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