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Mathematical modeling for the management of the carrying capacity of aquaculture enterprises in lakes and reservoirs

Abstract:

Flooded areas of reservoirs and artificial lakes have been increasingly used for fish production; however, the waste generated by aquaculture has become a concern for the sustainable development of this activity. One of the main strategies adopted by management and regulatory agencies is the use of hydrodynamic models that calculate the carrying or nutrient load capacity of a particular water body and the effect of fish farming. These models are precise in the development of optimal strategies for feeding and waste calculation. This review paper addresses this topic and describes the methodology developed for the analysis and simulation of the carrying capacity for fish production, based on the integration of the Fish-PrFEQ nutritional bioenergetic model and the hydrodynamic model of Dillon & Rigler. This methodology allows evaluating the real contribution of aquaculture waste and assists in the planning and management of aquaculture in these aquatic environments, besides enabling and encouraging producers and the aquaculture industry to use fish food with better nutritional quality and lower environmental impact.

Index terms:
hydrodynamic modeling; mass balance; nutritional bioenergetics; solid waste; sustainable aquaculture.

Resumo:

Áreas inundadas de reservatórios e lagos artificiais estão sendo cada vez mais utilizadas para a produção de peixes; contudo, os resíduos lançados pela aquicultura tornaram-se uma preocupação para o desenvolvimento sustentável desta atividade. Uma das principais estratégias adotadas pelos órgãos gestores e fiscalizadores consiste no uso de modelos hidrodinâmicos que calculam a capacidade de suporte ou de carga de nutrientes de um determinado corpo hídrico e a influência dos cultivos de peixes. Esses modelos são precisos no desenvolvimento de estratégias ideais de alimentação e cálculo de resíduos. Este artigo de revisão aborda esta temática e traz uma descrição da metodologia desenvolvida para análise e simulação da capacidade de suporte para produção de pescados, baseada na integração do modelo bioenergético nutricional “Fish-PrFEQ” com o modelo hidrodinâmico de Dillon & Rigler. Esta metodologia permite avaliar a real contribuição de resíduos aquícolas e auxilia no planejamento e na gestão da aquicultura nestes ambientes aquáticos, além de possibilitar e incentivar que os produtores e a indústria aquícola utilizem rações de melhor qualidade nutricional e menor impacto ambiental.

Termos para indexação:
modelagem hidrodinâmica; balanço de massa; bioenergética nutricional; resíduos sólidos; aquicultura sustentável.

Introduction

Aquaculture is considered a viable and cheap source of high-quality protein, especially in developing countries, where there is a need to increase food production to guarantee food security (Béné et al., 2016BÉNÉ, C.; ARTHUR, R.; NORBURY, H.; ALLISON, E.H.; BEVERIDGE, M.; BUSH, S.; CAMPLING, L.; LESCHEN, W.; LITTLE, D.; SQUIRES, D.; THILSTED, S.H.; TROELL, M.; WILLIAMS, M. Contribution of fisheries and aquaculture to food security and poverty reduction: assessing the current evidence. World Development, v.79, p.177-196, 2016. DOI: 10.1016/j.worlddev.2015.11.007.
https://doi.org/10.1016/j.worlddev.2015....
). For this reason, the flooded areas of artificial lakes and ponds have being increasingly used for the aquaculture industry (Ayer & Tyedmers, 2009AYER, N.W.; TYEDMERS, P.H. Assessing alternative aquaculture technologies: life cycle assessment of salmonid culture systems in Canada. Journal of Cleaner Production, v.17, p.362-373, 2009. DOI: 10.1016/j.jclepro.2008.08.002.
https://doi.org/10.1016/j.jclepro.2008.0...
; Barton & Fløysand, 2010BARTON, J.R.; FLØYSAND, A. The political ecology of Chilean salmon aquaculture, 1982-2010: a trajectory from economic development to global sustainability. Global Environmental Change, v.20, p.739-752, 2010. DOI: 10.1016/j.gloenvcha.2010.04.001.
https://doi.org/10.1016/j.gloenvcha.2010...
). In addition to food production, the expansion of this activity brings benefits to the regional economies, in the form of employment and income generation throughout the aquaculture production chain (Ross et al., 2011ROSS, L.G.; FALCONER, L.L.; CAMPOS MENDOZA, A.; MARTINEZ PALACIOS, C.A. Spatial modelling for freshwater cage location in the Presa Adolfo Mateos Lopez (El Infiernillo), Michoacán, México. Aquaculture Research, v.42, p.797-807, 2011. DOI: 10.1111/j.1365-2109.2010.02689.x.
https://doi.org/10.1111/j.1365-2109.2010...
), and is an important alternative productive activity for populations affected by dams, for example (Béné et al., 2016BÉNÉ, C.; ARTHUR, R.; NORBURY, H.; ALLISON, E.H.; BEVERIDGE, M.; BUSH, S.; CAMPLING, L.; LESCHEN, W.; LITTLE, D.; SQUIRES, D.; THILSTED, S.H.; TROELL, M.; WILLIAMS, M. Contribution of fisheries and aquaculture to food security and poverty reduction: assessing the current evidence. World Development, v.79, p.177-196, 2016. DOI: 10.1016/j.worlddev.2015.11.007.
https://doi.org/10.1016/j.worlddev.2015....
).

In this scenario, according to Montanhini Neto & Ostrensky (2015)MONTANHINI NETO, R.; OSTRENSKY, A. Nutrient load estimation in the waste of Nile tilápia Oreochromis niloticus (L.) reared in cages in tropical climate conditions. Aquaculture Research, v.46, p.1309-1322, 2015. DOI: 10.1111/are.12280.
https://doi.org/10.1111/are.12280....
, in order to produce a ton of tilapia, approximately 1,040 kg organic matter (OM), 45 kg N, and 14 kg P are released into the environment. Alves & Baccarin (2005)ALVES, R.C.P.; BACCARIN, A.E. Efeitos da produção de peixes em tanques-rede sobre sedimentação de material em suspensão e de nutrientes no Córrego da Arribada (UHE Nova Avanhandava), baixo rio Tietê. In: NOGUEIRA, M.G.; HENRY, R.; JORCIN, A. (Org.). Ecologia de reservatórios: impactos potenciais, ações de manejo e sistemas em cascata. São Carlos: Rima, 2005. p.329-347. reported that 66% of the P obtained by intensive feeding in fish farms is absorbed by the sediment, 11% is dissolved in water, and 23% is incorporated by the farmed fish.

Therefore, the solid wastes generated by aquaculture become a concern for the sustainable development of the activity. Several researchers have shown that the residual products from different types of fish farming can be estimated by factorial mathematical models (Cho & Bureau, 1998CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
; Lupatsch & Kissil, 1998LUPATSCH, I.; KISSIL, G.W. Predicting aquaculture waste from gilthead seabream (Sparus aurata) culture using a nutrional approach. Aquatic Living Resourses, v.11, p.265-268, 1998. DOI: 10.1016/S0990-7440(98)80010-7.
https://doi.org/10.1016/S0990-7440(98)80...
; Yi, 1998YI, Y. A bioenergetics growth model for Nile tilapia (Oreochromis niloticus) based on limiting nutrients and fish standing crop in fertilized ponds. Aquacultural Engineering, v.18, p.157-173, 1998. DOI: 10.1016/S0144-8609(98)00028-4.
https://doi.org/10.1016/S0144-8609(98)00...
; Bureau & Hua, 2010BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
; Azevedo et al., 2011AZEVEDO, P.A.; PODEMSKI, C.L.; HESSLEIN, R.H.; KASIAN, S.E.M.; FINDLAY, D.L.; BUREAU, D.P. Estimation of waste outputs by a rainbow trout cage farm using a nutritional approach and monitoring of lake water quality. Aquaculture, v.311, p.175-186, 2011. DOI: 10.1016/j.aquaculture.2010.12.001.
https://doi.org/10.1016/j.aquaculture.20...
).

In this context, this paper presents a review of the topic and a description of the methodology developed to analyze and simulate the carrying capacity for fish production based on the integration of the “Fish-PrFEQ” nutritional bioenergetics model of Cho & Bureau (1998)CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
with the hydrodynamic model of Dillon & Rigler (1974)DILLON, P.J.; RIGLER, F.H. A test of a simple nutrient budget model predicting the phosphorus concentration in lake water. Journal of the Fisheries Research Board of Canada, v.31, p.1771-1778, 1974. DOI: 10.1139/f74-225.
https://doi.org/10.1139/f74-225....
.

The adoption of this approach will allow evaluating each process or farm in a compartmentalized way, aiming to determine the real contribution of wastes in the aquatic environment, besides aiding in defining the carrying capacity of the reservoir for fish production. These measures will assist in monitoring zootechnical efficiency and in improving the regulations for public water concessions for aquaculture purposes, besides enabling and encouraging producers and the aquaculture industry to use feeds with better nutritional quality and lower environmental impact.

Environmental impact of aquaculture in lakes and reservoirs

The main impacts related to aquaculture in rivers, lakes, and reservoirs are associated to the increased flow of particles and dissolved nutrients in the environment (Sugiura et al., 2006SUGIURA, S.H.; MARCHANT, D.D.; KELSEY, K.; WIGGINS, T.; FERRARIS, R.P. Effluent profile of commercially used low-phosphorus fish feeds. Environmental Pollution, v.140, p.95-101, 2006.; Azevedo et al., 2011AZEVEDO, P.A.; PODEMSKI, C.L.; HESSLEIN, R.H.; KASIAN, S.E.M.; FINDLAY, D.L.; BUREAU, D.P. Estimation of waste outputs by a rainbow trout cage farm using a nutritional approach and monitoring of lake water quality. Aquaculture, v.311, p.175-186, 2011. DOI: 10.1016/j.aquaculture.2010.12.001.
https://doi.org/10.1016/j.aquaculture.20...
; Gondwe et al., 2011GONDWE, M.J.S.; GUILDFORD, S.J.; HECKY, R.E. Carbon, nitrogen and phosphorus loadings from tilapia fish cages in Lake Malawi and factors influencing their magnitude. Journal of Great Lakes Research, v.37, p.93-101, 2011. Supplement 1. DOI: 10.1016/j.jglr.2010.11.014.
https://doi.org/10.1016/j.jglr.2010.11.0...
; Canale et al., 2016CANALE, R.P.; WHELAN, G.; SWITZER, A.; EISCH, E. A bioenergetic approach to manage production and control phosphorus discharges from a salmonid hatchery. Aquaculture, v.451, p.137-146, 2016. DOI: 10.1016/j.aquaculture.2015.09.008.
https://doi.org/10.1016/j.aquaculture.20...
); the mortality and loss of biodiversity of fishes (Sang, 2006SANG, J.-S. Lawmaking for Management and Protection of Wetlands in China. Wetland Science and Management, v.3, p.50-53, 2006.); the contamination by chemical compounds (through the use of antibiotics, antiparasitics, anesthetics, and disinfectants) (Burridge et al., 2010BURRIDGE, L.; WEIS, J.S.; CABELLO, F.; PIZARRO, J.; BOSTICK, K. Chemical use in salmon aquaculture: A review of current practices and possible environmental effects. Aquaculture, v.306, p.7-23, 2010.); the lower dissolved oxygen concentrations (Hamblin & Gale, 2002HAMBLIN, P.F.; GALE, P. Water quality modeling of caged aquaculture impacts in Lake Wolsey, North Channel of Lake Huron. Journal of Great Lakes Research, v.28, p.32-43, 2002. DOI: 10.1016/S0380-1330(02)70560-1.
https://doi.org/10.1016/S0380-1330(02)70...
); the occurrence of harmful algal blooms (Sowles, 2009SOWLES, J. Aquaculture task force discussion paper on bio-physical carrying capacity. 2009. Available at: ˂Available at: ˂https://www1.maine.gov/dmr/aquaculture/reports/documents/carryingcapacity.pdf ˃. Accessed on: Mar. 11 2015.
https://www1.maine.gov/dmr/aquaculture/r...
); and the increase in the contents of organic matter and metals in the sediment (Xia et al., 2016XIA, B.; GUO, P.; LEI, Y.; ZHANG, T.; QIU, R.; KNORR, K.-H. Investigating speciation and toxicity of heavy metals in anoxic marine sediments-a case study from a mariculture bay in Southern China. Journal of Soils and Sediments, v.16, p.665-676, 2016. DOI: 10.1007/s11368-015-1267-3.
https://doi.org/10.1007/s11368-015-1267-...
). In addition to these factors, the following were observed: changes in the biodiversity of the microflora and benthic sediments (Buschmann et al., 2009BUSCHMANN, A.H.; CABELLO, F.; YOUNG, K.; CARVAJAL, J.; VARELA, D.A.; HENRÍQUEZ, L. Salmon aquaculture and coastal ecosystem health in Chile: Analysis of regulations, environmental impacts and bioremediation systems. Ocean and Coastal Management, v.52, p.243-249, 2009. DOI: 10.1016/j.ocecoaman.2009.03.002.
https://doi.org/10.1016/j.ocecoaman.2009...
); changes in the trophic structure and biological attributes of the diet of wild fishes due to the introduction of exotic species from aquaculture (Arthur et al., 2010ARTHUR, R.I.; LORENZEN, K.; HOMEKINGKEO, P.; SIDAVONG, K.; SENGVILAIKHAM, B.; GARAWAY, C.J. Assessing impacts of introduced aquaculture species on native fish communities: Nile tilapia and major carps in SE Asian freshwaters. Aquaculture, v.299, p.81-88, 2010. DOI: 10.1016/j.aquaculture.2009.11.022.
https://doi.org/10.1016/j.aquaculture.20...
; Carvalho et al., 2012CARVALHO, E.D.; DAVID, G.S; SILVA, R.J. (Ed.). Health and Environment in Aquaculture. Rijeka: Intech, 2012. 428p. DOI: 10.5772/2462.
https://doi.org/10.5772/2462....
; Ramos et al., 2014RAMOS, I.P.; FRANCESCHINI, L.; ZICA, É.O.P.; CARVALHO, E.D.; SILVA, R.J. The influence of cage farming on infection of the corvine fish Plagioscion squamosissimus (Perciformes: Sciaenidae) with metacercariae of Austrodiplostomum compactum (Digenea: Diplostomidae) from the Chavantes reservoir, São Paulo State, Brazil. Journal of Helminthology, v.88, p.342-348, 2014. DOI: 10.1017/S0022149X13000229.
https://doi.org/10.1017/S0022149X1300022...
); dissemination of diseases that may affect wild populations of aquatic organisms (Israel, 2007ISRAEL, D.C. The current state of aquaculture in Laguna de Bay. Makati City: Philippine Institute for Development Studies, 2007. p.1-65. (Discussion Paper Series No. 2007-20).); and, in some cases, direct conflicts with other users of water resources, which can cause adverse social effects (Béné & Obirih-Opareh, 2009BÉNÉ, C.; OBIRIH-OPAREH, N. Social and economic impacts of agricultural productivity intensification: the case of brush park fisheries in Lake Volta. Agricultural Systems, v.102, p.1-10, 2009. DOI: 10.1016/j.agsy.2009.06.001.
https://doi.org/10.1016/j.agsy.2009.06.0...
).

Aquaculture effluents

Most of the effluents from aquaculture come from diets and from excess feed not consumed during feeding, resulting in solid and dissolved wastes (Bureau & Hua, 2010BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
). The releases of P in continental water bodies (freshwater) are more alarming, because this nutrient is usually a limiting factor for plant (algae and macrophyte) growth. In marine environments, the outputs of nitrogenous wastes cause the greatest concern regarding environmental impact (Rabassó & Hernández, 2015RABASSÓ, M.; HERNÁNDEZ, J.M. Bioeconomic analysis of the environmental impact of a marine fish farm. Journal of Environmental Management, v.158, p.24-35, 2015. DOI: 10.1016/j.jenvman.2015.04.034.
https://doi.org/10.1016/j.jenvman.2015.0...
); however, in some reservoirs, the high entry of N (coming mainly from the protein in the feed) can generate toxic ammonia in the water and endanger fish survival.

Hua & Bureau (2006)HUA, K.; BUREAU, D.P. Modelling digestible phosphorus content of salmonid fish feeds. Aquaculture, v.254, p.455-465, 2006. DOI: 10.1016/j.aquaculture.2005.10.019.
https://doi.org/10.1016/j.aquaculture.20...
emphasize that solid waste (fecal material and food lost when feeding) can settle and impact the benthic ecosystem of inland and marine waters; therefore, estimating solid and dissolved wastes is the main strategy for monitoring and planning mitigation actions in environments where aquaculture farms are installed.

Nitrogenous wastes

The biological value of a given protein in the diet depends both on its digestibility and its balance of amino acids in relation to the nutritional requirements of fish (NRC, 2011NRC. National Research Council. Nutrient requirements of fish and shrimp. Washington: National Academy Press, 2011. 392p.). The imbalance of amino acids can lead to decreased protein deposition and to increased nitrogen excretion (Cai et al., 2016CAI, H.; ROSS, L.G.; TELFER, T.C.; CHANGWEN, W.; ZHU, A.; ZHAO, S.; XU, M. Modelling the nitrogen loadings from large yellow croaker (Larimichthys crocea) cage aquaculture. Environmental Science and Pollution Research, v.23, p.7529-7542, 2016. DOI: 10.1007/s11356-015-6015-0.
https://doi.org/10.1007/s11356-015-6015-...
).

Since the diets for fish contain high levels of protein (28 to 50%), a great amount of energy is supplied as nitrogen compounds, which leads to increased production of catabolites, as nitrite, nitrate, and ammonia, for example. In this way, saving protein content with the inclusion of digestible energy in the diet can significantly reduce pollution, due to the decrease in nitrogen end products.

Another strategy used to reduce pollution is using the ideal protein for the species. Botaro et al. (2007)BOTARO, D.; FURUYA, W.M.; SILVA, L.C.R.; SANTOS, L.D. dos; SILVA, T.S. de C.; SANTOS, V.G. dos. Redução da proteína da dieta com base no conceito de proteína ideal para tilápias-do-nilo (Oreochromis niloticus) criadas em tanques-rede. Revista Brasileira de Zootecnia, v.36, p.517-525, 2007. DOI: 10.1590/S1516-35982007000300001.
https://doi.org/10.1590/S1516-3598200700...
showed that it is possible to reduce the content of digestible crude protein (CP) from 27 to 24.3% in diets for Nile tilapia (Oreochromis niloticus) reared in cages, and that this reduction can be achieved by a supplementation with amino acids.

In this scenario, Bureau & Hua (2010)BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
highlighted the importance of digestible protein (DP) and digestible energy (DE) in the diet to increase N retention. Hargreaves (1998)HARGREAVES, J.A. Nitrogen biogeochemistry of aquaculture ponds. Aquaculture, v.166, p.181-212, 1998. DOI: 10.1016/S0044-8486(98)00298-1.
https://doi.org/10.1016/S0044-8486(98)00...
conducted a literature review to identify the percentage of N retained by fish and its release into the environment in several aquaculture production systems. The author found differences from 19 to 21% retention with 73 to 86% of excreted nitrogenous compounds for species such as Ictalurus pagrus, O. niloticus, and Clarias macrocephalus, and that the use of diets with reduced levels of protein and increased levels of DE resulted in a decrease in the effect of feed pollution in the aquatic environment.

Phosphate waste

The way in which P is excreted by fish can have a direct effect on the enrichment of the aquatic environment and on algae growth. Usually P is excreted in soluble forms and particles: the soluble forms consist of organic P and PO4 3-, which directly affect water quality, while the form of particles settles at the bottom of lakes and reservoirs or accumulates in the sediment (Tundisi & Tundisi, 2008TUNDISI, J.G.; TUNDISI, T.M. Limnologia. São Paulo: Oficina de textos, 2008. 631p.; Canale et al., 2016CANALE, R.P.; WHELAN, G.; SWITZER, A.; EISCH, E. A bioenergetic approach to manage production and control phosphorus discharges from a salmonid hatchery. Aquaculture, v.451, p.137-146, 2016. DOI: 10.1016/j.aquaculture.2015.09.008.
https://doi.org/10.1016/j.aquaculture.20...
).

Soluble P is readily available as a nutrient for plant growth, and a significant amount of the free fraction contained in total P is in the form of inorganic orthophosphate. The form of P consumed by fish will affect the amount of soluble P and particulate excreta, as well as the amount of P that could later be biologically degraded in the sediment (Canale et al., 2016CANALE, R.P.; WHELAN, G.; SWITZER, A.; EISCH, E. A bioenergetic approach to manage production and control phosphorus discharges from a salmonid hatchery. Aquaculture, v.451, p.137-146, 2016. DOI: 10.1016/j.aquaculture.2015.09.008.
https://doi.org/10.1016/j.aquaculture.20...
). Therefore, the definition of nutrient inputs via aquaculture feed is of extreme importance for the sustainable development of this activity.

Wang et al. (2012)WANG, X.; OLSEN, L.M.; REITAN, K.I.; OLSEN, Y. Discharge of nutrient wastes from salmon farms: environmental effects, and potential for integrated multi-trophic aquaculture. Aquaculture Environment Interactions, v.2, p.267-283, 2012. DOI: 10.3354/aei00044.
https://doi.org/10.3354/aei00044....
reported that wastes from salmon (Salmo salar) farms in Norway, in 2009, were released into the environment - equivalent to a discharge of about 404,000, 50,600, and 9,400 Mg C, N, and P, respectively, based on the total production of 1,02x106 Mg salmon. These results confirm those obtained by Chowdhury et al. (2013)CHOWDHURY, M.A.K.; SIDDIQUI, S.; HUA, K.; BUREAU, D.P. Bioenergetics-based factorial model to determine feed requirement and waste output of tilapia produced under commercial conditions. Aquaculture, v.410/411, p.138-147, 2013. DOI: 10.1016/j.aquaculture.2013.06.030.
https://doi.org/10.1016/j.aquaculture.20...
, who assessed O. niloticus fed different levels of protein in the diet (40, 38, and 35%) and found an increase of 4.2 to 5.0 kg in the excretion of P and a decrease of 46.2 to 40.9 kg in that of N per ton of tilapia produced. Montanhini Neto & Ostrensky (2015)MONTANHINI NETO, R.; OSTRENSKY, A. Nutrient load estimation in the waste of Nile tilápia Oreochromis niloticus (L.) reared in cages in tropical climate conditions. Aquaculture Research, v.46, p.1309-1322, 2015. DOI: 10.1111/are.12280.
https://doi.org/10.1111/are.12280....
also analyzed the potential waste load of the commercial production of O. niloticus. According to these authors, the total nutrient content in the waste generated per ton of biomass of produced tilapia was of 1,040.63 kg OM, 44.95 kg N, and 14.26 kg P, which represent 78% OM, 65% protein, and 72% P provided by feed.

Penczak et al. (1982)PENCZAK, T.; GALICKA, W.; MOLINSKI, M.; KUSTO, E.; ZALEWSKI, M. The enrichment of a mesotrophic lake by carbon, phosphorus and nitrogen from the cage aquaculture of rainbow trout, Salmo gairdneri. Journal of Applied Ecology, v.19, p.371-393, 1982. DOI: 10.2307/2403474.
https://doi.org/10.2307/2403474....
state that only 32% of P is used for the metabolism of fish, and the remaining 68% are transferred to the environment. Alves & Baccarin (2005)ALVES, R.C.P.; BACCARIN, A.E. Efeitos da produção de peixes em tanques-rede sobre sedimentação de material em suspensão e de nutrientes no Córrego da Arribada (UHE Nova Avanhandava), baixo rio Tietê. In: NOGUEIRA, M.G.; HENRY, R.; JORCIN, A. (Org.). Ecologia de reservatórios: impactos potenciais, ações de manejo e sistemas em cascata. São Carlos: Rima, 2005. p.329-347. also reported that 66% of the P obtained by intensive feeding is deposited in the sediment, 11% is dissolved in water, and 23% is incorporated by the farmed fish; this emphasizes the need for programs for the management and control of aquaculture waste.

Tacon (2005)TACON, A.G.J. Salmon aquaculture dialogue: Status of information on salmon aquaculture feed and the environment. Aquafeed International, v.8, p.22-37, 2005. points out that, in 1985, the diets used in salmon farming in Chile contained 60% CP and only 6 to 8% lipids; however, in 2005, the average percentage of each of these nutrients was 35%, causing a decrease in the rates of excretion of metabolites by fish. For this author, these practical results minimized the polluting potential of the fish farms evaluated.

A similar situation occurred in the Norwegian and Canadian salmon industry, where a series of measures were adopted to reduce the release of nutrients from fish farms. These actions involved the optimization of feed composition, and improvements in feed digestibility and in processing technologies (Technical..., 2005TECHNICAL Assistance Republic of the Philippines: strategy for sustainable aquaculture development for poverty reduction project. [S.l.]: Asian Development Bank, 2005. 16p. Technical Assistance Report. Project Number: 39031.; Bureau & Hua, 2010BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
).

The average feed conversion of the diets used in Norway’s salmon industry reduced from 2.08, in 1974, to 1.00 in 2005 (Technical..., 2005TECHNICAL Assistance Republic of the Philippines: strategy for sustainable aquaculture development for poverty reduction project. [S.l.]: Asian Development Bank, 2005. 16p. Technical Assistance Report. Project Number: 39031.). In Canada, the average feed conversion of the diets for salmon, in the 1980s, was 1.50, and, 20 years later, 1.10. Consequently, there was a decrease in excretion of 14 kg solid P per ton of fish produced (Bureau & Hua, 2010BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
).

Mathematical models applied to aquaculture

Factorial modeling has been successfully used to estimate amino acid requirements; to improve the energy protein balance of diets for several animals, such as laying hens (Gous & Nonis, 2010GOUS, R.M.; NONIS, M.K. Modelling egg production and nutrient responses in broiler breeder hens. Journal of Agricultural Science, v.148, p.287-301, 2010. DOI: 10.1017/S0021859610000183.
https://doi.org/10.1017/S002185961000018...
), poultry, and swine (Sakomura et al., 2015SAKOMURA, N.K.; GOUS, R.M.; KYRIAZAKIS, I.; HAUSCHILD, L. (Ed.). Nutritional modelling for pigs and poultry. Oxfordshire: Cabi, 2015. 318p. DOI: 10.1079/9781780644110.0000.
https://doi.org/10.1079/9781780644110.00...
); and also to determine the dietary needs of horses (Cordero et al., 2013CORDERO, V.V.; CAVINDER, C.A.; TEDESCHI, L.O.; SIGLER, D.H.; VOGELSANG, M.M.; ARNOLD, C.E. The development and evaluation of a mathematical nutrition model to predict digestible energy intake of broodmares based on body condition changes. Journal of Animal Science, v.91, p.2169-2177, 2013. DOI: 10.2527/jas.2011-4659.
https://doi.org/10.2527/jas.2011-4659....
) and cattle (Albertini et al., 2012ALBERTINI, T.Z.; MEDEIROS, S.R.; TORRES JÚNIOR, R.A.A.; ZOCCHI, S.S.; OLTJEN, J.W.; STRATHE, A.B.; LANNA, D.P.D. A methodological approach to estimate the lactation curve and net energy and protein requirements of beef cows using nonlinear mixed-effects modeling. Journal of Animal Science, v.90, p.3867-3878, 2012. DOI: 10.2527/jas.2010-3540.
https://doi.org/10.2527/jas.2010-3540....
).

In general, a deductive factorial model can be used to examine the relationship between the net requirement of an essential element for animals (the requirement for growth and the replacement of endogenous loss, for example) and the concentration in the diet needed to meet this requirement, with reduction in losses and excretions (NRC, 2011NRC. National Research Council. Nutrient requirements of fish and shrimp. Washington: National Academy Press, 2011. 392p.; Montanhini Neto & Ostrensky, 2015MONTANHINI NETO, R.; OSTRENSKY, A. Nutrient load estimation in the waste of Nile tilápia Oreochromis niloticus (L.) reared in cages in tropical climate conditions. Aquaculture Research, v.46, p.1309-1322, 2015. DOI: 10.1111/are.12280.
https://doi.org/10.1111/are.12280....
). It should be noted that each model considers the characteristics of the species, environment, and diet, among other factors that affect the final response to be evaluated.

Fish growth is a complex process that represents the results of a series of physiological and behavioral processes, involving food intake, the deposition of animal tissue, and the excretion of metabolites (Jobling, 2011JOBLING, M. Bioenergetics in aquaculture settings. In: FARRELL, A.P. (Ed.). Encyclopedia of Fish Physiology: from genome to environment. Amsterdam: Elsevier, 2011. p.1664-1674. DOI: 10.1016/B978-0-12-374553-8.00152-0.
https://doi.org/10.1016/B978-0-12-374553...
). In each situation in commercial fish production, the knowledge of the growth rates in a given period, in relation to feed consumption, is essential for the analysis of the future viability of the venture.

Mathematical models that predict fish growth rates and feed requirements can be used to maximize efficiency and improve animal growth. These models can be a useful tool both for planning and managing production, as well as describing future scenarios; however, they must be used properly (Iwama & Tautz, 1981IWAMA, G.K.; TAUTZ, A.F. A simple growth model for salmonids in hatcheries. Canadian Journal of Fisheries and Aquatic Sciences, v.38, p.649-656, 1981. DOI: 10.1139/f81-087.
https://doi.org/10.1139/f81-087....
; Cho & Bureau, 1998CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
; Dumas et al., 2010DUMAS, A.; FRANCE, J.; BUREAU, D. Modelling growth and body composition in fish nutrition: where have we been and where are we going? Aquaculture Research, v.41, p.161-181, 2010. DOI: 10.1111/j.1365-2109.2009.02323.x.
https://doi.org/10.1111/j.1365-2109.2009...
).

Despite the many attempts to develop mathematical expressions to describe fish growth, there is a wide range of approaches and concepts (Iwama & Tautz, 1981IWAMA, G.K.; TAUTZ, A.F. A simple growth model for salmonids in hatcheries. Canadian Journal of Fisheries and Aquatic Sciences, v.38, p.649-656, 1981. DOI: 10.1139/f81-087.
https://doi.org/10.1139/f81-087....
). It is common to find growth expressed in centimeters per month, instant growth rates, percentage in length change or percentage in weight change, often without any references to temperature, feed, or farming conditions (NRC, 2011NRC. National Research Council. Nutrient requirements of fish and shrimp. Washington: National Academy Press, 2011. 392p.).

Therefore, the adoption of an appropriate growth model allows estimating the (feed) requirements for the energy needs and growth rates of fish. This information allows the producer to solve several problems related to growth and feeding rates that arise in the routine of fish farming (Dumas et al., 2010DUMAS, A.; FRANCE, J.; BUREAU, D. Modelling growth and body composition in fish nutrition: where have we been and where are we going? Aquaculture Research, v.41, p.161-181, 2010. DOI: 10.1111/j.1365-2109.2009.02323.x.
https://doi.org/10.1111/j.1365-2109.2009...
).

Furthermore, it is possible, for example, to predict the average final weight of fish after a certain time of farming; to estimate the time required for the fish to reach a given commercial size, at a set temperature; or to decide on the necessary average temperature to produce a given size of fish in an exact period of time. In addition, a good mathematical model can also provide information about the biomass stock and daily feed, energy, and amino acid requirements (Iwama & Tautz, 1981IWAMA, G.K.; TAUTZ, A.F. A simple growth model for salmonids in hatcheries. Canadian Journal of Fisheries and Aquatic Sciences, v.38, p.649-656, 1981. DOI: 10.1139/f81-087.
https://doi.org/10.1139/f81-087....
; Bureau et al., 2002BUREAU, D.P.; KAUSHIK, S.J.; CHO, C.Y. Bioenergetics. In: HALVER, J.E.; HARDY, R.W. (Ed.). Fish Nutrition. 3rd ed. San Diego: Academic Press, 2002. p.78-95. DOI: 10.1016/B978-012319652-1/50002-1.
https://doi.org/10.1016/B978-012319652-1...
).

Prediction models of body growth applied in fish farming

To measure fish growth, the ratio of length or weight is usually used (Ricker, 1979RICKER, W.E. Growth rates and models. In: HOAR, W.S.; RANDALL, D.J.; BRETT, J.R. (Ed.) Fish physiology. London: Academic Press, 1979. v.8, p.678-743. DOI: 10.1016/s1546-5098(08)60034-5.
https://doi.org/10.1016/s1546-5098(08)60...
; Bureau et al., 2002BUREAU, D.P.; KAUSHIK, S.J.; CHO, C.Y. Bioenergetics. In: HALVER, J.E.; HARDY, R.W. (Ed.). Fish Nutrition. 3rd ed. San Diego: Academic Press, 2002. p.78-95. DOI: 10.1016/B978-012319652-1/50002-1.
https://doi.org/10.1016/B978-012319652-1...
; Jobling, 2011JOBLING, M. Bioenergetics in aquaculture settings. In: FARRELL, A.P. (Ed.). Encyclopedia of Fish Physiology: from genome to environment. Amsterdam: Elsevier, 2011. p.1664-1674. DOI: 10.1016/B978-0-12-374553-8.00152-0.
https://doi.org/10.1016/B978-0-12-374553...
). The simplest method of reporting growth is by evaluating the absolute increase in weight or growth. This implies that the relationship between time and weight is linear, and that the rate of absolute growth is the same, regardless of the size of the fish. However, the growth rate varies with the size of the fish, and the relative growth rate (GRR) will allow comparing between treatments with fishes of different sizes (Hopkins, 1992HOPKINS, K.D. Reporting fish growth: a review of the basics. Journal of the World Aquaculture Society, v.23, p.173-179, 1992. DOI: 10.1111/j.1749-7345.1992.tb00766.x.
https://doi.org/10.1111/j.1749-7345.1992...
). Relative growth (GR) and the GRR are mathematically expressed according to the following equations: GR=(WtWi)/Wi and GRR=(WtWi)/Wi×Δt , in which Wt is the weight at time t; Wi is the initial weight; and ∆t is the duration of the experiment (Ricker, 1979RICKER, W.E. Growth rates and models. In: HOAR, W.S.; RANDALL, D.J.; BRETT, J.R. (Ed.) Fish physiology. London: Academic Press, 1979. v.8, p.678-743. DOI: 10.1016/s1546-5098(08)60034-5.
https://doi.org/10.1016/s1546-5098(08)60...
; Hopkins, 1992HOPKINS, K.D. Reporting fish growth: a review of the basics. Journal of the World Aquaculture Society, v.23, p.173-179, 1992. DOI: 10.1111/j.1749-7345.1992.tb00766.x.
https://doi.org/10.1111/j.1749-7345.1992...
).

The relative growth rates are typically used in studies on fish nutrition and are presented as the percentage of weight gain per unit of time. However, the GRR is restricted to the period of time calculated and cannot be easily converted to another time period (Hopkins, 1992HOPKINS, K.D. Reporting fish growth: a review of the basics. Journal of the World Aquaculture Society, v.23, p.173-179, 1992. DOI: 10.1111/j.1749-7345.1992.tb00766.x.
https://doi.org/10.1111/j.1749-7345.1992...
). Therefore, other models and equations for growth can be used to obtain better growth simulations and values.

To eliminate the problem related with relative growth rates over time, another model of exponential growth rate recommended is the specific growth rate (SGR) coefficient (Ricker, 1979RICKER, W.E. Growth rates and models. In: HOAR, W.S.; RANDALL, D.J.; BRETT, J.R. (Ed.) Fish physiology. London: Academic Press, 1979. v.8, p.678-743. DOI: 10.1016/s1546-5098(08)60034-5.
https://doi.org/10.1016/s1546-5098(08)60...
; Hopkins, 1992HOPKINS, K.D. Reporting fish growth: a review of the basics. Journal of the World Aquaculture Society, v.23, p.173-179, 1992. DOI: 10.1111/j.1749-7345.1992.tb00766.x.
https://doi.org/10.1111/j.1749-7345.1992...
). It is usually reduced to an instantaneous growth rate or to a specific, intrinsic, exponential, logarithmic, or compound interest rate (Ricker, 1979RICKER, W.E. Growth rates and models. In: HOAR, W.S.; RANDALL, D.J.; BRETT, J.R. (Ed.) Fish physiology. London: Academic Press, 1979. v.8, p.678-743. DOI: 10.1016/s1546-5098(08)60034-5.
https://doi.org/10.1016/s1546-5098(08)60...
). The logarithm of final (lnPf) and initial (lnPi) weights at a given time in days (d) is used, as shown in the following equation: SGR=[(lnPflnPi)/d]×100 .

Another equation that is very used in aquaculture is the one to calculate daily growth coefficient (DGC), given by: DGC=[(Pf1/3Pi1/3)/d]×100 . Only the mean values of the weight at the beginning (Pi) and at the end (Pf) of animal growth are considered, being divided by the time in days (d) at a given exponential (1/3), which represents a ratio of exponential growth of 0.3333 and is used to adjust the growth curve that is not considered in the equation for SGR.

The equation for linear growth coefficient (LGC), as the other ones, does not reflect the actual trajectory of the animal during farming, since it considers only the final weight subtracted by the initial weight and divided by the number of farming days. It was believed that this would be a representation of what actually happened during farming; however, the used equations disregard oscillations and differences in growth related to water temperature and metabolic conditions during the period, as exemplified in the following equation: LGC=(PfPi)/d .

Due to the great diversity of models for the prediction and calculation of the growth trajectory of fish (SGR, DGC, and LGC), it is necessary to consider factors such as water temperature in the relationship between fish metabolism and growth. In this sense, Iwama & Tautz (1981)IWAMA, G.K.; TAUTZ, A.F. A simple growth model for salmonids in hatcheries. Canadian Journal of Fisheries and Aquatic Sciences, v.38, p.649-656, 1981. DOI: 10.1139/f81-087.
https://doi.org/10.1139/f81-087....
applied the concept of thermal unit to estimate growth in juvenile trout. Cho (1992)CHO, C.Y. Feeding systems for rainbow trout and other salmonids with reference to current estimates of energy and protein requirements. Aquaculture, v.100, p.107-123, 1992. DOI: 10.1016/0044-8486(92)90353-M.
https://doi.org/10.1016/0044-8486(92)903...
, in turn, explicitly introduced the concept of degree-days in his model and proposed a mathematical derivation for thermal growth coefficient (TGC), given by the following equation:

T G C = { [ P f ( 1 b ) P i ( 1 b ) ] / t × d } × 100 ,

in which Pi and Pf are the initial and final body weights, respectively; d is day; t is the temperature in °C; and (1 - b) is the exponent of body weight.

The TGC model, since then, has been widely used in aquaculture (Kaushik, 1998KAUSHIK, S.J. Nutritional bioenergetics and estimation of waste production in non-salmonids. Aquatic Living Resources, v.11, p.211-217, 1998. DOI: 10.1016/S0990-7440(98)89003-7.
https://doi.org/10.1016/S0990-7440(98)89...
; Bureau & Hua, 2010BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
; Milne et al., 2015MILNE, J.E.; MARVIN, C.H.; YERUBANDI, R.; MCCANN, K.; MOCCIA, R.D. Monitoring and modelling total phosphorus contributions to a freshwater lake with cage-aquaculture. Aquaculture Research, p.1-15, 2015. DOI: 10.1111/are.12881.
https://doi.org/10.1111/are.12881....
), allowing a fine adjustment of fish growth curves.

Integration between growth models and fish energy requirements

The prediction models were developed to determine animal growth and feed consumption, as shown by the studies of Pfeffer & Pieper (1979)PFEFFER, E.; PIEPER, A. Application of the factorial approach for determining nutrient requirements of growing fish. In: HALVER, J.E.; TIEWS, K. (Ed.). Fish nutrition and fish feed technology. Hamburg: Heeneman Verlagsgesell-schaft, 1979. p.123-156. and Ricker (1979RICKER, W.E. Growth rates and models. In: HOAR, W.S.; RANDALL, D.J.; BRETT, J.R. (Ed.) Fish physiology. London: Academic Press, 1979. v.8, p.678-743. DOI: 10.1016/s1546-5098(08)60034-5.
https://doi.org/10.1016/s1546-5098(08)60...
). These models are also used to determine metabolic excretion and nutrient bioavailability for several species and production systems, as observed in the works by Cho & Bureau (1998)CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
, Booth et al. (2010)BOOTH, M.A.; PIROZZI, I.; ALAN, G.A. Estimation of digestible protein and energy requirements of yellowtail kingfish Seriola lalandi using a factorial approach. Aquaculture, v.307, p.247-259, 2010., Bureau & Hua (2010)BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
, Chowdhury et al. (2013)CHOWDHURY, M.A.K.; SIDDIQUI, S.; HUA, K.; BUREAU, D.P. Bioenergetics-based factorial model to determine feed requirement and waste output of tilapia produced under commercial conditions. Aquaculture, v.410/411, p.138-147, 2013. DOI: 10.1016/j.aquaculture.2013.06.030.
https://doi.org/10.1016/j.aquaculture.20...
, Bouwman et al. (2013)BOUWMAN, A.F.; BEUSEN, A.H.W.; OVERBEEK, C.C.; BUREAU, D.P.; PAWLOWSKI, M.; GLIBERT, P.M. Hindcasts and future projections of global inland and coastal nitrogen and phosphorus loads due to finfish aquaculture. Reviews in Fisheries Science, v.21, p.112-156, 2013. DOI: 10.1080/10641262.2013.790340.
https://doi.org/10.1080/10641262.2013.79...
, Bueno (2015)BUENO, G.W. Modelo bioenergético nutricional e balanço de massas para o monitoramento e estimativa de efluentes da produção comercial de tilápia do Nilo (Oreochromis niloticus) em reservatório tropical. 2015. 127p. Tese (Doutorado) - Universidade de Brasília, Brasília., and Canale et al. (2016)CANALE, R.P.; WHELAN, G.; SWITZER, A.; EISCH, E. A bioenergetic approach to manage production and control phosphorus discharges from a salmonid hatchery. Aquaculture, v.451, p.137-146, 2016. DOI: 10.1016/j.aquaculture.2015.09.008.
https://doi.org/10.1016/j.aquaculture.20...
.

In general, the first models, of varying complexity, partition the energy ingested through the use of energy balance equations (Dumas et al., 2010DUMAS, A.; FRANCE, J.; BUREAU, D. Modelling growth and body composition in fish nutrition: where have we been and where are we going? Aquaculture Research, v.41, p.161-181, 2010. DOI: 10.1111/j.1365-2109.2009.02323.x.
https://doi.org/10.1111/j.1365-2109.2009...
). A simple model would be: C = ME + GR + E, in which C is the energy ingested, ME is the metabolizable energy, GR is the growth retention, and E is the endogenous excretion (Jobling, 2011JOBLING, M. Bioenergetics in aquaculture settings. In: FARRELL, A.P. (Ed.). Encyclopedia of Fish Physiology: from genome to environment. Amsterdam: Elsevier, 2011. p.1664-1674. DOI: 10.1016/B978-0-12-374553-8.00152-0.
https://doi.org/10.1016/B978-0-12-374553...
).

From this balance equation, an energy balance can be built using any period of time from the entire life cycle in a snapshot in time. Pfeffer & Pieper (1979)PFEFFER, E.; PIEPER, A. Application of the factorial approach for determining nutrient requirements of growing fish. In: HALVER, J.E.; TIEWS, K. (Ed.). Fish nutrition and fish feed technology. Hamburg: Heeneman Verlagsgesell-schaft, 1979. p.123-156. suggested a deductive model, containing empirical components, which was used to determine the dietary needs of essential elements for fish. The model included factors for dietary requirement (Edt), GR, E, and the availability of the element in the diet (A). These factors were empirically determined, but their relationship was deductively built as Edt = (GR + E) / A.

The factorial models evolved and, currently, are constructed by connecting a group of parameters based on scientific studies and empirical observations during farming, related to metabolic energy requirements for maintenance, fish growth potential, efficient use of energy and ingredients available in the feeds, and animal body composition. Therefore, growth scenarios, energy demand, and releases of wastes from aquaculture systems became more precise and applicable.

Nutritional bioenergetics

Bioenergetics describes the energy flow of nutrients within a biological system, for example, in a fish or a shrimp. This approach shows the biological process of using and transforming absorbed nutrients for energy, for the synthesis of the own body (NRC, 2011NRC. National Research Council. Nutrient requirements of fish and shrimp. Washington: National Academy Press, 2011. 392p.). The feed that is consumed is transformed in the body; complex chemical compounds are divided into more simple components - proteins into amino acids, carbohydrates into glucose, and lipids into fatty acids -; and the energy released from the metabolic processes, is used for maintenance, production, and reproduction (Strand, 2005STRAND, Å. Growth and Bioenergetic Models and their Application in Aquaculture of Perch (Perca fluviatilis). Umea: SLU, 2005. 61p. Rapport n. 42. Available at: ˂Available at: ˂http://www.haparanda.se/download/18.786ab49113d008f9ee5fdd/1362143818794/Growth-+and+Bioenergetic+Models+and+their+Applications+in+Aquaculture+of+Perch.pdf ˃. Accessed on: July 21 2016.
http://www.haparanda.se/download/18.786a...
).

The metabolic expenditure by an animal is often measured as the amount of heat produced, which is often called respiration (R). By analyzing the difference between ME and R, the retained energy is obtained, usually referred to as production (Pd): Pd = ME - R.

A part of this energy is lost in feces, but there are also losses by urinary excretion and by the gills through diffusion on body surface. Two forms of energy can be defined: DE and ME; DE is able to transform itself into ME.

According to Jobling (2011)JOBLING, M. Bioenergetics in aquaculture settings. In: FARRELL, A.P. (Ed.). Encyclopedia of Fish Physiology: from genome to environment. Amsterdam: Elsevier, 2011. p.1664-1674. DOI: 10.1016/B978-0-12-374553-8.00152-0.
https://doi.org/10.1016/B978-0-12-374553...
, when an animal is under starvation (C = 0), the body tissues are catabolized to support respiration, the production (retained energy) is negative, and the animal loses body mass. However, if an animal ingests some food, but the energy retained is null over time (i.e., Pd = 0), there is a balance, and the animal meets the requirements for maintenance.

Therefore, determining and providing diets that allow meeting the ideal energy requirements will make it possible to maintain the metabolic functions, increase the production (growth, fat, and reproduction), and minimize losses and wastes generated by the metabolism of fish.

Bioenergetic factorial model applied in fish farming

According to Cho et al. (1982)CHO, C.Y.; SLINGER, S.J.; BAYLEY, H.S. Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, v.73, p.25-41, 1982. DOI: 10.1016/0305-0491(82)90198-5.
https://doi.org/10.1016/0305-0491(82)901...
, the principles of the bioenergetic factorial model were applied to fish, in 1914, by Ege & KroghEGE, R.; KROGH, A. On the relation between the temperature and the respiratory exchange in fishes. International Review of Hydrobiology, v.7, p.48-55, 1914. DOI: 10.1002/iroh.19140070105.
https://doi.org/10.1002/iroh.19140070105...
and, in 1939, by IvlevIVLEV, V.S. Energy balance in the carp. Zoological Journal, v.18, p.303-318, 1939.. Many studies regarding the use and waste of energy have been carried out since then for various species of fish (Kaushik & Médale, 1994KAUSHIK, S.J.; MÉDALE, F. Energy requirements, utilization and dietary supply to salmonids. Aquaculture, v.124, p.81-97, 1994. DOI: 10.1016/0044-8486(94)90364-6.
https://doi.org/10.1016/0044-8486(94)903...
; Booth et al., 2010BOOTH, M.A.; PIROZZI, I.; ALAN, G.A. Estimation of digestible protein and energy requirements of yellowtail kingfish Seriola lalandi using a factorial approach. Aquaculture, v.307, p.247-259, 2010.; Canale et al., 2016CANALE, R.P.; WHELAN, G.; SWITZER, A.; EISCH, E. A bioenergetic approach to manage production and control phosphorus discharges from a salmonid hatchery. Aquaculture, v.451, p.137-146, 2016. DOI: 10.1016/j.aquaculture.2015.09.008.
https://doi.org/10.1016/j.aquaculture.20...
).

Strand (2005)STRAND, Å. Growth and Bioenergetic Models and their Application in Aquaculture of Perch (Perca fluviatilis). Umea: SLU, 2005. 61p. Rapport n. 42. Available at: ˂Available at: ˂http://www.haparanda.se/download/18.786ab49113d008f9ee5fdd/1362143818794/Growth-+and+Bioenergetic+Models+and+their+Applications+in+Aquaculture+of+Perch.pdf ˃. Accessed on: July 21 2016.
http://www.haparanda.se/download/18.786a...
reports that models based on similar principles had already been previously proposed by other researchers (Kerr, 1971KERR, S.R. A simulation model of lake trout growth. Journal of Fisheries Research Board of Canada, v.28, p.815-819, 1971. DOI: 10.1139/f71-122.
https://doi.org/10.1139/f71-122....
). However, the model developed by Kitchell et al. (1974)KITCHELL, J.F.; KOONCE, J.F.; O’NEILL, R.V.; SHUGART JR., H.H.; MAGNUSON, J.J.; BOOTH, R.S. Model of fish biomass dynamics. Transactions of the American Fisheries Society, v.103, p.786-798, 1974. DOI: 10.1577/1548-8659(1974)103<786:MOFBD>2.0.CO;2.
https://doi.org/10.1577/1548-8659(1974)1...
, used to simulate the growth of bluegill (Lepomis macrochirus), was the most effective and was later used as a standard in research on poikilotherms, representing the bioenergetics model approach (Cui & Xie, 2000CUI, Y.; XIE, S. Modelling Growth in Fish. In: THEODOROU, M.K.; FRANCE, J. (Ed.). Feeding Systems and Feed Evaluation Models. Wallingford: Cabi, 2000. p.413-434.).

This model has been applied to several different species, such as, for example: Phoxinus phoxinus (Cui & Xie, 2000CUI, Y.; XIE, S. Modelling Growth in Fish. In: THEODOROU, M.K.; FRANCE, J. (Ed.). Feeding Systems and Feed Evaluation Models. Wallingford: Cabi, 2000. p.413-434.), O. niloticus (Yi, 1998YI, Y. A bioenergetics growth model for Nile tilapia (Oreochromis niloticus) based on limiting nutrients and fish standing crop in fertilized ponds. Aquacultural Engineering, v.18, p.157-173, 1998. DOI: 10.1016/S0144-8609(98)00028-4.
https://doi.org/10.1016/S0144-8609(98)00...
; Chowdhury et al., 2013CHOWDHURY, M.A.K.; SIDDIQUI, S.; HUA, K.; BUREAU, D.P. Bioenergetics-based factorial model to determine feed requirement and waste output of tilapia produced under commercial conditions. Aquaculture, v.410/411, p.138-147, 2013. DOI: 10.1016/j.aquaculture.2013.06.030.
https://doi.org/10.1016/j.aquaculture.20...
; Bueno, 2015BUENO, G.W. Modelo bioenergético nutricional e balanço de massas para o monitoramento e estimativa de efluentes da produção comercial de tilápia do Nilo (Oreochromis niloticus) em reservatório tropical. 2015. 127p. Tese (Doutorado) - Universidade de Brasília, Brasília.), Oncorhynchus mykiss (Milne et al., 2015MILNE, J.E.; MARVIN, C.H.; YERUBANDI, R.; MCCANN, K.; MOCCIA, R.D. Monitoring and modelling total phosphorus contributions to a freshwater lake with cage-aquaculture. Aquaculture Research, p.1-15, 2015. DOI: 10.1111/are.12881.
https://doi.org/10.1111/are.12881....
), and Larimichthys crocea (Cai et al., 2016CAI, H.; ROSS, L.G.; TELFER, T.C.; CHANGWEN, W.; ZHU, A.; ZHAO, S.; XU, M. Modelling the nitrogen loadings from large yellow croaker (Larimichthys crocea) cage aquaculture. Environmental Science and Pollution Research, v.23, p.7529-7542, 2016. DOI: 10.1007/s11356-015-6015-0.
https://doi.org/10.1007/s11356-015-6015-...
).

In fish ecology, bioenergetic models have been used primarily to calculate the consumption of feed based on temperature and growth data (Kitchell et al., 1977KITCHELL, J.F.; STEWART, D.J.; WEININGER, D. Application of a bioenergetics model to yellow perch (Perca flavescens) and walleye (Stizostedion vitreum vitreum). Journal of the Fisheries Research Board of Canada, v.34, p.1922-1935, 1977. DOI: 10.1139/f77-258.
https://doi.org/10.1139/f77-258....
; Hanson et al., 1997HANSON, P.C.; JOHNSON, T.B.; SCHINDLER, D.E.; KITCHELL, J.F. Fish bioenergetics 3.0 for windows manual. Madison: University of Wisconsin, Centre for Limnology, 1997. 116p.), subsidizing the development of computer software, as Fish Bioenergetics, version 3.0 (Hanson et al., 1997HANSON, P.C.; JOHNSON, T.B.; SCHINDLER, D.E.; KITCHELL, J.F. Fish bioenergetics 3.0 for windows manual. Madison: University of Wisconsin, Centre for Limnology, 1997. 116p.). However, these software are very generalist because they use the same metabolic rate, regarding the natural food chain (plankton and wild fish) and disregarding oscillations in temperature and body energy retention rates in different life stages and species. This may generate inaccurate and little precise values to estimate wastes produced by the animal metabolism.

However, the application of the bioenergetic models for aquaculture takes into account all of these factors, as exemplified by the free software Aquability . These models are accurate in the development of ideal strategies for feed and waste calculation (Cho & Bureau, 1998CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
; Strand, 2005STRAND, Å. Growth and Bioenergetic Models and their Application in Aquaculture of Perch (Perca fluviatilis). Umea: SLU, 2005. 61p. Rapport n. 42. Available at: ˂Available at: ˂http://www.haparanda.se/download/18.786ab49113d008f9ee5fdd/1362143818794/Growth-+and+Bioenergetic+Models+and+their+Applications+in+Aquaculture+of+Perch.pdf ˃. Accessed on: July 21 2016.
http://www.haparanda.se/download/18.786a...
), and can be improved and become effective tools for farmers and for agencies funding and monitoring the activity.

Use of nutritional bioenergy to estimate aquaculture waste

The production of wastes from aquaculture can be estimated by simple principles of nutrition and bioenergetics, as observed in Cho & Bureau (1998)CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
, which adopt a “biological” approach, instead of a “chemical” one. Ingested food is digested and provides proteins, lipids, and carbohydrates, which are sources of energy and nutrients potentially available for animal maintenance, growth, and reproduction. The rest of the feed (not digested) is excreted in feces as solid waste (SW).

The by-products of the metabolism, such as ammonia, urea, phosphates, and carbon dioxide, are excreted as dissolved waste (DW), mainly through the kidneys. The total waste (TW) from fish feed during farming is composed by solid and dissolved wastes, along with the waste of apparent feed loss (AFL) during feeding, in which TS = SW + DW + AFL.

However, the SW, DW, and AFL outputs are biologically estimated by: SW = [food consumed × (1 - apparent digestibility coefficient, ADC)]; and DW = [(food consumed × ADC) - nutrients retained by the fish].

Therefore, the DW may be calculated by the difference between the digestible and retained nutrients in the carcass. The precise estimate of total SW requires a reliable calculation of the wastes of AFL. Therefore, the estimation of AFL is almost impossible. However, the best estimates can be made based on the energy requirements and the expected gain, as in Cho (1992)CHO, C.Y. Feeding systems for rainbow trout and other salmonids with reference to current estimates of energy and protein requirements. Aquaculture, v.100, p.107-123, 1992. DOI: 10.1016/0044-8486(92)90353-M.
https://doi.org/10.1016/0044-8486(92)903...
, in which the energy efficiency (energy gain/consumption) indicates the degree of AFL for a particular operation. In this context, the requirement and quantity of theoretical feed (QTF) can be calculated based on the nutritional energy balance (QTF = gain + excrete), which includes heat loss.

The amount of feed input that exceeds the QTF is assumed as AFL, and all nutrients that encompass AFL must be included in the quantification of solid waste. According to Cho (1992)CHO, C.Y. Feeding systems for rainbow trout and other salmonids with reference to current estimates of energy and protein requirements. Aquaculture, v.100, p.107-123, 1992. DOI: 10.1016/0044-8486(92)90353-M.
https://doi.org/10.1016/0044-8486(92)903...
, this approach can lead to a relatively conservative estimate.

However, biological procedures based on the ADC for SW and on comparative analyzes of carcasses for DW provide reliable estimates, and the biological methods are flexible and able to adapt to a variety of conditions and farming environments (Bureau & Hua, 2010BUREAU, D.P.; HUA, K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, v.41, p.777-792, 2010. DOI: 10.1111/j.1365-2109.2009.02431.x.
https://doi.org/10.1111/j.1365-2109.2009...
).

Mathematical models for the analysis of the carrying capacity of reservoirs

One of the main strategies adopted by the managing and monitoring agencies is the use of hydrodynamic models that calculate the carrying or nutrient load capacity of a particular water body, as well as the effect of fish farming.

Based on these aspects, several mathematical models were proposed: of Dillon & Rigler (1974)DILLON, P.J.; RIGLER, F.H. A test of a simple nutrient budget model predicting the phosphorus concentration in lake water. Journal of the Fisheries Research Board of Canada, v.31, p.1771-1778, 1974. DOI: 10.1139/f74-225.
https://doi.org/10.1139/f74-225....
, of Vollenweider (1975)VOLLENWEIDER, R.A. Input-output models with special reference to the phosphorus loading concept in limnology. Schweizerische Zeitschrift für Hydrologie, v.37, p.53-84, 1975. DOI: 10.1007/BF02505178.
https://doi.org/10.1007/BF02505178....
, Mike application, ECO Lab module (DHI Water and Environment), “Variáveis que Interagem de Modo Seminquantitativo” (Visq), Structural Thinking Experimental Learning Laboratory with Animation (Stella), Qualres, Ecopath Modeling, “Pegada Ecológica”, Delph 3D, and 3D Water Modeling System (Mohid), which are tools that simulate the dynamics of the variables that occur in the aquatic environment.

In general, these models are based on the direct relationship between P increase and algae growth. However, when these models are used to determine the carrying capacity for fish production, specific zootechnical and limnological factors are not always considered, which can under- or overestimate the real contribution of effluents from fish production. This shows the importance of the integration of bioenergetic models to determine the wastes from fish farms and to assist in the input of data for hydrodynamic modeling.

Integration between the mathematical models for the definition of carrying capacity

To define the carrying capacity, the Dillon & Rigler model (1974)DILLON, P.J.; RIGLER, F.H. A test of a simple nutrient budget model predicting the phosphorus concentration in lake water. Journal of the Fisheries Research Board of Canada, v.31, p.1771-1778, 1974. DOI: 10.1139/f74-225.
https://doi.org/10.1139/f74-225....
was applied, considering the P concentration (mg m-3) in water as a function of the annual P load (La, in mg m-2 per year), the P retention coefficient (Rp), average depth (z, in meters), and water residence time of the reservoir (ρ, in years). P concentration is given by the equation: [P]=La(1Rp)/(z×ρ) , in which z is calculated by the ratio between the volume and the area of the body of water; ρ is calculated by the ratio between the average and maximum flow volume of the reservoir; and Rp is the P retention coefficient from the study by Larsen & Mercier (1976)LARSEN, D.P.; MERCIER, H.T. Phosphorus retention capacity of lakes. Journal of the Fisheries Research Board of Canada, v.33, p.1742-1750, 1976. DOI: 10.1139/f76-221.
https://doi.org/10.1139/f76-221....
, with modifications by Canfield & Bachmann (1981)CANFIELD, D.E.; BACHMANN, R.W. Prediction of total phosphorus concentrations, chlorophyll a, and Secchi depths in natural and artificial lakes. Canadian Journal of Fisheries and Aquatic Sciences, v.38, p.414-423, 1981. DOI: 10.1139/f81-058.
https://doi.org/10.1139/f81-058....
, obtained by the following equation: Rp=1/(1+0.614×ρ0.491) .

The parameter for P content is Δ[P], which is the increase in the concentration of P in water for a given La. The following equation shows the relationship between these parameters: La=(Δ[P]×z×ρ)/(1R) , in which Δ[P] is given by subtracting the current P content in the water of the reservoir by the maximum concentration allowed by Resolution No. 357/2005 of Conselho Nacional do Meio Ambiente (Conama) (Brasil, 2005BRASIL. Resolução nº 357, de 17 de março de 2005. Dispõe sobre a classificação dos corpos de água e diretrizes ambientais para o seu enquadramento, bem como estabelece as condições e padrões de lançamento de efluentes, e dá outras providências. Diário Oficial da União, 18 mar. 2005. Seção 1, p.58-63.). From the Δ[P] permitted, the maximum La allowed is calculated, i.e., the amount of P that can be added to water.

Currently, Agência Nacional das Águas (ANA) takes into account the multiple uses of the reservoir in the issuance of permits for aquaculture activities, based on Resolution No. 357/2005 of Conama (Brasil, 2005BRASIL. Resolução nº 357, de 17 de março de 2005. Dispõe sobre a classificação dos corpos de água e diretrizes ambientais para o seu enquadramento, bem como estabelece as condições e padrões de lançamento de efluentes, e dá outras providências. Diário Oficial da União, 18 mar. 2005. Seção 1, p.58-63.). According to legislation, the limit for the total P is 30 mg m-3, in lentic environments, and 50 mg m-3 in intermediary environments, with water residence time varying from 2 to 40 days and permanent tributaries for lentic environments.

Based on these numbers and to standardize the amount of P allowed for aquaculture activities, the maximum amount of P allowed is limited to the fraction of 1/6 for lentic environments (30 mg m-3), i.e., the maximum load to be discharged by aquaculture is of 5 mg m-3 P per year (ANA, 2009ANA. AGÊNCIA NACIONAL DE ÁGUAS. Nota Técnica n.009/2009/GEOUT/SOF-ANA: atualização na metodologia de análise de pedidos de outorga para piscicultura em tanques-rede. Brasília, 2009. 3p. ).

The remaining 5/6 would be reserved for other uses with P contributions to water, such as the dilution of domestic and industrial sewages, besides the amount of natural P. It should be noted that, in specific cases, in which there is a prior study of the reservoir, analyzing its multiple uses, the ability of the hydric body for aquaculture activities may vary; however, it will depend on the analysis and approval of the regulatory agency.

Therefore, La was calculated in function of a Δ[P] of 5 mg m-3. Then, the P load allowed in all the reservoir (Lr) was determined, in mg per year, using the La, representing the maximum load of P allowed per square meter, multiplying the value obtained by the water surface area (A, in m2) from the reservoir, according to the equation: Lr = La × A. The water permanence of 90% was used, which is obtained by the equation: Lr=(Δ[P]×V90×ρ)/(1Rp) , in which V90 is the volume at 90% of water permanence (ANA, 2009ANA. AGÊNCIA NACIONAL DE ÁGUAS. Nota Técnica n.009/2009/GEOUT/SOF-ANA: atualização na metodologia de análise de pedidos de outorga para piscicultura em tanques-rede. Brasília, 2009. 3p. ). Then, Lr was converted into the annual authorized fish production. For this purpose, the amount of P in water for each ton of fish produced must be estimated.

Example of the application of the proposed methodology

The Fish-PrFEQ factorial bioenergetic model of Cho & Bureau (1998)CHO, C.Y.; BUREAU, D.P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquatic Living Resources, v.11, p.199-210, 1998. DOI: 10.1016/S0990-7440(98)89002-5.
https://doi.org/10.1016/S0990-7440(98)89...
is used to simulate the P load released by fish production (Pa). Different levels of total P in the feed (0.8, 1.0, and 1.5%) are considered for tilapia under different water temperatures (21, 25, and 29ºC, respectively) (Table 1). With Pa, the total P load allowed throughout the reservoir (Lr) is calculated by the equation that multiplies the L value (which represents the maximum load of permitted P per square meter) by A (total surface area, in m2), i.e., Lr = L × A. Then, having Lr and Pa, the authorized fish production is calculated (B, in mg per year) based on the allowed P load in the reservoir (Lr, in kg per year), with B = Lr / Pa.

Table 1.
Estimation of solid waste (total P) in the production of Nile tilapia (Oreochromis niloticus), at different temperatures, in cages, by the bioenergetic nutritional model.

Specifically, a simulation of the application of this methodology was carried out in the reservoir of Ilha Solteira, in Paraná river, in the state of São Paulo, Brazil (Table 2).

Table 2.
Application of the new methodology of the bioenergetic nutritional model used to determine the carrying capacity and to manage the maximum fish production of the reservoir of Ilha Solteira, in the state of São Paulo, Brazil.

Concluding remarks

The use of factorial bioenergetic models, integrated with the hydrodynamic model, aids in determining the waste load and in adjusting the values used to calculate the carrying capacity of the reservoir for fish production.

The approach presented allows monitoring and managing aquaculture enterprises installed in lakes and reservoirs, besides improving the analysis methodology used for licensing each aquaculture enterprise, considering water quality parameters, feed nutritional quality, and peculiarities of each species (feeding habits, genetics, and growth stages). In this way, it becomes possible to encourage producers and the industry to use feed with lower environmental impact and management techniques that promote aquaculture sustainability.

Regarding fish production, in loco joint inspection actions (production reports) are recommended, as well as programs for monitoring the quality of water and sediments for the control of the carrying capacity of lakes and reservoirs.

Acknowledgments

To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), to International Science and Technology Partnerships Canada (ISTP Canada, process No. 490226/2012-4), and to Fundação de Amparo à Pesquisa do Estado de São Paulo (Fapesp, project No. 2016/10.563-0), for financial support.

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Publication Dates

  • Publication in this collection
    Sept 2017

History

  • Received
    13 July 2015
  • Accepted
    11 July 2016
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