What is nitrogen?
Nitrogen (N) is one of the main elements that make up living organisms, along with carbon, oxygen and hydrogen. On average, it accounts for 2.5 to 3.5% of the dry organic matter in animals. Amino acids, which are the building blocks of proteins, are all composed of an amine group (-NH2) containing nitrogen and a carboxylic acid group (-COOH). Nitrogen is therefore the third most abundant element in amino acids, after carbon (50-55%) and oxygen (20-23%). Nitrogen is therefore essential for ensuring proper metabolism, protein synthesis and, consequently, animal growth.
1.Protein requirements, metabolism in aquaculture and nitrogen emissions
25 to 40%
These are the average dietary protein requirements of aquaculture species.
Aquaculture species generally have higher dietary protein requirements than other farm animals such as poultry (15–22%) (Applegate and Angel, 2014). These higher amino acid requirements are explained by the fact that amino acid oxidation is the primary source of energy in fish (Weber and Haman, 1996).The dietary protein requirements of fish vary according to species and diet, ranging from around 25-35% for omnivorous and herbivorous species such as tilapia and carp, to 35-40% for carnivorous species such as salmonids, sea bass and sea bream.
Proteins ingested by animals are rapidly broken down into amino acids in the digestive tract by the action of various specific enzymes: pepsins first break down proteins into peptides, then trypsin and chymotrypsin break down the peptides into amino acids (Engrola et al., 2009; Gamboa-Delgado et al., 2011). These amino acids are then absorbed by intestinal cells and used to synthesise new proteins or to produce energy through deamination (Bröer, 2008). The amine group is converted into ammonia (NH3), a metabolic waste product that is toxic to animals if it accumulates (Forster and Goldstein, 1969). Aquatic organisms can rapidly excrete NH3 into the water through their gills, thus avoiding its conversion and conserving energy compared to urothelial animals such as mammals and birds (Figure 1).
Figure 1: Protein metabolism and nitrogen excretion
2. The nitrogen cycle and its various forms in water
Once released into water, NH3 dilutes easily. Depending on water parameters, mainly pH and temperature, the dominant form will be NH3 or ammonium (NH4+), a form that is less toxic to fish and shrimp, by capturing an H+ ion (Thurston and Russo, 1983). At acidic pH, the dominant form is NH₄⁺, while at basic pH (>8.5), the most prevalent form is NH₃. Temperature also influences the ionisation of NH₃, with higher temperatures favouring the NH₃ form over NH₄⁺.
8.5
This is the pH that must not be exceeded in order to limit the formation of NH3.
It is the biological process that transforms NH3 into NO2- and then NO3- through the action of bacteria.
Next, the biological process of nitrification transforms NH3 into nitrate (NO3–) under the action of microorganisms. Nitrification is divided into two distinct stages: nitrosation and nitration, each carried out by different microorganisms. Nitrosation, carried out by bacteria of the genera Nitrosomonas, Nitrosococcus, and Nitrosospira, converts NH3 into nitrite (NO2–). Nitration, carried out in particular by the genera Nitrobacter, Nitrococcus, and Nitrospira, transforms NO2– into nitrate (NO3–). The oxidation of NH3 and NO2– provides bacteria with the energy they need to convert CO2 into organic matter (Figure 2).
Figure 2: Nitrogen cycle in water
(Robles-Porchas et al., 2020)
To optimize nitrification, it is crucial to maintain neutral pH, good oxygenation, and redox balance in fish and shrimp ponds (Molins-Legua et al., 2006). The NO3– produced by nitrification is then absorbed and used as a source of nitrogen by aquatic plants and algae, which reduce NO3– to NH4+ to synthesize amino acids and proteins. Any disruption of the nitrogen cycle can negatively affect the performance and survival of fish and shrimp by generating toxic nitrogen compounds, reducing the concentration of oxygen (O2), and altering the pH of the water.
- In lake trout (Salvelinus namaycush), exposure to 198 µg/L of ammonia for 60 days reduces protein efficiency by 7% (Beamish and Tandler, 1990).
- Rainbow trout fry (Oncorhynchus mykiss) exposed to 13 mg/L of ammonia for 90 days after hatching saw their weight decrease by 54% and their survival rate by 70% (Brinkman et al., 2009).
- In whiteleg shrimp, the accumulation of nitrite and ammonia from faeces and uneaten food over 33 days reduces survival rates by 2.5 times and growth rates by 20.5% (Han et al., 2017).
- In river catfish (Ictalurus punctatus), exposure to 3.71 mg/L for 31 days reduces growth by 20% (Colt et al., 1981).
3. Harmful effects of nitrogen in water on aquatic animals
Nitrogen released into water can affect aquatic animals directly or indirectly. The different forms of nitrogen described above, including NH3, NH4+, NO2–, and NO3–, have different levels of toxicity for fish and shrimp. While the limit concentrations in water for the various nitrogen compounds vary depending on the species, the order of toxicity remains the same for all species: NH3 is the most toxic, followed by NO2–, then NH4+ and finally NO3– (Figure 3).
Figure 3: Toxicity of nitrogen compounds to aquatic species (Lin et al., 2023; Tomasso, 1994)
a. Direct toxicity of nitrogen
Since NH3 is an uncharged molecule, it can easily diffuse through biological membranes, particularly gills (Klocke et al., 1972; Randall and Wright, 1987). Once in the blood, it disrupts many hematological parameters, including acid-base balance, coagulation, and molecule transport. In fish, the accumulation of NH3 disrupts the immune system, induces oxidative stress, and causes tissue damage in the gills, liver, kidneys, and intestines. In crustaceans, NH3 also induces oxidative stress and affects the innate immune system and molting (Bouwman et al., 2011; Chang et al., 2015; Cui et al., 2017; Hong et al., 2007; Rodríguez-Ramos et al., 2008; Romano and Zeng, 2013).
- Immunosuppression
- Oxidative stress
- Neurotoxicity
- Gill stress
NO2– is less toxic than NH3, but its toxicity remains very high. In fish, the main mechanism of NO2– toxicity is the formation of methemoglobin (MetHb) through the oxidation of iron (Fe) in hemoglobin. MetHb can no longer bind and transport O₂, causing hypoxia despite oxygenated water (Jensen, 2003). A similar phenomenon is observed in shrimp: NO₂⁻ oxidizes the copper (Cu) in hemocyanin, preventing O₂ binding. NO₂⁻ can also induce oxidative stress and disrupt the innate immune system of fish and shrimp. NO₂⁻ also impacts the biology and health of gills (Svobodová et al., 2005), reduces food intake in fish and shrimp (Ribeiro-de-Campos et al., 2021; Roques et al., 2013) and affects their growth (Ciji and Akhtar, 2020; Colt et al., 1981; Frances et al., 1998; Koo et al., 2005; Mallasen and Valenti, 2006; Siikavuopio and Sæther, 2006).
NH4+ is much less toxic, and its concentrations in water must be very high to affect aquatic animals. At high concentrations, NH4+ can limit the ability of gills to excrete NH3, leading to the accumulation of NH3 in fish and shrimp. NH4+ also substitutes for potassium (K+) in ion transporters, affecting the electrochemical gradient of the central nervous system (Cooper and Plum, 1987) and impairing brain function (Ip and Chew, 2010).
NO3– has low acute toxicity but can have significant chronic effects. NO3– can cause oxidative stress, which, if chronic, can weaken the immune system, affect reproduction, and slow growth. Its toxicity depends on concentration and exposure time (Pierce et al., 1993; Scott and Crunkilton, 2000), and also on salinity (Dowden and Bennett, 1965).
b. Indirect impacts of nitrogen emissions
When nitrogen discharge into water is excessive, nitrifying bacteria can be overwhelmed by high concentrations of NH3 and NO2–, causing them to accumulate in the water. Excess nitrogen stimulates the growth and proliferation of microalgae, leading to algal blooms. The high concentration of microalgae reduces light penetration in the water column, causing them to die. The decomposition of this organic matter by bacteria consumes large amounts of O₂, reducing its concentration in the water (Huo et al., 2013; Moss et al., 2013). This phenomenon is called eutrophication (Figure 4).
Figure 4: The process of eutrophication (Yang et al., 2008)
Eutrophication initiates a vicious cycle, with the lack of O2 in the water causing the death of other aquatic organisms, generating more organic matter and further reducing the O2 concentration (Yang et al., 2008). This has a serious impact on the growth and survival of fish and shrimp, particularly in ponds, which are closed systems with little water renewal. In particular, it has been observed that algae blooms in shrimp ponds in Mexico, caused by excessive nutrient input, have led to a 79.5% mortality rate among post-larvae, in addition to reducing growth (Licea, 1999).
In addition, eutrophication can lead to the proliferation of harmful species such as cyanobacteria, which often have an anaerobic metabolism, meaning that the decrease in oxygen concentration in the water promotes their proliferation (Codd, 2000). A decline in the survival of penaeid shrimp has been observed in China and Ecuador due to microalgae blooms causing anoxia in ponds (Alonso-Rodríguez and Páez-Osuna, 2003). In open systems such as sea cages, excessive nitrogen discharges can promote the proliferation of microalgae, some of which produce toxins (Anderson et al., 2002) or damage fish gills with their spicules (calcareous or siliceous spikes), potentially leading to significant mortality in affected fish farms (Burridge et al., 2010).
Recirculated aquaculture systems (RAS), thanks to their ability to control water parameters, are less affected by these issues. However, nitrogen discharge remains a significant problem even for the most technologically advanced systems. RAS filtration systems are very large and expensive to install. Reducing nitrogen levels in the water can help avoid oversizing filtration systems and thus limit costs. In addition, nitrification consumes the alkalinity of the water, requiring regular pH adjustments (Timmons et al., 2018).
4. The benefits of reducing nitrogen input in aquaculture systems
It is essential to control nitrogen levels, both in closed aquaculture facilities (such as tanks, ponds, and recirculation systems) to ensure animal performance and welfare, and in open systems (such as sea cages and raceways) to minimize their environmental impact. This can be achieved by reducing nitrogen emissions into the water or by improving the ability of nitrifying bacteria to convert nitrogen. Reducing nitrogen emissions involves optimizing feed distribution to avoid overfeeding and adjusting feed formulation to limit nitrogen intake. By precisely modulating the protein levels in feed in relation to other nutrients, protein catabolism and ammonia (NH3) emissions into water can be reduced.
This also involves choosing other raw materials, such as inorganic feed phosphates. It is crucial to choose products that limit phosphorus (P) and N emissions to prevent their accumulation in water and thus prevent eutrophication. For this purpose, monosodium phosphate (MSP) is the best choice, as it provides highly digestible P for fish and shrimp, while reducing N emissions into the water compared to monoammonium phosphate (MAP) (Morales et al., 2018). Although MAP phosphate also provides highly digestible P, it also provides excess NH3 that is not used by aquatic organisms in the same way as it is by ruminants.
Thus, while MAP is an effective phosphate for aquaculture, it increases nitrogen emissions into the water (Figure 5). Therefore, to provide an effective source of P while reducing P and N emissions, which affect fish health and the environment, it is preferable to opt for MSP.
4,2kg
This is the reduction in dissolved N excreted into the water per tonne of fish produced using MSP compared to MAP (Morales et al., 2018).
Figure 5: Diminution des rejets de N avec le MSP
Conclusion
Nitrogen is an essential element in aquaculture, but its metabolism can generate toxic waste such as NH3 when accumulated in water. Therefore, dietary adjustments to reduce N emissions and the creation of optimal conditions for nitrifying bacteria are necessary to minimize the harmful effects of N and ensure the health of aquaculture species. In terms of feeding and inorganic P intake, MSP is the most suitable source for ensuring the sustainability of aquaculture farms.
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