Review article
Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: A global assessment

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Abstract

We provide a global assessment, with detailed multi-scale data, of the ecological and toxicological effects generated by inorganic nitrogen pollution in aquatic ecosystems. Our synthesis of the published scientific literature shows three major environmental problems: (1) it can increase the concentration of hydrogen ions in freshwater ecosystems without much acid-neutralizing capacity, resulting in acidification of those systems; (2) it can stimulate or enhance the development, maintenance and proliferation of primary producers, resulting in eutrophication of aquatic ecosystems; (3) it can reach toxic levels that impair the ability of aquatic animals to survive, grow and reproduce. Inorganic nitrogen pollution of ground and surface waters can also induce adverse effects on human health and economy.

Because reductions in SO2 emissions have reduced the atmospheric deposition of H2SO4 across large portions of North America and Europe, while emissions of NOx have gone unchecked, HNO3 is now playing an increasing role in the acidification of freshwater ecosystems. This acidification process has caused several adverse effects on primary and secondary producers, with significant biotic impoverishments, particularly concerning invertebrates and fishes, in many atmospherically acidified lakes and streams. The cultural eutrophication of freshwater, estuarine, and coastal marine ecosystems can cause ecological and toxicological effects that are either directly or indirectly related to the proliferation of primary producers. Extensive kills of both invertebrates and fishes are probably the most dramatic manifestation of hypoxia (or anoxia) in eutrophic and hypereutrophic aquatic ecosystems with low water turnover rates. The decline in dissolved oxygen concentrations can also promote the formation of reduced compounds, such as hydrogen sulphide, resulting in higher adverse (toxic) effects on aquatic animals. Additionally, the occurrence of toxic algae can significantly contribute to the extensive kills of aquatic animals. Cyanobacteria, dinoflagellates and diatoms appear to be major responsible that may be stimulated by inorganic nitrogen pollution. Among the different inorganic nitrogenous compounds (NH4+, NH3, NO2, HNO2, NO3) that aquatic animals can take up directly from the ambient water, unionized ammonia is the most toxic, while ammonium and nitrate ions are the least toxic. In general, seawater animals seem to be more tolerant to the toxicity of inorganic nitrogenous compounds than freshwater animals, probably because of the ameliorating effect of water salinity (sodium, chloride, calcium and other ions) on the tolerance of aquatic animals.

Ingested nitrites and nitrates from polluted drinking waters can induce methemoglobinemia in humans, particularly in young infants, by blocking the oxygen-carrying capacity of hemoglobin. Ingested nitrites and nitrates also have a potential role in developing cancers of the digestive tract through their contribution to the formation of nitrosamines. In addition, some scientific evidences suggest that ingested nitrites and nitrates might result in mutagenicity, teratogenicity and birth defects, contribute to the risks of non-Hodgkin's lymphoma 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, causing nausea, vomiting, diarrhoea, pneumonia, gastroenteritis, hepatoenteritis, muscular cramps, and several poisoning syndromes (paralytic shellfish poisoning, neurotoxic shellfish poisoning, amnesic shellfish poisoning). Other indirect health hazards can also come from the potential relationship between inorganic nitrogen pollution and human infectious diseases (malaria, cholera). Human sickness and death, extensive kills of aquatic animals, and other negative effects, can have elevated costs on human economy, with the recreation and tourism industry suffering the most important economic impacts, at least locally.

It is concluded that levels of total nitrogen lower than 0.5–1.0 mg TN/L could prevent aquatic ecosystems (excluding those ecosystems with naturally high N levels) from developing acidification and eutrophication, at least by inorganic nitrogen pollution. Those relatively low TN levels could also protect aquatic animals against the toxicity of inorganic nitrogenous compounds since, in the absence of eutrophication, surface waters usually present relatively high concentrations of dissolved oxygen, most inorganic reactive nitrogen being in the form of nitrate. Additionally, human health and economy would be safer from the adverse effects of inorganic nitrogen pollution.

Introduction

Nitrogen is the most abundant chemical element of the Earth's atmosphere (almost 80%), and also one of the essential components of many key biomolecules (e.g., amino acids, nucleotides). It ranks fourth behind carbon, oxygen and hydrogen as the commonest chemical element in living tissues (Campbell, 1990). An increase in the environmental availability of inorganic nitrogen usually boosts life production, firstly increasing the abundance of primary producers. However, high levels of inorganic nitrogen that cannot be assimilated by the functioning of ecological systems (i.e., N saturated ecosystems) can cause adverse effects on the least tolerant organisms.

Ammonium (NH4+), nitrite (NO2) and nitrate (NO3) are the most common ionic (reactive) forms of dissolved inorganic nitrogen in aquatic ecosystems (Kinne, 1984, Howarth, 1988, Day et al., 1989, Wetzel, 2001, Rabalais, 2002). These ions 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 (Kinne, 1984, Howarth, 1988, Day et al., 1989, Wetzel, 2001, Rabalais, 2002). Ammonium tends to be oxidized to nitrate in a two-step process (NH4+  NO2  NO3) by aerobic chemoautotrophic bacteria (Nitrosomonas and Nitrobacter, primarily) (Sharma and Ahlert, 1977, Wetzel, 2001). The nitrification process can even occur if levels of dissolved oxygen decline to a value as low as 1.0 mg O2/L (Stumm and Morgan, 1996, Wetzel, 2001). NH4+, NO2 and NO3 may however be removed from water by macrophytes, algae and bacteria which assimilate them as sources of nitrogen (Howarth, 1988, Harper, 1992, Paerl, 1997, Wetzel, 2001, Dodds et al., 2002, Smith, 2003). Furthermore, in anaerobic waters and anoxic sediments, facultative anaerobic bacteria (e.g., Achromobacter, Bacillus, Micrococcus, Pseudomonas) can utilize nitrite and nitrate as terminal acceptors of electrons, resulting in the ultimate formation of N2O and N2 (Austin, 1988, Stumm and Morgan, 1996, Wetzel, 2001, Paerl et al., 2002).

During the past two centuries, and especially over the last five decades, humans have substantially altered the global nitrogen cycle (as well as the global cycles of other chemical elements), increasing both the availability and the mobility of nitrogen over large regions of Earth (Vitousek et al., 1997, Carpenter et al., 1998, Howarth et al., 2000, Galloway and Cowling, 2002). 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 (Howarth et al., 2000, National Research Council, 2000). Moreover, anthropogenic inputs of particulate nitrogen and organic nitrogen to the environment can also result in inorganic nitrogen pollution (National Research Council, 2000, Smil, 2001). Concentrations of inorganic nitrogenous compounds (NH4+, NO2, NO3) in ground and surface waters are hence increasing around the world, causing significant effects on many aquatic organisms and, ultimately, contributing to the degradation of freshwater, estuarine, and coastal marine ecosystems (Neilson and Cronin, 1981, Russo, 1985, Meybeck et al., 1989, Camargo, 1992, Gleick, 1993, Nixon, 1995, Paerl, 1997, Smith et al., 1999, Howarth et al., 2000, National Research Council, 2000, Smil, 2001, Anderson et al., 2002, Philips et al., 2002, Rabalais and Nixon, 2002, Constable et al., 2003, Jensen, 2003, Smith, 2003, Camargo et al., 2005a).

Nevertheless, in spite of the current worldwide environmental concern, no study has provided a global assessment, with detailed multi-scale data, of the ecological and toxicological effects generated by inorganic nitrogen pollution in aquatic ecosystems. We have performed such a study, and our synthesis of the published scientific literature shows three major environmental problems: (1) inorganic nitrogen pollution can increase the concentration of hydrogen ions in freshwater ecosystems without much acid-neutralizing capacity, resulting in acidification of those ecological systems; (2) inorganic nitrogen pollution can stimulate or enhance the development, maintenance and proliferation of primary producers, resulting in eutrophication of freshwater, estuarine, and coastal marine ecosystems. In some cases, inorganic nitrogen pollution can also induce the occurrence of toxic algae; (3) inorganic nitrogen pollution can impair the ability of aquatic animals to survive, grow and reproduce as a result of direct toxicity of inorganic nitrogenous compounds. In addition, inorganic nitrogen pollution of ground and surface waters can induce adverse effects on human health and economy.

Section snippets

Acidification of freshwater ecosystems

Sulphur dioxide (SO2), nitrogen dioxide (NO2) and nitrogen oxide (NO) have been traditionally recognized as the major acidifying pollutants in lakes and streams (Schindler, 1988, Irwin, 1989, Mason, 1989, Baker et al., 1991). Once emitted into the atmosphere, these gaseous pollutants can undergo complex chemical reactions (see, for example, Mason, 1989), resulting in the formation of sulfuric acid (H2SO4) and nitric acid (HNO3). The subsequent atmospheric (wet and dry) deposition of these acid

Eutrophication of aquatic ecosystems

Limitation of inorganic nitrogen characterizes large portions of the world´s coastal and estuarine environments, net primary production being mainly controlled by N inputs (Neilson and Cronin, 1981, Kinne, 1984, Howarth, 1988, Day et al., 1989, Nixon, 1995, Paerl, 1997, Howarth et al., 2000, Rabalais and Nixon, 2002). However, in estuaries and coastal marine ecosystems that are receiving high N inputs, phosphorus can become relatively more limiting as the N:P loading ratio tends to increase (

Occurrence of toxic algae

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 (Chorus, 2001, Landsberg, 2002). In consequence, animals may be directly exposed to toxins by absorbing toxins from water, drinking water with toxins, or ingesting algal cells

Toxicity of inorganic nitrogenous compounds

Aquatic animals are, in general, better adapted to relatively low levels of inorganic nitrogen since natural (unpolluted) ecosystems often are not N saturated and natural concentrations of inorganic nitrogenous compounds usually are not elevated (Wetzel, 2001, Constable et al., 2003, Jensen, 2003, Camargo et al., 2005a). Therefore, high levels of ammonia, nitrite and nitrate, derived from human activities, can impair the ability of aquatic animals to survive, grow and reproduce, resulting in

Adverse effects on human health and economy

There is no doubt that the increased use of inorganic fertilizers and fossil fuels around the world has brought enormous health and economic benefits to humans, dramatically increasing food production and human population. Nevertheless, because human society is greatly dependent on surface and ground water resources, as well as on fish and shellfish harvesting, it should be evident that the excessive nitrogen pollution of aquatic ecosystems can cause adverse effects on human health and economy.

Concluding remarks

This global assessment, with detailed multi-scale data, has clearly shown that inorganic nitrogen pollution of aquatic ecosystems may result in three major environmental problems: water acidification, cultural eutrophication (including occurrence of toxic algae), and direct toxicity of inorganic nitrogenous compounds (ammonia, nitrite and nitrate). Water acidification adversely affects freshwater ecosystems without much acid-neutralizing capacity (Table 2). Cultural eutrophication and toxicity

Acknowledgements

Funds for this research came from the Ministry of Science and Technology (research project REN2001-1008/HID) in Spain. The University of Alcala provided logistical support. Álvaro Alonso was supported by a predoctoral grant from the Council of Castilla-La Mancha. This work was presented at the 6th Iberian and 3rd Iberoamerican Congress on Environmental Contamination and Toxicology, held in Cadiz (Spain) from 25 to 28 September of 2005. We are grateful to Cristina Gonzalo-Gómez for her help

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