cobia (Rachycentron canadum Linnaeus, 1766) fed increasing dietary levels of shrimp protein hydrolysate. Aquaculture Research, 48(4), 1759-1766. DOI: https://doi.org/10.1111/are.13013
https://doi.org/https://doi.org/10.1111/...
) for daily feed intake (DFI). The equations (1, 2, 3, 4, 5, 6, and 7) can be seen as follows:

<mml:math><mml:mtext>Weight gain (WG) = final weight - initial weight</mml:mtext></mml:math> (1)

Apparent feed conversion (FC) = total apparent feed intake weightgain-1(2)

Specific growth rate (SGR) = [ln (final weight) - ln (initial weight) / feeding period (days)] × 100(3)

Hepatic-somatic index (HSI) = liver weight × 100 / live weight(4)

Survival rate (SR) = (final number of fish × 100) / initial number of fish(5)

Protein efficiency rate (PER) = (weight gain / protein intake)(6)

Daily feed intake (DFI) = (feed intake) / [(final weight + initial weight) / 2] / days of trial × 100(7)

Statistical analysis

The effects of the experimental diets on growth performance parameters in tambaqui were subjected to analysis of variance, Tukey test and, when significant, a regression test at 5% of significance was performed. Statistical analyses were performed using the statistical programme, Sisvar 5.6 (Ferreira, 2011Ferreira, D. F. (2011). Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia, 35(6), 1039-1042. DOI: https://doi.org/10.1590/S1413-70542011000600001
https://doi.org/https://doi.org/10.1590/...
).

Results and discussion

Composition of the guava agroindustrial residue was as follows: 4652.90 kcal kg-1 in CE, 917.0 g kg-1 in DM, 733.1 g kg-1 in NDF, 709.6 g kg-1 in TCHO, 154.9 g kg-1 in EE, 105.1 g kg-1 in CP and 30.4 g kg-1 in ASH. The guava residue can be considered an energetic ingredient due to the low protein concentration and high energy content.

Table 3 shows the mean values and standard deviation of IW, FW, WG, DFI, FC, SGR, HSI, SR and PER in tambaqui given diets containing 0, 50, 100, 150 and 200 g kg-1 guava residue. The analysis of variance showed that there was no significant difference (p > 0.05) between treatments in relation to FW, WG, SGR, HSI, SR and PER. Regarding the DFI and FC, a significant difference was observed.

Table 3
Mean values (±SD) of initial weight (IW), final weight (FW), weight gain (WG), daily feed intake (DFI), apparent feed conversion (FC), specific growth rate (SGR), hepato-somatic index (HSI), survival rate (SR) and protein efficiency rate (PER) of tambaqui, Colossoma macropomum, fed rations containing 0, 50, 100, 150 and 200 g kg-1 inclusion of guava residue.

The regression analysis indicated a quadratic effect in relation to the DFI and FC. For DFI, the optimum level was 4.86% inclusion of the guava residue, expressed bythe equation Y = 3.504 - 0.037x + 0.003x2 (R2 = 90.95%). In FC, the ideal level was 6.05% inclusion of guava residue, expressed by the equation: Y = 0.992 - 0.014x + 0.001x2 (R2 = 96.46%).

The effect of feed containing inclusion levels of guava agroindustrial residue on daily feed intake and apparent feed conversion in tambaqui is represented by means of scatter plots and quadratic regression equations that are represented in Figure 1 and 2.

The tambaqui showed satisfactory weight gain reaching approximately 9× (900%) their initial weight at day 45 of the experiment. The apparent feed conversion was also satisfactory, since fish needed to consume around 1 g of feed to gain the same value in body weight. As for the centesimal composition of the fish (Table 4), a significant difference (p <0.05) was observed only for the ethereal extract (EE) content among the tambaqui fed the diet without guava residue inclusion and those receiving the diets containing 150 and 200 g kg-1 residue.

The content of ash (3.04%), ethereal extract (15.49%), neutral detergent fibres (73.31%) and crude energy (4652.90 kcal kg-1) in the guava agroindustrial residue used in this study were higher than those reported by Silva et al. (2009Silva, E. P., Silva, D. A. T., Rabello, B. V. C., Lima, R. B., Lima, M. B., & Ludke, J. V. (2009). Composição físico-química e valores energéticos dos resíduos de goiaba e tomate para frangos de corte de crescimento lento. Revista Brasileira de Zootecnia, 38(6), 1051-1058. DOI: https://doi.org/10.1590/S1516-35982009000600012
https://doi.org/https://doi.org/10.1590/...
), where values were 1.25%, 11.71%, 64.06% and 4290 kcal kg-1, respectively. Santos et al. (2009Santos, E. L., Ludke, M. C. M., Barbosa, J. M., Rabello, C. B. V., & Ludke, J. V. (2009). Digestibilidade aparente do farelo de coco e resíduo de goiaba pela tilápia do Nilo (Oreochromis niloticus). Revista Caatinga, 22(2), 175-180. ) reported crude energy values of 5389 kcal kg-1 in guava residue, higher than the value obtained in this experiment. The content of dry matter (91.70%) and crude protein (10.51%) was similar to that found by Silva et al. (2009), 90.81% and 10.09% respectively. The different values of centesimal composition for this residue are related to the different conditions for cultivation and processing of the fruit.

Figure 1
Scatter plot of the means and quadratic regression equation showing the effect of rations containing 0, 50, 100, 150 and 200 g kg(1 of guava agroindustrial residue on the daily feed intake of tambaqui, Colossoma macropomum.

Figure 2
Scatter plot of the means and quadratic regression equation showing the effect of rations containing 0, 50, 100, 150 and 200 g kg-1 of guava agroindustrial residue on the apparent feed conversion of tambaqui, Colossoma macropomum.

Table 4
Proximate composition: dry matter (CM), crude protein (CP), ethereal extrfact (EE) and asches (ASH) of tambaqui, Collossoma macropomum fed diets containing 0, 50, 100, 150 and 200 g kg-1 inclusion of grava residue (neam ± SD, % dry matter).

In a study with Nile tilapia, O. niloticus, was estimated the digestibility the guava residue, obtaining 6.89% of digestible protein and 3601.13 kcal kg-1 of digestible energy (Santos et al., 2009Santos, E. L., Ludke, M. C. M., Barbosa, J. M., Rabello, C. B. V., & Ludke, J. V. (2009). Digestibilidade aparente do farelo de coco e resíduo de goiaba pela tilápia do Nilo (Oreochromis niloticus). Revista Caatinga, 22(2), 175-180. ). The inclusion to 15% of the agroindustrial residue of pineapple in diets for Nile tilápia did not compromise the weight gain and survival of the fish (Lima et al., 2012Lima, M. R., Ludke, M.C. M. M., De Holanda, M. C. R., Pinto, B. W C., Ludke, J. V., & Santos, E. L. (2012). Performance and digestibility of Nile tilapia fed with pineapple residue bran. Acta Scientiarum. Animal Sciences, 34(1), 41-47. DOI: https://doi.org/10.4025/actascianimsci.v34i1.12083
https://doi.org/https://doi.org/10.4025/...
). The results demonstrate that residues of pineapple and guava can be included in diets of omnivorous fish.

Tambaqui that were fed diets containing until 20% of guava residue demonstrated satisfactory weight gain, reaching approximately 9× (900%) their initial weight at day 45 of the experiment. This shows that the fish used in this study had a good productive development, since it is suggested that studies of growth performance in large fish are completed when a weight gain of 2 to 3× (200% to 300%) the initial weight has been reached, or after 8 to 12 weeks of feeding (Jobling, 2012Jobling, M. (2012). National research council (NRC): nutrient requirements of fish and shrimp.Aquaculture International , 20(1), 601-602. DOI: https://doi.org/10.1007/s10499-011-9480-6
https://doi.org/https://doi.org/10.1007/...
).

Development of the fish is mainly influenced by concentrations of energy and protein in the diet; imbalance of this relationship can compromise use of the protein fraction, adversely affecting animal growth (Ribeiro et al., 2016Ribeiro, F. M., Freitas, P. V. D. X., Santos, E. O., Sousa, R. M., Carvalho, T. A., Almeida, E. M., ... Costa, A. C. (2016). Alimentação e nutrição de Pirapitinga (Piaractus brachypomums) e Tambaqui (Colossoma macropomum). Publicações em Medicina Veterinária e Zootecnia, 10(12), 873-882. ). Energy is not a nutrient, but it is of paramount importance in biochemical and physiological processes related to growth, maintenance and reproduction (Boscolo, Signor, Freitas, Bittencourt, & Feiden, 2011Boscolo, W. R., Signor, A., Freitas, J. M. A., Bittencourt, F., & Feiden, A. (2011). Nutrição de peixes nativos. Revista Brasileira de Zootecnia, 40 (supl esp), 145-154. ). Protein is the main organic constituent of fish tissues, accounting for 65 and 75% of total body dry matter, which makes it key to structural conformation (muscle, collagen and keratin), regulation of metabolism (enzymes and hormones), transport (haemoglobin) and immune defense (antibodies) (Kaushik & Seiliez, 2010Kaushik, S. J., & Seiliez, I. (2010). Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquaculture Research, 41(3), 322-332. DOI: https://doi.org/10.1111/j.1365-2109.2009.02174.x
https://doi.org/https://doi.org/10.1111/...
).

Thus, we can explain the satisfactory weight gain of the tambaqui in this experiment, since the guava residue has a high energy level of 4652.90 kcal kg-1, may have a protein-sparing effect that was destined for fish growth (Ribeiro et al., 2016Ribeiro, F. M., Freitas, P. V. D. X., Santos, E. O., Sousa, R. M., Carvalho, T. A., Almeida, E. M., ... Costa, A. C. (2016). Alimentação e nutrição de Pirapitinga (Piaractus brachypomums) e Tambaqui (Colossoma macropomum). Publicações em Medicina Veterinária e Zootecnia, 10(12), 873-882. ). This same effect was observed when mango residue was added to the diet of tambaqui juveniles (Bezerra et al., 2014Bezerra, S. K., Souza, R. C., Melo, J. F. B., & Campeche, D. F. B. (2014). Crescimento de tambaqui alimentado com diferentes níveis de farinha de manga e proteína na ração. Archivos de Zootecnia, 63(244), 587-598. DOI: https://doi.org/10.4321/S0004-05922014000400003
https://doi.org/https://doi.org/10.4321/...
). The diet containing 20% guava residue produced a weight gain in tambaqui of 54.38 ± 6.2 g higher than that 18.92 g reported by Lopes et al. (2010Lopes, J. M., Pascoal, L. A. F., Silva-Filho, F. P., Santos, I. B., Watanabe, P. H., Araújo, D. M., ... Oliveira, P. S. (2010). Farelo de babaçu em dietas para tambaqui. Revista Brasileira de Saúde e Produção Animal, 11(2), 519- 526. ), using feed with inclusion of 12% babaçu residue.

With regard to the daily feed intake, the ideal level of guava residue inclusion was estimated at 4.86%, at this level the tambaqui increased their intake to maintain their weight gain, influencing the apparent feed conversion that presented level with 6.05% inclusion. Less satisfactory results were obtained for these parameters with 20% inclusion, suggesting that the high NDF content (73.31%) of the guava residue interfered with the utilisation of the rations. This is because the tambaqui, as with other fish species, do not produce the enzyme cellulase, reducing their capacity to digest structural carbohydrates (Boscolo et al., 2011Boscolo, W. R., Signor, A., Freitas, J. M. A., Bittencourt, F., & Feiden, A. (2011). Nutrição de peixes nativos. Revista Brasileira de Zootecnia, 40 (supl esp), 145-154. ).

The same effect was observed by Souza et al. (2013Souza, R. C., Melo, J. F. B., Nogueira-Filho, R. M., Campeche, D. F. B., & Figueiredo, R. A. C. R. (2013). Influência da farinha de manga no crescimento e composição corporal da tilápia do Nilo. Archivos de Zootecnia, 62(238), 217-225. DOI: https://dx.doi.org/10.4321/S0004-05922013000200007
https://doi.org/https://dx.doi.org/10.43...
), in a study where maize was replaced with mango residue in proportions of 0, 33, 66 and 100% in feed of Nile tilapia, and results showed an increase in feed conversion values as the replacement level increased. In general, the use of up to 9.0% crude fiber in the feed of omnivorous species such as tambaqui and tilapia is reported (Boscolo et al., 2011Boscolo, W. R., Signor, A., Freitas, J. M. A., Bittencourt, F., & Feiden, A. (2011). Nutrição de peixes nativos. Revista Brasileira de Zootecnia, 40 (supl esp), 145-154. ).

Specific growth rates of 4.84, 4.95, 5.38, 4.92 and 5.15% were achieved with 0, 50, 100, 150 and 200 g kg-1 of guava residue, respectively, and were considered to be satisfactory. Tambaqui presented similar results with a 4% growth rate when fed with diets containing 50% of mango residue (Bezerra et al., 2014Bezerra, S. K., Souza, R. C., Melo, J. F. B., & Campeche, D. F. B. (2014). Crescimento de tambaqui alimentado com diferentes níveis de farinha de manga e proteína na ração. Archivos de Zootecnia, 63(244), 587-598. DOI: https://doi.org/10.4321/S0004-05922014000400003
https://doi.org/https://doi.org/10.4321/...
). This parameter has been used to evaluate experimental diets and ingredients with regard to the relationship between weight gain and feeding period, and is an important indicator of fish growth (Fracalossi et al., 2012Fracalossi, D. M., Rodrigues, A. P. O., Silva, T. S. C. E., & Cyrino, J. E. P. (2012). Técnicas experimentais em nutrição de peixes. In D. M. Fracalossi, & J. E. P. Cyrino, Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira (p. 3-63). Florianópolis, SC: Gráfica e Editora Copiart Ltda. ).

Leporinus obtusidens juveniles fed with diets containing 7% of guava residue for 45 days, had a SGR of 0.73 ± 0.03% (Lazzari et al., 2015Lazzari, R., Uczay, J., Rodrigues, R. B., Pianesso, D., Adorian, T. J., & Mombach, P. I. (2015). Utilização de resíduos de frutas em dietas para piava. Boletim do Instituto de Pesca, 41(2), 227-237. ), lower than the tambaqui in this study (5.15 ± 0.1%) which received a diet containing 200 g kg-1 guava residue. This result shows that tambaqui demonstrate better body development than the piava, although these species have similar gastrointestinal tracts, with the presence of trypsin and chymotrypsin enzymes in the intestine (Rodrigues, 2014Rodrigues, A. P. O. (2014). Nutrição e alimentação do tambaqui (Colossoma macropomum). Boletim do Instituto de Pesca, 40(1), 135-145. ; Lazzari et al., 2015Lazzari, R., Uczay, J., Rodrigues, R. B., Pianesso, D., Adorian, T. J., & Mombach, P. I. (2015). Utilização de resíduos de frutas em dietas para piava. Boletim do Instituto de Pesca, 41(2), 227-237. ), and were fed with rations containing the same test ingredient.

The HSI represents the energy storage capacity of fish and indicates the effect of antinutritional factors present in food. Decrease in the hepato-somatic index shows that energy reserves present in the liver were used to compensate for energy losses, or, is a response to the action of antinutritional factors present in a certain ingredient (Lopes et al., 2010Lopes, J. M., Pascoal, L. A. F., Silva-Filho, F. P., Santos, I. B., Watanabe, P. H., Araújo, D. M., ... Oliveira, P. S. (2010). Farelo de babaçu em dietas para tambaqui. Revista Brasileira de Saúde e Produção Animal, 11(2), 519- 526. ).

In this study there was no effect of the experimental diets on the HSI, varying between 0.92 and 1.12% and demonstrating that the guava residue did not alter the hepatic metabolism of the tambaqui. These results differ to those reported by Lemos et al. (2011Lemos, M. V. A., Guimarães, I. G., & Miranda, E. C. (2011). Farelo de coco em dietas para o tambaqui (Colossoma macropomum). Revista Brasileira de Saúde e Produção Animal, 12(1), 188-198. ), 1.23 ± 0.25%, and Bezerra et al. (2014Bezerra, S. K., Souza, R. C., Melo, J. F. B., & Campeche, D. F. B. (2014). Crescimento de tambaqui alimentado com diferentes níveis de farinha de manga e proteína na ração. Archivos de Zootecnia, 63(244), 587-598. DOI: https://doi.org/10.4321/S0004-05922014000400003
https://doi.org/https://doi.org/10.4321/...
), 1.80 ± 0.44%, with rations containing 100% coconut meal and 50% mango residue, respectively. When the coconut concentration increased, there was a reduction in the hepato-somatic index, while the mango had a positive polynomial effect as the level of inclusion increased.

The survival rate of the tambaqui was 100% and was unaffected by the different inclusion levels of the guava residue in the diet. These results corroborate those of Souza et al. (2013Souza, R. C., Melo, J. F. B., Nogueira-Filho, R. M., Campeche, D. F. B., & Figueiredo, R. A. C. R. (2013). Influência da farinha de manga no crescimento e composição corporal da tilápia do Nilo. Archivos de Zootecnia, 62(238), 217-225. DOI: https://dx.doi.org/10.4321/S0004-05922013000200007
https://doi.org/https://dx.doi.org/10.43...
), where maize was replaced with mango residue at proportions of 0, 33, 66 and 100% in rations of Nile tilapia and no significant difference was observed in this parameter.

The efficacy of fish in converting protein to body weight can be determined using the protein efficiency rate (Fracalossi et al., 2012Fracalossi, D. M., Rodrigues, A. P. O., Silva, T. S. C. E., & Cyrino, J. E. P. (2012). Técnicas experimentais em nutrição de peixes. In D. M. Fracalossi, & J. E. P. Cyrino, Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira (p. 3-63). Florianópolis, SC: Gráfica e Editora Copiart Ltda. ). The tambaqui did not show a significant difference for this variable as observed by Lemos et al. (2011Lemos, M. V. A., Guimarães, I. G., & Miranda, E. C. (2011). Farelo de coco em dietas para o tambaqui (Colossoma macropomum). Revista Brasileira de Saúde e Produção Animal, 12(1), 188-198. ), replacing soybean meal with coconut meal.

Fruit residues may improve or impair the nutritional composition of cultured fish, according to the levels of inclusion in the diet, dietary habits and physiological adaptations of each species (Lazzari et al., 2015Lazzari, R., Uczay, J., Rodrigues, R. B., Pianesso, D., Adorian, T. J., & Mombach, P. I. (2015). Utilização de resíduos de frutas em dietas para piava. Boletim do Instituto de Pesca, 41(2), 227-237. ). In the proximate composition of fish, a significant difference was observed only for ethereal extract, showing the lowest content with 200 g kg-1 inclusion of the guava residue. This result demonstrates that the use of this ingredient reduced the lipid composition of the tambaqui, corroborating the results obtained by Souza et al. (2013Souza, R. C., Melo, J. F. B., Nogueira-Filho, R. M., Campeche, D. F. B., & Figueiredo, R. A. C. R. (2013). Influência da farinha de manga no crescimento e composição corporal da tilápia do Nilo. Archivos de Zootecnia, 62(238), 217-225. DOI: https://dx.doi.org/10.4321/S0004-05922013000200007
https://doi.org/https://dx.doi.org/10.43...
).

In the natural environment, the tambaqui diet is mainly composed of fruits, seeds and zooplankton, resulting in its classification as omnivorous/fructiferous, making possible its commercial creation associated to fruit cultivation (Bezerra et al., 2014Bezerra, S. K., Souza, R. C., Melo, J. F. B., & Campeche, D. F. B. (2014). Crescimento de tambaqui alimentado com diferentes níveis de farinha de manga e proteína na ração. Archivos de Zootecnia, 63(244), 587-598. DOI: https://doi.org/10.4321/S0004-05922014000400003
https://doi.org/https://doi.org/10.4321/...
). There are several morphological characteristics that enable this species to feed on fruits, such as: presence of molar teeth, strong mandibles (Dairiki & Silva, 2011Dairiki, J. K., & Silva, T. B. A. (2011). Revisão de literatura: exigências nutricionais do tambaqui - compilação de trabalhos, formulação de ração adequada e desafios futuros (Documentos, 91. M.I. N° 4/2011). Manaus, AM: Embrapa Amazônia Ocidental. ), short esophagus, bag-shaped stomach with large capacity to swell, about 43 to 75 pyloric cecum. The pyloric cecum are diverticula with a blind bottom that increase the intestinal absorption surface of tambaquis, also present in carnivorous species (Borges, Sanches, Oliveira, & Silva, 2010Borges, J. C. S., Sanches, E. G., Oliveira, M. S., & Silva, J. R. M. C. (2010). Anatomia e histologia gastrintestinal da garoupa-verdadeira Epinephelus marginatus (Lowe, 1834) (Teleostei, Serranidae). Acta Scientiarum. Biological Sciences, 32(4), 407-414. DOI: https://doi.org/10.4025/actascibiolsci.v32i4.4462
https://doi.org/https://doi.org/10.4025/...
).

The tambaqui has an extensive intestine, reaching about 2.5 times the standard length of the fish, being divided into proximal and distal portions (Carr, Weber-Iii, Murphy, & Zwingenberger, 2014)Carr, A., Weber-Iii, S., Murphy, C. J., & Zwingenberger, A. (2014). Computed tomographic and cross-sectional anatomy of the normal pacu (Colossoma Macroponum). Journal of Zoo and Wildlife Medicine, 45(1), 184-189. DOI: https://doi.org/10.1638/2013-0108R1.1
https://doi.org/https://doi.org/10.1638/...
. The main digestive enzymes present in the gastrointestinal tract of this species are amylase, maltase, acid protease, trypsin and chymotrypsin, exercising their enzymatic activities in the following organs: esophagus (amylase), stomach (amylase and acidic protease), pyloric cecum, proximal intestine and intestine distal (amylase, maltase, trypsin and chymotrypsin) (Rodrigues, 2014Rodrigues, A. P. O. (2014). Nutrição e alimentação do tambaqui (Colossoma macropomum). Boletim do Instituto de Pesca, 40(1), 135-145. ).

The results obtained in this study for WG, DFI, FC, SGR, HSI, SR and PER were satisfactory, demonstrating that the inclusion of up to 150 g kg-1 of the agroindustrial residue of guava did not compromise the growth performance of fish. The juveniles of tambaquis presented high zootechnical performance.

Previous studies have demonstrated that substitution of up to 30% of wheat bran by pupunha, plantain and yucca are feasible (Lochmann et al., 2009Lochmann, R., Chen, R., Chu-Koo, F. W., Camargo, W. N., Kohler, C. C., & Kasper, C. (2009). Effects of carbohydrate-rich alternative feedstuffs on growth, survival, body composition, hematology, and nonspecific immune response of black pacu, Colossoma macropomum, and red pacu, Piaractus brachypomus. Journal of the World Aquaculture Society, 40(1), 33-44. DOI: https://doi.org/10.1111/j.1749-7345.2008.00232.x
https://doi.org/https://doi.org/10.1111/...
), 100% of soybean meal by coconut meal (Lemos et al., 2011Lemos, M. V. A., Guimarães, I. G., & Miranda, E. C. (2011). Farelo de coco em dietas para o tambaqui (Colossoma macropomum). Revista Brasileira de Saúde e Produção Animal, 12(1), 188-198. ), inclusion of 12% babassu (Lopes et al., 2010Lopes, J. M., Pascoal, L. A. F., Silva-Filho, F. P., Santos, I. B., Watanabe, P. H., Araújo, D. M., ... Oliveira, P. S. (2010). Farelo de babaçu em dietas para tambaqui. Revista Brasileira de Saúde e Produção Animal, 11(2), 519- 526. ), 50% of the mango (Bezerra et al., 2014Bezerra, S. K., Souza, R. C., Melo, J. F. B., & Campeche, D. F. B. (2014). Crescimento de tambaqui alimentado com diferentes níveis de farinha de manga e proteína na ração. Archivos de Zootecnia, 63(244), 587-598. DOI: https://doi.org/10.4321/S0004-05922014000400003
https://doi.org/https://doi.org/10.4321/...
) and 8% banana meal (Silva et al., 2020Silva, A. F., Copatti, C. E., Oliveira, E. P., Bonfá, H. C., Melo, F. V. S. T., Camargo, A. C. S., & Melo, J. F. B. (2020). Effects of whole banana meal inclusion as replacement for corn meal on digestibility, growth performance, haematological and biochemical variables in practical diets for tambaqui juveniles (Colossoma macropomum). Aquaculture Reports, 17(1), 1- 8. DOI: https://doi.org/10.1016/j.aqrep.2020.100307
https://doi.org/https://doi.org/10.1016/...
) in rations for tambaqui juveniles, without compromising the growth performance of the fish. The agroindustrial residues of açaí, acerola and passion fruit are also alternative ingredients with the potential for use in the formulation of rations for tambaqui, C. macropomum (Silva et al., 2017Silva, F. N. L., Medeiros, L. R., Lima, A. A. N., Xavier, D. T. O., Macedo, A. R. G., Reis, A. A., ... Souza, R. A. L. (2017). Alimentos alternativos da agricultura familiar como proposta em rações para Tambaqui (Colossoma macropomum Cuvier, 1818). Publicações em Medicina Veterinária e Zootecnia, 11(2), 103-112. DOI: https://doi.org/10.22256/pubvet.v11n2.103-112
https://doi.org/https://doi.org/10.22256...
). Similar to guava residue, these alternative ingredients represent possible energy sources which can be used in feeding this species.

Conclusion

Results of this study enable us to conclude that the agroindustrial residue of guava can be included in rations in proportions of up to 150 g kg-1 without compromising the growth performance of tambaqui juveniles.

Acknowledgements

Thanks to Development Company of the São Francisco and Parnaíba Valleys (CODEVASF) for the fish donation, Pratigi Alimentos (Bahia, Brazil) for the ingredientes donation. This study was sponsored by scholarships and monetary support from the Coordination for the Improvement of Higher Education Personnel (CAPES) and Mobility Stimulus Program (PROMOB).

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Publication Dates

  • Publication in this collection
    20 Apr 2022
  • Date of issue
    Jan-Dec 2022

History

  • Received
    08 June 2020
  • Accepted
    15 Jan 2021
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