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1 Introduction ' ndicators are designed to provide clear signals about something of interest. Indicators communicate information about the status of ~ things, and, when recorded over time, can yield valuable information about changes or trends. The bar on a thermometer indicates the tem- perature of a room; the light on an appliance indicates that it is turned on; the gauge on a gasoline tank indicates the amount of remaining fuel; blooms of cyanobacteria of the genus Oscillatoria in temperate-zone lakes indicate that serious pollution problems are developing. The values of an indicator over time can inform decisions about whether an intervention is desirable or necessary, which of various interventions might yield the best results, and how successful interventions have been. Indicators there- fore can and should guide policy and help direct research. WHY ARE ECOLOGICAL INDICATORS NEEDED? Not everything in the environment can be measured; indicators are needed because ". . . of a very practical problem: too many needs, too few funds" (larvinen 1985~. Good indicators can reveal the more significant ecological changes with the most efficient use of resources. During the coming decades, the nation will need to develop and implement environ- mental policies that are likely to have major societal and economic effects. If these policy decisions are to be wise and achieve their desired results, decision makers will need data that capture the most critical dynamics of 18

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INTRODUCTION 19 ecological systems and the changes in their functioning. Good indicators serve that purpose. Indicators usually serve as clues that something more fundamental or complicated is happening than what is actually measured. Abnormal blood pressure signals that some physiological process is not functioning properly, although it may not indicate which process is malfunctioning or why. Recording indicators over time may also signal changes or trends that are difficult to detect immediately, as when cirrus clouds, or a falling barometer, indicate the approach of a storm. Experience amply demonstrates the power of indicators to influence human behavior. Changes in economic indicators appear to be especially motivating. When the Dow Tones index rises or falls, thousands of citi- zens make new financial decisions or reconsider old ones. Thousands of people pay close attention to changes in the gross domestic product. People respond to these highly aggregated indicators because they believe that these signs reveal something important about current conditions and are useful predictors of future trends and conditions. People also believe they understand what these indicators mean and what they predict. Currently, no indicators of ecological status or trends have the stature of the most influential economic indicators, although physical indicators, such as global mean temperature, sea surface temperatures, and atmo- spheric carbon dioxide concentrations, are attracting considerable atten- tion. Developing indicators of comparable power for ecological processes will help focus attention on environmental conditions, attention that may in turn stimulate significant and informed political action. Such ecologi- cal indicators are needed as yardsticks to measure public policies and their performance. These indicators must provide information in a simpler, more comprehensible form than the complex statistics usually assembled on ecological issues, and the relationship between these indi- cators and the complex phenomena they represent must be evident. During recent decades, because of growing environmental concerns, increasing efforts have been devoted to developing reliable and compre- hensive environmental indicators. Many countries and U.S. states now publish annual "State of the Environment" reports. International organi- zations, such as the United Nations Environment Programme (UNEP), analyze and report various types of environmental information. Because these reports contain large amounts of information that is difficult to digest, they often have not had much influence on decision makers. To simplify such information and make it more useful to decision makers, the Canadian government began to develop environmental indicator con- cepts in the late 1980s (Environment Canada 1991~. The Dutch govern- ment initiated similar efforts in 1987 (Government of the Netherlands 1991~. Agenda 21 of the United Nations Conference on Environment and

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20 ECOLOGICAL INDICATORS FOR THE NATION Development in Rio de laneiro, Brazil, called for the development of envi- ronmental indicators to ascertain whether developmental trajectories were in fact sustainable. In 1993, the United Nations Statistical Division (UNSTAT) and UNEP formed a Consultative Expert Group Meeting on Environment and Sustainable Development Indicators in Geneva to survey the variety of approaches being used to develop indicators. In 1994, the World Bank convened a workshop to find common ground in formulating indicators of sustainable development; and in 1995 an international policy confer- ence was hosted by the Belgian and Costa Rican governments, together with UNEP and the Scientific Committee on Problems of the Environ- ment (SCOPE), to seek consensus on international uses of environmental indicators (see Hammond et al. [1995] for a historical summary and refer- ences). The Santiago Declaration of February 3, 1995 (reprinted in the Journal of Forestry, April 1995, pp. 18-21) included criteria and indicators for the conservation and sustainable management of temperate and boreal forests. Thirteen countries that comprise the bulk of the world's temper- ate and boreal forests, including the United States, have agreed to monitor and report on these indicators. Over these same years, United States federal agencies, such as the Forest Service and other agencies within the Department of Agriculture, the Fish and Wildlife Service, the National Oceanic and Atmospheric Administration, and the U.S. Environmental Protection Agency (EPA) also engaged in efforts to develop environmental indicators. Private organizations developed indicators that helped launch "green" national accounting and natural resource accounting (Repetto et al. 1989, Lutz and El-Serafy 1989), and various projects were aimed at certifying that forest products were harvested in a sustainable manner (Forest Stewardship Council 1996~. These projects have all laid important foundations for developing comprehensive, national-level indicators to inform major public policy decisions. The committee's work builds on this important work. How- ever, the committee's focus is different from those of most previous stud- ies because it concentrated exclusively on ecological indicators and sought to identify key ecological processes and patterns for which data could be collected as a basis for national indicators. This focus led the committee to identify the smallest number of indicators that could capture key trends in the nation's ecosystems. The committee did not propose indicators of stressors, preferring to focus on indicators of ecological conditions, most of which are influenced by multiple stressors. Some of the indicators the committee recommends, such as productivity, nutrient-use efficiency, and soil organic matter, have been recommended by others and are to some degree already in use. Others, especially those dealing with biological

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INTRODUCTION 21 diversity, have not been proposed in the form proposed here. The rela- tionship of the proposed indicators to previous recommendations is dis- cussed in the rationale for each indicator (Chapter 4~. THIS STUDY The Committee to Evaluate Indicators for Monitoring Aquatic and Terrestrial Environments (Indicators Committee) was formed in response to a request from the EPA for a critical scientific evaluation of indicators to monitor environmental change. Part of the motivation for the request was an earlier National Research Council (NRC) review of the EPA's Environmental Monitoring and Assessment Program (EMAP). In its over- all evaluation of that program, the NRC (1995a) recommended that EMAP develop a focused indicator-research program, that each EMAP resource group develop a mechanistic conceptual model to underlie its indicators, that EMAP provide program-wide guidance for indicator development to ensure at least a consistent philosophy behind the indicators developed for the various resource groups, and that EMAP evaluate each indicator at incrementally larger spatial scales. Recognizing the difficulty of imple- menting these recommendations, then Assistant Administrator of the EPA's Office of Research and Development Robert Huggett requested the NRC's help. In his request, Dr. Huggett also emphasized the broad need for useful indicators throughout federal agencies and even beyond them. Therefore, while the committee hopes this report is useful to EMAP, its intended audience is much broader. Indicators of physical aspects of our environment have received con- siderable attention and many of them are now in wide use in the United States and elsewhere. However, ecological indicators do not command such national confidence and use, although many have been developed and used regionally and locally. Therefore, the committee devoted most of its attention to ecological measurements that can be aggregated into useful nationwide indicators. The process and criteria that the committee used to choose these indicators should be applicable at many spatial scales, and in Chapter 5 we suggest procedures for developing regional indicators, with some examples. The task that faced the committee was enormous, and its financial and human resources were finite. To keep its task manageable, the com- mittee focused mainly on terrestrial, freshwater, and estuarine, but not marine, environments. Additionally, it is not obvious how data on marine environments might be aggregated into national indicators. The need for marine indicators is great, and the committee hopes that different people and insights will be brought to bear on this important task. We believe that the methods and criteria presented in this report will be useful to the

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22 ECOLOGICAL INDICATORS FOR THE NATION development of marine ecological indicators at a national scale as well as regional and local indicators in all environments. The committee was not asked to and did not review any existing indicator-development pro- grams, including the EPA's extensive program. It did benefit from much previous work, including work performed or supported by the EPA. Indicators differ in their generality and their spatial and temporal scales. Indicators of the status of a particular lake may be highly relevant to local decisions about regulating pollutant discharges into the lake and its upstream watershed, but that information may not be of much use to managers living in different watersheds. Indicators are useful at many levels community, state, regional, national, and international and new indicators need to be developed at all such scales. Ecological indicators, the charge to the committee and focus of this report, are urgently needed. Little attention is given here to many other important types of environmental indicators, such as those relating to climate change, ozone depletion, acidification of precipitation, and air quality. Our selective focus does not imply that these other environmental indicators are less important. The goals of this report are (1) to summarize sources of data that can be used to design and compute indicators, (2) to suggest criteria that should be used in selecting comprehensive indicators, (3) to provide methods for integrating complex ecological information into indicators that summarize briefly but powerfully important ecological states and changes, (4) to propose indicators that meet these criteria, and (5) to offer guidance for gathering, storing, interpreting, and communicating infor- mation for ecological monitoring. KEY ECOLOGICAL PROCESSES AND PRODUCTS THAT PEOPLE VALUE Typically, ecological indicators are designed to assess processes and products that have value to people. People value ecological goods and services for a variety of reasons. In this report, ecological goods and services refer not only to food, fiber, building materials, and medicines, but also to the roles of ecosystem processes in protecting watersheds, reducing the frequency and severity of floods, purifying waters, and shap- ing local, regional, and global climates. The term also includes the services that natural environments provide for recreation, aesthetic enjoyment, and spiritual experience. Generally, relatively constant and predictable flows of goods and ser- vices are regarded as desirable, and so indicators are needed to track changes in the processes that maintain these flows. Because environ- mental outputs may depend on the contributions of different sets of

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INTRODUCTION 23 organisms in different ecosystems, the organisms that maintain any given ecological process are often varied both spatially and temporally. Another guideline for identifying useful indicators is to focus on changes in states or processes that are irreversible or that can be reversed only at extremely high costs or very slowly. An example is the extinction of species, which is clearly irreversible. Although history demonstrates that the diversity of life recovers following mass extinctions, recovery may take from one to 10 million years and lost species are not necessarily replaced by anything similar. Other ecological changes that can be reversed only very slowly are loss of soils through erosion and salination. Thus, the committee devoted considerable effort to developing indicators of biological diversity and soil status. Changes that are difficult to reverse are sometimes associated with systems that have alternative stable states. The system tends to return to its former state following a perturbation, but if pushed too far, the system may shift to an alternative stable state. Such shifts are not necessarily undesirable, but some have been. Returning the system to its earlier condition may be extremely difficult. The best known examples involve commercial fisheries. Some fisheries have collapsed to the point at which the exploited species is rare, and from which recovery has not taken place despite the cessation of commercial fishing. Examples include changes in intertidal and subtidal ecosystems from exploitation that led to local extinction of sea otters (Simenstad et al. 1978~; and the disappearance of sardines off California's coast (Lluch-Belda et al. 1989~. In other cases, there have been fairly persistent changes in community or ecosystem structures, as has occurred in the Bering Sea ecosystem (NRC 1996a) and for groundfish off the New England coast (NMFS 1996, NRC 1999a). In some or all of the above cases, environmental fluctuations have been a contributing factor to the problem in addition to human exploitation. ESTABLISHING BASELINES TO EVALUATE TRENDS To evaluate and use indicators, it is often highly informative to com- pare status and trends measured by the indicator against some "reference state." Without such a baseline, it is hard to assess the magnitude of change objectively, whether the magnitude of change is important, or if any efforts at amelioration are succeeding. A reference state is an opera- tional concept that may be based on some knowledge of the characteristics of the "natural" state. This baseline could be a "magnitude of control or reference ('baseline') variability in what is being tested" (NRC 1992~. Alternatively, the reference state may be based on a maintenance of eco- logical processes. The phrase ecosystem health has often been used to identify and char-

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24 ECOLOGICAL INDICATORS FOR THE NATION acterize the reference states used to gauge environmental status and trends. A major problem with this notion is the lack of clearly defined measures by which the "health" of an ecosystem can be judged. A wheat field differs dramatically from the prairie that it replaced, but a question- able amount of insight is gained by declaring the wheat field to be "unhealthy." More recently, the concept of biological integrity has emerged as a replacement for the term ecosystem health because this new term avoids some of the connotations of the word health. The concept of bio- logical integrity is based more on the maintenance of ecosystem processes than on identification of any specific "natural" state. The term was first used in 1972 to define the goals of the U.S. Clean Water Act, "to restore and maintain the chemical, physical, and biological integrity of the Nation's waters." Biological integrity has been defined as "the capacity to support and maintain a balanced, integrated, adaptive biological system having the full range of elements (genes, species, and assemblages) and processes (mutation, demography, biotic interactions, nutrient and energy dynamics, and metapopulation processes) expected in the natural habitat of a region" (Kerr 1996, emphasis added). In other words, a set of natural processes is identified and used as a reference state for evaluating current conditions and trends. Although reference states generally are needed to evaluate current conditions, identifying the appropriate and specific reference states is difficult. First, many ecosystems and habitats are so poorly understood that specifying "natural" states and processes is possible only within broad limits. Considerable research may be necessary before specific reference states can be developed for these systems. Second, large-scale fluctuations characterize most ecosystems. The abundances of species may change dramatically seasonally and from year to year. Rates of photosynthesis may vary greatly in response to changes in temperature, precipitation, and soil fertility. Therefore, baselines must specify typical patterns of variation and incorporate ways of deciding whether a particular fluctuation or trend falls outside the bounds of "normal" variation. The greater the normal variability in an ecosystem, the more difficult it is to identify abnormal variation. Third, directional change occurs for various reasons, making the choice of appropriate reference states additionally difficult. Species evolve, and their larger biological communities and ecosystems can change as a result. In addition, environmental processes such as glaciation, other climatic changes, and geological forces alter the distributions and abundances of species and biological communities. Some of these changes are so slow that they are unlikely to affect the choice of reference states or reading of indicators over periods of several hundred years, but some can occur at rates roughly similar to changes caused by human population growth

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INTRODUCTION 25 and technology. The choice of reference states should be made carefully by considering the implications of adopting fixed or moving baselines. Climatological "normals," for example, are 30-year averages, usually updated every 10 years, because weather patterns change over decadal and longer scales. For some purposes, a shifting baseline is appropriate, but a particular choice of averages might not be appropriate in the face of long-term direc- tional trends. Using shifting baselines for environmental conditions may well also lead to a relaxation of standards: gradual environmental dete- rioration can pass unnoticed under such a regime, in what has been called the "shifting baseline syndrome" (Pauly 1995~. For example, Trautman (1981) described Ohio in the late 18th century as characterized by a "pro- fusion of 'durable springs and small brooks,' both flowing throughout the year, and the great amount of bog, prairie, and swamp and forest lands which were covered with water during all or much of the year." The surface water was pure and clear. The change in the distribution, avail- ability, and quality of water in Ohio and many other places throughout the world since 1800 is dramatic and is an example of the shifting baseline syndrome. If the change had occurred in the past 20 years, it would have caused widespread dismay and concern, but because the change took 200 years (or before current environmental awareness), the baseline for comparison has shifted and the change seems acceptable. While recognizing all these difficulties, the committee attempted to identify products and processes for which "normal" or "baseline" condi- tions may be specified with sufficient rigor that they can be used as standards to evaluate important environmental changes. EVALUATING INDICATORS If the nation is to adopt an ecological indicator and invest the human and financial resources necessary to gather, assemble, and interpret the data the indicator is based on, the indicator's value and rationale must be clear. Therefore, for each recommended indicator, we discuss the follow- ing subjects insofar as the available information permits: Why the indicator is useful. The ecological model that underlies the indicator. The range of values the indicator can take and what the values mean. change. Whether the needed input data are already being gathered, and, if so,by whom. The temporal and spatial scales over which the indicator is likely to

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26 ECOLOGICAL INDICATORS FOR THE NATION If the needed data are not being gathered, what new data are needed and who should collect them. The probable effects of new technologies on our ability to make the required measurements and how soon significant technological changes are likely. For each indicator, it is of course essential to periodically evaluate its usefulness, reliability, and cost-effectiveness. REALISTIC EXPECTATIONS ABOUT THE VALUE OF INDICATORS The value of ecological indicators rests on the premise that better understanding of what is happening in the nation's ecosystems leads to better and more effective policies for encouraging desirable changes, dis- couraging undesirable changes, and maintaining variability within "tolerable" limits. Indicators must be developed with the knowledge that there is much that is not known about ecosystems and how they function (see Landres t1992} for a thoughtful discussion of the value and limits of ecological indicators). For example, the number of species on Earth is not known within an order of magnitude; so the current extinction rate as a fraction of all species cannot be known, even if the number of species becoming extinct each year were known (this number is known for a few groups). Only rough estimates of the value to society of ecological goods and services are available. With good investment of financial and human resources, some current unknowns will become better understood, but some things that would be useful to know are intrinsically unknowable. No amount of effort will provide an accurate census of the number of species on Earth or their extinction rates. The exact weather several months in advance is unknow- able, as is the exact rate of change in global mean temperature as a result of greenhouse gas forcing. Future research can reduce the degree of uncertainty in these estimates, but no amount of research can eliminate uncertainty completely. Ecological indicators must be developed and used with the knowledge that substantial uncertainty will always exist. The allocation of human and financial resources to obtain the data needed for ecological indicators should be evaluated in terms of the degree of uncertainty removed per unit of effort and the resulting marginal increase in value of the indicators. Research to reduce uncertainties that have little effect on the value of currently used indicators should clearly be given lower priority than research that reduces significant uncertain- ties in indicators. The committee's recommendations for research have been developed with these criteria in mind.