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4 Indicators for National Ecological Assessments ' n the preceding chapters, we have discussed the desirable characteris- tics of indicators, the sources of data that underlie them, the models ~ that support them, and the criteria by which good indicators can be identified. Based on those discussions and the conceptual model we used, the committee recommends national indicators for three major categories of ecological information. These categories encompass the nation's most important ecological issues. By computing them and paying attention to them, the nation should be aware of the status of its ecosystems, be alerted to changes that may require management interventions and policy changes, and have a basis for ensuring that future generations will have access to ecosystem goods and service as rich as those enjoyed today. In some cases, noted for each indicator, some experience will need to be gained on details of the indicator's behavior, but all the indicators are based on soundly established scientific experience and principles. The proposed indicators are in general applicable to both managed (e.g., agri- cultural) and unmanaged ecosystems; the indicators of nutrient-use effi- ciency and overall nutrient balance are specific to agricultural ecosystems. Information about the extent and status of the land use and cover types that together make up the nation's ecosystems. Information about the extent of the nation's land use and cover types informs us about the extent of ecosystem types in the nation, and it is needed to calculate several other indicators. The information and technology to calculate land cover is currently available. Land use in some ways is more informa- 64

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 65 live because it provides additional information on the status of areas and hence their ability to provide goods and services. Also, information on how land is used is predictive of future land cover and hence predicts the ability to provide goods and services. However, a land use indicator requires much synthesis of existing information and some new informa- tion, and thus will take longer to develop than a land cover indicator. Meanwhile, land cover can serve as a valuable indicator. Information about the nation's ecological capital. This informa- tion measures the nation's natural capital, or raw materials, both abiotic and biotic. Abiotic raw materials essential for ecosystem functioning include soil (also partly biotic) and its nutrients. Biotic raw material includes the number of species still present in the country relative to their number at the time of European contact, their distribution over today's natural and human-modified environments, and the number of species present today that are exotics, those species introduced, deliberately or inadvertently, that have become established or naturalized. Indicators of biological capital are important for several reasons. Knowing what portion of our biological capital is native provides a sensi- tive measure of humans' environmental impacts, as described below. Assessing the status of the nation's biological capital is important for ethical and aesthetic reasons. Also, biological diversity is an indicator of the capacity of ecosystems to function effectively. An important but controversial theory holds that because species differ, species-rich eco- systems are more likely than species-poor ecosystems to contain some species that can thrive during an environmental perturbation (Mooney et al. 1996~. As a result, species-rich systems should be buffered against disturbances and continue to perform better in fluctuating environments than species-poor systems. Empirical studies are still few, but they pro- vide some support for the hypothesis (Tilman 1996, Tilman and Downing 1994, Naeem et al. 1994~. Further investigations will clarify relationships between biological diversity and ecosystem processes. Meanwhile, it is prudent to monitor the status of the nation's biological resources. Information about the functioning (performance) of the nation's ecosystems and how it is changing. This information includes measures of productivity and other ecosystem processes. Changes in the produc- tivity of ecosystems are generally accompanied by changes in their ability to provide goods and services. Usually, declines in productivity are undesirable, but in freshwater ecosystems, increases in productivity asso- ciated with eutrophication can be undesirable. For each of these major categories of information we recommend indicators (Table 4.1) that are described in detail below. Although the categories apply to all ecosystems, they differ in many details for marine,

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66 ECOLOGICAL INDICATORS FOR THE NATION TABLE 4.1 National Indicators of Ecological Condition Category of Recommended Reasons for EcologicalInformation Indicators Choosing Indicator Extent and Status of the Nation's Ecosystems Ecological Capital Biotic Raw Materials Land Cover and Land Use* Total Species Diversity Native Species Diversity Needed for calculation of most other indicators. Inform us about the overall extent of different ecosystem types. Measures nation's biological resources (what is present relative to what is expected). Measures the amount of biological diversity that is native. Ecological Capital Nutrient Runoff Estimator of total losses of Abiotic Raw Materials nutrients. Nutrient runoff has major effects on receiving waters. Soil Organic Matter* Best single indicator of soil condition, related to erosion. Ecological Functioning (Performance) Productivity, including Carbon Storage, Net Primary Production (NPP), and Production Capacity Lake Trophic Status Stream Oxygen Soil Organic Matter* Nutrient-Use Efficiency and Nutrient Balance Land Use* Direct measures of the amount of carbon sequestered or retained in an ecosystem (NEP), energy and carbon brought into an ecosystem (NPP), and energy- capturing capacity of ecosystems (chlorophyll). Direct measure of ability of lakes to provide goods and services. Captures the balance between instream primary production and respiration. Single most important indicator of soil quality and productivity. Inefficient use of nutrients is costly in terms of economics and damage to ecosystems to which nutrients are discharged. Provides information about ecosystem functioning. *Indicators in more than one category.

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 67 freshwater, and terrestrial ecosystems. Because marine ecosystems were not specifically covered by the committee's charge, we focus on terrestrial and freshwater ecosystems and the interface between them-wetlands. More research is needed for the full implementation of these indicators. We offer some suggestions for the order in which some components might best be initiated. Although the national-level indicators we propose are highly aggre- gated, most of them require detailed input data. If these data are archived in a disaggregated form, the indicators can be computed in a variety of ways to provide a rich array of indicators of great local and regional value. Chapter 5 describes how that can be done and describes additional regional and local indicators. THE EXTENT AND STATUS OF THE NATION'S ECOSYSTEMS To estimate the capacity of U.S. ecosystems to continue to provide the goods and services that society depends on, one needs to know the status of the different types of natural and human-modified ecosystems and how much of each major type of ecosystem remains in the country. Infor- mation is also needed on what the committee calls the matrix that the ecosystems are in, i.e., the physical aspects of the land. Thus the indica- tors in this category include land cover and land use; nutrient runoff to coastal waters (a measure of loss of an element of the matrix); and soil quality as measured by soil organic matter. Land Cover and Land Use Land cover refers to the ecological status and physical structure of the vegetation on the land surface (e.g., forests, grasslands, wetlands, crop- lands) (Meyer and Turner 1994~. However, land cover depends in part on land use, the way the land is used by people (e.g., a forest managed for timber, a forest used to conserve biological diversity, industrial areas, areas of human settlements) (Meyer and Turner 1994~. Because changes in land use often (but not always) affect land cover, land use is itself an indicator of land cover. In general, land cover can be detected and moni- tored from remotely sensed imagery, but detection and classification of land use usually requires on-the-ground measurements. Often, especially in industrialized countries, information about land use can be obtained from maps and other data sources at local and regional scales, but such compilation is more labor-intensive and expensive than getting informa- tion on land cover. Data on current land cover and trends in those values are essential for the derivation and use of most indicators the committee recommends.

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68 ECOLOGICAL INDICATORS FOR THE NATION Therefore, we present the land cover indicator first and recommend that top priority be given to developing this indicator as rapidly as possible. A reliable land use indicator, although more difficult to develop, is also of great importance. The mathematical tools needed to assess land cover patterns and how they change are detailed in Appendix B. To assess this component of human impacts on the land, the commit- tee recommends a land cover indicator to track the amount of land in each of an array of land cover types, such as croplands, forestlands, wetlands, and nature reserves. A large fraction of the Earth's land surface is devoted to agriculture, and so agroecosystems ecological systems that are intensively managed for the production of food or fiber are essential components of any land cover and land use indicators. Agricultural systems are managed for high production, and typically are characterized by intensive nutrient and pesticide inputs, fast growth/harvest cycles, and low plant and animal diversity (Odum 1984, Matson et al. 1997~. Negative effects that may accompany these patterns include increases in soil erosion, groundwater contamination, eutrophication of lakes and rivers, and increased resis- tance of pest and plant pathogens to the chemicals used to kill them (Matson et al. 1997~. Nevertheless, intensively managed agroecosystems usually contain parcels of unmanaged or lightly managed areas, such as woodlots, fencerows, or riparian areas that can act both as refuges for beneficial predators of insect pests (Letourneau 1997) and as reserves for insect pests, weed seeds, plant pathogens, and alternate hosts of fungal pathogens of crops, such as cedar apple rust or crown rust of oats (Schumann 1991~. Because high-value farmland is being lost to commercial, industrial, and residential land uses (USDA 1997), the amount of agroecosystems is a component of the land cover indicator. Both land cover and land use indicators are extremely important. Although this section focuses on land cover, because data are more readily available at present, much of it is relevant to land use, which should also soon become a usable indicator. The land cover indicator can be applied to all environments, includ- ing those in which the "land" is submerged. Therefore, the land cover indicator recommended by the committee, includes rivers, wetlands, and riparian zones as well as dry land. The land cover indicator records the percentage of land in each of a variety of land cover categories. Every time land cover is computed, the proportional representations should be compared with those that existed at the previous recording time. To provide a useful indication of the status of the nation's lands, many cat- egories of land cover types must be recognized and the input data entered and stored separately for each one. Because the proportion of land in

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 69 each land cover category changes relatively slowly, land cover needs to be reported only once every five years, but its values need to be computed annually as inputs to other indicators. Supporting Models and Data Requirements. The conceptual model for land cover is simple. Land cover measures the proportion of the land- scape (and waterscape) occupied by each member of a set of land cover types that must, by definition, add up to the total area of the nation. The major decisions concern the number of land cover categories to recognize, how to account for their spatial configurations, and how to accommodate changes in the number and kinds of categories that are recognized. Change in the Proportional representation of various land cover cate~o- ries is the variable of interest. Visually representing proportional changes for a large number of land cover categories is difficult, but pie or star diagrams may serve that purpose. More sophisticated analyses of changes in land cover categories are also possible through the use of Markovian models (Appendix B). Those models assemble the transition probabilities between categories into matrices. From the matrices the steady-state distribution of categories and the rate of approach to the steady state can be calculated. As a result, one can obtain an indication of what the landscape will eventually look like under selected policies, and how long it will take to reach that state. Data Needs. Current capabilities of satellite imagery are sufficient for identifying a large number of categories of land cover. Very complex classification schemes are possible by combining imagery from several sensors with scenes from different seasons. As pointed out in Chapter 2, such techniques depend either on the Advanced Very High Resolution Radiometer (AVHRR), because of its more frequent sampling, or on a combination of the coarse spatial resolution of AVHRR and the finer reso- lution of Landsat Thermatic Mapper (TM). The forthcoming map by the U.S. Geological Survey (USGS) with a 100 meter resolution, based on Landsat TM data, also may serve as the basis for establishing categories. The condition of the nation's flowing waters is clearly an important element of the land cover indicator. An aggregated measure of flow patterns of the nation's rivers would be useful, but the complexities of river-flow dynamics make such a measure computable and understand- able only at the level of river basins. For the land cover indicator, a simpler measure percent free-flowing (as explained below) captures enough of the pattern to serve as a useful surrogate. Dams, regardless of their purposes, change discharge patterns, in- hibit movement of fishes, and impound sediments and their contained organic carbon, nutrients, and contaminants (Poff et al. 1997~. Water is

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70 ECOLOGICAL INDICATORS FOR THE NATION retained in reservoirs to alter the pattern of peak flows and rates of flow during storms. The timing of water release determines the timing and magnitude of seasonal runoff maxima, which often differ from those in free-flowing streams in the region. Therefore, for this reason it will be desirable for the land cover indicator to include a measure of percent free- flowing, or the length of free-flowing parts of streams and rivers divided by their total length. The percentage can be computed for each river basin and then aggregated into a single nationwide value. Percent free-flowing can change in response to policy and manage- ment decisions. Benke (1990) estimated that of the 5,200,000 km of streams in the contiguous 48 states, only 42 streams flowed unimpeded for more than 200 km. This is much less than 1 percent of the length of the nation's rivers. Of these 42 rivers, only six, all of which are in the southeastern United States, flow to the sea. Damming of rivers may continue, at least for hydropower generation, with the greatest number of undeveloped sites in the Pacific, mountain, and northeastern states. On the other hand, sentiment is increasing for removing some dams. Data on the length of large rivers impounded behind dams can be obtained using satellite mea- surements, but information on dams on small rivers can be gathered only by field surveys. However, because the number of dams built or destroyed over a short period is a very small percentage of all dams, the percentage free-flowing would change extremely slowly. Updating the data base would be relatively simple once it had been compiled. As mentioned previously, the U.S. Department of Agriculture's National Resources Inventory (NRI) provides a comprehensive assess- ment of the state and performance of natural and agricultural ecosystems on 800,000 sites on private lands every five years. The NRI is a compre- hensive sampling of land cover, land use, soil erosion, prime farmland, wetlands, and other characteristics on nonfederal lands in the United States. These data show that although soil erosion and agricultural wet- lands loss have decreased, 6 million acres of prime farmland were con- verted to nonagricultural uses between 1982 and 1992. NRI data can form part of a system to confirm ground truth of land use categories identified by satellite imagery. The U.S. Geological Survey (USGS), through its Biological Resources Division, and in collaboration with other federal agencies, is creating a vegetation map for the United States at 1:100,000 scale from Landsat TM data. The USGS is also more than halfway through a major effort to map existing land cover for the United States, at approximately 100 m resolu- tion, also using Landsat TM data. Several national- and continental-scale data sets acquired by federal agencies over the past few years to pro- mote land cover studies for the United States, the humid tropics, and North American boreal forests are now available to the scientific com-

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 71 munity for analysis. At a global scale, the first complete 1 km resolution global land-cover product was released by the International Geosphere Biosphere Program (IGBP) in Summer 1997. A land use indicator will need to distinguish among forms of a gen- eral category of land use depending on the criteria by which they are managed. For example, forest lands should be segregated into categories such as primary forest, unmanaged second-growth forest, forest man- aged primarily for timber production (referred to here as timberland), recently burned forest, forest managed for biodiversity preservation (e.g., forests in Safe Harbor agreements), and forest reserves, as well as into categories such as deciduous forest, boreal forest, and Pacific coast rain- forest. Such categories can be aggregated into fewer categories as needed, but to identify forests in which the human impact is being reduced, is not changing, or is increasing, the disaggregated input data will be needed. As an example, we discuss wetlands in some detail. Categories of aquatic habitats include wetlands, fresh and saline lakes, reservoirs, rivers, and bays. Most difficult to identify and monitor are wetlands water- logged landscapes that are inhabited by distinctive biotas (NRC 1995b). Wetlands cover 26 percent more area in the coterminous United States than all other categories of aquatic habitat combined (Frayer 1991~. Their biotic communities respond chiefly to the influence of hydrology, driven by topography and climate, but also to nutrient supply related to geology and soils. In many locations, because of anaerobic conditions, wetlands accumulate substantial deposits of organic detritus. Wetlands are called peatlands when accumulations of partly decomposed organic matter reach a depth of 30 cm. Many diverse oxidation/reduction reactions mediate elemental fluxes between the atmosphere and wetlands (Mitsch and Gosselink 1993~. Wetlands are of major significance for the cycles of carbon, nitrogen, and sulfur, and peatlands are a reservoir of at least 400 billion tons of carbon worldwide (Woodwell et al.1995~. Significant losses of carbon from that reservoir are projected if the global climate warms (Gorham 1991, 1995a). Therefore, monitoring the extent and status of various categories of wetlands is extremely important. Many physical, chemical, and biological criteria have been used to categorize and monitor wetlands (Adamus and Brandt 1990, NRC 1995b), and a land use indicator will need to recognize a substantial number of wetland types. As in the case of terrestrial land use types, specific catego- ries of wetlands should be separated according to the criteria by which they are managed. A particularly important category is wetlands created as part of mitigation settlements under Section 404 of the Clean Water Act (Kusler and Kentula 1989), because created wetlands seldom fully replace naturally functioning wetlands (Erwin 1991, Gorham 1995b, NRC 1995b, Race and Fonseca 1996~. It is also important to recognize as a separate

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72 ECOLOGICAL INDICATORS FOR THE NATION category wetlands restored after years of tile drainage and crop produc- tion under the government's Wetlands Reserve Program, which since 1990 has been administered by the Natural Resource Conservation Service (formerly the Soil Conservation Service) under the Food and Security Act of 1985. Wetland types can be distinguished using data from the National Wetland Inventory (NWI) carried out by the U.S. Fish and Wildlife Service since the mid-1970s, mostly by means of 1:60,000 color-infrared photogra- phy. By late 1991, 70 percent of the coterminous states and 22 percent of Alaska had been mapped (NRC 1995b), the basic mapping units being the set of wetland categories devised by Cowardin et al. (1979~. The NWI has prepared a report on wetland status as of the mid-1980s, and on the trend of losses since the mid-1970s (Dahl and Johnson 1991), based on a repre- sentative sample of U.S. wetlands. Future reports are planned at 10 year intervals. Other NWI products include reports to accompany each 1:100,000 scale wetland map, reports on state wetlands, and a wetland- plant database (Mitsch and Gosselink 1993~. NWI maps are being digi- tized for a computerized geographic information system that will facilitate both analysis and display of the data. In only ten states, however, was the process near completion in 1994 (NRC 1995b). Reliability. Calculating changes in the proportions of land cover in the United States with fully replicable techniques will require integrating remotely sensed information with data from statistically based, in situ sampling programs. A growing number of examples exist in which such information has been collected on regional scales, especially using remote sensing. Of particular interest to the scientific community are studies of tropical deforestation (Skole and Tucker 1993; Laporte et al. 1995; lanetos et al. 1997 [GOFC]), in which changes in proportions of land cover types have been calculated and full transition-probability matrices have been derived. Temporal and Spatial Variability. The land cover indicator itself does not retain the spatial information in the underlying data. However, if the underlying data are archived with all their spatial information intact, then more complex, spatially explicit measures of land cover changes can be computed (Appendix B). These measures are likely to be of substantial regional and local interest. Many natural processes cause changes in land cover, but typically they result in relatively small annual changes. Appreciable changes typi- cally occur only over decades. However, some anthropogenic changes, such as clearing forests for rangeland or farmland, and large fires, happen

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 73 quickly. Therefore, land cover needs to be computed annually but it need not be formally reported more often than once every five years. Statistical Properties. The statistical properties of land cover are clearly a function of the reliability of identification of land cover types from remote sensing and of the statistics of the in-situ sampling program. Because the use of remote sensing to quantify land cover change is an active area of research and application within the scientific community and operational agencies, the statistical properties of land cover should be clarified in the near future. The classification of land cover types in the land cover indicator must be sufficiently comprehensive for all the additional indicators that are derived from it. Classification issues can be addressed in two ways. One would be to determine the number of classes required by the most demanding indicator and use that classification in all input data. This method would force the unification of classification schemes for all indi- cators. The other would be to have a more flexible, hierarchical classifica- tion scheme that would allow the unfolding of additional classes of land cover from a smaller number of aggregated classes from the same under- lying data. The latter approach has been used by the IGBP (IGBP 1992b; Defries and Townshend 1994; Townshend et al. 1994) in its global 1 km land cover product. A flexible, hierarchical classification system would best serve the needs of a variety of environmental indicators. The rate of land cover change determines the most appropriate sam- pling intervals, but there are also practical limitations on sampling fre- quencies. For example, analyses of satellite data are constrained by both the technical features of the satellite itself and by the ability of investiga- tors to handle and interpret the very large volume of data. In addition, the return time for sampling NRI plots or CFI plots is largely determined by the availability of field crews. However, the mean resampling time for CFI plots is approximately 10 years, which compares favorably with theo- retically determined appropriate sampling frequencies for forest produc- tivity (Appendix A). Scientists who use remote sensing have addressed issues of sampling intervals at some length (Skole et al. 1997; IGBP 1992b; Justice and Townshend 1988~. As a rule of thumb, they have suggested that five-year intervals of complete remote-sensing surveys at national, continental, and global scales are generally adequate. Complete surveys could be inter- spersed with annual stratified samples to detect rapid changes without overwhelming the capacities of investigators and systems to perform the analyses. Necessary Skills. The collection of remotely sensed data obviously

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74 ECOLOGICAL INDICATORS FOR THE NATION demands a high degree of familiarity and experience with the instru- ments and data-handling capabilities. However, technological barriers to handling remotely sensed data are shrinking as computer technology improves and costs decline. The greatest barriers to developing and using the land cover indicator are probably conceptual: developing the detailed techniques for classifying, combining, and interpreting changes in land cover categories by means of which remote-sensing and in situ data are evaluated. Data Quality Control, Archiving, and Access. The input data for land cover should be archived at the most highly resolved and disaggregated levels, and the techniques used to generate land cover classes need to be described clearly and documented. Only in this way will the land cover indicator be replicable and real changes detectable. Sources of error in both measurements and classifications should also be clearly defined and documented. Comparing maps derived at different times, although fea- sible, is not a good method of documenting changes in land cover because it confounds measurement errors, interpretation errors, and cartographic errors in ways that would be extremely difficult to quantify. It is more straightforward and desirable to detect change in the underlying data themselves, use those differences for quantitative analyses, and then derive maps for presentation purposes. Robustness. Although tremendous strides have been made in recent years, the use of remotely sensed information for ecological analyses is still in its infancy. For many years, the technical challenges of simply handling and processing the data were so large that they inhibited the use of the systems by all but the most sophisticated laboratories. Rapid improvements in cost and performance of computer hardware and soft- ware are removing many of these technical impediments, but other issues remain. The most important ones include the care, maintenance, and accessibility of data archives, and the intercalibration of the remote- sensing instruments themselves. The land cover indicator is likely to be robust to reasonable sources of interference, especially if the original data are archived carefully. How- ever, the time series of measurements can be compromised by technologi- cal changes unless sufficient care is taken to ensure that new instruments are cross-calibrated, and that the calibration of instruments is maintained and monitored carefully over their lifetimes. Achieving calibration precise enough for these quantitative scientific measurements is difficult, but it can be achieved, as the Landsat data record shows. For data sets that last longer than the lifetime of any one instrument, successive instruments must be flown and cross-calibrated for a period of overlap. In this way,

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 105 the past five decades, increased demand, trends in dietary preferences, and the development of new technologies have led to greatly expanded use of chemical fertilizers, pesticides, and water for irrigation and live- stock production. Research to find ways to reduce the deleterious effects of these practices on surface and groundwater quality and on soils is leading to policies to protect soil and water while sustaining the profit- able production of agricultural goods, but considerable improvements can still be made (NRC 1993~. Nutrient cycles differ dramatically between agricultural ecosystems and the natural ecosystems they replaced. The most significant recent change involves massive movements of nutrients across landscapes. For example, fertilizers are transported to crop-producing areas in the spring, grain is transported to animal-producing areas in the fall, and animal manures become wastes or excess fertilizer because the rate of production exceeds local needs and the cost of transport make redistribution eco- nomically infeasible (Magdoff et al. 1997~. More land, fertilizer, pesticides, and irrigation water are needed to support animal production, and the environmental impacts are greater than if dietary choices demanded less animal protein. The importance of animal protein in human diets, which is consumer-driven, is an important factor in agriculture's impacts on the biosphere. Nations, such as the United States, with extensive concentrated animal production facilities generate large amounts of excess nutrients because nutrient use in animal production is much less efficient than in producing crops (van der Ploeg et al. 1997~. The NRC (1993) analyzed agricultural practices and impacts to iden- tify opportunities that held the most promise for "improving the environ- mental performance of farming systems while maintaining profitability." The broad recommendations of that report were the following: 1. Conserve and enhance soil quality as a fundamental first step to environmental improvement. systems. 2. Increase nutrient, pesticide, and irrigation efficiencies in farming 3. Increase the resistance of farming systems to erosion and runoff. 4. Make greater use of field and landscape buffer zones. Following this framework, the committee evaluated and recommends national-level indicators of nutrient-use efficiency and balance. The high productivity of most modern agriculture depends on added nutrients. In most agroecosystems, more nutrients are added to the sys- tem than are extracted from it in harvested products; and the imbalance is

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106 ECOLOGICAL INDICATORS FOR THE NATION far greater for animal production than for crop production. These excess nutrients find their way into the soil, the atmosphere, and water. We define the proportion of added nutrients removed in products as nutrient-use efficiency. Because the efficiency with which nutrients espe- cially N and P are used in the production of crops and animal products is of great economic and environmental significance, it is important to monitor changes in inputs and outputs from agricultural lands. Losses of agricultural chemicals account for a major share of nonpoint-source N and P pollution of ground and surface waters (NRC 1993~. Because point- source control of N and P inputs to surface and groundwaters has been easier to achieve, nonpoint sources account for an increasing share of the total inputs (Sharpley and Meyer 1994~. The increasing demand for agri- cultural products will generate powerful pressures for increased agricul- tural chemical use. N export from agroecosystems is known to adversely affect drinking- water supplies. Nitrate (NO3) in drinking water can be acutely toxic, and it can cause methemoglobinemia in infants (Spaulding and Exner 1993~. The maximum contaminant level has been set at 10 mg NO3-N LO for drinking water. Regions of irrigated agriculture such as the wheat belt and California's Central Valley have the highest incidence of elevated NO3 levels, but many other such areas are scattered about the United States (Spaulding and Exner 1993, Kolpin 1997, Lichtenberg and Shapiro 1997~. N also contributes to eutrophication of aquatic and estuarine systems (Spaulding and Exner 1993~. Local, regional, and national annual N budgets for cropland and agri- cultural watersheds indicate that more N is added to croplands (manure N plus fertilizer N plus N fixed by legumes) than is removed in crops. The amount of N not transferred to crops varies widely as a function of site conditions and management practices. Site conditions that control N transformations vary among regions, along topographic gradients, and with different cropping practices. Also gaseous losses from and additions to the soil are difficult to measure; and cropping practices other than fertilization can release stored soil N at substantial rates (Keeney and DeLuca 1993, David et al. 1997~. Therefore it is difficult to rigorously determine the fate of excess fertilizer and manure N. and difficult to relate the excesses directly to elevated ground- and surface-water N levels (Keeney and DeLuca 1993, David et al. 1997, Kolpin 1997~. Gaseous losses of N (as N2O and NH3) have other influences. N2O is a significant greenhouse gas. NH3, volatilized from fertilizers and animal manure, is eventually deposited as NH4. After being taken up by plants, atmospherically deposited NH4 acidifies the soil and, in some regions (e.g., the montane watersheds of the northeastern United States), contrib-

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 107 utes substantially to the N and H+ loads that must be assimilated by sensitive landscapes (Iohnson and Lindberg 1992, Vitousek et al. 1997~. Soil phosphorus lost from agricultural systems to watersheds acceler- ates eutrophication of lakes and streams. Productivity and algal blooms in lakes and streams are promoted by elevated inputs of dissolved inorganic P. and by labile P ("algal-available P") bound to sediments or in labile organic combinations. In general, P is less mobile than N. because it adheres strongly to soil constituents. P applied in excess of crop uptake is retained to a considerable extent in nonsandy mineral soils. Quantita- tively important leaching losses of P through the soil to ground and sur- face waters are limited to areas of sandy soils, organic soils, and cases of extreme P loading. Surface runoff and tile-drain effluent from fertilized cropland, pastures, and animal-feeding operations and the accompany- ing suspended sediment are thus the most important vectors for P deliv- ery to surface waters. The importance of each source varies according to region, soil conditions, and management practices. As concern about environmental impacts of agricultural nutrient losses has grown over the past decade, so has research on how to manage agricultural nutrient use to minimize loss, while maintaining productivity and profitability. Because nutrient loss from agricultural systems is a site- specific problem (NRC 1993, Harris et al. 1995), site- and practice-specific mitigation measures are required. Many efforts are under way to gain the understanding necessary to balance environmental and productivity needs (see reviews by NRC 1993, Harris et al. 1995, Daniel et al. 1998, Sharpley et al. 1996~. Changes in nutrient-use efficiency in agricultural systems and nutri- ent losses from these systems have been driven by the increased availabil- ity of chemical fertilizer since World War II; by the availability of trans- portation for fertilizer, feed, and agricultural products; and by increases in meat consumption, which has led to the growth of specialized animal- production systems. The trend toward greater livestock production in the Western world during the latter half of this century is a major con- tributor to overall loss rates of nutrients used in agriculture, because the nutrients in manure are much less efficiently incorporated into animal products than into crops (e.g., van der Ploeg et al. 1997~. This situation is magnified in small meat-producing countries such as the Netherlands, where animal feeds grown on five to seven times the Dutch agricultural land area are imported. This large import of nutrients is driving country- wide nutrient enrichment as the manure is applied to Dutch agricultural land and excess nutrients make their way into ground and surface waters (Van der Molen et al. 1998~.

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108 ECOLOGICAL INDICATORS FOR THE NATION The Indicators. Nutrient leakage is an inherent property of current agricultural activities (see review by Magdoff et al. 1997) and will remain so for the foreseeable future. Because the demand for agricultural prod- ucts will increase as the human population and economic activity increase, the only way to reduce losses of nutrients to ground and surface waters (and to the atmosphere in the case of gaseous N losses) is to develop and implement site-specific and practice-specific management techniques that improve the efficiency of nutrient use in crop-producing areas, and that limit the leaching and runoff of nutrients from animal-producing opera- tions. Considerable agricultural research is being conducted on this matter; NRC (1993) covers useful management alternatives. If animal products become less important in people's diets, overall agricultural nutrient losses will decrease (van der Ploeg et al. 1997~. However, even if substantial improvements in nutrient-use efficiency occur, overall losses from agricultural lands will increase if demands for agricultural products outpace improvements in nutrient-use efficiency. Accordingly, it is use- ful to have indicators of both the overall efficiency of nutrient use in the production of crops and animal products and the overall nutrient bal- ance. Efficiency indicators are ratios or percentages that can increase or decrease with time. Balance indicators record the excess of nutrients applied to agricultural land over nutrients removed in harvested prod- ucts. Indicators of nutrient-use efficiency and overall balance can be created for use at virtually any scale from farm fields to countries. Nutrient-Use Efficiency. N and P use-efficiency indicators are useful for crops or industries, for counties, and for watersheds in which ground or surface waters are perceived to be adversely affected. These indicators can be used in testing trends in the effectiveness of management pro- grams locally, regionally, nationally, or on a crop-specific basis. Aggre- gated data at a national scale have been useful for detecting and under- standing trends in N-use efficiency in Germany (van der Ploeg et al.1997~. N and P budgets for cropland are often very hard to construct given the difficulties in tracking nutrients applied in excess of crop uptake, and especially in determining gaseous inputs and outputs of N. Different authors have used different indicators to represent fertilizer-use efficiency, and several assumptions are usually made in estimating N budgets for croplands (e.g., lenkinson and Smith 1988, Black 1993, NRC 1993~. We have adapted the approach and budget methods used by the NRC (1993) and van der Ploeg et al. (1997) in constructing the following indicators to monitor trends in agricultural nutrient-use efficiency at a national scale. For cropland:

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS (1) Nitrogen-use efficiency Nc = N removed in crop biomass (mass y-l) chemical fertilizer N applied + animal manure N applied + N fixed by legumes (mass ye) (2) Phosphorus-use efficiency Pc = P removed in crop biomass (mass y-l) chemical fertilizer P applied + animal manure P applied (mass ye) 109 Data inputs for N and P removed in crops are crop yields by type, dry-matter percentages, and biomass N and P content. Fertilizer sales by county (e.g., EPA 1990, Smith et al. 1997), county animal censuses (e.g., U.S. Bureau of Census 1987), and per-animal nutrient excretion rates (U.S. Soil Conservation Service 1992) can be used as estimates of the terms in the equations. Legume N fixation requires assumptions, but they are straightforward and useful if they are uniformly applied (NRC 1993~. Because the indicators are percentages, they take values ranging from O to 100 percent, higher values indicating greater efficiency. Depending on availability of data, these indicators could be calcu- lated annually and should be able to detect changes in nutrient-use effi- ciency on a decadal scale. For example, in the former West Germany, crop N-use efficiency, calculated as shown above (without N fixed by legumes), decreased from about 100 percent in 1964 to a low of 72 percent in 1984, then increased to about 81 percent in 1990 (van der Ploeg et al. 1997~. Using NRC (1993) data for 1987 (NRC's Table 6-3, medium N- fixation scenario), N-use efficiency for U.S. cropland was 59 percent and for P 31 percent. Because such large quantities of nutrients in excess of those harvested are applied to U.S. agroecosystems, the potential for improvements in nutrient-use efficiency is great (NRC 1993~. Nutrient-use efficiency indicators should provide integrated mea- sures of how well management strategies are working. Application of the indicators at smaller scales would provide opportunities to target specific geographic areas or crop-production systems. A rough but potentially useful measure of the efficiency of N and P use in agriculture on a national scale can be approximated by the equation (3) Na = N content of crops produced for human consumption + N content of animal products produced (mass N ye) Chemical N fertilizer applied to cropland + N fixed by legumes (mass N ye)

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110 (4) Pa = ECOLOGICAL INDICATORS FOR THE NATION P content of crops produced for human consumption + P content of animal products produced (mass p y-l) Chemical P fertilizer applied to cropland (mass P ye) These indicators could be applied to smaller scales such as states, counties, or watersheds, but at these smaller scales the indicators would need to be modified to account for imported (or exported) nutrients in crops produced for animal feed. The large decrease in N-use efficiency for agriculture as a whole (i.e., animal and crop production) from 1951 (77 percent) to 1980 (27.2 percent) in West Germany resulted from increasing rates of applications of chemical fertilizers, the rise of livestock produc- tion (a much less efficient user of nutrients than crop production), and an attendant 10-fold increase in imported N in feed (van der Ploeg et al. 1997). Nutrient Balance. The same data can be used to compute indicators of overall nutrient balance. Changes in these indicators reflect the combined effects of changes in nutrient-use efficiency and in the quantity of agricul- tural products. Tables 4.3 and 4.4 show the mass-balance approach used by the NRC (1993) for N and P applied to cropland. Such budgets require several assumptions, but they are straightforward. For nitrogen, the indi- cator would be N fertilizer applied plus recoverable N in animal waste (manure) applied plus N fixed by legumes minus N removed in harvested crops (assuming steady-state nutrient pools in crop residues). A similar indicator could be used for P. as described for the nutrient-use efficiency indicator. These national-level indicators would provide important input for understanding changes in water quality and other aspects of nutrient cycling. The units of the indicators are Mg/year for the area of interest. Nutrient-balance indicators could also be used at local and regional scales. States and counties conduct censuses of farm animals, and methods are available for estimating per capita manure production by poultry and livestock (NRC 1993). The indicator would not be affected by variations in the distances between the animal production facilities and the crop- lands that support them. The indicator would have smaller values in areas of crop-only production and higher values where animal produc- tion is concentrated. Such indicators would help states and counties evaluate their agricultural practices in light of potential nutrient losses to surface water and groundwater.

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112 oo V) o o V) u V) o V) H V) o V) o o V) V) o o . V) ~U 5- ~ E~ ~ U - o E~ O > ~ CD O CD 5- ~ o E~ CD O CD 5- O ~ 5- ~0 ~ . O O O O O O O O O ~ Lr) 00 ~ ~ O O O O O O O ~ 00 Lr) Lr) O O O O O O O O 0 ~1 0 0 C~ 00 00 ~ O O O O O O O O O C~l O ~ Lr) ON ~ ON ~ ~ 00 Lr) ~ O O O O O O O O O O O Ct) ~ O O O O O O Lr) Lr) - ` ON ~ ~ C~ 0 00 ~ ~ 00 ~ ~ ~ Lr) ~ ~ o o o o o o o o o o o o o o o o o o o o co Lr) oo o o ~ o ~ Lr oo o ~ oo ~ ~ ~ c~ co ~ Lr) ~ ~ ~ Lr) o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o ON Lr) O Lr) O ~ Lr) 00 ~h ~ co oo o ~ Lr) Lr) o ~ Lr) oo ~ ~ ~ Lr) ~) ~ ~ ~ ~ ~ o o o o o c~i o o o o o o o o o o o o o o o o o Lr) o o o o o o o o o o o o ~ o o o o o o Lr) o ON ~ O ~ 00 CO Lr) ~ O ON CO ~ C~ O 00 ~ ~ 00 C~ co ~ c~ o o o o o o o o o o o o o o o o o o o o o o Lr) o ~ o ~ ~ ~ o C~ C~ 00 Lr) C~ O ON CO ~ Lr) Lr) Lr) Lr) Lr) o o o o o o o o o o o o Lr) Lr ~ co o o o o o o o o o o o o o o o o o o ~ ~ o oo ~ ~ ~ ~ Lr) co co .= .= 'o = .= z . . o v,

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS RESEARCH NEEDS 113 Although the committee's recommended indicators are based on solid theoretical justification and extensive data, the precision and interpreta- tion of the indicators should be improved by additional research and development. Moreover, future research may suggest new indicators that may be better than existing indicators or may be usefully added to the set of regularly reported indicators. More research is needed to iden- tify organisms and biological processes that are especially sensitive to stresses and perturbations and to determine more accurately the temporal behavior of indicators. To address problems associated with spatial scale in indicator performance, it is important to test new indicators carefully in pilot programs before implementing them nationally (NRC 1995a). For the recommended indicators that are new, especially the ones that mea- sure land cover, land use, and species diversity, further work is needed on how best to operationalize the indicators and to help identify future research plans. This work, which should include one or more workshops, should include academic scientists, practitioners, agency scientists, and other interested parties. Temporal Behavior of Ecological Indicators Knowing temporal variations in indicator values is important for interpreting monitored data. Because very few monitoring efforts exceed a decade, and many for no more than a few years, other methods need to be used to provide a record long enough to capture normal variations in the proposed indicator values, as well as to investigate surprise variations. The source of much of the variation in indicators may be found at the interface between population and ecosystem processes. Population cycles are well studied, but how population cycles affect temporal patterns of species diversity, carbon storage and flow, and nutrient runoff is unknown. Experimental and theoretical investigations into the relationship between current population cycles and related ecosystem processes will provide the mechanistic understanding needed to improve predictions and inter- pret the causes of indicator behavior. In addition, research is needed on applications of the mathematical techniques of spectral analysis (Platt and Denman 1975) and wavelet analysis (Wickerhauser 1994) to time series of model outputs and to patterns in the paleorecord. Spectral analysis identifies the periods and amplitudes of fluctuations in a time series of data. An example of how this method can assist in the design of sampling systems is provided in Appendix A. Wavelet analysis identifies periods in which there is a sudden change in system behavior. These periods may correspond to

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4 ECOLOGICAL INDICATORS FOR THE NATION "surprises." These mathematical techniques have been developed for analysis of digital signals and other relatively clean data sets free from stochastic effects. Ecological data, in contrast, are often incomplete be- cause of gaps in the record. In addition, in ecological research, stochastic noise often obscures the detection of fluctuations of long periods or low amplitudes, and the detection of sudden changes in the data spectrum. Research is required on adapting these mathematical techniques to the more problematic data sets typical of environmental monitoring and the paleorecord. Keystone Species Species whose removal results in a large effect on some functional property of an ecosystem called keystone species are good targets for indicators. Research is needed to develop a predictive theory of keystone species and to identify tolerant species. Traditionally, ecologists have looked for and identified keystone species by their effects on the species richness and composition of the community in which they live. Keystone species also may have major effects on primary and secondary productiv- ity and nutrient cycling. Unfortunately, although a number of keystone species have been identified, no predictive theory of keystone species yet exists. Tolerant Species and Assessing the Regional Importance of Local Sites Evaluating places using only indicators that focus on each site sepa- rately would not lead to decisions that would sustain the greatest amount of species diversity. A hypothetical example suffices to explain why. Suppose a company intends to build a factory but it does not care on which of two equal-sized natural areas it builds. For purposes of preserv- ing biological diversity, it might appear obvious that the site with the fewest species is preferable for the factory. The issue is more complicated than that because one needs to know if the diversity on the richer site is sustainable (as has been taken into account for measuring species densities), and also the extent to which the site is redundant in the system of reserves that maintains S for the region as a whole. If the richer site has virtually the same list of species as another site and the species appear to be sustainable at the other site, the value of the rich site is lower. Conversely, if the alternate site for the factory, although relatively poor in diversity, harbors species found nowhere else in the region, or nowhere else in the world, it has higher biodiversity value than the richer site. The lessons of this simple example

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INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 115 can be used to suggest ways to evaluate the contribution of a site, Ri, to regional diversity. To achieve this, for example, separate Si into two components. The species not found in sustainable condition elsewhere are Ri. The defini- tion of "elsewhere" may vary depending on the objective of the group doing the evaluation. In other words, elsewhere means "anywhere else in the area whose diversity one is trying to protect." In this context, a species whose range is so fragmented that its survival depends on a number of sites should be counted as a full species in the Ri of each site that forms a necessary part of its support range. To use Ri one must be able to measure sustainability. Sustainability is increased by avoiding overload in Di, but understanding sustainability fully also requires knowledge of the population dynamics, meta- population dynamics, and species interactions of the species contributing to Ri. Because obtaining all this knowledge is difficult and laborious, it cannot be done for all the species in a place. A reasonably accurate esti- mate of Ri can probably be obtained by focusing investigations on a few, charismatic taxa, such as birds, fishes, mammals, butterflies, wildflowers, and trees, instead of a random scattering of species in many taxa. How- ever, considerable research will be needed to generate the data necessary for computing measures of sustainability. As human uses take more of a region's area, many sites will shrink or disappear. As a result, the list of species restricted to a critical few sites and the average value of Ri will both climb. A place that lacks importance today may become important in the future. Thus, Ri must be reassessed periodically, probably once each decade. Ri is not an indicator but com- puting its values is an important part of an overall assessment of the performance of a system of reserves, so that biodiversity protection is achieved most efficiently.