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Annu. Rev. Ecol. Evol. Syst. 2004. 35:89–111
doi: 10.1146/annurev.ecolsys.35.112202.130132
APPLICATION OF ECOLOGICAL
INDICATORS
∗
Gerald J. Niemi
1
and Michael E. McDonald
2
1
Natural Resources Research Institute and Department of Biology, University of
Minnesota, Duluth, Minnesota 55811; email: gniemi@d.umn.edu
2
U.S. Environmental Protection Agency, Environmental Monitoring and Assessment
Program, Reston, Virginia 20191; email: McDonald.Michael@epa.gov
Key Words
assessment, condition, monitoring, responses, stressors
■ Abstract Ecological indicators have widespread appeal to scientists, environ-
mental managers, and the general public. Indicators have long been used to detect
changes in nature, but the scientific maturation in indicator development primarily
has occurred in the past 40 years. Currently, indicators are mainly used to assess the
condition of the environment, as early-warning signals of ecological problems, and
as barometers for trends in ecological resources. Use of ecological indicators requires
clearly stated objectives; the recognition of spatial and temporal scales; assessments
of statistical variability, precision, and accuracy; linkages with specific stressors; and
coupling with economic and social indicators. Legislatively mandated use of ecological
indicators occurs in many countries worldwide and is included in international accords.
As scientific advancements and innovation in the development and use of ecological
indicators continue through applications of molecular biology, computer technology
such as geographic information systems, data management such as bioinformatics, and
remote sensing, our ability to apply ecological indicators to detect signals of environ-
mental change will be substantially enhanced.
INTRODUCTION
Humans trying to understand the current condition or predict the future condition
of ecosystems have often resorted to simple, easily interpreted surrogates. Often
these surrogates have been indicators that allow humans to isolate key aspects of the
environment from an overwhelming array of signals [National Research Council
(NRC) 2000]. Early humans used indicators like seasonal migratory movements
of animals or flowering by spring flora to provide insight into changing environ-
mental conditions. The first reference to environmental indicators is attributed
to Plato, who cited the impacts of human activity on fruit tree harvest (Rapport
1992). Morrison (1986) reviewed the work of Clements (1920) and noted that the
∗
The U.S. Government has the right to retain a nonexclusive, royalty-free license in and to
any copyright covering this paper.
89
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90 NIEMI
MCDONALD
concept of indicators for plant and animal communities can be traced to the 1600s.
Clements’s (1920) work set the scientific stage for using plants as indicators of
physical processes, changes to soil conditions, and other factors. In the 1920s,
indicators were also being successfully used to determine changing environmental
conditions, such as water clarity (Rapport 1992) or air quality with “the canary in
the mine” (Burrell & Siebert 1916), which we continue to use (Van Biema 1995).
One of the more elaborate early environmental indicators was the saprobian sys-
tem (Kolkwitz & Marsson 1908), which used benthic and planktonic plants as
indicator species for classifying stream decomposition zones.
The past 40 years have seen a rapid acceleration of scientific interest in the de-
velopment and application of ecological indicators. This focus on indicators stems
from the need to assess ecological condition in making regulatory, stewardship,
sustainability, or biodiversity decisions. For example, the Clean Water Act of 1972
requires that each state produce a report every two years on the condition of all
its waters to the U.S. Environmental Protection Agency (US EPA) for Congress.
Decisions regarding sustainability and biodiversity involve both research and pol-
icy issues (e.g., Mann & Plummer 1999, Ostrom et al. 1999, Tilman 1999). In
the United States, this research has been legislatively mandated to various federal
agencies, in particular to the U.S. Department of Agriculture through the Na-
tional Forest Management Act of 1976, to the U.S. Department of Interior (1980,
Parsons 2004), and to the US EPA (2002b). These mandates have resulted from the
increasing concern for the loss of species, deteriorating water quality and quan-
tity, sustainability of resource use, climate change, and overall condition of the
environment. This interest has generated many new books, articles, and reviews
on ecological indicators (e.g., McKenzie et al. 1992; US EPA 2002b,c), as well as
a new journal (Ecological Indicators in 2001).
The public has increasingly demanded a better accounting of the condition or
health of the environment and whether it is improving or getting worse (Heinz
Center 1999; www.heinzctr.org/ecosystems). Developing scientifically defensible
indicators to establish environmental baselines and trends is a universal need at
a variety of levels. For instance, federal governments in the United States and
Canada (Environment Canada and US EPA 2003), Europe (www.eionet.eu.int),
and Australia (www.csiro.au/csiro/envind/index.htm) have developed or are de-
veloping programs for routine reporting on ecological indicators. Recent interna-
tional accords (e.g., RIO Accord) have demanded an accounting and reporting of
indicators on the state of the environment. The Montr´eal Process (www.mpci.org)
representing 12 countries was established in 1994 to develop and implement inter-
nationally agreed upon criteria and indicators for the conservation and sustainable
management of temperate and boreal forests. In 2003, US EPA (2003a) released
its first state of the environment report (www.epa.gov/indicators/roe/index.htm).
As the world human population continues to increase exponentially (Cohen
2003), and with consequent environmental demands, the applications of indica-
tors to determine status and trends in environmental condition will continue to
grow.
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ECOLOGICAL INDICATORS 91
DEFINITIONS
Early uses of indicators primarily reflected environmental conditions, and the terms
environmental and ecological indicators have often been used interchangeably. En-
vironmental indicators should reflect all the elements of the causal chain that links
human activities to their ultimate environmental impacts and the societal responses
to these impacts (Smeets & Weterings 1999). Ecological indicators are then a sub-
set of environmental indicators that apply to ecological processes (NRC 2000). For
policy makers, the amount of ecological data is often overwhelming. Environmen-
tal indicators are an attempt to reduce the information overload, isolate key aspects
of the environmental condition, document large-scale patterns, and help determine
appropriate actions (Niemeijer 2002). An example of a large-scale, policy relevant
environmental indicator is the environmental sustainability index (ESI). The ESI
was developed to allow quantitative international comparisons of environmental
conditions (World Economic Forum 2002). The ESI has five major categories:
environmental systems, reducing environmental stresses, reducing human vulner-
ability, social and institutional capacity, and global stewardship. In 2001 the ESI
included information on 68 indicators within these categories from 142 countries
(World Economic Forum 2002).
Ecological indicators embody various definitions of ecology, such as the “inter-
actions that determine the distribution and abundance of organisms” (Krebs 1978),
or more broadly the “structure and function of nature” (Odum 1963). Thus, they are
often primarily biological and respond to chemical, physical, and other biological
(e.g., introduced species) phenomena. We have chosen to combine the definitions
of the US EPA (2002b) and the hierarchy of Noss (1990), and we define ecological
indicators as: measurable characteristics of the structure (e.g., genetic, population,
habitat, and landscape pattern), composition (e.g., genes, species, populations,
communities, and landscape types), or function (e.g., genetic, demographic/life
history, ecosystem, and landscape disturbance processes) of ecological systems.
Ecological indicators are derived from measurements of the current condition
of ecological systems in the field and are either used directly or combined into
one or more summary values (US EPA 2002b). These ecological indicators can
be aggregated into ecological attributes with reporting categories, such as biotic
condition, chemical and physical characteristics, ecological processes, and distur-
bance (Harwell et al. 1999, US EPA 2002b). Ecosystem disturbance can be natural
(e.g., fire, wind, and drought) and part of the functional attributes of ecosystems
(Noss 1990), or it can be anthropogenic. Ecological indicators have been applied
in many ways in the context of both natural disturbances and anthropogenic stress.
However, the primary role of ecological indicators is to measure the response of the
ecosystem to anthropogenic disturbances, but not necessarily to identify specific
anthropogenic stress(es) causing impairment (US EPA 2002b). These indicators
have been referred to as “state indicators” in the State of the Lakes Ecosystem
Conference (SOLEC), which is a joint effort of Canada and the United States to
develop indicators for the Great Lakes (Environment Canada and US EPA 2003).
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SOLEC defines state indicators as response variables (e.g., fish, bird, amphibian
populations) and pressure indicators as the stressors (e.g., phosphorus concentra-
tions, atmospheric deposition of toxic chemicals, or water level fluctuations).
In this review we focus on ecological indicators, but clearly they can be in-
tegrated with the broader issues of ecosystem health (Rapport et al. 1998) and
ultimately with economic indicators (Milon & Shogren 1995) to be even more
useful for making policy decisions. There is a continuing debate on how to ac-
complish this integration. A common goal of linking economic and environmental
indicators is often based on the concept of sustainability. For example, Ekins et al.
(2003) provided a framework for linking economic, social, and environmental
sustainability. Their approach identified how economic and social options were
constrained if critical environmental functions were sustained. Lawn (2003) ex-
plored the theoretical foundation of several indexes of sustainability, including
the Index of Sustainable Economic Welfare and the Genuine Progress Indicator.
He found that these indexes were theoretically sound, but more robust valuation
methods were necessary. Although progress is being made, there are no indicators
that link economic, social, or environmental trends in a way that is meaningful to
the public.
USE OF ECOLOGICAL INDICATORS
Ecological indicators are primarily used either to assess the condition of the en-
vironment (e.g., as an early-warning system) or to diagnose the cause of environ-
mental change (Dale & Beyeler 2001). The widespread decline of the peregrine
falcon (Falco peregrinus) in the 1950s is an excellent example of both uses. The
catastrophic decline of the species served as an early-warning system of problems
in the environment, and research on the cause of the decline led to the diagnosis
of widespread contamination by chlorinated hydrocarbons such as DDT (Ratcliffe
1980). The widespread decline of amphibians has also been viewed as an early-
warning system of problems in the environment, yet further research has failed to
identify a specific cause for the decline. Amphibian declines are likely due to a
variety of factors, including habitat change, global climate change, chemical con-
tamination, disease and pathogens, invasive species, and commercial exploitation
(Blaustein & Wake 1995, Semlitsch 2003).
The information gathered by ecological indicators can also be used to fore-
cast future changes in the environment, to identify actions for remediation, or, if
monitored over time, to identify changes or trends in indicators (Figure 1). As the
complexity of the system being monitored increases (e.g., greater spatial scales
and levels of biological organization) or as the temporal scale increases, the cost
of gathering, analyzing, and reporting on indicators increases. Complexity also
arises from the need to quantify linkages between specific stressors and ecolog-
ical indicators (Table 1). In the few cases in which such relationships have been
determined, these ecological indicators are often considered diagnostic; however,
these linkages have seldom been made (Suter et al. 2002). A major challenge
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ECOLOGICAL INDICATORS 93
Figure 1 Illustration of the suite of ecological indicators (left) for which a suite of
assessment capabilities (right) are desired. Constraints on the development of ecolog-
ical indicators at all levels for all assessment endpoints are due to a lack of scientific
understanding and the predominance of policies requiring low cost monitoring. Goals
in applications generally include a compromise between cost-effectiveness and the
ability to defend the ecological indicator scientifically at the spatial and temporal scale
appropriate to answer the desired management objectives.
continues to be the difficulty of discerning specific stressor-response relationships
in a multiple stressor environment and the difficulty of separating anthropogenic
from natural sources of variation (Niemi et al. 2004).
Ecological indicators are usually developed by scientists and focused on as-
pects of ecosystems they believe are important for the assessment of condition.
However, environmental managers and policy makers require indicators that are
understood by the public (Schiller et al. 2001). Ideally, policy-relevant indicators
would allow: (a) assessment of both existing and emerging problems; (b) diagnosis
of the anthropogenic stressors leading to impairments; (c) establishment of trends
in condition for measuring environmental policy and program performance; and
(d) ease of communication to the public. Besides capturing the complexities of an
ecosystem and being easy to communicate, an indicator should also be easily and
routinely measurable (Dale & Beyeler 2001). Moreover, the cost of monitoring and
subsequent analyses is also a consideration for state and federal agencies. Clas-
sifications of indicators that include scientific performance, policy relevance, and
public acceptance have been proposed (Noss 1990, Cairns et al. 1993). However,
the final choice of indicators should depend on the questions being asked and the
quality of the science supporting the indicator.
Frost et al. (1992) suggest that ecological indicators should trade off two po-
tentially contradictory endpoints. They should be sensitive enough to react in a
detectable way when a system is affected by anthropogenic stress, and they should
also remain reasonably predictable in unperturbed ecosystems. McGeoch (1998)
