Nitrogen Toxicity in Aquatic Ecosystems

The effects of nitrogen in freshwater, estuarine, and coastal marine ecosystems are very different from those in terrestrial ecosystems. This is partly because the dominant nitrogen forms differ between the two types of ecosystems and also because these ecosystems differ in type of species found (e.g., angiosperms are not well represented in aquatic ecosystems whereas they dominate terrestrial ecosystems), and because they differ in terms of pollutant mixing, micro-niches/environments, etc. However, some general patterns in the effects of reactive nitrogen on organisms and ecosystem processes can be identified in terrestrial and aquatic ecosystems.

Direct Toxicity

Nitrogen enters aquatic ecosystems via surface and groundwater runoff, atmospheric deposition, nitrogen fixation by prokaryotes (cyanobacteria, blue-green algae), dissolution ofnitrogen rich material, and decomposition. It occurs in water in four important, potentially toxic, forms: NH4, NH 3, NO2 , and NO3. NH3 is the most toxic form to biota. However, since NH4 and NH3 are readily oxidized to NO2, this is a more common form of nitrogen in water, although this strongly depends on factors such as sources and mixing, and abiotic parameters such as pH and temperature. A large amount of NO2 enters the aquatic environment directly via effluents from wastewater treatment. Background NO2 concentrations in natural waters typically range between 0 and 3 mg l2 . However, due to anthropogenic sources, many waters exceed this concentration and concentrations above 100 mgl 2 have been recorded. Concentrations of NO2 as low as 3 mgl 21 can result in physical and behavioral abnormalities and egg mortality in amphibians in different life stages (e.g., eggs, tadpoles, and adults) and fish (e.g., rainbow trout).

Elevated NO- levels can also reduce the oxygen-carrying capacity of oxygen-carrying pigments (e.g., hemoglobin). High concentrations (>10 mg l - ) nearly always result in high mortalities even in the later life stages and subsequently a decline in amphibian and fish populations. An additional negative effect for amphibians is that adult fish are less susceptible to elevated NO3- concentrations. Increased NO3- concentrations will thus not only affect juvenile life stages directly through toxicity but also increase predation pressure on the tadpoles.

A more toxic component is the nitrite ion, NO-. NO- in water forms a chemical equilibrium with nitrous acid (HNO2): NO- 4 H4 $ HNO2. Both forms can be directly toxic to organisms, but the equilibrium strongly depends on pH and, in general, NO2- is a more common form than HNO2. As with NO-, NO- strongly affects the oxygen-carrying capacity of organisms. In addition, NO2- is known to cause electrochemical imbalances in the cells, membrane malfunctions, and repression of the immune system. In high concentrations (>0.25 mgl-1), NO- is toxic, and crustaceans (decapods, amphipods), insects (ephemeropterans), and fishes (salmonids) are among the most vulnerable groups. Since chloride (Cl-) ions are taken up by fish via the same mechanisms in their gills, Cl- uptake inhibits NO-uptake and protects the fish against NO- toxicity. Seawater therefore reduces the toxicity of NO- considerably.

NH3 mainly affects biota close to point sources such as agricultural and industrial effluents or sewage and waste-water treatment plants which lack nitrification steps. In these environments, plants are more tolerant ofNH3 than animals, and invertebrates are more tolerant than fish. Elevated NH3 results in lower hatching and growth rates of fish. Normally, fish excrete NH3 but with elevated concentrations in the water; excretion becomes difficult and high internal NH3 concentrations can cause poor development and damage to gill, liver, and kidney tissues, repression of the immune system, and a reduction in oxygen-carrying capacity. Increased NH44 concentrations in water occur mostly near agricultural point sources or in anoxic waters. Many freshwater plants (e.g., Potamogeton ssp., Ranunculus ssp.) and the salt water eelgrass (Zostra marina) all show poor growth rates, discoloration of the chloroplasts and a higher mortality at elevated NH4 concentrations.

Indirect Toxicity

Aquatic ecosystems in Europe and North America, like terrestrial ecosystems, have suffered from acidification in sensitive poorly buffered areas due to nitrogen, as well as sulfur, deposition. A change in pH in streams and lakes can cause significant changes in plant and animal species composition. In general, juvenile life stages are more sensitive to pH changes than adult life stages, and a decrease in pH below 5.0, for example, has resulted in complete disappearance of snails in Norwegian lakes.

Figure 3 Algae bloom in Scandinavian lake.

Mollusks (snails, clams), arthropods (crustaceans, crayfish), and amphibians are particularly vulnerable to a pH drop to below 5. Direct negative effects of low pH on fish reproductive rate and survival rates occur, but reduced availability of their food source (crayfish and insects) also has an indirect negative effect on populations of numerous fish species. Increased acidification of aquatic environments results, as for terrestrial ecosystems, in increased solubility of metal ions such as Al34 and trace metals (Cd, Cu, Pb, and Zn). This can cause direct metal toxicity to organisms both in the sediment and in the water. Increased Al34 concentrations can also reduce phosphate availability and disrupt P cycling.

An increase in nitrogen availability in water can stimulate or enhance the growth and proliferation of primary producers (phytoplankton, benthic algae, and macrophytes). In nitrogen-limited freshwaters and coastal regions, this enhanced growth of highly competitive species reduces light penetration to the sediment and consequently, slow-growing and sensitive species may decline and disappear. The eutrophication of aquatic environments can result in huge expansive growth of primary producers (Figure 3). Some algal blooms (e.g., Microcystis cyanobacteria in freshwaters and Alexandrium dinoflagellates in coastal waters) are known to release toxic products which attack the nervous system, liver tissues, and cytoskeletons of many aquatic organisms. In addition, the decomposition of this algal organic matter when it dies and sinks to the bottom uses oxygen; with greatly increased rates of decomposition, the oxygen content of the water body is depleted. Because of the vast scales of such algal blooms, anoxic conditions can develop - a situation which is known as hypoxia. Hypoxia is known to be responsible for the death of a vast majority of the fish in these waters. Well-known cases of these hypoxic conditions as a direct result of nitrate occur in the Gulf of Mexico and the Baltic Sea. An additional negative effect of the hypoxic conditions is the formation

Table 1a Direct effects of different forms of nitrogen to terrestrial and aquatic ecosystems including mechanisms and examples of effects

Toxicity

Major direct effects

Mechanisms

Examples of sensitive species and species groups

Terrestrial ecosystems

NH3 Growth suppression, increased mortality, chlorosis

Growth suppression, increased mortality, chlorosis

Not toxic

Aquatic ecosystems

NH3 Increased mortality, suppressed growth, poor egg development, damage to tissues

NHJ Increased mortality, suppressed growth

NO2, HNO2 Physical and behavioral abnormalities, poor development, increased mortality

NO3 Physical and behavioral abnormalities, increased mortality

Base cation depletion, reduction of photosynthetic capacity, cell charge imbalances Base cation depletion, reduction of photosynthetic capacity, cell charge imbalances

Charge imbalances in cells, direct toxicity due to accumulation

Base cation depletion, reduced photosynthesis capacity, carbon limitation

Reduces oxygen carrying capacity, electrochemical imbalances in cells, repression of the immune system

Reduces oxygen carrying capacity

Bryophytes, lichens

Antennaria dioca, Cirsium dissectum

Fish, invertebrates

Eelgrass, Stratioites aloides, Potamogeton species

Crustaceans, insects, fish (salmonids) effects are more pronounced in freshwater

Amphibians, tadpoles, rainbow trout

Table 1b Indirect effects of different forms of nitrogen to terrestrial and aquatic ecosystems including mechanisms and examples of effects

Major indirect effects

Mechanisms

Examples of sensitive species and species groups

Terrestrial ecosystems NH3

Total N

Aquatic ecosystems NH3

Species composition changes, increased competition between species, growth suppression, mortality Species composition changes, increased competition between species, growth suppression, mortality Species composition changes, increased competition between species, growth suppression, mortality Species composition changes, increased competition between species, increased susceptibility to herbivores and pathogens

Inhibition of nitrification

Growth suppression, higher mortality

Acidification of rhizosphere as a result of uptake by plants, depletion of base cation availability, decreased pH.

Acidification of rhizosphere as a result of uptake by plants and conversion via nitrification, depletion of base cation availability, decreased pH.

Acidification via acid rain, depletion of base cation availability, decreased pH.

Increase of nitrogen availability

Increases NHJ concentrations

Acidification via nitrification in the sediments

Decline of pine forests

Changes in under story vegetation in pine forests and heathlands

Al3+ toxicity in Arnica montana

Grass encroachment in Dutch heathlands

Nitrosomonas and Nitrobacter bacteria directly and all NH4 sensitive species indirectly Mollusks, arthropods, amphibians

(Continued )

Table 1b (Continued)

Major indirect effects

Mechanisms

Examples of sensitive species and species groups

Total N

Species composition changes, increased competition between species, growth suppression, mortality Species composition changes, increased competition between species

Acidification via acid rain, heavy metal toxicity

Increase of nitrogen availability, hypoxia

Mollusks, arthropods, amphibians

Fish and invertebrate mortality in anoxic conditions of reduced compounds such as hydrogen sulfide (H2S), which is responsible for acute lethal effects on fish and macrofauna, as it attacks the nervous system, and also causes root decay and plant mortality in wetlands.

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