Inorganic nitrogen pollution in aquatic ecosystems: causes and consequences
Contents
Introduction
Ammonium (NH4+), nitrite (NO2–) and nitrate (NO3–) are the most common ionic (reactive) forms of dissolved inorganic nitrogen in aquatic ecosystems. These ions (Inorganic nitrogen pollution in aquatic ecosystems: causes and consequences) can be present naturally as a result of atmospheric deposition, surface and groundwater runoff, dissolution of nitrogen-rich geological deposits, N2 fixation by certain prokaryotes (cyanobacteria with heterocysts, in particular), and biological degradation of organic matter. However, humans have substantially altered the global nitrogen cycle, increasing both the availability and the mobility of nitrogen over large regions of Earth. Consequently, in addition to natural sources, inorganic nitrogen can enter aquatic ecosystems via point and nonpoint sources derived from human activities (Table 1). Nonpoint sources generally are of greater relevance than point sources since they are larger and more difficult to control. Moreover, anthropogenic inputs of particulate nitrogen and organic nitrogen to the environment can also result in inorganic nitrogen pollution.
Three major environmental problems appear to be associated to inorganic nitrogen pollution in aquatic ecosystems:
- it can increase the concentration of hydrogen ions in freshwater ecosystems without much acid-neutralizing capacity, resulting in acidification of those ecological systems;
- it can stimulate or enhance the development, maintenance and proliferation of primary producers, resulting in eutrophication of estuarine, and coastal marine ecosystems. In some cases, inorganic nitrogen pollution can also induce the occurrence of toxic algae;
- it can impair the ability of aquatic animals to survive, grow and reproduce as a result of direct toxicity of ammonia, nitrite and nitrate. In addition, inorganic nitrogen pollution of ground and surface waters could induce adverse effects on human health.
Acidification
| Table 2. Adverse Effects |
|---|
| Reduction of the net photosynthesis and productivity in planktonic and attached algae |
| Increased bioaccumulation and toxicity of aluminum and other trace metals in aquatic plants and animals |
| Disruption of the ionic regulation in aquatic animals |
| Respiratory and metabolic disturbances in aquatic animals |
| General loss of sensitive species, resulting in declined species diversity |
| Source: Julio Camargo |
Reductions in sulfur dioxide (SO2) emissions throughout the 1980s and 1990s have reduced the atmospheric deposition of sulfuric acid (H2SO4) across large portions of North America and Europe, while emissions of nitrogen oxides (NOx) have gone unchecked. In consequence, nitric acid (HNO3) is now playing an increasing role in the acidification of freshwater ecosystems without much acid-neutralizing capacity (i.e., with moderate or low alkalinity). A decrease in the pH value of water (i.e., an increase in the hydrogen ion [H+] concentration) can also increase the concentration of dissolved aluminum (and other trace metals) owing to enhanced metal mobilization and/or decreased metal sedimentation. Part of the dissolved aluminum can subsequently settle in the sediments of atmospherically acidified lakes and reservoirs, reducing orthophosphate availability and disrupting the phosphorus cycling in those water bodies.
The anthropogenic acidification of lakes and streams can cause several adverse effects on primary and secondary producers (Table 2). Additionally, key microbial processes for nutrient cycling and ecosystem functioning may also be inhibited or altered as a consequence of decreased pH values.
Eutrophication
| Table 3. Ecological Effects |
|---|
| Increased biomass and productivity of primary producers (phytoplankton, benthic algae, freshwater macrophytes, marine macroalgae) |
| Shifts in species composition of phytoplankton, periphyton, macroalgae and macrophyte communities |
| Increased biomass, and changes in productivity and species composition, of zooplankton, being usually favoured invertebrate grazers at the expense of other trophic groups |
| Changes in biomass, productivity and species composition of benthic invertebrates and fish, often with mass mortality events in sensitive populations |
| Losses of species diversity in phytoplankton, periphyton, macroalgae and macrophyte communities |
| Losses of species diversity in zooplankton, benthic invertebrates and fish communities |
| Losses of species diversity in marine coral communities |
| Alterations in the food web structure of freshwater, estuarine, and coastal marine ecosystems, with ramifying effects on every trophic level |
| Source: Julio Camargo |
Elevated concentrations of ammonium (NH4+), nitrite (NO2–) and nitrate (NO3–), derived from human activities, can stimulate or enhance the development, maintenance and proliferation of primary producers (phytoplankton, benthic algae, macrophytes), contributing to the widespread phenomenon of the cultural (human-made) eutrophication of aquatic ecosystems. The nutrient enrichment can cause important ecological effects on aquatic communities (Table 3), since the overproduction of organic matter and its subsequent decomposition usually lead to low dissolved oxygen concentrations in bottom waters and sediments of eutrophic and hypereutrophic aquatic ecosystems with low water turnover rates.
Extensive kills of both invertebrates and fishes (sensitive benthic species, particularly) are probably the most dramatic manifestation of hypoxia (or anoxia) in eutrophic and hypereutrophic aquatic ecosystems, with significant reductions in the area of suitable habitat for food, growth and reproduction. The decline in dissolved oxygen concentrations can also promote the formation of reduced compounds, such as hydrogen sulphide (H2S), resulting in higher adverse effects on aquatic animals. In addition, mass occurrences of toxic algae, currently a global phenomenon that appears to be favored by nutrient pollution, can significantly contribute to the extensive kills of aquatic animals.
Occurrence of Toxic Algae
| Table 4. Major groups of toxins in cyanobacteria, dinoflagellates and diatoms | |||
|---|---|---|---|
| Toxins | Chemical Structure | Site of Action | Typical Species |
| Anatoxin-a | Secondary amine alkaloid | Nervous system | Anabaena circinalis Aphanizomenon flos-aquae |
| Anatoxin-a(s) | Organophosphate | Nervous system | Anabaena flos-aquae Anabaena lemmermannii |
| Brevetoxins | Polycyclic ethers | Nervous system | Karenia brevis |
| Domoic acid | Tricarboxylic amino acid | Nervous system | Pseudo-nitzschia australis Pseudo-nitzschia multiseries |
| Hemolysins | Cyclic heptapeptides | Target cells | Alexandrium monilatum Gymnodinium aureolum |
| Microcystins | Cyclic heptapeptides | Liver, hepatopancreas | Microcystis aeruginosa Planktothrix agardii |
| Nodularins | Cyclic pentapeptides | Liver, hepatopancreas | Nodularia spumigena |
| Saxitoxins | Carbamate alkaloids | Nervous System | Aphanizomenon flos-aquae Alexandrium tamarense |
| Source: Julio Camargo | |||
Algae can cause toxicity to aquatic (and terrestrial) animals because of the synthesis of certain toxins (harmful metabolites). These toxins can remain inside algal cells (intracellular toxins), or they may be released into the surrounding water (extracellular toxins) during active algal growth or when algal cells lyse. In consequence, animals may be directly exposed to toxins by absorbing toxins from water, drinking water with toxins, or ingesting algal cells via feeding activity. Additionally, because algal toxins can be bioaccumulated, biotransferred and biomagnified through food chains and food webs, aquatic and terrestrial animals can also be indirectly exposed to toxins when they consume other animals containing toxins. Among the different taxonomic groups contributing to the occurrence of toxic algae, cyanobacteria, dinoflagellates and diatoms appear to predominate and may be stimulated by inorganic nitrogen pollution.
The genera most often implicated in the toxicity of freshwater cyanobacteria are Anabaena, Aphanizomenon, Microcystis, Nodularia and Planktothrix. Wild populations of Microcystis are almost always toxic, while species of other genera usually comprise toxic and non-toxic strains. Laboratory and field studies have shown that toxicity of a strain ultimately depends both on whether or not it contains the gene for toxin production and on environmental factors promoting the gene expression. Major groups of toxins found in species/strains of cyanobacteria are anatoxins, microcystins, nodularins and saxitoxins (Table 4). In the case of marine dinoflagellates (red tides), the genera most often implicated in the toxicity to aquatic animals are Alexandrium, Gymnodinium and Karenia. Major groups of toxins found in species/strains of these genera are brevetoxins, hemolysins and saxitoxins (Table 4). Lastly, diatoms of the ubiquitous marine genus Pseudo-nitzschia have been implicated in intoxications to aquatic animals by the synthesis of domoic acid (Table 4).
Toxicity of Ammonia, Nitrite and Nitrate
The ionized ammonia (NH4+) and unionized ammonia (NH3) are interrelated through the chemical equilibrium NH4+ + OH- ? NH3•H2O ? NH3 + H2O, the relative concentrations of NH4+ and NH3 being basically dependent on the pH and temperature of the water. Unionized ammonia is very toxic to aquatic animals, particularly to fish, whereas ionized ammonia is nontoxic or appreciably less toxic. The toxic action of NH3 on fish and other aquatic animals may be due to one or more of the following causes:
- damage to the gill epithelium causing asphyxiation;
- stimulation of glycolysis and suppression of Krebs cycle causing progressive acidosis and reduction in blood oxygen-carrying capacity;
- uncoupling oxidative phosphorylation causing inhibition of Adenosine triphosphate (ATP) production and depletion of ATP in the basilar region of the brain;
- disruption of blood vessels and osmoregulatory activity upsetting the liver and kidneys;
- repression of immune system increasing the susceptibility to bacterial and parasitic diseases.
Water quality criteria within the range 0.01-0.02 mg NH3-N/L have been proposed to protect sensitive aquatic animals.
The nitrite ion (NO2-) and unionized nitrous acid (HNO2) are interrelated through the chemical equilibrium NO2- + H+ ? HNO2, the relative concentrations of NO2– and HNO2 being basically dependent on the pH of the water. Because in aquatic ecosystems the NO2– concentration usually is much higher (about 4-5 orders of magnitude) than the HNO2 concentration, nitrite ions are considered to be major responsible for nitrite toxicity to aquatic animals. The main toxic action of nitrite on aquatic animals is due to the conversion of oxygen-carrying pigments to forms that are incapable of carrying oxygen, causing hypoxia and ultimately death. In fish, entry of nitrite into the red blood cells is associated with the oxidation of iron atoms (Fe2+ ? Fe3+), functional hemoglobin being converted into methemoglobin that is unable to release oxygen to body tissues because of its high dissociation constant. Similarly, in crayfish, entry of nitrite into the blood plasma is associated with the oxidation of copper atoms (Cu1+ ? Cu2+), whereby functional hemocyanin is converted into methemocyanin that cannot bind reversibly to molecular oxygen. Water quality criteria within the range 0.08-0.35 mg NO2-N/L have been proposed to protect sensitive aquatic animals, at least during short-term exposures.
The nitrate ion (NO3–) does not form unionized species in the aquatic environment and, consequently, nitrate toxicity to aquatic animals is due to nitrate ions. The main toxic action of NO3– on aquatic animals, particularly on fish and crayfish, seems to be the conversion of oxygen-carrying pigments (hemoglobin, hemocyanin) to forms that are incapable of carrying oxygen (methemoglobin, methemocyanin). However, owing to the low branchial permeability to nitrate ions, the NO3– uptake in aquatic animals is more limited than the NO2– uptake, which contributes to the relatively low toxicity of nitrate. A maximum level of 2 mg NO3–N/L has been proposed to protect sensitive aquatic animals.
Adverse Effects on Human Health
Ingested nitrites and nitrates, from polluted drinking water exhibiting elevated concentrations higher than 1 mg NO2-N/L and 10 mg NO3-N/L, might induce methemoglobinemia in humans by the blockade of the oxygen-carrying capacity of hemoglobin, resulting in the formation of methemoglobin. Typical symptoms of methemoglobinemia are cyanosis, headache, stupor, fatigue, tachycardia, convulsions, asphyxia and ultimately death. Infants less than 4 months of age seem to be particularly susceptible.
Ingested nitrites and nitrates also have a potential role in developing cancers of the digestive tract through their contribution to the bacterial formation of nitrosamines, which are among the most potent of the known carcinogens in mammals. In addition, some scientific evidences suggest that ingested nitrites and nitrates could result in mutagenicity, teratogenicity and birth defects, contribute to the risks of non-Hodgkin’s lymphoma, coronary heart disease, and bladder and ovarian cancers, play a role in the etiology of insulin-dependent diabetes mellitus and in the development of thyroid hypertrophy, or cause spontaneous abortions and respiratory tract infections.
Indirect health hazards can occur as a consequence of algal toxins. Blooms of toxic cyanobacteria in water storage reservoirs, lakes and rivers, leading to adverse health effects following consumption of contaminated drinking water or after recreational exposure, have been reported from Australia, Brazil, Canada, China, Sweden, United Kingdom, USA and other countries. Blooms of toxic dinoflagellates in estuaries and coastal waters, leading to several poisoning syndromes following consumption of contaminated seafood or after water or aerosol exposure, have been reported from Australia, Europe, Japan, North America, Southeast Asia and other parts of the world. Human intoxications by consuming blue mussels that were contaminated with domoic acid have been reported from Canada.
Other indirect health hazards can also come from the potential relationship between inorganic nitrogen pollution and human infectious diseases since increasing nutrient availability may often favor opportunistic, disease-causing organisms. Several studies have shown positive correlations between concentration of inorganic nutrients in surface waters and larval abundance of mosquitoes which may be carriers of pathogenic microorganisms. High nutrient conditions favoring coastal algal blooms have also been associated with some cholera outbreaks.
Further Reading
- Alonso, A. and Camargo, J.A. 2003. Short-term toxicity of ammonia, nitrite, and nitrate to the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bulletin of Environmental Contamination and Toxicology, 70:1006-1012.
- Alonso, A. and Camargo, J.A. 2004. Toxic effects of unionized ammonia on survival and feeding activity of the freshwater amphipod Eulimnogammarus toletanus (Gammaridae, Crustacea). Bulletin of Environmental Contamination and Toxicology, 72:1052-1058.
- Alonso, A. and Camargo, J.A. 2006. Toxicity of nitrite to three species of freshwater invertebrates. Environmental Toxicology, 21:90-94.
- Camargo, J.A., Alonso, A. and Salamanca, A. 2005. Nitrate toxicity to aquatic animals: a review with new data for freshwater invertebrates. Chemosphere, 58:1255-1267.
- Camargo, J.A., Alonso, A. and de la Puente M. 2005. Eutrophication downstream from small reservoirs in mountain rivers of Central Spain. Water Research, 39:3376-3384.
- Camargo, J.A. and Alonso, A. 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International, 32:831-849.
