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Nutrients and coastal waters: too much of a good thing?

Some years ago, I received an invitation from the US Fish and Wildlife Service to address a scientific meeting in New Orleans about the importance of maintaining freshwater flows into estuaries and coastal lagoons. My specific task was to point out that rivers and streams bring nutrients (nitrogen and phosphorus) into estuaries, and thus make them productive. The Fish and Wildlife Service was trying to convince the US Army Corps of Engineers, among others, not to build so many dams and freshwater diversion projects. I accepted their invitation.

Three days later, another invitation arrived. This one came from the organizers of a workshop sponsored by the National Science Foundation. They were interested in working with farmers and the agricultural chemicals industry to reduce nonpoint-source pollution in estuaries. The term "nonpoint source" is used loosely to mean pollution that doesn't enter from a sewage treatment plant or an industrial discharge pipe. Rainfall running off a field is an excellent example of a diffuse (or nonpoint) source of pollution. My task was to point out the serious problems that nutrients from fertilizers can cause if they get into estuaries and coastal waters. I accepted their invitation, too.

I still remember the week of the two invitations for several reasons. First, it was a surprising burst of popularity--I seldom receive two invitations of any kind in one week. Second, by agreeing to speak on both sides of the same issue, I felt embarrassingly like the typical academic scientist in the cartoons. We've all heard the joke about the corporate executive who only hired one-armed scientists so they couldn't say, "on the one hand...but on the other hand...." Third, the obvious conflict in the invitations made me realize that we have to think about the issue of nutrient inputs differently than we think about almost all other pollutants or contaminants. For example, it is hard to imagine anyone giving a talk on the importance of maintaining or increasing the discharge of petroleum hydrocarbons to estuaries. We many argue about how much copper is required to cause a measurable reduction in estuarine productivity or biodiversity, but there is virtually no question that we should discharge as little copper as economically and technologically possible. The questions surrounding nutrients are more difficult.

On the One Hand

For about 100 years we have recognized that the supply of inorganic nitrogen and phosphorus is an important factor regulating the productivity of the sea. Across a broad scale, it is now possible to see a rough quantitative relationship between the rate of nutrient supply and the annual primary production and average standing crop of phytoplankton. If a logarithmic scale is used to capture the large ranges observed, the data will fall along a straight line, but on a regular or arithmetic scale, the plot is hyperbolic. Productivity and chlorophyll first rise rapidly with increasing nitrogen input, then level off or rise much more slowly at higher rates of input. This is the familiar limiting-factor curve that illustrates the law of diminishing returns. We are accustomed to seeing similar plots for algal cultures grown with different rates of nutrient supply, or for yields of crops with different amounts of fertilizer applied. Of course, other factors in addition to nutrient supply influence productivity and chlorophyll, and it is difficult to estimate nutrient fluxes, primary production, or mean chlorophyll concentrations for large areas. For all of these reasons, it is not surprising that there is more scatter in this relationship than we see in controlled laboratory cultures or field plots. The substance of the relationship, however, confirms that higher nutrient inputs, at least up to a point, are associated with increasing productivity. Since it is also possible across a very broad scale to relate primary production to the yield of fish and shellfish from marine systems, we can link nutrient inputs in a quantitative way with increased secondary production.

On the Other Hand

If nutrients added to the sea do the same general things they do on land--increase the production and standing crop of plants and the yield of animals--why is there so much concern about nutrient inputs to estuaries, lagoons, and other coastal ecosystems? In its 1990 Report to Congress on the National Water Quality Inventory, the Environmental Protection Agency (EPA) ranked "nutrients" as the major cause of impaired estuaries in the US. The National Oceanic and Atmospheric Administration (NOAA) and the EPA jointly produced a national strategic assessment of the susceptibility of US estuaries to nutrient discharges, and they are now involved in a national assessment of the state of nutrient impact in our coastal waters. AMBIO, the journal of the Swedish Academy of Sciences, recently devoted a special issue to nutrient impacts in the Baltic Sea area. A 1990 report from the United Nations Environmental Programme on The State of the Marine Environment predicted that increased nutrient discharges from the growing human population will create a worldwide problem in the next 20 to 30 years if corrective measures are not taken, and the Danish Environmental Protection Agency is sponsoring an international scientific meeting on coastal marine nutrient enrichment in the fall of 1993.

Most of the concern over nutrient inputs arises because of a fundamental difference between the environments of terrestrial and marine plants. The land plants we fertilize so eagerly and at such great expense live and die in air containing about 210 grams of oxygen in each cubic meter. The atmosphere above the soil contains a vast, relatively well-mixed reservoir of oxygen to which the plants contribute when they are photosynthesizing during the day. At night, after photosynthesis has ceased, the plants continue to respire and take up oxygen from the atmosphere. So long as the plants are growing, they produce more oxygen during the day than they consume at night. After the plants die, the animals, fungi, and bacteria that metabolize and decompose the organic plant matter also draw oxygen from the large supply in the atmosphere. But because the air around the animals and decomposing plant material is always being mixed by the wind and other currents, the local oxygen supply remains high.

In contrast to the air, coastal seawater is completely saturated with oxygen when it contains only some 5 to 10 grams per cubic meter. When the water is warm, it holds the least oxygen. This is unfortunate, because plants, animals, and bacteria have higher oxygen consumption rates at warmer temperatures. Even more important, however, is the fact that water is less easily mixed than air. As a result, it is easier to deplete the smaller reservoir of oxygen in local areas. This problem is particularly acute when seawater becomes stratified. In this situation, there is little or no mixing between the surface water and the bottom. As oxygen is depleted in the bottom water, there is no way for it to be mixed up to the surface where it can take up more oxygen from the atmosphere through diffusion.

Stratification occurs in two ways. First, surface water traps most of the heat from the sun and becomes increasingly warmer and lighter than the deeper water. Second, fresh water is lighter than salt water and tends to float at the surface where it enters the sea. Salinity differences promote much stronger stratification than temperature differences. Of course, the sea is not still, and even though it is less turbulent than the air, there are waves and currents acting to mix the surface waters with those below. The degree of stratification in any area varies, depending on the balance between factors that increase the buoyancy of the surface and the energy that is available to mix waters of different densities.

While coastal areas are obviously particularly susceptible to stratification because they receive freshwater runoff from land, they are also the areas in which large amounts of tidal energy are often available for mixing. As a result, it is possible to find estuaries and other coastal systems with a great range of stratification. Most of Narragansett Bay is relatively well-mixed all year; the deeper areas of Chesapeake Bay are strongly stratified all summer; the Pamlico River estuary is intermittently stratified through much of the year. Many lagoons are connected to the sea only through narrow channels or passes between barrier spits and islands. The narrow passes allow only a small amount of tidal energy into these systems, so they must be mixed largely by the wind. If the lagoon is very shallow and well-oriented with respect to the prevailing winds, the waters may be well-mixed virtually all the time. If instead it has a large freshwater input, deep areas, or only a short fetch, the lagoon may be mixed only by less frequent higher energy winds.

The practical impact of these differences between air and water is that water exhibits a delicate balance between the oxygen consumed in the metabolism of organic matter and the rate at which physical mixing processes can renew the oxygen-depleted bottom water. If the mixing is too slow, oxygen levels in the deeper water will decline. When the oxygen falls below about three grams per cubic meter, the water is called "hypoxic," and fish, benthic animals, and other organisms that require oxygen to respire become increasingly stressed. When all of the oxygen is consumed, only specialized organisms that consume organic matter using sulfate, nitrate, and a few other oxidized compounds instead of free oxygen can survive. When sulfate, rather than oxygen, is being used in respiration, hydrogen sulfide is produced instead of carbon dioxide. Hydrogen sulfide causes the "rotten egg" smell often associated with badly polluted marine areas. Even among two-armed scientists, there is general agreement that this is not a desirable condition. Since increasing the nutrient input will increase the production of organic matter by marine plants, there is great concern that the consumption of this additional material will deplete the oxygen from the bottom waters of a larger and larger area of the coastal environment.

A Note on Hugging Green Plants

Some of my botanist friends have bumper stickers on their cars asking, "Have you hugged a green plant today?" We are supposed to engage in this unusual practice in order to show our appreciation for all the oxygen that plants put into the atmosphere, thus making it possible for us to breathe. This idea is carried forward in arguments for saving rain forests and protecting phytoplankton from such dangers as increased ultraviolet radiation, etc. Unfortunately, the popular notion that more plants mean more oxygen has made it hard for some people to understand why growing more plants with more nutrients may mean less oxygen in coastal waters.

The problem arises because the production of organic matter by plants during photosynthesis (which produces oxygen) and the consumption of organic matter by plants, animals, and microorganisms during respiration (which consumes oxygen) are separated in space and/or time. A simple example is that of a stratified bay, where net plant growth through photosynthesis takes place in the sunlit surface water. During the day, the phytoplankton produce more oxygen than they consume; oxygen concentrations in the surface water become supersaturated, and oxygen diffuses into the atmosphere. At the same time, dead organic matter, including phytoplankton, zooplankton fecal pellets, etc., sinks through the bottom waters and onto the sediments, where it is respired. There is little or no light, and no photosynthetic production of oxygen. Oxygen concentrations in the bottom water decline. During the night, phytoplankton and other organisms in the surface water continue to respire, and oxygen concentrations there begin to drop. As soon as the water is less than 100 percent saturated, however, oxygen begins to diffuse into the surface water from the atmosphere. In the bottom water, respiration continues and, because the water is stratified, the diffusion of oxygen from the surface water into the bottom is much slower than the consumption of oxygen in respiration. Oxygen concentrations continue to decline. It is not hard to see that this situation will soon lead to bottom waters and sediments that are first hypoxic (oxygen deficient), then anoxic (devoid of oxygen). As more plant material is produced in the surface, more oxygen may be added to the atmosphere, but more organic matter will also fall to the bottom, and bottom-water oxygen supplies will be exhausted more rapidly.

Even in unstratified waters it is possible to have a large bloom of plants resulting in a large net production of organic matter and oxygen, followed by a period of net consumption when oxygen concentrations fall significantly. During the bloom, oxygen becomes supersaturated and diffuses into the atmosphere. Organic matter may accumulate over many days of net growth and net oxygen loss to the atmosphere. At some point, conditions become unfavorable for the plants and many die during a short period of time. The large pulse of dead organic matter is quickly respired by animals and bacteria, and oxygen cannot diffuse into the water from the atmosphere fast enough to balance respiration. Unless there is lateral mixing with oxygen-rich water from outside the bloom area, conditions may become hypoxic or even anoxic.

The same separation of production and consumption occurs on land, but the well-mixed reservoir of oxygen in the atmosphere is so large that we do not notice the cycle. However, there used to be a quaint and quite unnecessary Victorian ritual of removing the house plants from sickrooms at night, lest they compete with the invalid for air. On a longer time scale, most of the oxygen produced by land plants during their growing season is later consumed. Net oxygen production only occurs where and when there is a long-term net accumulation of organic matter as in peat bogs, forest floor litter, or accumulation of detritus in river or stream beds.

Nutrients and Eutrophication

So far I have only focused on the potential for increased nutrient inputs to result in oxygen depletion. This consequence of nutrient enrichment is the best understood, and the consequences of hypoxia and anoxia are straightforward--reduced diversity, fish kills, mass mortality of benthic animals, bad odors, bacterial slimes, etc. There are, however, a variety of other changes that may take place in coastal ecosystems if they are exposed to increasing nutrient enrichment. I have to say may take place because the evidence documenting these changes is less compelling or complete than that for oxygen depletion.

In a recent series of workshops sponsored by EPA and NOAA, experts from around the country identified what they felt were characteristic features of coastal environments that had been over-enriched with nutrients. Their list included such things as: * reduced diversity, * a shift from large to small phytoplankton, * a shift in the species composition of the phytoplankton from diatoms

to flagellates, * increased incidence of toxic phytoplankton blooms * increased incidence of undesirable phytoplankton blooms, * increased seaweed biomass, * loss of seagrasses, * a shift from filter-feeding to deposit-feeding benthos, * a shift from larger, long-lived benthos to smaller, rapidly growing but

shorter-lived species, * increased disease in fish, crabs, and/or lobsters, and * increased production of some greenhouse gases.

From this exercise it became obvious that the potential exists for a very complex series of changes to occur in coastal ecosystems exposed to nutrient enrichment. Some of these changes, such as the loss of seagrasses, are much better documented than others, such as the link between nutrients and fish disease.

All of the conditions listed above, plus increases in plant biomass and production, and the reduced oxygen concentrations described earlier, are often cited as symptoms of coastal marine eutrophication. This is a somewhat fuzzy term borrowed from our colleagues who work on lakes. They, in turn, borrowed it even earlier from medicine, where eutrophy meant healthy or adequate nutrition or development.

The traditional view in limnology was that lakes became more eutrophic over time as they accumulated nutrient inputs from the watershed. As a lake aged, it accumulated organic matter and sediment, and eventually became a wetland, then dry land. The concept of eutrophication as a part of landscape evolution was later modified to include "cultural eutrophication," the rapid aging of lakes due to human nutrient discharges. By comparing the productivity and chlorophyll levels of lakes receiving different rates of nutrient input, it was possible for limnologists to develop rather specific operational definitions for lakes that were considered oligotrophic (slightly productive), mesotrophic (moderately productive), eutrophic (highly productive), and hypertrophic or dystrophic (so productive that normal lake trophic structure and biogeochemical cycles were severely disturbed).

Until about the last 25 years, there was little concern about eutrophication in coastal marine systems. It was generally believed that rapid flushing rates of estuaries (compared to most lakes), as well as the greater mixing energy (from the tides) would prevent them from responding to nutrient enrichment in the same way that lakes did. That view has clearly changed as more estuarine research has been carried out and as nutrient inputs to many estuaries and lagoons around the world have continued to increase dramatically. As yet, however, we do not have general agreement about reliable quantitative definitions for different degrees of eutrophication in coastal marine ecosystems.

Increasing Inputs

Prior to European settlement, the watershed of Narragansett Bay (the estuary I know best) was about 95 percent forested, and the human population was very small. We know from modern studies that intact, mature forests hold tightly to the nitrogen and phosphorus they contain. Before the industrial revolution, the concentrations of nutrients in rain must also have been very low. Under these conditions, I have estimated that the combined nutrient inputs from land and atmosphere to Narragansett Bay were about equal to those entering the surface waters of the Sargasso Sea, a well-known area of very low productivity in the open ocean. The impressive fisheries of New England's estuaries that were described by William Wood and other early visitors must have been sustained by the nutrients in coastal ocean waters that were continually brought inshore by the tides and estuarine circulation. My best estimate is that this source was five to ten times larger than inputs from land and atmosphere, at least up to about 1800. Today, the situation is quite different, and about five times more inorganic nitrogen enters Narragansett Bay from the land and atmosphere than from the coastal ocean. How and when did this come about?

Human activities have increased nutrient flows to the coast in many ways, including forest clearing, the destruction of riverine swamps and wetlands, the application of large amounts of synthetic fertilizers, the use of large amounts of nitrogen and phosphorus in various industrial processes, the addition of phosphorus to detergents, the production of large populations of livestock, the high-temperature combustion of fossil fuels that has added large amounts of nitrogen to acid rain, and the expansion of human population in coastal areas. The relative importance of these activities obviously varies from place to place, but in older urban, industrial areas like Narragansett Bay, one particular event had a dramatic impact on the fertilization of the estuary.

On Thanksgiving Day 1871, running water was introduced in the city of Providence, Rhode Island, to the accompaniment of a 13-gun salute and the ringing of church bells. Once running water became available, indoor plumbing and flush toilets soon followed. This technology almost immediately required the construction of sewer systems to collect wastewaters and carry them out of the city for discharge into various rivers and the bay.

Public water and sewer systems proliferated rapidly throughout the urban areas of the northeast between about 1870 and 1910. Before this, the disposal of human waste, the major source of nitrogen and phosphorus in the watershed, had involved a relatively dry technology--cesspools and privy vaults. With the introduction of the water-carriage system of waste disposal, however, the intensive fertilization of urban estuaries began. Early sewage-treatment plants reduced the nutrient flow somewhat between about 1900 and the 1920s or 1930s, but many cities failed to maintain the plants or to expand them as population grew. As a result, they became increasingly ineffective. The economic stresses of the Depression and World War 11 continued the decline.

I have tried to estimate the historical input of nutrients to Narragansett Bay using a complex mix of data on human population, street paving, horse populations, water and sewer systems, calculated atmospheric nutrient deposition, changing land use, analyses of textile-industry nutrient emissions, old chemical analyses of rivers, etc. The surprising result suggests that inputs of nitrogen and phosphorus increased dramatically over just a 30-year period between about 1880 and 1910. The increase since that time has been modest. Unfortunately, there are no data to tell us what the bay was like before nutrient inputs increased so sharply.

The history of other estuaries may be very different, of course, and many of those along the southeastern and Gulf coasts of the US have experienced rapid population growth only in recent decades. Because shallow coastal lagoons everywhere were less desirable as ports, they were often spared from the urban and industrial development found in larger river-mouth estuaries. Nutrient inputs to those systems have been driven largely by agriculture and, in recent years, by suburban and vacation housing. In rural areas, houses are served by individual on-site sewage disposal systems consisting of septic tanks and leach fields. Unlike the old privies, these systems process large amounts of water as well as human waste, and they contaminate the groundwater with nitrate that eventually reaches coastal ecosystems.

It is almost certain that the world's coastal waters will continue to receive ever-increasing amounts of nitrogen and phosphorus from the growing human population. Because both of these elements are essential in human nutrition, we cannot help releasing them to the environment. The large amount of protein we consume makes us particularly important as emitters of nitrogen. While it has proven practical to remove many metals and organic pollutants from wastewater, only a very few sewage-treatment plants have been able to sustain an effective nitrogen-removal program. Phosphorus removal is more economical, but nitrogen is the nutrient having the greatest impact on the productivity of most of the world's coastal marine waters. The situation is different in lakes, where phosphorus control is an effective strategy to prevent eutrophication.

Many estuaries and bays are already among the most intensively fertilized environments on earth, and we are still far from fully understanding the long-term consequences of further enrichment.

Scott W. Nixon is a Professor of Oceanography at the University of Rhode Island and Director of the Rhode Island Sea Grant College Program. Both titles make him uncomfortable, since he is in no position to profess anything about oceanography and his colleagues would laugh if he claimed to direct the diverse Sea Grant research and outreach program. He received his Ph.D. in Botany (another uncomfortable title) from the University of North Carolina at Chapel Hill in 1970 and has spent the past 23 years studying the nutrient dynamics and productivity of estuaries, bays, and shallow lagoons in Rhode Island and other interesting places.
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Author:Nixon, Scott W.
Date:Jun 22, 1993
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