22

Environmental Bioindicators, 1:2239, 2006

Copyright Taylor & Francis Group, LLC
ISSN: 1555-5275 print/ 1555-5267 online
DOI: 10.1080/15555270590966483
UEBI 1555-5275 1555-5267 Environmental BioIndicators, Vol. P, No. 01, JUNE 2005: pp. 00 Environmental Bioindicators
Bioindicators: Types, Development, and Use
in Ecological Assessment and Research
Bioindicators in Ecological Assessment and Research J. Burger
JOANNA BURGER
Division of Life Sciences, Environmental and Occupational Health Sciences
Institute, and Consortium for Risk Evaluation with Stakeholder Participation,
Rutgers University, Piscataway, New Jersey, USA
Government, scientists, managers, and the public are interested in assessing the health
of ecosystems. Initially ecologists concentrated on assessing condition, reproductive
success, and survival of a wide range of individual species, but this approach quickly
broadened to include the health of communities, ecosystems, and landscapes, as well as
the human dimension. Monitoring ecosystem health requires the use of a suite of bioin-
dicators that are biologically, methodologically, and societally relevant, and can be
used effectively over time to assess trends and provide early warning. Bioindicators can
be developed for ecosystem health assessment, for human effects and interventions,
human health assessment, and for evaluating sustainability. Whereas ecologists initially
developed indicators to measure health or well-being of relatively pristine environ-
ments, the usefulness of indicators is enhanced if they can assess both ecological and
human health, provide trends data, and be used to examine a wide range of stressors,
from natural to anthropogenic. A literature review indicated that most ecological indi-
cators have been developed for ecosystem function, followed by political, regulatory,
cost, and risk assessment considerations. There are four main types of indicators, which
are not mutually exclusive, including 1) ecosystem health assessment, 2) human effects,
3) human interventions, and 4) human health and well-being. These indicators can then
be used to assess the current health of a species or system, the effects of particular
human activities on ecosystems, and the efficacy of management, remediation, and res-
toration, or just to track trends over time. Bioindicators that encompass several catego-
ries have the greatest chance of being implemented over the long term.
Keywords bioindicator, environmental, contaminants, ecological receptors, vertebrates
Governmental agencies, tribal nations, scientists, conservationists, managers, regulators,
and the public are increasingly interested in assessing the well-being of our earths diverse
ecosystems, including individual species and species groups. This interest has led to
Many people contributed to various aspects of my research and thinking about bioindicators
over the years, and I thank then now: M. Gochfeld, M. Greenberg, B. D. Goldstein, C. W. Powers,
K. Cooper, I. L. Brisbin Jr., R. Ramos, C. Dixon, C. Jeitner, K. F. Gaines, R. A. Kennamer, C. Lord,
C. Safina, T. Shukla, and S. Shukla. The research reported herein was conducted under approved
Rutgers University protocols, and was funded by NIMH, NIEHS (ESO 5022), EPA, US Fish &
Wildlife Service, National Wildlife Foundation, NJ Endangered and NonGame Species Program,
Wildlife Trust, Consortium for Risk Evaluation with Stakeholder Participation (CRESP) through the
Department of Energy cooperative agreement (AI # DE-FC01-95EW55084), and the Environmental
and Occupational Health Sciences Institute. The views expressed in this paper are solely the respon-
sibility of the author, and do not represent those of the funding agency.
Address correspondence to Joanna Burger, Division of Life Sciences, Rutgers University, 604
Allison Road, Piscataway, NJ 08854-8082, USA. E-mail: burger@nel-exchange.rutgers.edu
Bioindicators in Ecological Assessment and Research 23
establishment of local, state, and federal agencies, conservation/preservation societies, and
recreational and hunting/fishing groups. Assessing ecological and human health involves
establishing biomonitoring plans that use indicators and biomarkers of exposure and effects.
Since humans substantially influence ecosystems and can be severely and negatively
impacted by unhealthy environments, they are considered in the context of both roles.
Assessing ecological health for species, populations, communities, and ecosystems
involves evaluating the current condition or status, and monitoring changes over time.
The latter can be retrospective or prospective. Monitoring, or biomonitoring, is the
centerpiece of ecological assessment. Monitoring or surveillance are key to assessing
the status or well-being for ecological receptors within functioning ecosystems. Moni-
toring data can be obtained from many sources, involving many abiotic and biotic
systems, at a variety of spatial and temporal scales. Ideally, monitoring data are tailored to
meet the needs of a particular question or situation, and normally provide information
on status and trends. Monitoring can provide early warning of any changes that could
result in significant risk to individual species (including humans), populations,
communities or ecosystems. Since the multitude of species in an ecosystem cannot all
be monitored, it is essential to develop a suite of bioindicators that can be used to
assess status and trends within that ecosystem (Table 1; Piotrowski 1985; Peakall
1992; Burger and Gochfeld 2001a; Carignan and Villard 2001). Bioindicators and
biomarkers need to be developed in conjunction with biomonitoring plans because they
are the primary assessment tool. Long-term monitoring programs, and their associated
bioindicators, require the interest and support of the general public, as well as govern-
ment acceptance and commitment, as public funds are needed to conduct these pro-
grams. Such interest is more easily gained if the bioindicators provide information
about both human and ecosystem health.
In this paper I consider some monitoring plans and bioindicators, attributes of suc-
cessful bioindicators, types of bioindicators, some specific bioindicators, and how bioindi-
cators are used in management and research. Bioindicators can be defined as relatively
simple measurements that relay scientific information about complex ecosystems and
their component parts (Stahl et al. 2000).
Monitoring and Bioindicators
Biological systems or processes can be monitored for a wide range of goals, including
establishing health status for temporal or spatial trends, evaluating the effects of particular
natural or anthropogenic stressors, and evaluating the efficacy of deliberate anthropogenic
measures (e.g., remediation, restoration, reintroduction). Although some people believe
Table 1
Indicators and definitions
Indicator: Index or measurement endpoint to evaluate health of a system (economic,
physical, biological, human)
Bioindicator: Biota that are developed as indicators of the quality of the environment, the
biotic component, or humans within an ecosystem.
Environmental: Measures quality in media (water, soil, sediment, air)
Ecological: Measures quality of biological component within the broader physical
ecosystem.
Human Health: Measures quality of human health
24 J. Burger
that the goal of biomonitoring is to evaluate the effect of human activities on biological
resources (Fore et al. 1996), goals can be broader and encompass developing a basic
understanding of how natural forces (weather, storms, competition, and other interspecific
interactions) affect population stability, community structure, and ecosystem functioning.
Monitoring data may reflect abiotic systems (air, water, soil, sediment), biological
processes (numbers of organisms, mortality rates, reproductive rates), biochemical mark-
ers (enzyme activity, hormone levels), or toxicological markers (blood lead, urinary
metabolites) and effects. Although biological processes have usually involved individuals
or populations, recent attention has focused on ecosystem structure and function, such as
species diversity, productivity, nutrient cycles, and food web relationships (Rapport et al.
1992). Similarly, there are larger-scale human processes that are of interest (disease rates,
migrations).
Sources of monitoring data may be low tech (field observations) or high tech (real-time
data acquisition by satellites). Data sets may be sparse (one observation per year) or dense
(updated several times a minute), and the scale of spatial resolution varies greatly as well.
Although monitoring data can be qualitative, they are usually quantitative in nature. Qual-
itative observations may lead to the establishment of monitoring plans with very specific
quantitative endpoints. A number of tools are available to aid in developing monitoring
schemes, including sophisticated toxicity tests, remote sensing, GIS, and spatially explicit
simulation models (Cairns and Niederlehner 1992, 1996; Cairns et al. 1992; Aspinall and
Pearson 2000). GIS tools can be used to show 1) spatial and temporal patterns of bioindi-
cators and biomarkers, 2) the relationships between different types of indicators, and
3) spatial and temporal patterns in the stressors and effects. The available tools should not
dictate the choice of monitoring plans and indicators. In many cases, suites of indicators
will be required (Harwell and Kelly 1990).
Monitoring plans should take into account the value and vulnerability of the ecosystems,
the relative susceptibility of the ecosystem, the resiliency of the system, and the level of
sustainability desired (Burger 1997a, 2002). Monitoring schemes will be most useful if
they include 1) many species representing different trophic levels, 2) indicator selection
based on sound quantitative, existing information, 3) standardized protocols, and 4) cau-
tion in interpreting population trends, levels of anthropogenic stressors, contaminant lev-
els, and other parameters (Peakall 1992; Burger and Gochfeld 2001a; Carignan and Villard
2001). Although monitoring data for contaminants are useful for risk assessment (Suter
1990, 1993, 1997), such data are also useful for assessing status and trends without formal
risk assessment. There are several paradigms to assess human and ecological health, but
both human and ecological health risk assessment emerged as paradigms embodying the
disciplines of toxicology and exposure assessment (NRC 1983, 1993; Burger 1997b). Other
regulatory frameworks have been developed for ecological and human health risk assess-
ment/management (NRC 1986; Norton et al. 1992; EPA 1997; Rand and Zeeman 1998).
It is not the purpose of this paper to examine a wide range of monitoring programs,
but three in the United States are worth mentioning: 1) the US Environmental Protection
Agencys (EPA) Environmental Monitoring and Assessment Program (EMAP), 2) the
National Oceanic and Atmospheric Administrations (NOAA) Status and Trends Program,
and 3) the Great Lakes colonial bird program. There are also several long-term biomoni-
toring programs worldwide, including monitoring of acidification in lakes in Europe
(Vesely et al. 1998a,b; Vrba et al. 2003) and contaminants in seabirds in the German
North Sea (Becker 1989). These established, large-scale monitoring programs provide
information on both current status and long-term trends, which allows evaluation of
species, population, and ecosystem effects.
Bioindicators in Ecological Assessment and Research 25
The EMAP of the US EPA examines the health of a suite of indicator species
throughout the country (Summers et al. 1995). The National Oceanic and Atmospheric
Administrations Status and Trends Program provides information on many marine
species in the US coastal waters. NOAA uses a few bioindicators to examine marine
pollution, providing data on population dynamics and stability (OConnor and Ehler
1991), but not on the effects of other physical or biological stressors. The NOAA program
is extremely useful because it provides comparative data on the relative contaminant
levels in different bays and estuaries in coastal US waters. In the Great Lakes, populations
of colonial and fish-eating birds, such as herring gull (Larus argentatus) and their eggs,
are used as bioindicators of the water and environment (Fox et al. 1978, 1991). Levels of
PCBs and other contaminants in the Great Lakes were associated with chick abnormali-
ties, parental neglect, and reproductive impairment in some fish-eating birds, leading to
populations declines (Fox et al. 1991; Gilbertson et al. 1991; Fox 1994). The Great Lakes
program has provided a monitoring program that employs a wide range of species at different
trophic levels. Other seabirds and predatory birds have been used elsewhere for geographical
comparisons (Newton 1991; Thompson et al. 1998; Burger and Gochfeld 2004a). The
acidification biomonitoring program from central European lakes spans the period from
1871 to 2000, with more detailed information since 1984 (Vesely et al. 1998a,b; Vrba
et al. 2003). In these lakes there has been a remarkable decline in nitrogen deposition that
parallels a drop in sulphur. Other biomonitoring programs are just starting, such as the
monitoring of effects from nuclear power plants in Europe (Svadlenkova et al. 1990,
1996; Moravec et al. 1997; Axelrod 2004).
Attributes of Successful Bioindicators
Bioindicators must be developed in such a way that they have long-term support, or they
will not be conducted for a useful time period (Stout 1993; OConnor and Dewling 1986;
Suter 1990). This is especially true today where there is increasing interest in efforts to
manage and use ecosystems sustainably (Marques 2001; Wells 2003; Gauthier and Wiken
2003; Beratan et al. 2004). Thus, indicators should be selected to maximize their biological,
methodological, and societal relevance (Table 2, after Burger and Gochfeld 2004b). First
and foremost, an indicator must exhibit changes in response to a stressor, but not be so
sensitive that changes occur when there is no cause for concern (no lasting reproductive,
survival, or population effects). The response should not be so sensitive that it indicates
trivial or biologically unimportant variations, or simply varies randomly. The changes
must be attributable to a particular stressor (or series of stressors), and important to the
well-being of the organism (Linthurst et al. 1995). Further, the changes being measured
should reflect not only impairment to the species itself, but to populations, communities,
and ecosystems (EPA 1997).
An indicator that is biologically relevant, but is not methodologically relevant, will
simply not be employed (Burger and Gochfeld 2001a, 2004b). A good indicator should be
easy for scientists to measure, for managers to use in their resource management, for
conservationists to employ in species preservation, and for regulators to employ in compliance
mandates. Ease of measurement is a key characteristic, and includes such aspects as clar-
ity in objectives, relationship to a problem, ease of identification of important features,
and ease of data gathering and analysis. To be assured that an indicator is easy to use
requires extensive field testing with a range of sampling and observational scenarios by
multiple technicians.
26 J. Burger
Societal relevance is an important attribute of a useful indicator because without pub-
lic and governmental support, the indicator will not be used over appropriate spatial and
temporal scales that provide meaningful information (Fox 1994). Collecting data on a
bioindicator for only one site, or for only one or two years, generally will not provide
usable data for scientists to evaluate populations, for managers to select among management
methods, or for regulators to identify species requiring protection or restrictions. Govern-
mental agencies must be willing both to fund the implementation of the indicators, and to
act on the results. Institutional controls are essential to ensure the continuation of the mon-
itoring schemes, including funding, analysis, and corrective actions. Charismatic species,
such as bald eagles (Haliaeetus leucocephalus) or peregrine falcons (Falco peregrinus),
Table 2
Features of bioindicators for environmental and ecological health assessment
Biological Relevance Provides early warning
Exhibits changes in response to stress
Changes can be measured
Intensity of changes relate to intensity of stressors
Change occurs when effect is real
Changes are biologically important and occur early
enough to prevent catastrophic effects
Change can be attributed to a cause
Change indicates effects on both organisms themselves,
and on others higher on trophic scale
Can be used as sentinels for humans
Methodological Relevance Easy to use in the field
Can be used by nonspecialists
Easy to analyze and interpret data
Measures what it is supposed to measure
Useful to test management questions
Can be used for hypothesis testing
Can be conducted in reasonable time
Doesnt require expensive or complicated equipment
Easily repeatable with little training
Societal Relevance Of interest to the public
Of interest to regulators and public policy makers
Easily understood by the public
Methods transparent to the public
Measures related to environment, ecological integrity,
and human health
Cost-effective
Adds measurably to other indicators
Complements other indicators
These features apply for a wide range of indicators for physical, biological, chemical and radio-
logical stressors, and can be used to assess ecological quality, and to evaluate the efficacy and integ-
rity of management, remediation, restoration, or other environmental actions (after Cole et al. 1998,
Burger 1999, and unpublished, Burger and Gochfeld 2001a, 2004b, Carignan and Villard 2002).
Bioindicators in Ecological Assessment and Research 27
are often used as indicators (Fox 1994) because there is sustained public and governmen-
tal interest. Population failures of these species in the early 1950s served as bioindicators
of chlorinated hydrocarbon pesticide contamination long before the term was used.
Further, charismatic or large species, such as colonial waterbirds, raptors, and loons, have
proved to be of great interest to the public (Risebrough 1991; Kushlan 1993; Burger et al.
1994; Evers 2001; Evers et al. 2003; Burger and Gochfeld 2004a).
Types of Bioindicators
In this section, I discuss the different types of bioindicators. The term indicator was ini-
tially used for economic (e.g., GNP), and later social, indicators and was used to refer to
measures used to assess the health of the economy. In its broadest sense, three kinds of
ecological indicators can be distinguished, including media indicators (soil, air, water),
ecosystem health assessments, and human health indicators (Figure 1). To this traditional
matrix, I add human intervention indicators that can be used to evaluate interventions such
as remediation, restoration, and sustainability.
The Environmental Monitoring and Assessment Program (EMAP) of the US EPA
(Summers et al. 1995) defines three types of indicators: 1) response indicators that quantify
condition of the ecosystem, 2) exposure indicators that can be related to direct exposure,
and 3) stress indicators that relate to the probable sources of pollution or degradation
(Messer et al. 1991). This distinction is worth critical thought during selection of bioindi-
cators, as different indicators may be required for each of the three indicator types. The
Figure 1. Different kinds of indicators, and their relationship to assessment, biomonitoring,
management, policy, and sustainability.
28 J. Burger
importance of selecting bioindicator endpoints that can be measured cannot be underesti-
mated (Suter 1990; Norton et al. 1992). Human and ecological well-being, however, also
includes social/economic features, requiring indicators as well (Figure 1). To be most useful,
ecological and human health indicators should be combined or coordinated (Burger and
Gochfeld 1996, 2001a, 2004b).
There are several axes for development of bioindicators that include: 1) biological
level of organization (Table 3), 2) type of stressor (physical, biological, chemical, and
radiological), 3) single versus multiple stressors, and 4) degree of anthropogenic effects
(pristine to human-dominated). These categories are not mutually exclusive, but bear
consideration and suggest the importance of clearly defining the objective of the monitoring
plan why is a particular indicator being developed?
The recent emphasis on indicators of sustainability brings us closer to the original use
of indicators for economic and societal stability (Hart 1999). Although some argue that
even ecological indicators of sustainability are mainly public policy issues (McCool and
Stankey 2004), the importance of developing these indicators for managing specific
Table 3
Usefulness of indicators at different biological levels of organization to ecological health
(modified after Burger and Gochfeld 2004b, and unpublished).
Ecological Level Type of Indicator Ecological Health
Individual Contaminant levels
Lesions
Disease
Tumors
Infertility
Growth
Longevity
Reproduction
Age of reproduction
Used to evaluate health of individuals;
For evaluation of risk to higher-level
consumers;
As an indicator of health of its foods,
including prey.
Population Reproductive rates
Growth rates
Survival rates
Movements
Biomass
Energy flow
Used to evaluate health of populations
of species, particularly endangered
or threatened species;
For comparison among populations;
For temporal comparisons.
Community Foraging guilds
Breeding guilds
(groups of related species)
Predator-prey interactions
Competitive interactions
Measures health of species using the
same niche, such as colonial birds
nesting in a colony,or foraging
animals such as dolphins and tuna;
Indicates relationship among different
species within guilds or
assemblages;
For spatial and temporal comparisons;
For evaluating efficacyof management
options.
Continued
Bioindicators in Ecological Assessment and Research 29
ecosystems is clearly established (Gauthier and Wiken 2003; Wells 2003; Diaz-Balteiro
and Romero 2004). Managers often use indicators specifically to evaluate the effective-
ness of particular measures on the sustainability of populations or ecosystems (Barnthouse
et al. 2002), and may integrate a suite of indicators of sustainability for specific habitats
(Wulf 2003). There is disagreement about the meaning of sustainability, as well as what is
being sustained. For example, whereas most ecologists use sustainability to refer to natu-
ral resources, the Department of Energy uses sustainability to refer to continued safety or
protection from risks due to chemicals and radionuclide wastes. Although sustainability is
a laudable goal, it is also difficult to accomplish (Beratan et al. 2004), and developing
indicators for ecological sustainability is a daunting task. Finally, developing bioindica-
tors for sustainability (often a combination of other types of indicators) represents a forward-
looking approach to management, since indicators are not only being used to evaluate past
human disruptions, but to predict and manage future populations or ecosystems.
Most books devoted to environmental monitoring and ecological risk assessment
provide methods for evaluation at different levels of ecological organization, but do not
provide a comprehensive plan for any one habitat or land type, although some have pro-
vided plans for regions (see Hunsaker et al. 1990; Suter 1990; Cairns 1990). Excellent
methods are available (Linthurst et al. 1995), but authors seldom commit to a specific
plan, or to a specific set of indicators, although there have been attempts to rank the utility
Table 3
Continued
Ecological Level Type of Indicator Ecological Health
Ecosystem Species diversity
Decomposition rates
Erosion rates
Primary productivity
Energy transfer
Nutrient flow
Relationship among
different trophic levels
Measures changes in relative presence
of species, how fast nutrients and
energy will become available, how
fast nutrients in soil will no longer
be available, how much photosyn-
thesis is occurring;
Examines overall structure of the
ecosystem in terms of the relation-
ships among trophic levels;
For evaluating efficacy of management
options.
Landscape Relative amounts of
different habitats
Patch size
Corridors between habitat
types or different
ecosystems
Measures dispersion of different
habitat types, indicates relative spe-
cies diversity values;
Measures the differences among habi-
tats;
Measures distribution of corridors and
refugia within the landscape;
Also can measure the relationship
between developed and natural
areas;
For evaluating the importance of
specific ecosystems within the land-
scape.
30 J. Burger
of individual species as bioindicators (Golden and Rattner 2003). In the next section, I dis-
cuss examples of bioindicators to illustrate the complexity that surrounds a given bioindi-
cator, and the levels of biological organization that can be examined with them.
Specific Bioindicators
Toxicology, conservation, and biology have largely developed bioindicators for their
respective stressors, without considering the implications of other stressors. Environmental
protection agencies have dealt primarily with understanding how levels of contaminants in
organisms, and their effects, have varied over time and space, often in relation to point
source pollution. Fish and wildlife departments, and environmental conservation pro-
grams have examined changes in wildlife and habitats as a function of predator changes,
competition, invasive species, weather, and human disturbance. Biologists have some-
times developed bioindicators for reproductive success, survival, and behavior without
taking into account the effects or presence of contaminants. Sometimes they have even
ignored human effects, preferring instead to study pristine populations removed from
human intervention. It is important, however, to remember that biological, physical, and
chemical (and radiological) stressors all affect ecological receptors, including humans.
Interpretation of data from monitoring schemes with indicators should incorporate a range
of stressors.
A wide range of species or tissues have been used as bioindicators, such as algae and
other plants (Manning et al. 2002; Manning and Godzik 2004; Madejon et al. 2004;
Poikolainen et al. 2004; Wallberg and Moberg 2002), invertebrates (Berger and Dallinger
1993; Goldberg and Bertine 2000; Berny et al. 2002; Chou et al. 2003; Izquierdo et al.
2003; Reid and MacFarlane 2003 ), fish (Baumann 1992; Corsi et al. 2003; Iliopoulou-
Georgudaki et al. 2003; Burger and Campbell 2004), amphibians (Pollet and Bendell-
Young 2000), birds (Fox et al. 1978, 1991; Becker 1989; Gilbertson et al. 1991; Burger
1993; Fox 1994; Burger and Gochfeld 1995, 2001b), seabird eggs (Cifuentes et al. 2003;
Burger and Gochfeld 2004a), bird blood (Evers et al. 1998), and mammals (Wren 1986),
to name just a few. The main objective of this paper is not to develop or describe specific
indicators (a monumental task that several agencies and organizations have undertaken;
Harwell and Kelly 1990; Hunsaker et al. 1990; Norton et al. 1992; Peakall 1992; Holl and
Cairns 1995; Burger and Gochfeld 2001b, 2004b). However, two examples will be given
to illustrate that any species (or species group) can serve a multitude of bioindicator roles,
for itself, for organisms it eats, and for organisms that eat it.
Bass (or any predatory fish) can serve a range of bioindicator functions because of
their complex role in their communities (Figure 2, see Burger 1999a). Largemouth bass
(Micropterus salmoides) are ideal as indicators because they are widespread, numerous,
and are a popular sport fish (Burger et al. 2001a,b,c; Burger and Campbell 2004). Other
intermediate-sized predatory fish are also ideal, including bowfin (Amia calva), chain
pickerel (Esox niger), yellow perch (Perca flavescens), and bluefish (Pomatomus saltatrix).
Measuring contaminants in bass is useful because of the risk that such contaminants pose
to higher-level carnivores, such as larger fish, predatory birds, and humans. Understanding
reproductive success, growth rates, survival, and population dynamics of bass in a region
can lead to information that can serve as a baseline for establishing trends, which in turn
are useful indicators of bass populations, community structure, and fish guilds. Because
fishing is such a popular pastime, and bass are a preferred fish in many regions (Fleming
et al. 1995; Burger et al. 2001a; Campbell et al. 2002), indicators of bass population stabil-
ity lead directly to establishing creel and size limits for fishing. Bass can also be directly
Bioindicators in Ecological Assessment and Research 31
indicative of the health and well-being of the organisms they ingest (plants and animals),
of their own populations, of populations with which they interact with (as competitors for
space, food, and habitat), and of populations that consume them. All of these interactions
have cascading effects, in that if the population of bass decline (due to a range of
stressors), then: 1) species that compete directly with bass for food may increase (due to a
lack of competition with bass); 2) some species of prey may increase because their own
competitors are being eaten by the bass competitors (which have now increased); 3) spe-
cies that prey upon bass will decline, causing their own predators to decline; and 4) the
disruptions in the normal population numbers could affect nearly all trophic levels
because of a change in the relative number of different organisms (to serve as predators,
competitors, and prey). In summary, bass can serve as bioindicators at several ecological
levels to evaluate individual and population health, as well as community and ecosystem
health (Table 3).
Raccoons are an example of a mid-level omnivore and predator that has a complex
range of plants and animals it eats, and a complex array of animals that consume them
Figure 3, Burger 1999a). Raccoons are useful bioindicators because they are abundant and
widespread throughout the United States, occupy a variety of habitats from rural to urban,
are omnivores and eat some organisms that are both high and low on the trophic scale, are
relatively sedentary, and are hunted and eaten in some parts of the United States (Burger
Figure 2. Schematic of bioindicator properties of bass, and other predatory fish. Ingestion
exposures of bass are shown on bottom of diagram. Measurement of population, reproduction,
growth, human disturbance level, and contaminant levels can all serve as indicators. The three main
categories of stressors are biological (e.g., disease, competition, predation), habitat changes, and
contaminants.
32 J. Burger
et al. 1999). Further, they are terrestrial animals that eat prey both on land and from the
water. Raccoon hunting is a popular sport in the south, and they are eaten by people or
their pets (SCDNR 1996a,b). Because hair can be used, museum collections can provide
samples for temporal analyses (Porcella et al. 2004).
Raccoons obtain contaminants from their water and food, which includes fruits, nuts,
seeds, vegetable crops, invertebrates, small vertebrates (frogs, snakes), fish, and anything
else they can find, including garbage (Burger 1999b). Because males can travel a few kilo-
meters in their daily movements, they are useful for monitoring off-site movement of pol-
lutants from contaminated sites, such as Superfund sites, or those owned by the
Department of Defense or Department of Energy (Gaines et al. 2000; Burger et al. 2000,
2002). They may also serve as prey for larger predators (including humans) and their car-
casses are eaten by scavengers (microbes return the rest of the contaminants and nutrients
to the ecosystem). Understanding contaminant levels in their tissues can provide informa-
tion on the health of raccoon populations themselves, on their predators (including
humans), on other organisms that occupy the same trophic level, and on other parts of the
ecosystem, including the ultimate decomposition of their carcasses. Other stressors, such
as habitat changes, can lead to population changes, with associated changes on other
organisms within their food web. The complexity shown in Figure 3 illustrates how one
species within its food web can link multiple measurement endpoints (shown in rectangles
on the figure) that can serve bioindicator roles.
Figure 3. Schematic of bioindicator properties of raccoon, and other mid-level predators. Ingestion
exposures of raccoons are shown on bottom of diagram. Measurement of population, reproduction,
growth, human disturbance level, and contaminant levels can all serve as indicators.
Bioindicators in Ecological Assessment and Research 33
Use of Bioindicators in Management and Research
The development of bioindicators has both a research and a management component, and
therefore can be much improved by the inclusion of a wide range of stakeholders in the
process (Presidents Commission 1997). Nowhere is the distinction between pure research
and management less clear than in the development of bioindicators. Managers are depen-
dent upon scientists to develop and test bioindicators, and often to collect the data on the
bioindicators. Scientists are dependent upon managers for identification of a particular
problem or stressor requiring indicators, and to managers and regulators for the funds and
permits to conduct research to develop suitable indicators. Indicators are most useful when
both managers and scientists (as well as the public) are involved in their development
from the outset.
Understanding how bioindicators are used in both management and research requires
surveying what types of indicators are used, for what stressors, and for what species, com-
munities or ecosystems. A review of the articles published in the journal Ecological Indi-
cators reveals the main focus of bioindicator research by scientists and managers (Figure 4).
More than twenty percent of the papers in this journal (which began in 2001) dealt with
aspects of ecosystem functioning, and another fifteen percent dealt with political, regula-
tory, and cost considerations. Only twelve percent of the papers dealt with pollution and
contaminants, and another eight percent dealt directly with human activities (such as min-
ing, agriculture, transportation and the military). It is these two categories (pollution,
human activities) that have most often been addressed by formalized risk assessment.
There are, of course, many other journals that publish papers on indicators.
These data, and my own research and observations suggest that there are four main
types of ecological indicators: 1) ecosystem health assessment, 2) human effects,
Figure 4. Percentage of articles in the journal Ecological Indicators that fall into each category. All
articles published in the journal from its inception through 2004 are included in this table.
34 J. Burger
3) human interventions, and 4) human health and well-being (Table 4). Although the latter
represents one receptor within ecological systems, it deserves special mention because of
our self-interest in our health and well-being, and in the user services provided to us by
ecosystems (clean air and water, hunting and fishing, recreation, and aesthetics). Animals
can also serve a special bioindicator role as sentinels for human health hazards, where ani-
mals are placed in specific environments for that purpose (NRC 1991; van der Schalie
1997; van der Schalie et al. 1999; Rabinowitz et al. 1999; Stahl 1997; Fox 2001).
Ecosystem health assessment indicators are those traditionally developed by ecolo-
gists for relatively pristine environments. They help us understand the pure aspects of
community and ecosystem functioning, and they form the basis for examining both the
human effects of stressors and whether human interventions (remediation, restoration) are
successful. Used in the latter context, they can help managers, regulators, and the public
make decisions about future remediation and restoration options; for example, what
actions have been successful in maintaining healthy populations and communities?
Conclusions
Bioindicators (and biomarkers) were developed along with biomonitoring plans because
they are the main tool for such plans. The formalized process of risk assessment, which
developed in the early 1980s, stimulated the further development of key indicators by state
Table 4
Types of environmental and ecological indicators that can be
developed singly or in combination.
A. Ecosystem Health Assessment
1. Media (soil, water, air)
2. Species, population, and community health
3. Ecosystem and landscape health
4. Regional and global health
B. Human Effects
1. Point source or specific activities
(military, agricultural, forestry, transportation)
2. Nonpoint source (pollution, global warming, nutrient cycling)
3. Specific stressors vs. mixtures and multiple stressors
C. Human Interventions (corrective)
1. Remediation
2. Restoration
3. Sustainability
D. Human Health and Well-being
1. Individual and population health
2. Cost and regulatory issues
3. Environmental justice
4. Recreational (natural resource use) and existence values
5. Clean water, air, and ecosystems
6. Animals as sentinels
7. Quality of life and well-being
Bioindicators in Ecological Assessment and Research 35
and federal governmental agencies, as well as other land and ecosystem managers. Some
federal government agencies, such as EPA and NOAA, underwent a formalized process of
establishing risk assessment guidelines that codified some bioindicators (or at least types
of bioindicators, such as top-level predators within ecosystems). To be of greatest use to
managers, regulators, and the public, bioindicators should be part of a long-term biomoni-
toring plan that examines both temporal and spatial trends. This requires that bioindicators
be biologically, methodologically, and societally relevant. They should measure responses
to stressors before the effects become catastrophic, be easy to use, be cost-effective, and
important to the public.
There are four main types of indicators, which are not mutually exclusive, that relate
to ecosystem health assessment, human effects, human interventions, and human
health and well-being. All of these can be used as indicators of sustainability, which
can in turn be used for a range of purposes, including 1) assessing past damage, 2)
evaluating the efficacy of restoration of ecosystems and remediation from biological,
chemical/radiological, physical and other insults, and 3) predicting future health and
well-being. Most ecologists deal mainly with ecosystem health assessment, but the
separation of ecosystem health indicators from a range of human-dominated indica-
tors limits both their applicability and their interest to the public, regulators, and poli-
ticians. Moreover, bioindicators can be selected that encompass more than one type.
For example, to examine the effects of remediation or restoration, it is essential to
select ecosystem health assessment indicators as the measurement endpoints. Further,
indicators can be selected that tell us something about both human and ecological
health (Burger and Gochfeld 2001a, 2004b), and these will often receive greatest societal
support.
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